OCEANOGRAPHY AND MARINE BIOLOGY AN ANNUAL REVIEW Volume 28
OCEANOGRAPHY AND MARINE BIOLOGY AN ANNUAL REVIEW
Volume 2...
28 downloads
961 Views
6MB Size
Report
This content was uploaded by our users and we assume good faith they have the permission to share this book. If you own the copyright to this book and it is wrongfully on our website, we offer a simple DMCA procedure to remove your content from our site. Start by pressing the button below!
Report copyright / DMCA form
OCEANOGRAPHY AND MARINE BIOLOGY AN ANNUAL REVIEW Volume 28
OCEANOGRAPHY AND MARINE BIOLOGY AN ANNUAL REVIEW
Volume 28
HAROLD BARNES, Founder Editor
MARGARET BARNES, Editor The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland
Assistant Editors A.D.Ansell R.N.Gibson T.H.Pearson
ABERDEEN UNIVERSITY PRESS Member of Maxwell Macmillan Pergamon Publishing Corporation
FIRST PUBLISHED IN 1990 This edition published in the Taylor & Francis e-Library, 2002. This book is copyright under the Berne Convention. All rights reserved. Apart from any fair dealing for the purpose of private study, research, criticism or review, as permitted under the Copyright Act, 1956, no part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, electrical, chemical, mechanical, optical, photocopying, recording or otherwise, without the prior permission of the copyright owner. Enquiries should be addressed to the Publishers. © Aberdeen University Press 1990
British Library Cataloguing in Publication Data Oceanography and marine biology: an annual review. —Vol. 28 1. Oceanography—Periodicals 2. Marine biology—Periodicals 551.46´005 GCI ISBN 0-08-037981-8 (Print Edition) ISBN 0075-3218 (Print Edition) ISBN 0-203-01480-4 Master e-book ISBN ISBN 0-203-19131-5 (Glassbook Format)
PREFACE The twenty-eighth volume of this series of Annual Reviews contains seven articles covering a wide range of topics. In recent years the Benguela Ecosystem has been considered in some detail. The present volume sees the start of what it is anticipated will be a series of papers dealing with the Kuroshio in much the same way. As promised last year, this and future volumes will contain the full titles of all references. It is hoped that this will satisfy the popular demand for their inclusion. Our thanks go, as always, to everyone who makes our editorial task a pleasure rather than a chore.
CONTENTS page 7
PREFACE The Kuroshio. Part I. Physical Features Microbial Exopolymer Secretions in Ocean Environments: their Role(s) in Food Webs and Marine Processes A Review of the Ecology of Surf-zone Diatoms, with Special Reference to Anaulus australis Patterns of Reproduction, Dispersal and Recruitment in Seaweeds Interactions between Bivalve Molluscs and Bacteria in the Marine Environment
The Fundamentals of Insemination in Cirripedes The Ecology of Tropical Soft-bottom Benthic Ecosystems
J.L.SU, B.X.GUAN AND J.Z.JIANG
11
ALAN W.DECHO
73
M.M.B.TALBOT G.C.BATE AND E.E.CAMPBELL
155
BERNABÉ SANTELICES
177
D.PRIEUR, G.MÉVEL, J.-L.NICOLAS, A.PLUSQUELLEC, AND M.VIGNEULLE
277
W.KLEPAL
353
DANIEL M.ALONGI
381
AUTHOR INDEX
497
SYSTEMATIC INDEX
527
SUBJECT INDEX
535
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 11–71 Margaret Barnes, Ed. Aberdeen University Press
THE KUROSHIO. PART I. PHYSICAL FEATURES J.L.SU Second Institute of Oceanography, State Oceanic Administration, P.O. Box 1207, Hangzhou, Zhejiang, 310012 China
B.X.GUAN Institute of Oceanology, Academia Sinica, 7 Nanhai Road, Qingdao, Shangdong, 266071 China and
J.Z.JIANG Second Institute of Oceanography, State Oceanic Administration, P.O. Box 507, Hangzhou, Zhejiang, 310012 China
ABSTRACT A broad view of the main physical features of the Kuroshio is presented. The characteristics of the Kuroshio are discussed in three separate geographical divisions, namely, the Philippine Sea between Luzon and Taiwan, the East China Sea, and the area south of Japan. Special attention is also given to the interaction of the Kuroshio with marginal seas and epicontinental seas in the first two geographical divisions. Physical features of these seas per se are, however, not covered in this review. In the area south of Japan special attention is given to the large stationary meander path pattern of the Kuroshio, which is a unique feature among all western boundary currents of the world.
INTRODUCTION Kuroshio is the counterpart of the Gulf Stream in the North Pacific Ocean. It is the meridian segment west of the North Pacific anticyclonic gyre, defined geographically as the intensified current running from the east of Philippines to the south of Japan via the East China Sea (Fig 1). The name Kuroshio is derived from Japanese, meaning black current because of its dark cobalt-blue colour. Discovery of this strong current can be traced as far back as around the fourth century BC and mention of it can be found in historical records of both China and Japan (Su & Pu, 1987). Scientific observations of the Kuroshio were initiated by the Japanese in 1893 (Teramoto, 1972). Systematic hydrographic observations of the Kuroshio have been made by Japanese oceanographers four times a year since 1954. Large scale observational activities were launched under
12
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 1. —Schematic diagram of the North Pacific surface circulation. NEC, North Equatorial Current; NECC, North Equatorial Countercurrent; SEC, South Equatorial Current; K, Kuroshio; KE, Kuroshio Extension; NPC, North Pacific Current, CC, California Current; OC, Oyashio.
both the 13-year (1965–1977) international programme, “Cooperative Study of the Kuroshio and Adjacent Regions” (CSK), and the 10-year (1977–1986) Japanese national programme, “Kuroshio Exploitation and Utilization Research” (KER). These efforts helped a great deal in understanding the characteristics of the Kuroshio (e.g., Stommel & Yoshida, 1972; Anonymous, 1985b). Recently, a 7-year (1986– 1992) bilateral programme, “China-Japan Joint Research Program on the Kuroshio” (JRK), has also started. This review aims to present a broad view of the main physical features of the Kuroshio. The choice of the topics covered reflects what the authors think is essential to an overview of the physical aspects of the Kuroshio. We shall begin with a description of the large-scale features of the western North Pacific Ocean. Then the characteristics of the Kuroshio are discussed in three separate geographical divisions, namely, the Philippine Sea between Luzon and Taiwan, the East China Sea, and the area south of Japan. Interaction of the Kuroshio with marginal seas and coastal waters on its left flank will also be elaborated along with these discussions. Physical features of the marginal seas and coastal waters themselves will, however, not be discussed in this review. As will become evident from the following text, knowledge of the Kuroshio is gained mainly through extensive hydrographic observations. Compared with the Gulf Stream there have been fewer long duration direct current measurements of the Kuroshio. This review also complements other review articles on the biological aspects of the Kuroshio due to appear in subsequent volumes of “Oceanography and Marine Biology: An Annual Review”.
LARGE-SCALE PHYSICAL FEATURES A description of topographic features, circulation and water masses of the western part of the North Pacific Ocean is necessary to a discussion of the physical features of the Kuroshio.
THE KUROSHIO. PART I. PHYSICAL FEATURES
13
TOPOGRAPHIC FEATURES
Figure 2 is a schematic topography map of the Kuroshio region. The major part of the region is occupied by the Philippine Sea of the Pacific Ocean. The Philippine Sea is bounded on the west by the southern half of Japan, the Ryukyu Islands and the Philippines, and on the east by the Izu-Ogasawara Ridge, the Mariana Ridge and the Yap Ridge. The abyssal basin of the Philippine Sea is separated into east and west basins by the Kyushu-Palau Ridge. The east basin is divided into two parts, Shikokn Basin and West Mariana Basin north and south of 23°N, respectively. The west basin is the Philippine Basin and the region of rugged topography at the nothernmost part of it is the Daito Ridges. The Philippine Sea is connected to the South China Sea through the Bashi Channel which is spanned by three ridges. The sill depth in the channel is about 2400 m (Gilg, 1970), which limits the penetration of deep water from the Pacific
Fig 2. —Topographic feature of the Kuroshio region (modified from Mogi, 1972). Ridges: A, Izu-Ogasawara; B, Mariana; C, Yap; D, Kyushu-Palau; E, Daito; F, Ryukyu. Basins: 1, Shikoku; 2, West Mariana; 3, Philippine; 4, South China Sea. Others: I, Okinawa Trough; II, Bashi Channel; III, Sakishima Depression; IV, Tokara Strait.
14
J.L.SU, B.X.GUAN AND J.Z.JIANG
Ocean into the South China Sea. Northwest of the Philippine Sea borders the East China Sea through the Ryukyu Ridge, on which lie the Ryukyu Islands. There are three depressions along the Ryukyu Ridge. The northern depression where the Tokara Strait is located is deeper than 1000 m, and the shallow depression (called Sakishima Depression in this review) next to Taiwan has a trough over 700 m deep (Chern, 1983). The middle depression along the Ryukyu Ridge is also deeper than 1000 m. To the west of the Ryukyu Ridge there is the elongated Okinawa Trough with a maximum depth of around 2300 m. The continental slope of the broad and shallow East China Sea shelf forms the western wall of the Okinawa Trough.
LARGE-SCALE CIRCULATION IN THE WESTERN NORTH PACIFIC
Hasunuma & Yoshida (1978) constructed a long-term mean of surface dynamic height in the western North Pacific (Fig 3). It is seen that the North Equatorial Current flows westward between about 10°N to 15°N. This current is divided into two currents off the coast of Samar. The southward current is the Mindanao Current which gradually turns east joining the Equatorial Countercurrent, while the northward current forms the origin of the Kuroshio. According to Nitani (1972) the variation of this region of divergence at the sea surface can shift as far north as to the coast of southern Luzon. The North Equatorial Current has an obvious banded structure (Fig 3). The Kuroshio flows northward along the coast of Luzon and makes a slight excursion into the Bashi Strait (Fig 3). It enters the East China Sea over the Sakishima Depression from the east coast of Taiwan. In the East China Sea the Kuroshio flows northeasterly over the continental slope at the western edge of the Okinawa Trough. At around 29.5°N it backs away from the slope and re-enters the Philippine Sea through the Tokara Strait. Once inside the Pacific Ocean the Kuroshio immediately turns north and flows along the Japan coast until around 36°N, where it turns away from the coast. The meandering current after the Kuroshio leaves Japan coast is called the Kuroshio Extension. A part of this current returns westward south of the Kuroshio and is referred to as the Kuroshio Countercurrent (Uda & Hasunuma, 1969). Two cores of easterly currents are also evident between 21°N and 28°N (Fig 3). These are the north and south branches of the Subtropical Countercurrent. This banded current structure was shown to be quasistationary bands of intensified easterly zonal flow centred near 23°N and 28°N, respectively (White & Hasunuma, 1982). The mid-depth circulation of the North Pacific also shows an eastward flow from the Kuroshio region along about 20°N (Reid & Mantyla, 1978). The southeasterly current north of the Kuroshio Extension is the Oyashio Current.
WATER MASSES IN THE PHILIPPINE SEA
Water masses in the North Pacific have been discussed in many texts (e.g., Sverdrup, Johnson & Fleming, 1942; Tchernia, 1980). Masuzawa (1972) and Nitani (1972) summarised the characteristics of water masses in the western North Pacific, including Kuroshio waters.
THE KUROSHIO. PART I. PHYSICAL FEATURES
15
Fig 3. —Annual long-term mean map of the synoptic dynamic height (0/1000 db) in 10-1 dynamic metre (after Hasunuma & Yoshida, 1978). Broken lines indicate half values or, when a continuation of a solid line, they indicate insufficient data.
Figure 4 gives the T-S diagram of four stations in the Philippine Sea away from the Kuroshio. The warm surface water shows a large scatter because of the different atmospheric effects at each location. The subsurface salinity maximum water is believed to have been formed at the sea surface of the central North Pacific by both strong evaporation in winter and long residence time. This water is called the (North Pacific) Tropical Water whose maximum salinity, being slightly higher than 35.50‰, is lower than in any other ocean. The salinity minimum water is the (North Pacific) Intermediate Water. Reid (1965) and Hasunuma (1978) showed that the Intermediate Water is formed in winter at subsurface depths at the west in the Subarctic Gyre by vertical mixing. The Intermediate Water, although formed east of Japan, does not flow directly underneath the Kuroshio to the south of Japan. Instead, it roughly circulates clockwise so that the maximum salinity-minimum is found in the Kuroshio region due to mixing in the Central Pacific. The salinity-minimum layer also deepens to over 800 m south of the Kuroshio near Japan. Kawai (1979) showed that cyclonic
16
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 4. —T-S diagram in the Philippine Sea in the summer of 1965 and 1966. Inset shows positions where profiles were obtained.
rings south of the Kuroshio Extension sometimes can carry low salinity-minimum water to the Shikoku Basin through the gaps across the Izu-Osagawa Ridge. The nearly linear and uniform temperature—salinity curves between the Tropical Water and the Intermediate Water represent the Thermocline Water (Masuzawa, 1972). This water, with temperature range between 8 and 18°C, forms the main thermocline. The water between the surface thermocline and the subsurface permanent thermocline has a small vertical temperature gradient. The distribution of water volume against temperature for the central North Pacific shows a remarkable mode at 16°C (see Fig 11b of Masuzawa, 1972), which represents the thermostad layer mentioned above. This 16°C water corresponds to the 18°C water in the North Atlantic and is called by Masuzawa the (North Pacific) Subtropical Mode Water. The Subtropical Mode Water is formed at the sea surface of the northern portion of the Central North Pacific in winter. Water colder than 8°C shows the next largest scatter on the T-S diagram (Fig 4). Below 3°C the temperature-salinity curves converge to the (North Pacific) Deep and Bottom Water, which lies below about 2000 m. As is well known, the Pacific Deep and Bottom Water comes from the other oceans and has rather uniform properties. Water of the Northwest Pacific occupying depths greater than 3500 m are farthest from regions of ventilation and may be the oldest abyssal waters (Mantyla & Reid, 1983). The abyssal water enters the West Mariana Basin through a gap south of Guam. It then spreads northward to the Shikoku Basin and
THE KUROSHIO. PART I. PHYSICAL FEATURES
17
westward to the Philippine Basin through a gap in the Kyushu-Palau Ridge at about 20°N.
BEGINNING OF THE KUROSHIO The term “beginning of the Kuroshio” here takes on the usual meaning of referring to the current east of Luzon and Taiwan, although Nitani (1972) has used this term to include the Kuroshio in the East China Sea as well.
CURRENTS AND VOLUME TRANSPORT
Figure 5 shows the dynamic height distribution at the sea surface relative to 1200 db in the beginning of the Kuroshio in summer 1965. Bifurcation of the North Equatorial Current off the coast of southern Luzon is evident. As was shown in Figure 3 the average position of this current division is to the south off the coast of Samar. The Kuroshio moves northward along the Luzon coast, makes a slight
Fig 5. —Distribution of dynamic height (0/1200 db) in the beginning of the Kuroshio in summer 1965 (adopted from Nitani, 1972). Units are in 10-1 dynamic metre.
18
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 6. —Distribution of dynamic height east of Taiwan in February-March 1940 at 0/1200 db (left-hand side) and 800/1200 db (right-hand side) (after Guan, 1984a). Units are in 10-1 dynamic metre.
excursion into the Bashi Channel, flows north-northeast along the eastern coast of Taiwan and finally enters the East China Sea. There is a conspicuous warm eddy to the east of the Bashi Strait. This warm eddy seems to exist permanently, although its scale and position vary from time to time (Nitani, 1972). It is of interest to note that this warm eddy lies just south of the Sakishima Depression (see Fig 2), which blocks most of the Kuroshio Current below 500 m depth from entering the East China Sea. The blocking effects of the Sakishima Depression may have been responsible for the lower layer eddy east of Taiwan in winter 1940 (Fig 6). Similar features are often found in the flow structure east of Taiwan, e.g., in September 1965 and March 1966 (Zhou & Yuan, 1989). Geostrophic velocity sections across the Kuroshio off Luzon and Taiwan both show intensified northward currents next to the land boundary (Fig 7). The section off Luzon shows that the Kuroshio there has two northward bands. Data in this area for different years and seasons all showed similar features (see Fig 26 of Nitani, 1972). Nitani suggested that they are the continuation of the banded structure of the North Equatorial Current mentioned earlier. In the section east of Taiwan, the flow becomes simpler (Fig 7). The average width of the Kuroshio here is about 140 km (Chu, 1970). A countercurrent is often present near 124°E (Nitani, 1972; Zhou & Yuan, 1989). GEK observations (Nitani, 1972) indicate that the maximum velocity is about 2.0 knots off Luzon, 3.0 knots at Bashi Channel, and 3.0 knots or more east of Taiwan. The countercurrent associated with the warm eddy east of the Bashi Channel has a GEK velocity of 1.0–2.0 knots. Using 1200 db as the reference surface, Nitani (1972) estimated the volume transport of the Kuroshio and its countercurrent to be 28 and 9 million m 3·s -1 on the average, respectively, while the corresponding values east of central Taiwan are 40 and 12 million m3·s -1. The Kuroshio and its countercurrent have large average
THE KUROSHIO. PART I. PHYSICAL FEATURES
Fig 7. —Geostrophic velocity sections in 10-1 m·s-1 based on 1200 db surface (after Nitani, 1972). a, east of Luzon at 17.75°N in August 1965; b, east of Taiwan at 23°N in July 1966.
19
20
J.L.SU, B.X.GUAN AND J.Z.JIANG
transports in the Bashi Channel, being 47 and 15 million m 3 ·s -1 , respectively, because of the existence of the warm eddy mentioned earlier. Recently, Toole, Zou & Millard (1988) confined their attention to waters warmer than 12°C and deduced the net transport east of Luzon to be 25×10 6 m 3 ·s 1 from annual mean hydrographic sections and water mass budgets. Nitani (1972) tried different reference levels for the geostrophic transport estimation. He finds that, for the areas east of Luzon and Taiwan, the transport estimates are on the average 10% more if 1500 db, instead of 1200 db, surface is used as the reference level and 20% less if 800 db surface is used. The average total volume transport east of Taiwan computed from the results of Chu (1970), who used the 800 db reference surface, is around 19×10 6 m 3 ·s -1 . Chu’s data sets are different from those used by Nitani, but their estimates are compatible because Nitani’s result when converted to the 800 db reference surface would yield (4012)×0.8=22 million m 3·s -1.
TEMPERATURE AND SALINITY DISTRIBUTIONS
The horizontal temperature and salinity distributions at 200 m depth in the beginning of the Kuroshio in summer 1965 are shown in Figure 8. Both distributions have similar patterns as the surface dynamic topography (see Fig 5). A large horizontal temperature gradient is evident in the Kuroshio region. Nitani (1972) determined that the 18°C isotherm at 200 m is a good indicator of the main axis
Fig 8. —Distribution of temperature (a, intervals in 1°C) and salinity (b, intervals in 0.10‰) at 200-m depth in the beginning of the Kuroshio in summer 1965 (adopted from Nitani, 1972).
THE KUROSHIO. PART I. PHYSICAL FEATURES
21
Fig 9. —Temperature (a, °C) and salinity (b, ‰) sections across the Bashi Channel along 19.5°N in summer 1965 (after Nitani, 1972).
of the Kuroshio at the sea surface, i.e., the position of maximum surface current speed, in the regions from the Bashi Channel to the east of Taiwan. The elongated warm core east of the Bashi Channel is situated to the west of the southward part of the eddy current field (see Fig 5). Figure 9 shows the vertical temperature and salinity distributions across the Bashi Channel. The largest slope of the isotherms, corresponding to the Kuroshio, lies between 121°N and 123°N. The Subtropical Mode Water is discernible east of the Kuroshio as the 15–18°C water layer. The subsurface salinity maximum and lower layer salinity minimum are clearly seen in the salinity section. They slope up suddenly to the west from 123°E associated with the Kuroshio. Their core structures are due to mixing with upwelled water along the course of the Kuroshio. West of 121°E into the South China Sea both salinity-maximum and salinity-minimum values are significantly weakened, indicating that the Kuroshio does not intrude into the South China Sea. In winter the surface salinity is slightly higher than the summer value, but the surface temperature is lower by about 5°C (e.g., see Watts, 1972). There is no appreciable change below about 150 m depth. Along the east coast of Taiwan near 23°N upwelling phenomenon is often found (Tominaga, 1972; Bodvarsson, 1976; Hung, 1979). This phenomenon was first detected by a photograph taken from Satellite Gemini X in 1966, and upwelling is also evident just below the surface even during unfavourable
22
J.L.SU, B.X.GUAN AND J.Z.JIANG
winds (Hung, 1979). Interaction of the Kuroshio with an offshore shallow ridge south of 23°N seems to play an important role in the occurrence of upwelling there.
KUROSHIO AND CIRCULATION IN THE SOUTH CHINA SEA
Water exchange through the Bashi Channel As mentioned earlier, the Bashi Channel is traversed by three ridges. Seamounts and islands are found on the ridges, especially to the southern end. The sill depth is only around 2400 m, which effectively blocks abyssal waters from entering the South China Sea. Potential temperature-salinity analyses (Nitani, 1972; He & Guan, 1984) show that the bottom water of the South China Sea originates from the deep water (1500–2000m) of the Philippine Sea. Comparison of dissolved oxygen contents of the bottom water in different years suggests that it is being constantly renewed (He & Guan, 1984). Hydrographic data of the abyssal layer in the northern South China Sea showed the existence of a cyclonic gyre in winter, spring, and summer of 1985 (Wang, 1986). He estimated an in-flow of 0.7×10 6 m 3 ·s -1 abyssal water through the Bashi Channel to replenish the upward loss of abyssal water in the South China Sea Basin. An 82-day deep-sea moored current meter record (dates not given) by Liu & Liu (1988) shows a continuous westward current through the Luzon Trough of the Bashi Channel into the South China Sea. The current has a mean speed of 0.14 m·s -1 at the 2000–2700 db layer. In addition to the excursion pattern (see Fig 5) the Kuroshio sometimes loops clockwise around the northeastern part of the South China Sea (Fig 10). Probably because of the many islands north of Luzon, in the looping pattern the Kuroshio usually goes into the South China Sea above 20°N and re-enters the Pacific Ocean near the southern tip of Taiwan. This flow pattern is in a certain way similar to the Loop Current in the Gulf of Mexico. Unlike the Loop Current, however, no shedding of this Kuroshio loop has ever been reported. Numerical studies by Hurlburt & Thompson (1980) indicate that shedding of the Loop Current depends on the smallness of the beta Rossby number which is inversely proportional to the square of the inlet-outlet separation distance. The South China Sea has different topographic features from those of the Gulf of Mexico, especially in the inletoutlet region. If the stability criterion of Hurlburt & Thompson is nevertheless applied to the South China Sea, we find the inlet-outlet distance here too short to result in a pinch-off of the loop. The looping pattern of the Kuroshio seems to be inherent to its own dynamics. Its occurrence can be found during either of the two monsoon periods (Chu, 1972; Nitani, 1972; Wang & Chern, 1987). A cold eddy is always present northwest of Luzon (Figs 5 and 10) and it is stronger when the Kuroshio takes on the looping pattern. So far there is no reliable estimate of the exchange of water volume across the channel. It is, however, generally believed that during the northwest monsoon (November to March) a net surface flow is driven into the South China Sea and during the southwest monsoon (May to September) a net outflow (Wyrtki, 1961). Consequently, surface salinity in the northern South China Sea is close to the Kuroshio water in the winter monsoon but is lower than the Kuroshio in the summer monsoon because of large run-off from lands surrounding the sea.
THE KUROSHIO. PART I. PHYSICAL FEATURES
23
Fig 10. —Distribution of dynamic height (0/1200 db) near the Bashi Channel in summer 1966 (adopted from Nitani, 1972). Units are in 10-1 dynamic metre. Heavy lines indicate 5 unit intervals, thin lines indicate 1 unit intervals.
South China Sea warm current and Kuroshio ‘branches’ in the South China Sea Figure 11 is a temperature section in the northern South China Sea in January 1985. The location of this section is indicated on the bathymetric chart (Fig 12). Figure 13 shows the surface dynamic topography referred to 500 db during the same observation. The Helland-Hansen method (Defant, 1961) was used in computing the dynamic heights over the shelf. A northeastward current is seen to be present near the shelf-break and further offshore a southwestward current is evident. In summer the flow pattern is more complicated. The northeastward current is, however, still evident near the shelfbreak region and the southwestward current, now narrower in width, seems to originate from a more easterly direction upstream (Anonymous, 1985a). The constant northeastward current near the shelf-break of the South China Sea was named by Guan (1978) the South China Sea Warm Current because of its warm characteristics in winter. Existence of this current has also been supported
24
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 11. —Temperature (°C) section in the northern South China Sea in January 1982 (after Anonymous, 1985a). Section location is shown by broken line in Figure 12.
by many 25-h anchored measurements, as well as a few short-time moored current meter records (e.g., see Anonymous, 1985a). The maximum 25-h average current speed reaches close to 0.8 m·s -1, while the highest geostrophic velocity computed is 1.7 m·s -1 . Numerical results of a barographic model by Su & Wang (1987) suggest that meridional surface elevation gradient induced by the Kuroshio is partly responsible for driving this continental slope-trapped current northward. The South China Sea Warm Current is guided by the continental slope into the Taiwan Strait through a submarine canyon close to the west coast of Taiwan (Fig 12). Long-time moored current meter measurements 20 m above bottom at 100m depth of water inside the submarine canyon in 1984 (Chuang, 1986a) show a continuous northward current during either the winter or the summer monsoon. Mean speeds measured during the winter and the summer monsoon were, respectively, 0.18 and 0.32 m·s -1. Another study by Chuang (1985), based on earlier winter monsoon measurements at the same location, estimated that a negative meridional surface elevation gradient with a magnitude around 2×10 -7 is needed to drive this current against both the wind stress and bottom friction. Chuang’s estimate of the meridional surface elevation gradient agrees, in order of magnitude, with the diagnostic results of Yuan, Su & Xia (1987) for the East
THE KUROSHIO. PART I. PHYSICAL FEATURES
25
Fig 12. —Bathymetric chart of the northern South China Sea. Contours are in metres. Broken line indicates the location of the temperature section in Figure 11.
China Sea. As was pointed out by Su & Pu (1987), the participation of the Kuroshio in the year-round, large-scale shelf circulation is one of the outstanding features that distinguish it from the Gulf Stream. The south westward current offshore of the South China Sea Warm Current was named by Anonymous (1985a) as the South China Sea Branch of the Kuroshio. There are few direct measurements of this current and the maximum computed geostrophic velocity is around 1.5 m·s -1 . Based on both their own observed and historical hydrographic data Anonymous (1985a) estimated the volume transport of this southwestward current to vary between 4 to 8 million m 3·s -1 . This current, if it is a continuous feature, does not, however, seem to be a direct branch of the Kuroshio. Su & Wang’s barotropic model (1987) suggests that the Kuroshio only makes a slight excursion into the Bashi Channel. The model also predicts that the Kuroshio induces a cyclonic gyre inside the South China Sea. This gyre’s western segment consists of intensified southwestward currents, lying offshore of the continental slope. We have also employed a reduced gravity model to study the effects of the Kuroshio on the circulation in the South China Sea. The results (in preparation) also support the conclusions of the barotropic model. Analyses of the summer temperature-salinity diagrams of waters in the sea near the southern tip of Taiwan show that waters on both sides have distinct characteristics, at least in the top 150 m layer (Fan & Yu, 1981). The same study also finds no such clear distinction between the two groups of TS-diagrams in either winter or spring because the prevailing northeasterly winds result in a net surface flow from the Pacific into the South China Sea. Being less controlled by topography than the South China Sea Warm Current, this southwestward current probably has a more variable path than that
26
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 13. —Distribution of dynamic height (0/500 db) in the northern South China Sea in December 1981-January 1982 (after Anonymous, 1985a). Units are in 10-1 dynamic metre and intervals are 0.5 units.
of the South China Sea Warm Current. For example, a 97-day moored current meter record taken on the continental slope near (22.3°N:119°E) in 1986 shows that the current direction was steady towards SW-WSW for a 48-day period but variable during the rest of the measurement period (Chuang, 1986b). There have been suggestions that a small part of the Kuroshio branches out at the Bashi Channel and proceeds northward along the western side of Taiwan (e.g., Niino & Emery, 1961; Guan, 1988). These are based primarily on ship-drift records, which are susceptible to wind-drift effects. Available hydrographic observations offshore of southwest Taiwan during either summer (Fan & Yu, 1981) or winter (Tseng, 1970, 1972) do not, however, support such a conjecture. Numerical model results (Su & Wang, 1987) also do not show such a branching phenomenon.
KUROSHIO IN THE EAST CHINA SEA A large area of the East China Sea is part of a broad shallow epicontinental sea (Fig 14) which includes the semi-enclosed Yellow Sea to the north. It is connected with the Japan Sea to the northeast through the Korea Strait and with the South China Sea to the south through the Taiwan Strait.
CURRENTS AND VOLUME TRANSPORT
THE KUROSHIO. PART I. PHYSICAL FEATURES
27
Fig 14. —Bathymetric chart of the East China Sea. Contours are in metres. Heavy broken lines denote hydrographic sections referred to in the text.
As explained earlier, the Kuroshio enters the East China Sea over the Sakishima Depression and re-enters the Pacific through the Tokara Strait. Around 24°N south of the Sakishima Depression the centre of the Kuroshio approaches very close to the coast of Taiwan (Chu, 1976). As the Kuroshio crosses the ridge potential-vorticity conservation effects cause the Kuroshio to veer to the right. This tendency was confirmed by a 78-day moored current meter measurement over the ridge between October and December 1975 (Chern, 1983). Once inside the East China Sea the Kuroshio follows the continental slope northeastward until around 29.5°N when it gradually leaves the slope (Fig. 15). The bulk of
28
J.L.SU, B.X.GUAN AND J.Z.JIANG
the Kuroshio then flows east or east-southeast and re-enters the Pacific through the northern half of the Tokara Strait. Part of the Kuroshio, however, frequently returns to the Pacific through the Osumi Strait which is situated immediately north of the Tokara Strait. The Osumi Current seems to fluctuate with periods of several tens of days, but the nature of the fluctuations is very changeable from year to year (Nagata & Takeshita, 1985). North of the Sakishima Depression countercurrents are sometimes found east of 123°E (Chu, 1976). These currents seem to be part of an often-found anticyclonic eddy (Figs 15 and 16) induced
Fig 15. —Surface currents in the East China Sea from GEK observations in summer 1966 (data taken from the Results of the Marine Meteorological and Oceanographic Observations, No. 40, Nagasaki Marine Observatory). Dotted lines, depth in m.
THE KUROSHIO. PART I. PHYSICAL FEATURES
29
Fig 16. —Surface currents northeast of Taiwan from GEK observations in January 1968 (data taken from the Results of the Marine Meteorological and Oceanographic Observations, No. 50, Nagasaki Marine Observatory). Dotted lines, depth in m.
by the veering back of the Kuroshio to the left, due to the same effects as mentioned above. The geostrophic velocity distribution across Section PN (Fig 14) is shown in Figure 17. Like the section east of Taiwan (Fig 7b, p. 19), it shows the Kuroshio with width of about 150 km close to the continental slope and a weaker countercurrent to the east of the main current. The velocity structure in Figure 17 looks more complicated than that in Figure 7b because the stations in Figure 17 are more closely spaced. Section PN is a constantly monitored section. Guan (1980) computed the mean surface velocity normal to this section (Fig 18), using GEK observations from 54 transects between 1956 and 1975. The maximum of this mean surface velocity is located on the continental slope and the weak countercurrent lies over the southwest slope of the Okinawa Trough. Guan also found that the width of the core of the Kuroshio, in which the current speed is greater than 0.4 m·s -1, varies between 70 and 110 km. GEK observations indicate that the maximum surface velocity reaches over 3.5 knots both in the area north of the Sakishima Depression and along Section PN and over 2 knots in the countercurrent (Guan, 1988).
30
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 17. —Geostrophic velocity section in 10-1 m·s-1 based on 800 db surface along Section PN in April, 1978 (after Nagata, 1981).
Fig 18. —Distribution of the mean surface velocity normal to Section PN compared with submarine topography (after Guan, 1980).
THE KUROSHIO. PART I. PHYSICAL FEATURES
31
TABLE I Statistics of the volume transport of the Kuroshio based on transect data from 1954 to 1984 (after Saiki, 1985). S.D., standard deviation; N.T., number of transects used; 700 db surface is referred for the volume transport through Section PN and 1000 db for the other three sections
Saiki (1985) computed the annual and seasonal mean values and standard deviations of the volume transport through Section PN referred to 700 db (Table I). His data are from 93 transects between 1955 and 1984. The annual mean volume transport is 21.4×10 6 m 3·s -1 and the corresponding standard deviation is 4.9×106 m3·s -1. The maximum and minimum volume transports through this section are found to be over 34 and under 7 million m3·s -1, respectively. Earlier, using data between 1956 and 1975, Guan estimated that the annual mean and the standard deviation of the volume transport through this section were 21.3 and 5.4 million m 3 ·s -1 , respectively (see Guan, 1988), while estimates based on observations between 1972 and 1981 were 25.5 and 2.65 million m3·s -1 (Fujiwara, Hanzawa, Eguchi & Hirano, 1987). The last two estimates were also referred to 700 db. Considering the difference of data sets, method of computing dynamic heights in water shallower than 700 db and interpolation technique used by these studies, the three sets of estimates are quite compatible with one another. All these estimates show that the autumn mean transport is noticeably lower than the other seasonal means. Short-
32
J.L.SU, B.X.GUAN AND J.Z.JIANG
term variation of the volume transport through Section PN has also been studied (Fujiwara et al., 1987). They found the transport to be 26.1, 24.4, and 23.3 million m3·s -1 on 5–6, 12–13, and 17–18 October 1981, respectively. Gaun (1988) also discussed the moored current meter measurement results of Yamashiro & Ichiwara in June-October 1984 at an area near Section PN with a 1060-m water depth. The 100-day record at a depth of about 600 m showed a steady northeasterly, i.e., approximately parallel to the isobath lines, current with an average speed around 0.24 m·s -1 . The 89-day record at a depth close to 1000 m also showed a stable north-northeasterly flow with an average speed of 0.04 m·s -1 . Recently, another long-time current measurement was made from October 1987 to February 1988 about 60 km northeast of Section PN in an area on the continental slope with a 900-m depth (S. Ishii, pers. comm.). The 131day current record at a depth around 580 m and showed fluctuations with a small mean of 0.014 m·s -1 to the south-southwest. Thus the use of 700 db reference surface in arriving at the estimates discussed above seems to be a reasonable choice.
TEMPERATURE AND SALINITY DISTRIBUTIONS
The horizontal temperature and salinity distributions at 100-m depth of the Kuroshio in the East China Sea in summer 1987 are shown in Figure 19. A large horizontal temperature gradient, i.e., the Kuroshio front, is found near the shelfbreak south of 29.5°N, whence the high gradient zone moves away from the shelf-break area and turns sharply eastward. The anticyclonic eddy to the right of the Kuroshio after it enters the East China Sea and the countercurrent through Section PN are related, respectively, to the southern two warm centres in the Okinawa Trough. Near the southern part of the Tokara Strait there is another warm centre which is related to a surface anticyclonic eddy often found there. Over the shelf there are two conspicuous cold areas. The one north of Taiwan is related to the upwelling of subsurface water from the Kuroshio (see p. 38 ) and the one to the north is related to a remnant cold water pool formed in winter. Nitani (1972) suggested that in the East China Sea the 18°C isotherm at 200-m depth can also be used as an indicator of the axis of Kuroshio, i.e., the position of the maximum surface current speed. This is probably only valid when the Kuroshio axis is over the deeper part of the continental slope but not when the Kuroshio axis is close to the shelf-break as in summer 1987 (Figs 19 and 20). The vertical temperature and salinity distributions across Section A (see Fig 14) are shown in Figure 21. Both the largest slope of the isotherms and the largest slope of the isohalines are found on the continental slope. The Subtropical Mode Water is clearly seen extending from the Pacific Ocean to the East China Sea as the 16 to 19°C water layer. The 16 to 19°C water loses its thermostad characteristics as the isotherms approach the continental slope. It merges into the Kuroshio Subsurface Water, part of which is uplifted onto the East China Sea shelf northeast of Taiwan (see p. 38 ). Below about 900 m the temperature in the Okinawa Trough is higher than that of the Pacific Ocean at the same depth. The difference increases downward, reaching around 1.5°C at the bottom of the Trough. On the other hand, salinity in the deep layer of the Trough is lower than that of the Pacific Water at the same level. Both features can probably be attributed to the renewal of bottom
Fig 19. —Distribution of temperature (a, intervals 1°C) and salinity (b, intervals 0.05‰) at 100-m depth in the East China Sea in summer, 1987 (adopted from the Oceanographic Atlas, 1989). Dotted line is 200 m isobath.
THE KUROSHIO. PART I. PHYSICAL FEATURES 33
34
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 20. —Distribution of temperature (in 1°C intervals) at 200-m depth in the East China Sea in summer 1987 (adopted from the Oceanographic Atlas, 1989). Dotted line is 200 m isobath.
water in the Trough by the Pacific Water over the northern two depressions of the Ryukyu Ridge which have sill depths around 1000 m. Both the salinitymaximum and salinity-minimum layers slope upwards towards the shelf, the latter being more pronounced just as the isotherms at the same level. Both salinity-maximum and salinity-minimum values are weaker than those of the Pacific Water. This is probably due to strong mixing when the Kuroshio enters the East China Sea over the shallow Sakishima Depression. Because of the influence of the shelf water there are large changes in the surface water characteristics of the Kuroshio in the East China Sea. Yang (1984) analysed hydrographic data taken at 1302 stations with water depths over 200 m. The surface temperature has a range 15 to 31°C and its seasonal mean is highest in summer, followed by autumn, spring, and winter, in that order. The surface salinity varies between 34.00 and 34.50‰; its seasonal means are in the opposite order to that of the seasonal means of the surface temperature. At the entrance into the East China Sea the average temperature of the Kuroshio ranges from 28.7 to 23.3°C at the sea surface and from 22.8 to 20.7°C at 100 m, the maximum in
THE KUROSHIO. PART I. PHYSICAL FEATURES
35
Fig 21. —Distribution of temperature (a, °C) and salinity (b, ‰) across Section A in summer, 1965 (after Nitani, 1972). Location of Section is shown in Figure 14.
September and the minimum in March, and indicates no regular annual variation at 200 m (Masuzawa, 1972). Like the Florida Current in the South Atlantic Bight, frontal eddies are often found along the Kuroshio front in the East China Sea. From the records of an array of three current meters moored on the shelf in winter 1975, Trump & Burt (1981)
36
J.L.SU, B.X.GUAN AND J.Z.JIANG
inferred the presence of quasi-sinusoidal meanders in the mean flow. Hydrographic studies of Kuroshio frontal eddies was conducted by Shibata & Eguchi (1985) in May and October of 1982. They also reviewed previous satellite imagery studies of this phenomenon and noted that the Kuroshio frontal eddies are often found downstream of two bumps of the continental slope at latitudes of about 28°N and 29°N, respectively. After the main stream of the Kuroshio leaves the continental slope north of 29.5°N, the filament of a frontal eddy sometimes will be greatly extended because the tip of the filament is still trapped in the shelf-break region. Such filament development processes have been observed from two series of satellite imageries in March 1986 and April 1988, respectively (Guo, Xiu, Ishii & Nakamura, in press). Guo et al. suggest that this mechanism is likely to be responsible for the warm plumes of Kuroshio water often found west of Kyushu in winter and spring (Huh, 1982).
KUROSHIO AND CIRCULATION IN THE EAST CHINA SEA
Even in winter, when the northerly wind is very strong, there are always strong northward currents over the shelves in the China Seas. The South China Sea Warm Current already discussed is one example. In the East China Sea they are the Taiwan Warm Current, Yellow Sea Warm Current, and the Tsushima Current (Fig 22). Involvement of the Kuroshio Water in the formation of these currents makes them warmer than the colder coastal currents in winter. In the South Atlantic Bight the Gulf Stream, i.e., the Florida Current, also participates in local shelf circulations (Atkinson, Lee, Blanton & Paffenhöffer, 1987; Oey, Atkinson & Blanton, 1987). Unlike the continuous shelf currents induced by the Kuroshio in the East China Sea, shelf circulations generated by the Florida Current in the South Atlantic Bight are, however, of episodic nature, probably due to the narrower shelf there.
Taiwan Warm Current The oceanography of the western East China Sea is dominated by the influence of the Taiwan Warm Current which flows to the north year-round between about 50 to 100 m isotherms. Even in winter when the north wind is quite strong, northeasterly currents with half a knot speed have been measured just below the surface (Su & Pan, 1987) and the high temperature and high salinity characteristics of this warm current can be distinguished off the Changjiang River mouth (Wang, Su & Dong, 1983). The origin of this current has attracted much attention from Chinese and Japanese oceanographers. Part of the surface water of the Taiwan Warm Current seems to have originated from the Taiwan Strait (Weng & Wang, 1984; Guo, Lin & Song, 1985; Su & Pan, 1987), which is likely to be traced back to the South China Sea Warm Current (Guan, 1984b). The Kuroshio, through shelf intrusion northeast of Taiwan, is, however, responsible for all the lower layer, as well as part of the surface layer, water of the Taiwan Warm Current (Fukase, 1975; Sawara & Hanzawa, 1979; Weng & Wang, 1984; Guo et al., 1985; Su& Pan, 1987).
THE KUROSHIO. PART I. PHYSICAL FEATURES
37
Fig 22. —Schematic picture of the Kuroshio and its branches in the China Seas: 1, Kuroshio; 2, South China Sea Warm Current; 3, Taiwan Warm Current; 4, Yellow Sea Warm Current; 5, Tsushima Current.
The winter hydrographic distribution north of Taiwan (Figs 23b and 24b) shows that the upper layer of the Kuroshio intrudes right onto the shelf. Most of this intruded water returns to the shelf-break region downstream around 27°N (see also Fig 16). The rest spreads northward over the shelf east of the southerly coastal current which is located west of about the 50-m isobath. Moored current meter records (Su & Pan, 1987) and many 25-h anchored station measurements (Guan, 1984b) support this description of the circulation pattern. The numerical results of a barotropic model also yield similar flow features (Wang & Su, 1987). The model demonstrates that both topographic and beta effects contribute to the intensified
Fig 23. —Distribution of temperature (°C) and salinity (‰) at 75-m depth north of Taiwan in (a) summer 1984 and (b) winter 1984–1985 (after Su & Pan, 1987). Broken lines are salinity; dotted line is 200 m isobath.
38 J.L.SU, B.X.GUAN AND J.Z.JIANG
THE KUROSHIO. PART I. PHYSICAL FEATURES
39
northward currents close to the coast, i.e., east of the coastal current. Su & Pan’s asymptotic solution of a barotropic model after Csanady (1979) suggests that the loss of the Taiwan coast to support the surface elevation gradient of the Kuroshio as it enters the East China Sea is one major factor responsible for the shelfintrusion of the Kuroshio north of Taiwan. The summer hydrography north of Taiwan assumes a different and complicated distribution (Fig 23a). The temperature distribution across Section B (Fig 24a) resembles that of a frontal eddy (Lee, Atkinson & Legeckis, 1981). While frontal eddies are travelling disturbances which propagate down the front of a western boundary current, this feature north of Taiwan has always been found to be present in hydrographic observations between late spring and earlier autumn (Su & Pan, in press). Furthermore, no evidence of downstream propagation of this feature has ever been reported. The baroclinic model proposed by Su & Pan (1987) offers the following dynamical explanation. In summer the shelf water is slightly less dense than the surface water of the Kuroshio, which makes it impossible for the surface water of the Kuroshio to intrude onto the shelf to release the unbalanced surface elevation gradient as in winter. Instead, the ‘frontal eddy’ system, maintained by upwelled Kuroshio Subsurface Water, supports most of the unbalanced gradient. Some surface water of the Kuroshio goes around the cold eddy and contributes to part of the upper layer water of the Taiwan Warm Current. Coastal upwelling induced both by the Taiwan Warm Current itself and by the prevailing southerly winds is found in summer at many places along the left flank of the Current (Su & Pan, 1987; Yuan, Su & Xia, 1987). Temperature distribution in the lower layer of Figure 24a shows such a trend near the coast. Most of the bottom water on the East China Sea shelf originates from the Kuroshio Subsurface Water. Upwelling onto the shelf of this subsurface water along the Kuroshio front does not, however, seem to happen often north of 25.5°N (Sawara & Hanzawa, 1979; Miao, Su & Yu, 1987). Instead, most of the upwelling is likely to take place at two areas (Su & Pan, in press). One area is near the northeastern coast of Taiwan next to the Sakishima Depression. Current meter records north of Taiwan ranging from a half to over one month between 1980 and 1981 show constant northwesterly currents at middle and near-bottom depths with average speeds often greater than half a knot at mid-depth (Guo et al., 1985). Kuroshio Subsurface Water upwelled here seems to spread over the shelf about the 100-m isobath (Figs 23 and 24). The other area is near Section B where the shelf-break turns sharply towards east-northeast (Fig 14, p. 27). Moored current meter measurements conducted here for 25 days in early summer 1986 (Yuan & Su, 1989) showed a steady on-shelf current at both the middle and near-bottom depths with average speeds of 0.26 and 0.16 m·s -1 , respectively. Kuroshio Subsurface Water upwelled here seems to spread along the shelf-break region (Figs 23 and 24). Tsushima Current A major hydrographic feature in the Japan Sea is the Tsushima Current which enters the Japan Sea through Korea Strait. The Tsushima Current carries warm water of high salinity into the cold and less saline Japan Sea comparable, on a small scale, to the branch of the North Atlantic Current which flows into the Arctic
Fig 24. —Distribution of temperature (°C) and salinity (‰) across Section B in (a) summer 1984 and (b) winter 1984–1985 (after Su & Pan. 1987). Location of Section is shown in Figure 14. Broken lines are salinity.
40 J.L.SU, B.X.GUAN AND J.Z.JIANG
THE KUROSHIO. PART I. PHYSICAL FEATURES
41
Mediterranean (Sverdrup, Johnson & Fleming, 1942). In the past it had been generally believed that the Tsushima Current branches out from the Kuroshio southwest of Kyushu (e.g., Moriyasu, 1972). The mean current vector chart determined from GEK data collected between 1953 and 1977 shows, however, a general southward flow west of Kyushu except in spring when weak northerly flows below 0.4 knots are found (Ichiye, 1984). Hydrographic analyses by Lim (1971) and Sawara & Hanzawa (1979) suggest that the Tsushima Current should be regarded rather as originating from the mixture of Kuroshio and coastal waters. Numerical results demonstrate that barotropic dynamics are conducive to such a flow description (Wang & Su, 1987). In the past few years moored current meter records with duration ranging from 6 to 30 days have been obtained over the East China Sea shelf west of Kyushu in areas with water depth around 200 m (Song, Lin & Guo, in press). The residual currents near the bottom have large fluctuations compared with their means. At mid-depths they flow steadily northward in spring and summer, but in winter they fluctuate with periods around 4 days, apparently in response to wind events. By analysing satellite imageries Huh (1982) and Muneyama et al. (1984) proposed that, in winter, plumes or eddies of warm water detached from the Kuroshio provide one important source for the Tsushima Current Water. As mentioned earlier, using satellite imageries from consecutive days, Guo et al. (in press) suggest that these plumes or eddies are more probably due to stretched filaments of frontal eddies. The Tsushima Current has been intensely studied near the Korea Strait by both the Japanese and Korean oceanographers. Thus, its volume transport characteristics are better understood than the other Kuroshio ‘branches’. Yi (1966) estimated that the average transport is 1.3×10 6 m 3·s -1 with an annual variation of 2.0×10 6 m 3·s -1, minimum in February through April and maximum in July through November. The ratio of the transports between the west channel and the east channel of the Korea Strait is 3 to 1. These estimates are based on geostrophic computations referred to the 125 db surface. Using massive direct current measurements with duration each longer than 24 h in summer of 1942 and 1943, Miita estimated (Ichiye, 1984; Miita & Ogawa, 1984) that the transport through the west and east channel were 1.8 and 1.7 million m 3·s -1, respectively (Fig 25). Apparently, there is a significant barotropic component in the flow field. This was confirmed by Miita & Ogawa (1984) via a comparison between the Eulerian measurement and the dynamic computation of the speed distribution across the northeasternmost section in the Korea Strait. There seems to be large short-term variation in the Tsushima Current transport. Using the 150 db surface as the reference level, Shim, Wiseman, Huh & Chuang (1984) estimated the transport through the west channel of the Korea Strait to be 0.89, 1.37, and 1.60 million m 3 ·s -1 on 15, 16, and 21 October 1972, respectively. Yellow Sea Warm Current The winter distribution of surface temperature and salinity in the northern East China Sea (Fig 26) suggests that a mixture of the Kuroshio Water and shelf water intrudes northward into the Yellow Sea from the west of Kyushu. This is known as the Yellow Sea Warm Current which penetrates all the way up to the mouth of the Bohai Sea north of the Yellow Sea. This warm current is believed to be responsible
42
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 25. —Volume transport through sections in the Korea Strait in summer (after Miita & Ogawa, 1984). Units are in 106 m3·s-1. Clear arrow indicates a current reversal.
for some of the Chinese ports in the northern Yellow Sea being ice-free in winter. In summer the remnant winter water of the Yellow Sea Warm Current forms a large cold water pool in the Yellow Sea at depths below about 40 m (e.g., see Zhao, 1987). Thus, the Yellow Sea Warm Current has great influence on the hydrographic structure of the Yellow Sea throughout the year. In conformance with the original proposition that the Tsushima Current may be a direct branch of the Kuroshio, Uda (1934) suggested that the Yellow Sea Warm Current was a branch of the Tsushima Current. Furthermore, the same northward penetration was believed to be representative of the Yellow Sea circulation even in summer (Uda, 1934; Niino & Emery, 1961). Noting the semi-enclosed nature of the basin of the Bohai Sea and Yellow Sea, Yuan, Su & Zhao (1982), however, showed with a steady-state barotropic numerical model that in winter northward currents originating from the northeast East China Sea are driven by northerly winds through the deep trough of the Yellow Sea just as they would be in a lake. Because winds in winter have frequencies ranging mostly from 3 to 10 days, an unsteady barotropic numerical model by Hsueh, Romea & DeWitt (1986) found that the northward flow is particularly noticeable during relaxation when the north wind abates. Therefore, it seems more appropriate to regard both the Tsushima Current and Yellow Sea Warm Current as having originated in the same shelf sea west of Kyushu, at least in winter.
THE KUROSHIO. PART I. PHYSICAL FEATURES
43
Fig 26. —Distributions of surface temperature (a, °C) and salinity (b, ‰) in the northern East China Sea and southern Yellow Sea in winter 1987 (adopted from the Oceanographic Atlas, 1989). Dotted line is 200 m isobath. Results of a two-layer numerical model suggest that in summer the Yellow Sea Warm Current is weakened in strength and it intrudes not much further north beyond the Cheju Island (Yuan & Su, 1983). Hydrographic analyses by Park (1986) and Zhao, Xiong & Zhang (1987) support this proposition. Diagnostic results (Yuan, Su & Xia, 1986) indicate that in summer, guided by the topography, the Taiwan Warm Current seems to provide part of the water for the Yellow Sea Warm Current.
KUROSHIO SOUTH OF JAPAN The Kuroshio south of Japan is very closely associated with the lives of the Japanese. Because of its great influence on climate, fisheries and other maritime
44
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 27. —Bathymetric chart of region south of Japan. Contours are in metres. Heavy broken lines denote hydrographic sections referred to in the text.
activities in the vicinity of Japan, scientific observations of this area have been maintained by various Japanese governmental agencies. Compared with both the upstream and the downstream part of the Kuroshio system, the Kuroshio south of Japan is more intensely observed and more thoroughly studied. The topography south of Japan is marked by narrow continental shelves, ranging from a few to tens of kilometres (Fig 27). The narrowest shelf lies off Cape Shionomisaki at the southern tip of the Kii Peninsula. The deeper part of the continental slope does not follow closely the change of the coastline. At about 34.5°N south of the Izu Peninsula the continental slope meets the Izu-Ogasawara Ridge. Except for a narrow channel deeper than 1 km at 34°N, the ridge is a shallow and broad rise north of 32.5°N. The ridge deepens gradually to the south so that at 30°N the minimum depth of the ridge is greater than 2 km. In between there are isolated elevations with depths shallower than 1 km and two east-west passages with sill depths greater than 1 km centred at 32°N and 30.5°N, respectively.
PATH PATTERNS, CURRENTS AND VOLUME TRANSPORT
The Kuroshio south of Japan does not always flow close to the continental slope. Its path exhibits conspicuous variability especially east of Shionomisaki, which has been classified by Nitani (1969) into five typical patterns (Fig 28). The Ntype pattern is a straight path which follows the Japan coast and goes through the
THE KUROSHIO. PART I. PHYSICAL FEATURES
45
Fig 28. —Schematic diagram of the five typical flow patterns of the Kuroshio near the Izu-Ogasawara Ridge (after Anonymous, 1985b). For designation of A, B, etc. see text, pp. 44–45.
channel on the Izu-Ogasawara Ridge near 34°N. The A-type meander makes a detour around a stable large cold eddy southeast of Shionomisaki and usually crosses over the ridge north of the channel at 34°N. The B-type meander is similar to the A-type except that the cold eddy is relatively small. The C-type meander straddles over the ridge and the D-type meander has its cold eddy to the east of the Izu-Ogasawara. The large meander of A-type path is of a quasi-stationary nature which lasts for 2–10 years, whereas the other four types are non-stationary patterns (Anonymous, 1985b). In the period of non-stationary pattern, the types change in order of N?B?C?D?N?…, two to three times a year with a probability of about 70%. Detailed analysis by Ishii, Michida & Kosugi (see Yoon & Yasuda, 1987) found that the A and N-type paths occupied 35.9% and 23.6% of the 1955–1984 period, respectively. The average lifetimes of the A and N-type paths during this period were 12.7 and 2.6 months, respectively, while those of other type of paths were about one month. The existence of a large stable meander path mode south of Japan is one of the outstanding features that distinguish the Kuroshio from the Gulf Stream. Figure 29 shows the dynamic height distributions at the sea surface relative to 1000 db in the sea south of Japan of an A-type pattern (winter 1979) and an N-type pattern (autumn 1980). It is readily seen that both path patterns conform to the general descriptions given above. In the straight path pattern the Kuroshio Countercurrent mentioned on p. 14 can be clearly seen as the southern segment of an elongated anticyclonic gyre (Fig 29b). In the meander pattern this gyre seems to have moved to the west with a smaller scope but stronger intensity (Fig 29a). Geostrophic velocity sections across the Kuroshio along Section KG (Fig 27) in summer 1980 and spring 1982 are shown in Figure 30. In the straight path pattern
Fig 29. —Distribution of dynamic height (0/1000 db) in the sea south of Japan in (a) winter 1979 (after Oceanographic Atlas of KER, 1980) and (b) summer 1980 (after Oceanographic Atlas of KER, 1983). Units are in 10-1 dynamic metres.
46 J.L.SU, B.X.GUAN AND J.Z.JIANG
THE KUROSHIO. PART I. PHYSICAL FEATURES
47
(Figs 29b and 30a) the Kuroshio flows over the continental slope with a width about 300 km and the Kuroshio Countercurrent is evident to the south. The section shown in Figure 30b corresponds to another A-type meander occurrence (see Fig 34, p. 52 ). It is seen that now countercurrents, i.e., the northern part of the stable large cold eddy, occupy the nearshore region along Section KG and the Kuroshio has moved off the continental slope to over the abyssal plain. Deep-sea current measurements with periods ranging from six months to a year between 1981 and 1985 showed a steady eastward abyssal flow with a vertical extent of about 2000 m above the sea floor (Fukasawa, Teramoto & Taira, 1986). The moorings were placed at the north and northwest peripheries of the Shikoku Basin and the mean current speeds ranged between 0.05 to 0.1 m·s -1 . The geostrophic velocity sections in Figure 30 are in general agreement with these measured results. When the Kuroshio flows over the continental slope a weak countercurrent seems to develop under the Kuroshio (Fig 30a). Lagrangian measurements with neutrally buoyant floats off Shikoku by Worthington & Kawai (1972) showed the same results. Deep-current meter observations by Taft (1978) at stations off Kyushu, Shikoku, and Kii Peninsula of various record lengths between July and September 1971 also yielded similar characteristics of the mean currents. Taft’s measurements
Fig 30. —Geostrophic velocity sections in 10-1 m·s -1, based on inverse method, along Section KG in (a) summer 1980 and (b) spring 1982 (after Pan, 1989).
48
J.L.SU, B.X.GUAN AND J.Z.JIANG
also indicated the existence of significant current fluctuations with a dominant period of about 20 days. GEK observations south of Japan indicated that the maximum velocity reached about 5 knots (Taft, 1972). Using the GEK data south of Japan between March 1956 and November 1964 Taft (1972) computed the mean of the axial surface current speed, i.e., the maximum surface speed across each transect, for both the period when a stable large meander was present (July 1959 to November 1962) and the rest of the period when the large meander was absent (Fig 31). Both means show a maximum at the 137°E longitude, the maximum for the mean with meander absent being higher than the other. Furthermore, west of 137°E the meander-absent mean is in general lower than the meander-present mean, whereas the opposite is true east of 137°E. Table I (see p. 31 ) gives the statistics of the volume transport through three sections south of Japan (see Fig 27, p. 44 ), Section KD crosses the Kuroshio immediately after it leaves the East China Sea, Section KF runs along 135.33°E where the Kuroshio usually starts to leave the continental slope during the large meander mode, and Section KG cuts across the cold eddy along 137°E when the large meander is present. It is seen that the mean transport of the Kuroshio in the south of Japan increases dramatically over its value in the East China Sea. The choice of 1000 db reference surface probably results in under-estimating the transport as Figure 30 seems to imply, although long-period multi-level current measurements in the top 1000 m south of Kyushu indicate a reversal of flow direction around 600 m depth (Takematsu et al., 1986). Part of the reason for the increase of the Kuroshio transport south of Japan is no doubt due to the recirculation of the Kuroshio Countercurrent through the anticyclonic gyre (Fig 29). Another possible cause is the merging of the Kuroshio from the East China Sea with northeasterly currents east of the Ryukyu Islands (Konaga, Nishiyama, Ishizaki & Hanzawa, 1980; Yuan, Endoh & Ishizaki, in press).
Fig 31. —Longitudinal distribution of axial GEK surface speed of the Kuroshio (after Taft, 1972). The solid dots denote the meander-absent mean and the 95% confidence limits are marked by horizontal lines on the vertical line, while clear dots and semi-circular arcs are the counterparts for the meander-present statistics. Data periods are given in the text.
THE KUROSHIO. PART I. PHYSICAL FEATURES
49
The latter currents seem to be highly variable as a drifter buoy was caught by a cyclonic eddy east of Okinawa Island in March 1980 and spent about six months there slowly circulating and moving northeastward (Anonymous, 1985b). Table I (see p. 31 ) also shows that the seasonal mean transports through the three sections south of Japan are generally higher in summer than in the other seasons. In addition, at Section KD the mean transport during the large-meander mode is significantly higher than that during the meander-absent mode and the opposite at Section KG. These are probably related to the westward shift of the elongated anticyclonic gyre which becomes an intensified anticyclonic eddy. At Section KF the two means are almost identical.
TEMPERATURE AND SALINITY DISTRIBUTIONS
The horizontal temperature and salinity distributions at 200-m depth of the Kuroshio south of Japan in a straight path mode (summer 1980) are shown in Figure 32. Both distributions have similar patterns to the surface dynamic topography (Fig 29b). A cold eddy, known to be ever present except when a large cold eddy is formed, is evident east of the Kii Peninsula. The anticyclonic gyre south of Kuroshio does not stand out distinctly because the 200-m depth there happens to be the thermostad, i.e., Subtropical Mode Water, as well as the salinity-maximum layer. This warm gyre shows up clearly in deeper layers (e.g., see Fig 33). Figure 34 shows the horizontal temperature distribution at 200-m depth in a large meander mode. The large cold eddy southeast of the Kii Peninsula is conspicuous. For the same reason as given above the intense anticyclonic eddy usually found just west of a large meander (e.g., see Fig 29a) becomes evident in deeper depths all the way down to 3000 m (see Oceanographic Atlas of KER, 1983). Based on findings by Kawai, Taft (1978) proposed to use the 15°C isotherm at 200 m as an indicator of the axis of the Kuroshio, i.e., the line connecting the maximum surface current, for the region south of Japan, although the best temperature indicator at 200-m depth may vary between 15–17°C. Figure 35 shows the vertical temperature and salinity distributions across Section KG in summer 1980. The largest slope of the isotherms and isohalines, corresponding to the Kuroshio, lies between 32°N and 34°N. The next steepest isolines, which slope up southward between about 30.5°N and 31.25°N, represent the Kuroshio Countercurrent. The thermostad characteristics of the Subtropical Mode Water are preserved south of 32.5°N as the 17 to 20°C-water layer. We also note that the Mode Water now coincides with the salinitymaximum layer, whereas in the upstream area along the Kuroshio it lies below the salinity maximum (see also Fig 23 of Nitani, 1972). As shown by Masuzawa (1972) the Mode Water has the largest thickness south of Japan. Figure 36 gives the temperature distribution across Section KG in spring 1982 when the Kuroshio was in the large-meander mode. The Kuroshio front has moved southward to around 31.5°N. The isotherms inside the cold eddy have been lifted by as much as over 350 m. Uplifting of isotherms is still appreciable below 1200-m depth. Similarly the upstream region surface water south of Japan also has higher temperature and lower salinity in the summer. Masuzawa (1972) analysed a set of 4-year data from an ocean weather station at (29°N:135°E) where the Kuroshio Countercurrent flows. He found the lowest monthly mean sea surface temperature
Fig 32. —Distribution of temperature (a, °C) and salinity (b, ‰) at 200-m depth south of Japan in summer 1980 (adopted from Oceanographic Atlas of KER, 1983).
50 J.L.SU, B.X.GUAN AND J.Z.JIANG
THE KUROSHIO. PART I. PHYSICAL FEATURES
51
Fig 33. —Distribution of temperature (°C) at 600-m depth south of Japan in summer 1980 (adopted from Oceanographic Atlas of KER, 1983).
(19.5°C) in February and March and the highest (28.7°C) in August. The monthly mean surface salinity exceeds 34.8‰ between February and April. It drops rapidly in June with the onset of Meiyu rainy season, reaching below 34.4‰ in July and August. Below 150 m there are only slight changes in the mean temperature and mean salinity.
LARGE-MEANDER MODE
As already pointed out the existence of a stable large meander mode distinguishes the Kuroshio from the Gulf Stream. Although there is also a bimodality of the Gulf Stream path (Bane & Dewar, 1988), both its scope (deflected tens of kilometres offshore of the normal position) and duration (up to several months) are far less spectacular than the Kuroshio meander. In addition, while the large meander of the Kuroshio is found upstream of the Izu-Ogasawara Ridge the large deflection of the Gulf Stream path is always found downstream of the Charleston Bump. The first scientific report about the Kuroshio was made by Uda (1937). That meander was generated in 1934. In 1934 Japan first experienced an exceptionally cold winter and then a huge typhoon in summer (Teramoto, 1972). The meander was
52
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 34. —Distribution of temperature (°C) at 200-m depth south of Japan in spring 1982 (adopted from Oceanographic Atlas of KER, 1985).
first reported by merchant ships in spring 1934, but the Japanese Navy learned of its occurrence only after a missed encounter of opposing fleets in an exercise in 1935 (Shoji, 1972). Thereafter, intense hydrographic observations were maintained south of Japan by fisheries, meteorological, and naval (maritime, after 1946) agencies. These observations revealed the presence of a large meander in 1934 to 1945, August 1951 to April 1952, September 1953 to December 1955, June 1959 to December 1962, May 1969 to May 1970, August 1975 to August 1980, November 1981 to September 1984, and December 1986 to September 1988 (Sekine, 1985; Hydrographic Bulletin of Japanese Maritime Safety Agency, 28 September 1988). In addition, Okada & Nishimoto (1978) analysed the tidal records at several stations along the south coast of Japan and pointed out that the Kuroshio meander may have also occurred in 1906 to 1912 and 1917 to 1922. The rationale for their arguments will become clear in the later text of this review. Therefore, more than 40% of the time in this century the Kuroshio south of Japan is in the large-meander mode. ‘Trigger’ meander and its development into a large meander
THE KUROSHIO. PART I. PHYSICAL FEATURES
53
Fig 35. —Temperature (a, °C) and salinity (b, ‰) sections across Section KG in summer 1980 (R.V.SHUMPU MARU).
From historical observation data, it has been recognised that small meanders are often generated off the southern coast of Kyushu (Yoshida, 1961). They move slowly eastward and some of them develop into a large stationary meander a few months later (Fig 37), while others decay. All the large stationary meanders of the Kuroshio that have appeared since 1959 were preceded by such a small meander (Solomon, 1978a; Sekine & Toba, 1981a; Hydrographic Bulletins of the Japanese Maritime Safety Agency). Observations before 1955 were not frequent enough to determine the generation processes of previous large meanders. Both in 1934 and 1953 departure of the Kuroshio from the coast of Kyushu prior to the development of a large meander off the Kii Peninsula was, however, observed (Shoji, 1972). The small meander is observed usually in winter or early spring every year but only occasionally in other seasons (Sekine & Toba, 1981a). During or prior to the period of small-meander formation, there is a tendency for an abrupt increase in the current velocity west of Yakushima, an island to the south of Kyushu. This represents an increase in the main current intensity upstream. Indeed, numerical experiments by Sekine & Toba (1981b) demonstrated that the increase in current
54
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 36. —Temperature (°C) section across Section KG in spring 1982 (R.V. SHUMPU MARU).
velocity may possibly cause the formation of the small meander off southern Kyushu. Because the Kuroshio flows close to Cape Shionomisaki during the straight path mode and it leaves the continental slope there in the meander mode, the continuous sea level data from the two tidal stations on both faces of the Cape should also reflect such bimodal characteristics (Moriyasu, 1961). Several investigations (see Kawabe, 1980) found that the sea level west of the Cape was significantly higher than that east of the Cape when the Kuroshio takes its straight path, whereas no appreciable difference is seen when the Kuroshio is in its meander state. As mentioned earlier, Okada & Nishimoto (1978) used this fact to infer the presence of a large meander in two earlier periods of this century when there were no oceanographic data. Kawabe (1980) analysed sea level data at nine tidal stations on the south coast of Japan from 1974 through 1976. He found that the 25-day running averages of sea level anomalies of the nine stations all showed a sharp rise almost simultaneously just prior to the establishment of the large meander in 1975. Similar characteristics were also
THE KUROSHIO. PART I. PHYSICAL FEATURES
55
Fig 37. —The eastward propagation of a small meander in 1975 prior to the establishment of a large meander (after Nishida, 1982). Dotted lines are 1000 m isobaths.
found in the 5-day mean sea level anomalies on the south coast of Japan during the generation of the large meander in 1959. Because the nine tidal stations are spaced over a distance of about 700 km, Kawabe concluded that the generation of large meander could hardly be attributed solely to the small meander generated off Kyushu. The small meander probably acted only as a trigger for the transition when a favourable large-scale oceanic condition existed. By fully exploring the characteristics of the sea level data of coastal and island tidal stations, Kawabe (1985) proposed a different classification for the Kuroshio path patterns south of Japan. His classification gives three typical paths, namely, the nearshore and offshore non-large meander paths and the typical large-meander path (Fig 38). Spectral analyses of sea level data of these and other stations revealed that the typical large-meander path occurs with a primary period of about 20 years and secondary period of 7 to 8.5 years (Kawabe, 1987). During the nonlarge-meander period, the Kuroshio takes the nearshore and offshore non-large-
56
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 38. —Schematic diagram of Kawabe’s classification of the Kuroshio path patterns south of Japan (after Kawabe, 1987): A, nearshore non-large meander path; B, offshore non-large meander path; C, typical large meander path.
meander paths alternatively with a primary period of 1.6–1.8 years and secondary periods of 110 days, 200 days, and one year. The large meander in 1975–1980 Because of the dense data coverage in both space and time and deep observation nearly down to the bottom, the large meander in 1975–1980 has been studied in detail and thoroughly by Japanese oceanographers. The most striking feature of the large meander in this period is the thrice separation or cut-off of a cold core ring from the Kuroshio meander, which has not been observed before in this area. Prior to the establishment of the Kuroshio large meander, a small meander occurred southeast of Kyusyu and moved eastward slowly until reaching in the offing of Enshunada (Fig 37). It grew large there resulting in the large Kuroshio meander. During the five-year meander period, the meander was generally stable in autumn, but rather unstable in spring. In May 1977, the meander off Kii Peninsula became slender with its axis extending in the NNW-SSE direction and the southern part of it was eventually separated from the main meander as a cold core ring (Fig 39). The reduced meander proceeded eastward and disappeared in a month, while a new meander was generated east of Kyusyu in June. The new meander moved eastward and the detached ring moved northwestward. In August they coalesced with each other resulting in a large Kuroshio meander again. This kind of separation or cut-off phenomenon was actually observed for the first time in the history of the Kuroshio observations. Detailed descriptions of the separation process of this cold ring were given by Solomon (1978b), Kamihira et al. (1978),
THE KUROSHIO. PART I. PHYSICAL FEATURES
57
Fig 39. —The separation of the cold eddy in May 1977 and its subsequent coalescence with the small meander off Shikoku (after Nishida, 1982). Dotted lines are 1000 m isobaths.
and Nishida (1982). The cold ring occurred twice more during the five-year meander period, in April and August 1979. In the April instance there was also a new small meander generated off Kyusyu which moved eastward and coalesced with the cold ring. In the August case, however, no small meander was generated off Kyusyu, and the Kuroshio meander remained reduced in size, entering into the disappearing stage. The isolated cold core ring typically has a diameter of about 200 km. Its maximum velocity was found in the region 30 to 70 km away from the centre. Isotherms and isohalines inside the ring were usually uplifted by about 200 m compared with the ones outside the ring. Distributions of GEK currents together with the water temperature at 200-m depth in May 1977 and the vertical temperature distribution across the cold ring at the same time are shown in Figures 40 and 41, respectively. Observations with deep hydrographic casting and deep current mooring stations made in the period 1975–1980 revealed two important facts of the deep sea structure of the Kuroshio meander which were hitherto unknown. First, a horizontal temperature gradient was found to exist down to over 3500 m (Fig 42) throughout the meander period, indicating the existence of geostrophic currents even in the near-bottom layer. The maximum geostrophic currents at 1000 db and 2000 db referred to 3000 db were 0.1 m·s -1 and 0.03 m·s -1, respectively. In addition, the temperature gradient next to the Izu-Ogasawara Ridge at 2000-m depth (Fig 42) indicated that the influence of the Izu-Ogasawara Ridge on the deep flow of the Kuroshio was significant. Secondly, a rather strong deep current which was fairly consistent with the surface current was observed (Nishida & Kuramoto, 1982). Direct current measurements west of Izu-Ogasawara Ridge showed that a cyclonic flow with speeds often above 0.1–0.2 m·s -1 around a cold water mass was evident at a depth of 2450 m, i.e., the Kuroshio extended deeper than the sill depth of the ridge. This was in agreement with the fact that horizontal temperature gradients existed
58
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 40. —Distributions of GEK currents (a) and the 200-m depth water temperature (b, °C) of the cold core ring south of Japan in May 1977 (after Kamihara et al., 1978). L=low temperature centre, H=high temperature centre.
THE KUROSHIO. PART I. PHYSICAL FEATURES
59
Fig 41. —The vertical temperature distribution across the cold core ring in May 1977 (after Kamihara et al., 1978).
at 3000 m in the cold eddy region. The deep-current pattern did not follow the movement of the surface-meander pattern in the disappearing stage of the meander. When the meander crossed over the ridge in the decaying stage, the deep circulation in the cold eddy remained to the west of the ridge, evidently due to the influence of the ridge. Schematic diagrams of the deep current around the Izu-Ogasawara Ridge in three typical Kuroshio meander patterns are shown in Figure 43. Kuroshio cold eddy Nearly 40 years ago, Uda (1949) pointed out the good correlation between the Oyashio strength and the generation of the Kuroshio large meander. He suggested that the water mass of the Kuroshio cold eddy was supplied by the Oyashio Undercurrent, which flows to the south from the Oyashio region on the eastern
60
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 42. —Temperature distributions at 2000 m (a) and 3500 m (b) in the region south of Kii Peninsula in November 1976 (after Nishida, 1982). Dotted line is 2000 m isobath in a and 3000 m isobath in b.
side of the Izu-Ogasawara Ridge. Recent T-S and T-O analyses by Nishida (1982), using all the serial observation data taken by the Hydrographic Department of Japan during the period from August 1975 to November 1978, showed, however, that the water mass of the cold eddy was the same as the water of the Kuroshio main current. In addition, the 136°E temperature section in November 1976 (Nishida, 1982), which crossed the centre of the cold eddy, showed that the Kuroshio water upwelled by an amount of 300–400 m in every layer from the surface to the near-bottom at the time of the beginning stage of the large meander (see also Fig 36, p. 54 ). Therefore, the cold eddy water was derived from the up welling of the Kuroshio water and was not caused by the southerly invasion of the cold Oyashio undercurrent as originally suggested by Uda. Nishida (1982) also found that, in the disappearing stage of the large meander when the cold eddy straddles the ridge, waters deeper than 800 m on both sides of the Izu-Ogasawara Ridge have different water characteristics while the characteristics of the shallower waters are the same on both sides. This means that when the pattern of the Kuroshio meander changes from Aor B- type to C-type, only the surface pattern moves but the deep water does not cross the ridge. Using the serial observations down to the bottom from 1975 to 1980, it is found that the life cycle of the cold eddy includes several repetitions of spin-down and spin-up processes (Ishii, 1982; Ishii, Sekine & Toba, 1983; Sekine, Ishii & Toba, 1985). In other words, the warming of the cold water mass is not monotonous throughout its life and some cooling periods occur in between (Fig 44). The spindown (or the spin-up) process is accompanied by warming (cooling) of the cold water mass and descending (ascending) motion of the inner water. The area of cold water also expands with the spin-up period and contracts in the spin-down period.
THE KUROSHIO. PART I. PHYSICAL FEATURES
Fig 43. —Schematic diagrams of the deep current around the Izu-Ogasawara Ridge in three typical (a, b, c) Kuroshio patterns (after Nishida & Kuramoto, 1982). Depth contours in b and c are as in a. Heavy solid line indicates surface Kuroshio path, broken line is current path at 1000 m, broken and dotted line is current path at 2000 m.
61
62
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 44. —Time variation of temperature at several depths in the cold eddy of the 1975–1980 large meander (after Ishii, 1982). Different symbols represent different depths; bars on left are standard deviations. Depth range at base of figure should read 2000–2500 m.
The rate of spin-down of the cold water mass, three years undisturbed decay time, is approximately equal to that of the Gulf Stream rings. The spin-up process is not observed in the Gulf Stream rings, and the Kuroshio cold eddy is apparently replenished by intermittent up welling when the isotherms rise 350–450 m over 1– 2 months (Ishii, 1982). The longer life-time of the cold water mass of Japan, in comparison with the Gulf Stream rings, is partly due to the existence of the spinup periods (Sekine et al., 1985). In addition, the coastline geometry and bottom topography of the Izu Ridge, as well as cold and warm eddies inside and outside the Kuroshio may also play significant roles in the long stay of the large meander (Anonymous, 1985b). Causes of the bimodality There have been many studies attempting to explain the bimodality character of the path of the Kuroshio south of Japan. Studies before 1972 were reviewed by Yoshida (1972). Since then there have been several theoretical studies on the dynamics of the large meander. These works have been reviewed in two recent numerical studies (Yasuda, Yoon & Suginohara, 1985; Yoon & Yasuda, 1987).
THE KUROSHIO. PART I. PHYSICAL FEATURES
63
It seems that the coexistence of Kyushu and Izu-Ogasawara Ridge with a channel close to the coast at 34°N is largely responsible for the bimodality of the Kuroshio path. The two-layer numerical model of Yoon & Yasuda (1987) indicates that the path dynamics of the Kuroshio depends on two dimensionless parameters. One is the beta Rossby number, R, which is the square of the ratio of the beta-plane inertial boundary-layer thickness over the characteristic length between Kyushu and the Izu-Ogasawara Ridge, and the other is the Reynolds number related to the inlet width and the horizontal eddy viscosity. They found that there exist two critical values of the beta Rossby numbers, say, R
64
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fig 45. —Time series of the annual mean wind-stress curl (vertical axis) in the area adjacent to Hawaiian Islands and the periods of large meander south of Japan (after Guan, 1982, 1988).
frequently occurs towards the end of an ENSO event (Saiki, 1985; Yamagata, Shibao & Umatani, 1985; Liu & Guan, 1986). Like the many characteristics of the Kuroshio discussed before the dynamics and global causes of the bimodality of the Kuroshio path south of Japan are far from well understood.
KYUCHO
Unlike in the upstream region where the Kuroshio participates in year-round large circulation over the broad shelves or in marginal seas, the Kuroshio south of Japan does not seem to have such kind of persistent interaction with the shelf waters. The Kuroshio south of Japan does, however, interact strongly with the coastal waters albeit intermittently. It is named Kyucho by Kimura (see Takeoka & Yoshimura, 1988), meaning rapid current in Japanese. In a Kyucho event a sudden and swift current accompanied by a sudden rise in water temperature is commonly observed, usually in a bay. Such events have been observed in many bays along the south coast of Japan, although there have been also reports of Kyucho along Japan’s eastern and northern coasts. In Uwajima Bay such events have been observed frequently at about 15-day intervals in summer (Takeoka & Yoshimura, 1988). The currents may reach over 4 knots (Ishino & Otsuka, 1970) and the rise of temperature can exceed 5°C in a day (Takeoka & Yoshimura, 1988). The Kyucho is important in the renewal of bay water but it also brings damage to fishing nets deployed in the bay. The dynamics of the Kyuchos have been well explored. Depending on the characteristic length of a bay and the internal radius of deformation of the sea a Kyucho may be modelled either as a density induced current in a rotating fluid or as a lock exchange flow in a non-rotating regime (see references listed in Takeoka & Yoshimura, 1988). Generation of the Kyuchos in bays along the southern coast of Japan is believed to be related to the shoreward intrusion of the Kuroshio (Ishino & Otsuka, 1970; Yoshioka, 1988). We note that the Oyashio Current flows south along the eastern coast of Japan and a branch of the Tsushima Current flows northward along Japan’s northern coast. Therefore, shifting of the axes of these currents may also be responsible for the Kyucho
THE KUROSHIO. PART I. PHYSICAL FEATURES
65
events along the eastern and western coasts of Japan. As pointed out by Takeoka & Yoshimura (1988), there remain many unanswered questions about the Kyuchos. For example, along the southern coast of Japan Kyuchos seem to occur at different seasons in different bays, even for bays along the same channel connecting the Pacific Ocean and the Seto Inland Sea. Within a given bay Kyuchos with different dynamic structures have been observed in two consecutive events.
ACKNOWLEDGEMENTS Preparation of this review was funded by a grant from the National Natural Science Foundation of China.
REFERENCES Anonymous, 1985a. Report of the 1979–1982 Multidisciplinary Research Program of the Northern South China Sea, Vol. II. China Science Press, Beijing, 432 pp. (in Chinese). Anonymous, 1985b. Kuroshio Exploitation and Utilization Research (KER), Summary Report 1977–1982. Japan Marine Science and Technology Center, 125 pp. Atkinson, L.P., Lee, T.N., Blanton, J.O. & Paffenhöfer, G.A., 1987. Summer upwelling on the southeastern continental shelf of the U.S.A. during 1981, Hydrographic Observations. Prog. Oceanogr., 19, 231–266. Bane, Jr, J.M. & Dewar, W.K., 1988. Gulf Stream bimodality and variability downstream of the Charleston Bump. J. Geophys. Res., 93C, 6695–6710. Bodvarsson, G.M., 1976. On upwelling along the eastern coast of Taiwan: a review of hydrographic and chemical data. Acta Oceanogr. Taiwanica, 6, 98–117. Chern, C.S., 1983. On the characteristics of current at the offshore region of Suao. Acta Oceanogr. Taiwanica, 14, 75–87. Chu, T.Y., 1970. Report on the variation of velocity and volume transport of the Kuroshio. In, The Kuroshio, edited by J.C.Marr, East-West Center Press, Honolulu, pp. 163–174. Chu, T.Y., 1972. A study of the water exchange between Pacific Ocean and the South China Sea. Acta Oceanogr. Taiwanica, 2, 11–24. Chu, T.Y., 1976. Study of the Kuroshio Current between Taiwan and Ishigakijiwa. Acta Oceanogr. Taiwanica, 6, 1–24. Chuang, W.S., 1985. Dynamic of subtidal flow in the Taiwan Strait. J. Oceanogr. Soc. Japan, 41, 65–72. Chuang, W.S., 1986a. A note on the driving mechanisms of current in the Taiwan Strait. J. Oceanogr. Soc. Japan, 42, 355–361. Chuang, W.S., 1986b. The branching of Kuroshio into Taiwan Strait. Eos, 67, 1063 only. Csanady, G.T., 1979. The pressure field along the western margin of the North Atlantic. J. Geophys. Res., 84, 4905–4915. Defant, A., 1961. Physical Oceanography, Vol. 2. Pergamon Press, New York, 729 pp. Fan, K.L. & Yu, C.Y., 1981. A study of water masses in the seas of southernmost Taiwan. Acta Oceanogr. Taiwanica, 12, 94–111.
66
J.L.SU, B.X.GUAN AND J.Z.JIANG
Fujiwara, L, Hanzawa, Y., Eguchi, I. & Hirano, K., 1987. Seasonal oceanic condition on a fixed line in the East China Sea. Oceanogr. Mag., 37, 37–46. Fukasawa, M., Teramoto, T. & Taira, K., 1986. Abyssal current along the northern periphery of Shikoku Basin. J. Oceanogr. Soc. Japan, 42, 459–472. Fukase, S., 1975. Bottom water on the continental shelf in the East China Sea. Mar. Sci. Monthly, 7, 19–26(in Japanese). Gilg, J.G., 1970. Bathymetry of the South China Sea. In, The Kuroshio, edited by J. C.Marr, East-West Center Press, Honolulu, pp. 21–28. Guan, B.X., (Kwan Pinghsien), 1964. A preliminary study of the distribution and variation of the velocity and volume transport of the Kuroshio and their relation to the topography. Oceanol. Limnol. Sin., 6, 229–251(in Chinese). Guan, B.X. (Kwan Pinghsein), 1978. The warm current in the South China Sea. Oceanol. Limnol. Sin., 9, 117–127(in Chinese). Guan, B.X., 1980. Some results from the study of the variation of the Kuroshio in the East China Sea. In, The Kuroshio IV, Saikon Publishing Co., Tokyo, pp. 897–911. Guan, B.X., 1982. Analysis of the variations of volume transport of the Kuroshio in the East China Sea. In, Proc. Japan-China Ocean Study Symp., Shimizu, pp. 118– 137. Guan, B.X., 1984a. Current path in a deep layer of the Kuroshio east of Taiwan— a case study of an observation result of February to March, 1940. La Mer, 22, 156– 162. Guan, B.X., 1984b. Major features of the shallow water hydrography in the East China Sea and Huanghai Sea. In, Ocean Hydrodynamics of the Japan and East China Sea, edited by T.Ichiye, Elsevier, New York, pp. 1–13. Guan, B.X., 1988. Major features and variability of the Kuroshio in the East China Sea. Chin. J. Oceanol. Limnol., 6, 35–48. Guo, B.H., Lin, K. & Song, W.X., 1985. On the summer current field in the southern East China Sea. Acta Oceanol. Sin. (Chinese edition), 7, 143–153. Guo, B.H., Xiu, S.M., Ishii, H. & Nakamura, Y., in press. On the Kuroshio filaments and the source of Tsushima Current water. (Tentative). Proc. Symp. Japan-China Joint Res. Prog, on the Kuroshio, Tokyo, in press. Hasunuma, K., 1978. Formation of the Intermediate Salinity Minimum in the Northwest Pacific Ocean, Bull. No. 9. Ocean Res. Inst., University of Tokyo, 47 pp. Hasunuma, K. & Yoshida, K., 1978. Splitting of the subtropical gyre in the western North Pacific. J. Oceanogr. Soc. Japan, 34, 160–172. He, C.B. & Guan, B.X., 1984. Analysis of the thermohaline structure of the sea water on NE-SW section and the origin of the cold water in the basin of central South China Sea. Oceanol. Limnol. Sin., 15, 411–418(in Chinese). Hsueh, Y., Romea, R.D. & DeWitt, P.W., 1986. Wintertime winds and coastal sea-level fluctuations in the northwest China Sea. Part II. Numerical model. J. Phys. Oceanogr., 16, 241–261. Huh, O.K., 1982. Spring season flow of the Tsushima Current and its separation from the Kuroshio: satellite evidence. J. Geophys. Res., 87, 9687–9693. Hung, T.C., 1979. On upwelling along the southeastern coast of Taiwan. Acta Oceanogr. Taiwanica, 10, 151–159. Hurlburt, H.E. & Thompson, J.D., 1980. A numerical study of Loop Current intrusion and eddy shedding. J. Phys. Oceanogr., 10, 1611–1651. Ichiye, T., 1984. Some problems of circulation and hydrography of the Japan Sea and the Tsushima Current. In, Ocean Hydrodynamics of the Japan and East China Sea, edited by T.Ichiye, Elsevier, New York, pp. 15–54. Ishii, H., 1982. Variation of the Kuroshio cold eddy-large meander of the Kuroshio in 1975–1980 (II). Rep. Hydrogr. Res., 17, 209–228. Ishii, H., Sekine, Y. & Toba, Y., 1983. Hydrographic structure of the Kuroshio large meander-cold water mass region down to the deeper layers of the ocean. J. Oceanogr. Soc. Japan, 39, 240–250.
THE KUROSHIO. PART I. PHYSICAL FEATURES
67
Ishino, M. & Otsuka, K., 1970. On the coastal “Kyucho”, a catastrophic influx offshore water from the Kuroshio. In, The Kuroshio, edited by J.C.Marr, East-West Center Press, Honolulu, pp. 61–67. Kamihara, E., Minami, H., Ishizaki, H., Eguchi, H. & Nishizawa, J., 1978. The cutoff phenomenon of the large cold water mass off Tokaido. Bull. Kobe Mar. Obs., 195, 1–15(in Japanese). Kawabe, M., 1980. Sea level variations around the Nansei Islands and the large meander in the Kuroshio south of central Japan. J. Oceanogr. Soc. Japan, 36, 97–104. Kawabe, M., 1985. Sea level variations at the Izu Islands and typical stable paths of the Kuroshio. J. Oceanogr. Soc. Japan, 41, 307–326. Kawabe, M., 1987. Spectral properties of sea level and time scales of Kuroshio path variations. J. Oceanogr. Soc. Japan, 43, 111–123. Kawai, H., 1979. Rings south of the Kuroshio and their possible roles in transport of the intermediate salinity minimum and in formation of the skipjack and albacore fishing grounds. In, The Kuroshio IV, Saikon Publishing Co., Tokyo, pp. 250–273. Konaga, S., Nishiyama, K. & Ishizaki, H., 1980. Geostrophic transport in the East China Sea and southeast of Yakushima Island. A case study. Oceanogr. Mag., 31, 33–46. Konaga, S., Nishiyama, K., Ishizaki, H. & Hanzawa, Y., 1980. Geostrophic current southeast of Yakushima Island. La Mer, 18, 1–16. Kutsuwada, K., 1988. Interannual correlations between sea level difference at the south coast of Japan and wind stress over the North Pacific. J. Oceanogr. Soc. Japan, 44, 68–80. Lee, T.N., Atkinson, L.P. & Legeckis, R., 1981. Observation of a Gulf Stream frontal eddy on the Georgia continental shelf, April 1977. Deep-Sea Res., 28A, 347–378. Lim, D.B., 1971. On the origin of Tsushima Current Water. J. Oceanogr. Soc. Korea, 6, 85–91. Liu, C.T. & Liu, R.J., 1988. The deep current in the Bashi Channel. Acta Oceanogr. Taiwanica, 20, 107–116. Liu, J.P. & Guan, B.X., 1986. On the relation between the large meander of the Kuroshio and El Niño. Acta Oceanol. Sin, (Chinese edition), 8, 541–546. Mantyla, A.W. & Reid, Jr, J.L., 1983. Abyssal characteristics of the World Ocean waters. Deep-Sea Res., 30A, 805–833. Masuzawa, J., 1972. Water characteristics of the North Pacific central region. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 95–128. Miao, Y.T., Su, J.L. & Yu, H.H., 1987. Summer mixing condition of water masses in the East China Sea. In, Proc. Investigation and Res. on the Kuroshio, China Ocean Press, Beijing, pp. 217–226(in Chinese). Miita, T. & Ogawa, Y., 1984. Tsushima Currents measured with current meters and drifters. In, Ocean Hydrodynamics of the Japan and East China Sea, edited by T.Ichiye, Elsevier, New York, pp. 67–76. Mogi, A., 1972. Bathymetry of the Kuroshio region. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 53–80. Moriyasu, S., 1961. On the difference in the monthly sea level between Kushimoto and Uragami, Japan. J. Oceanogr. Soc. Japan, 17, 197–200. Moriyasu, S., 1972. The Tsushima Current. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 353– 369. Muneyama, K., Asanuma, L, Sasaki, Y., Saitoh, S., Tozawa, Y. & Ichiye, T., 1984. An application of NOAA AVHRR for oceanography in the East China Sea. In, Ocean Hydrodynamics of the Japan and East China Sea, edited by T.Ichiye, Elsevier, New York, pp. 375–386. Nagata, Y., 1981. Oceanic conditions in the East China Sea. In, Proc. Japan-China Ocean Study Symp., Shimizu, pp. 25–41. Nagata, Y. & Takeshita, K., 1985. Variation of the sea surface temperature distribution across the Kuroshio in the Tokara Strait. J. Oceanogr. Soc. Japan, 41, 244–258.
68
J.L.SU, B.X.GUAN AND J.Z.JIANG
Niino, H. & Emery, K.O., 1961. Sediments of shallow portions of East China Sea and South China Sea. Geol. Soc. Am. Bull., 72, 731–762. Nishida, H., 1982. Description of the Kuroshio meander in 1975–1980. Large meander of the Kuroshio in 1975–1980 (I). Rep. Hydrogr. Res., 17, 181–207. Nishida, H. & Kuramoto, S., 1982. Deep current of the Kuroshio around the Izu Ridge. Large meander of the Kuroshio in 1975–1980 (IV). Rep. Hydrogr. Res., 17, 241– 255. Nitani, H., 1969. The variation of the Kuroshio in recent several years. Bull. Japanese Soc. Fish. Oceanogr., 14, 13–18(in Japanese). Nitani, H., 1972. Beginning of the Kuroshio. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida. University of Tokyo Press, Tokyo, pp. 129– 163. Oceanographic Atlas, 1989. Vol. 2, China-Japan Joint Research Program on the Kuroshio, National Oceanographic Data Center of the People’s Republic of China, Tianjing, 134 pp. Oceanographic Atlas of KER, 1980. Vol. 2, Japan Oceanographic Data Center, Tokyo, 48 pp. Oceanographic Atlas of KER, 1983. Vol. 4, Japan Oceanographic Data Center, Tokyo, 48 pp. Oceanographic Atlas of KER, 1985. Vol. 6, Japan Oceanographic Data Center, Tokyo, 48 pp. Oey, L.Y., Atkinson, L.P. & Blanton, J.O., 1987. Shoreward intrusion of upper Gulf Stream Water onto the U.S. southeastern continental shelf. J. Phys. Oceanogr., 17, 2318–2333. Okada, M. & Nishimoto, K., 1978. Mean sea level along the south coast of Japan and the large meanders of the Kuroshio from 1894 through 1924. Umi to Sora, 54, 91– 97(in Japanese). Pan, Z.Q., 1989. Application of the Inverse Method to Computation of the Current Velocities of the Kuroshio, M.S. thesis, Second Inst. of Oceanogr., Hangzhou. China, 66 pp. (in Chinese). Park, Y.H., 1986. Water characteristics and movements of the Yellow Sea Warm Current in summer. Prog. Oceanogr., 17, 243–254. Reid, Jr, J.L., 1965. Intermediate waters of the Pacific Ocean, Johns Hopkins Oceanogr. Studies 2, 85 pp. Reid, Jr, J.L. & Mantyla, A.W., 1978. On the mid-depth circulation of the North Pacific Ocean. J. Phys. Oceanogr., 8, 946–951. Saiki, M., 1982. Relations between the geostrophic flux of the Kuroshio in the Eastern China Sea and its large meanders South of Japan. Oceanogr. Mag., 32, 11–18. Saiki, M., 1985. On the volume transport of the Kuroshio. Mar. Sci. Monthly, 17, 267–273(in Japanese). Sawara, T. & Hanzawa, Y., 1979. Distribution of water type in the East China Sea. Umi to Sora, 54, 135–148(in Japanese). Sekine, Y., 1985. Generation and formation of the large meander of the Kuroshio. Mar. Sci. Monthly, 17, 274–282(in Japanese). Sekine, Y., Ishii, H. & Toba, Y., 1985. Spin-up and spin-down processes of the large cold water mass of the Kuroshio south of Japan. J. Oceanogr. Soc. Japan, 41, 207– 212. Sekine, Y. & Toba, Y., 1981a. Velocity variation of the Kuroshio during formation of the small meander south of Japan. J. Oceanogr. Soc. Japan, 37, 87–93. Sekine, Y. & Toba, Y., 1981b. A numerical study of the generation of the small meander of the Kuroshio off southern Kyushu. J. oceanogr. Soc. Japan, 37, 234–242. Shibata, A. & Eguchi, I., 1985. Frontal eddies observed in the East China Sea. Oceanogr. Mag., 35, 21–29. Shim, T., Wiseman, Jr., W.J., Huh, O.K. & Chuang, W.S., 1984. A test of geostrophic approximation in the western channel of the Korea Strait. In, Ocean Hydrodynamics
THE KUROSHIO. PART I. PHYSICAL FEATURES
69
of the Japan and East China Sea, edited by T.Ichiye, Elsevier, New York, pp. 263– 272. Shoji, D., 1972. The variation of the Kuroshio south of Japan. In Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 217–234. Solomon, H., 1978a. Occurrence of small “trigger” meanders in the Kuroshio off southern Kyushu. J. Oceanogr. Soc. Japan, 34, 81–84. Solomon, H., 1978b. Detachment and recombination of a current ring with the Kuroshio. Nature (London), 274, 580–581. Song, W.X., Lin, K. & Guo, B.H., in press. On the origin of the Tsushima Current. (Tentative). Proc. Symp. Japan-China Joint Res. Progr. on the Kuroshio, Tokyo, in press. Stommel, H. & Yoshida, K., 1972. Editors. Kuroshio—Its Physical Aspects, University of Tokyo Press, Tokyo, 517 pp. Su, J.L. & Pan, Y.Q., 1987. On the shelf circulation north of Taiwan. Acta Oceanol. Sin. 6 (Suppl. I), 1–20. Su, J.L. & Pan, Y.Q., in press. On the areas of shelf-intrusion of the Kuroshio north of Taiwan. In, Selections of Kuroshio Studies. Vol. II, China Ocean Press, Beijing, in press. Su, J.L. & Pu, Y.X., 1987. The Kuroshio. Endeavour, (N.S.), 11, 137–142. Su, J.L. & Wang, W., 1987. On the sources of the Taiwan Warm Current from the South China Sea. Chin. J. Oceanol. Limnol, 5, 299–308. Sverdrup, H.U., Johnson, M.W. & Fleming, R.H., 1942. The Ocean, their Physics, Chemistry and General Biology, Prentice-Hall, New York, 1087 pp. Taft, B.A., 1972. Characteristics of the flow of the Kuroshio south of Japan. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 165–216. Taft, B.A., 1978. Structure of the Kuroshio south of Japan. J. Mar. Res., 36, 77–117. Takematsu, M., Kawatate, K., Koterayama, W., Suhara T. & Mitsuyasu, H., 1986. Moored instrument observations in the Kuroshio south of Kyushu. J. Oceanogr. Soc. Japan, 42, 201–211. Takeoka, H. & Yoshimura, T., 1988. The Kyucho in Uwajima Bay. J. Oceanogr. Soc. Japan, 44, 6–16. Tchernia, P., 1980. Descriptive Regional Oceanography, Pergamon Press, Oxford, 253 pp. Teramoto, T., 1972. History of the Japanese observation program of the Kuroshio and adjacent regions. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 3–52. Tominaga, M., 1972. Brief analyses of the upwelling phenomenons near the eastern coast of Taiwan. Acta Oceanogr. Taiwanica, 2, 25–38. Toole, J.M., Zou, E. & Millard, R.C., 1988. On the circulation of the upper water in the western equatorial Pacific Ocean. Deep-Sea Res., 35A, 1451–1482. Trump, C.L. & Burt, W.V., 1981. Wintertime current meter measurements from the East China Sea. J. Phys. Oceanogr., 11, 1300–1306. Tseng, W.Y., 1970. A preliminary report on cypridinids (Ostracoda) from Taiwan Strait. In, The Kuroshio, edited by J.C.Marr, East-West Center Press, Honolulu, pp. 339– 346. Tseng, W.Y., 1972. The zooplankton community in surface waters of Taiwan Strait. In, Kuroshio II, edited by K.Sugawara, Saikon Publishing Co., Tokyo, pp. 261– 271. Uda, M., 1934. The results at simultaneous oceanographical investigations in the Japan Sea and its adjacent waters in May and June, 1932. J. Imp. Fisher. Exp. Sta., 5, 57–190. Uda, M., 1937. On the recent abnormal condition of the Kuroshio to the south of Kii Peninsula. Kagaku, 7, 360–361(in Japanese).
70
J.L.SU, B.X.GUAN AND J.Z.JIANG
Uda, M., 1949. On the correlated fluctuation of the Kuroshio Current and the cold water mass. Oceanogr. Mag., 1, 1–12. Uda, M. & Hasunuma, K., 1969. The eastward subtropical countercurrent in the western North Pacific Ocean. J. Oceanogr. Soc. Japan, 25, 201–210. Wang, J., 1986. Observation of abyssal flows in the northern South China Sea. Acta Oceanogr. Taiwanica, 16, 36–45. Wang, J. & Chern, C.S., 1987. The warm-core eddy in the northern South China Sea, I. Preliminary observations on the warm-core eddy. Acta Oceanogr. Taiwanica, 18, 92–103(in Chinese). Wang, K.S., Su, J.L. & Dong, L.X., 1983. Hydrographic features of the Changjiang Estuary. In, Proc. Int. Symp. on Sedimentation on the Continental Shelf, China Ocean Press, Beijing, pp. 125–133. Wang, W. & Su, J.L., 1987. A barotropic model of the Kuroshio system and eddy phenomena in the East China Sea. Acta Oceanol. Sin., 6 (Suppl. I), 21–35. Watts, J.D., 1972. Current characteristics and trace element concentrations in the northern waters of the South China Sea. In The Kuroshio II, edited by K. Sugawara, Saikon Publishing Co., Tokyo, pp. 113–119. Weng, X.C. & Wang, C.M., 1984. A preliminary study on the T-S characteristics and the origin of Taiwan Warm Current Water in summer. Stud. Mar. Sin., 21, 113– 133(in Chinese). White, W.B. & Hasunuma, K., 1982. Quasi-stationary banded structure in the mean zonal geostrophic current regimes of the western North Pacific. J. Mar. Res., 40, 1035–1046. Worthington, L.V. & Kawai, H., 1972. Comparison between deep sections across the Kuroshio and the Florida Current and Gulf Stream. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 371–385. Wyrtki, K., 1961. Physical Oceanography of the Southeast Asian Waters, NAGA Report No. 2, 195pp. Yamagata, T., Shibao, Y. & Umatani, S.L, 1985. Interannual variability of Kuroshio Extension and its relation to the Southern Oscillation/El Niño. J. Oceanogr. Soc. Japan, 41, 274–281. Yang, T.H., 1984. A preliminary investigation of the Kuroshio watermass in the East China Sea. Stud. Mar. Sin., 21, 165–179(in Chinese). Yasuda, I., Yoon, J.H. & Suginohara, N., 1985. Dynamics of the Kuroshio large meander-barotropic model. J. Oceanogr. Soc. Japan, 41, 259–273. Yi, S.U., 1966. Seasonal and secular variation of the water volume transport across the Korea Strait. J. Oceanol. Soc. Korea, 1, 7–13. Yoon, J.H. & Yasuda, I. 1987. Dynamics of the Kuroshio large meander: Two layer model. J. Phys. Oceanogr., 17, 66–81. Yoshida, K., 1972. Some aspects of theoretical studies of the Kuroshio—A review. In, Kuroshio—Its Physical Aspects, edited by H.Stommel & K.Yoshida, University of Tokyo Press, Tokyo, pp. 433–440. Yoshida, S., 1961. On the variation of Kuroshio and cold water mass off Enshunada. Hydrogr. Bull., 67, 54–57(in Japanese). Yoshioka, H., 1988. The coastal front in the Kii Channel in winter. Umi to Sora, 64, 79–111. Yuan, Y.C., Endoh, M. & Ishizaki, H., in press. The study of the Kuroshio in the East China Sea and the current east of the Ryukyu Islands. Proc. Symp. Japan-China Joint Res. Progr. on the Kuroshio, Tokyo, in press. Yuan, Y.C. & Su, J.L., 1983. A two-layer circulation model of the East China Sea. In, Proc. Int. Symp. Sedimentation on the Continental Shelf, China Ocean Press, Beijing, pp. 335–345. Yuan, Y.C. & Su, J.L., 1988. The calculation of Kuroshio current structure in the East China Sea—early summer 1986. Prog. Oceanogr., 21, 343–361
THE KUROSHIO. PART I. PHYSICAL FEATURES
71
Yuan, Y.C., Su, J.L. & Zhao, J.S., 1982. A single layer model of the continental shelf circulation in the East China Sea. La Mer, 20, 131–135. Yuan, Y.C., Su, J.L. & Xia, S.Y., 1986. A diagnostic model of summer circulation on the northwest shelf of the East China Sea. Prog. Oceanogr., 17, 163–176. Yuan, Y.C., Su., J.L. & Xia, S.Y., 1987. Three dimensional diagnostic calculation of circulation over the East China Sea shelf. Acta Oceanol Sin. 6 (Suppl. I), 36–50. Zhao, B.R., 1987. A preliminary study of continental shelf fronts in the western part of southern Huanghai Sea and circulation structure in the front region of the Huanghai Cold Water Mass. Oceanol. Limnol. Sin., 18, 217–226(in Chinese). Zhao, B.R., Xiong, Q.C. & Zhang, F.G., 1987. The internal hydrographic structure of the Huanghai Cold Water Mass in summer. Stud. Mar. Sin., 28, 57–68(in Chinese). Zhou, W.D. & Yuan, Y.C., 1989. Application of the beta spiral method in computing current field of the Kuroshio—east of Taiwan. Acta Oceanol. Sin. (Chinese edition), 11, in press.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 73–153 Margaret Barnes, Ed. Aberdeen University Press
MICROBIAL EXOPOLYMER SECRETIONS IN OCEAN ENVIRONMENTS: THEIR ROLE(S) IN FOOD WEBS AND MARINE PROCESSES ALAN W.DECHO Marine Sciences Research Center, State University of New York at Stony Brook, NY 11794, and U.S. Geological Survey, Water Research Division, Mail Stop 465, Menlo Park, CA 94025, USA
ABSTRACT Microbial exopolymers are high molecular-weight mucous secretions of bacteria and microalgae. They range from tight capsules which closely surround cells to the loose-slime matrix associated with aggregates, sediment, detritus, and other surfaces. By virtue of their physical properties, exopolymers are highly adsorptive, and readily sequester dissolved organic matter and metals. Exopolymers are largely polysaccharide in composition, and can exist in ‘dissolved’ and ‘particulate’ form. These secretions serve many functions which enhance the survival and competitive success of microbial cells under natural conditions. While they have been well studied in other disciplines, the investigation of exopolymers in marine systems has been largely overlooked. Accumulating evidence, however, suggests that they influence a wide range of marine processes such as aggregate formation in the water column, benthic larval settlement, microscale biogeochemical processes, sediment stability, and metal sequestering by hydrothermal vent bacteria. In addition, when microbial consumers feed they coincidentally ingest exopolymers (and their adsorbed compounds). These secretions may, therefore, represent an effective vehicle to transfer nutrients and metals through lower marine food webs. This suggests a dynamic role for exopolymers in marine systems. As ocean paradigms are further revised, the potential roles of these secretions must certainly be addressed. The present review examines the properties, processes, and methodologies pertinent to the study of microbial exopolymers in ocean systems. Literature has been purposefully cited from various other disciplines where exopolymer-related processes have been well studied. A focus is made on attempting to understand the interactive roles of these secretions in food webs and other marine processes.
INTRODUCTION AND OVERVIEW: WHAT IS EXOPOLYMER AND WHY STUDY IT? Bacteria and microalgae have been intensively studied in the oceans. This is because of their controversial importance in the mineralisation of dissolved organic (DOM) and inorganic compounds, their roles as consumer food resources, and in the cycling of carbon and nitrogen (Pomeroy, 1974).
74
ALAN W.DECHO
A largely overlooked aspect of microbial cells, however, is their release of copious extracellular slime-secretions called mucus-exopolymers or EPS (Geesey, 1982). These secretions are recognised as an important part of many other systems and have received considerable attention (Costerton et al., 1987). In the investigation of marine systems, however, they represent a relatively novel area, and have not been incorporated into our understanding of microbial-related processes in oceans. These secretions, which are difficult to measure quantitatively in natural systems, have been virtually ignored in estimates of microbial production, studies of the utilisation of food resources by consumers, and the cycling of nutrients and energy. Mucus-like substances commonly occur throughout the marine environment. They are secreted by a wide variety of plants, animals and microbial flora (e.g. Rosen & Cornford, 1971; Ducklow & Mitchell, 1979a). The “gel” consistency and adsorptive nature (Rees, 1976) of mucus are ideally suited for many biological functions of the organisms which produce it. Examples of such functions of mucus range from the reduction in water friction by fish slime (Rosen & Cornford, 1971; Sar & Rosenberg, 1989) to the maintenance of symbiotic relationships in plants (Vasse, Dazzo & Truchet, 1984) and animals (Müller et al., 1981). Microbial cells growing in natural environments (be it infected host tissues or marine sediments) differ greatly from cells of the same species grown in vitro (Costerton et al., 1987). One important difference is that many natural populations grow in secreted adherent biofilms (composed of EPS) and structured consortia not typically seen in pure cultures (Costerton et al., 1987). It has been our pre-occupation to examine microbial processes as the resulting effects of microbial cells only. This understates the roles of micro-environments which envelope many bacterial communities. As we shall see, microbial flora under natural conditions often create protective microhabitats enclosed within extracellular secretions. These secretions greatly affect both the physical and biogeochemical environment in proximity to the cells. It is such microenvironments which structure the recycling of nutrients, house the potential food resources of microbial consumer animals, and ultimately foster the development of microbial communities within. In natural environments, exopolymers ubiquitously occur wherever microbial flora are associated with surface and particles (Fig. 1). Their presence, however, is not readily observed because these secretions are easily destroyed or distorted. Special fixation and staining techniques must often be employed to verify their presence (Roth, 1977). Close examinations, however, of bacteria growing in a wide variety of aquatic systems, especially marine sediments, aggregates, and detrital particles (Paerl, 1973; Sieburth, 1975) have shown that virtually all of the cells are surrounded by extracellular glycocalyx of varying thickness (Costerton, 1984; Yokote, Honjo & Asakawa, 1985), and many are enclosed within adherent biofilms (White, 1986). Much of our knowledge regarding exopolymers has come from the study of nonmarine systems, where these secretions are acknowledged to have important functional roles. For example, exopolymers are involved in the formation of dental plaque on teeth (Carlsson, 1967), in the anaerobic corrosion of metals (Hamilton, 1985), the attachment and survival of gastrointestinal microflora (Savage, 1977), and the pathogenic nature of microbial flora (Jann & Jann, 1985). They also play important roles in sewage treatment flocculation (Busch & Stumm, 1968), cause
MICROBIAL EXOPOLYMER SECRETIONS
Fig 1. —Schematic diagram showing (a) bacterial cells and secreted exopolymers on the surface of a sediment or detrital particle; (EPSSlime = bacterial exopolymer slime; EPS-Capsule = bacterial exopolymer capsule; Cell = bacterial cell); and (b) bacterial cell and exopolymer-capsule; note the tightly wound fibrous nature of capsule, and its close association to the cell
75
76
ALAN W.DECHO
reductions in heat-transfer in industrial cooling systems (Characklis, Nimmons & Picologlou, 1981), and in the speed and fuel efficiency of large ships. Studies of these systems have defined the fundamental properties of exopolymers under a variety of conditions. Exopolymers can exist as tight capsules which closely surround microbial cells, or as a dispersed slime in no apparent association with any one cell (Fig. 1). They occur in both colloidal and particulate form, depending on whether or not they are particle-associated. Therefore, colloidal-slime exopolymers can often be operationally classified as part of the “DOM” pool because they often pass through a 0·5 µm filter (Burney, 1986). Laboratory studies have shown that exopolymers are primarily composed of polysaccharides with high molecular weight (100000 to 300000 daltons) whose specific composition can be quite variable (Sutherland, 1977a). A large portion (up to 62%) of the carbon metabolised and ATP expended by microbial cells can be funnelled into production of these extracellular secretions, especially during later stages of growth (Norberg & Enfors, 1982; Jarman & Pace, 1984). Thus, under certain conditions, exopolymers may account for a potentially large, but as yet, unknown portion of microbial production (Paerl, 1974). Exopolymers have several key functions to the microbial cell. They create a micro-environment around the microbial cell, which allows it to operate, metabolise, and reproduce more efficiently. Their presence buffers cells against quick ionic and environmental changes such as pH, salinity, desiccation or nutrient regimes (Darbyshire, 1974; Boyle & Reade, 1983). These secretions are also important in the attachment of microbial cells to surfaces. In addition, exopolymers sequester and concentrate nutrients (Marshall, 1976a; Costerton, Irvin & Cheng, 1981), and help to localise and maintain the activity of exoenzymes (Tonn & Gander, 1979). Finally, they provide protection against heavy metals and other toxins (Daniel & Chamberlain, 1981; Kaplan, Christiaen & Arad, 1987). Recent evidence suggests that these microbially produced secretions are closely linked with several marine processes. In the water column, exopolymers are now commonly observed as part of sedimenting phytoplankton blooms (Riemann, 1989) and other types of marine snow (Alldredge, Cole & Caron, 1986; Smetacek & Pollehne, 1986; and others), and have a major role in aggregate formation. In addition, they influence the transfer of heavy metals from water column to sediments and through food webs, and may constitute an important energy source for protozoan grazers. In benthic systems, exopolymers exist abundantly as the copious slime associated with sediments and detrital particles (Uhlinger & White, 1983), and may affect several processes. First, they may directly constitute a food resource for animals. Secondly, in adsorbing DOM, exopolymers may act as a vehicle for DOM to reach directly higher trophic levels. Thirdly, certain capsular exopolymers may actually protect microbial cells from digestion, and may therefore influence the utilisation of microbial cells by animals as food. In addition, they affect sediment binding and stabilisation, and regulate the attachment of certain invertebrate larvae to surfaces. Exopolymers appear closely associated with mineral scavenging by microbial flora in hydrothermal vent systems. They also play a paramount role in biofilm formation and biofouling, and in the localisation of microbiogeochemical processes within aggregates and sediments. A growing number of studies from a variety of research areas now suggest that these
MICROBIAL EXOPOLYMER SECRETIONS
77
secretions, although previously unrecognised, may have dynamic roles in marine systems. The mechanisms which regulate these all-important processes are of both ecological and applied interest to marine investigators, and are just now being explored. When observing the accumulating data from a wide variety of research areas it becomes increasingly clear that exopolymers warrant further investigation in marine environments. In this review, the roles of exopolymers in food webs, aggregate formation and biofilm development will be emphasised and integrated with existing data from studies of other systems. Furthermore, their involvement in nutrient and metal fluxes, exoenzyme processes, the degradation of detritus, microbiogeochemical processes, and DOC-POC fluxes will also be considered. It is the purpose of this review to familiarise the marine investigator with the properties, methodologies, and existing data pertinent to the study of EPS. Through the separate efforts of workers in a wide variety of fields (mostly nonmarine), fundamental properties regarding exopolymers, and how those properties interact in aquatic systems have been explored. In referencing the literature, citations are purposefully compiled from many different disciplines. As the study of exopolymers in marine systems is relatively new, these citations are assembled in a context which focuses on their understanding and future investigation in food webs specifically, and other marine processes in general. Available evidence which support or refute the roles of exopolymers in these processes will be discussed. This work does not intend to be comprehensive in its discussion of feeding relationships, per se, nor does it attempt to be all inclusive in referencing the vast literature of exopolymers in other disciplines. These have been discussed in detail elsewhere. Instead, this review will cite and discuss keynote papers which, it is hoped, will direct investigators in the further study of exopolymers in marine processes. The investigation of exopolymers is vital to a clearer understanding of several ocean processes. As paradigms of food webs and our understanding of other ocean processes are further revised, the roles of exopolymers must be assessed and appropriately integrated. Many experimental avenues can be followed once these fundamental processes have been examined and evaluated.
FUNCTIONAL ROLES OF MICROBIAL CELLS Exopolymer secretions (EPS) represent a primary mechanism by which a microbial cell establishes and maintains an association between itself and another cell, or itself and its environment (Geesey, 1982). EPS should not be considered ‘essential’ to the cell per se, because a cell can remain viable, metabolise, and reproduce without an EPS coating. These secretions, however, serve many functions which enhance the survival and competitive success of microbial cells under varying natural environments (Costerton, 1974). They are therefore found associated with most attached cells in nature. Examples of the functions of EPS include: (1) the buffering against microenvironmental changes and the localisation of extracellular enzymes; (2) the sequestering and concentration of nutrients; (3) the protection against metals and other toxins; (4) the attachment to surfaces; (5) movement; and (6) the maintenance of symbiotic relationships, etc. While EPS coatings create a protective microhabitat around microbial cells, their presence
78
ALAN W.DECHO
also modifies the local environment near the cell. The various functions of microbial EPS are discussed below.
MAINTENANCE OF A STABLE ENVIRONMENT AND LOCALISATION OF EXOENZYMES IN PROXIMITY TO THE CELL
The access of molecules and ions to the cell wall and cytoplasmic membrane are influenced by the EPS-capsule layer (Cheng, Ingram & Costerton, 1970). Exopolymer capsules and slime, therefore, act as a buffer zone around the cell against sudden changes in its local osmotic environment (Dudman, 1977). The capsule also affects the access and utilisation of nutrients by the cell, especially large molecular weight DOM. Bacteria secrete extracellular enzymes, called exoenzymes, which process DOM into a more readily utilisable form before it enters the cell. Exoenzymes hydrolyse large macromolecules into smaller molecules such as small peptides, amino acids and simple sugars. These small molecules can be quickly taken up, and once in the cell, can be efficiently metabolised for energy and biomass. The exoenzymatic mobilisation and transformation of organic matter is a key process, a rate-limiting step, which regulates the cycling of both inorganic and organic compounds in marine environments. At the molecular level, the exopolymer capsule provides a mechanism for retaining exoenzymes within a localised area near the cell (Tonn & Gander, 1979). It has been recently suggested (Lock et al., 1984) that exoenzymes and enzymes derived from cell lysis, become attached to the polysaccharide matrix in a manner analogous to the enzyme-humic complexes observed in soils. In soils, such binding may protect enzymes bound to humus from proteolysis, and yet still allow accessibility to substrates (Ladd & Butler, 1975). Similar protective mechanisms may exist for enzyme-exopolymer complexes. Exopolymers are hydrophilic (i.e. they readily bind water) (Sutherland, 1977a). This hydrated property is thought to facilitate the maintenance of exoenzyme activities during local osmotic changes (Darbyshire, 1974). The binding of exoenzymes to exopolymer polysaccharides may allow the enzymes to retain their activity within an exopolymer matrix for several microbial generations, thus benefiting the daughter colonies (see pp. 115–117 ). This is an area which requires further study. Finally, the water-holding capacities of bacterial capsules and slime, and their importance in preventing desiccation becomes apparent in intertidal zones with heavy wave action and intermittent exposure to air. Bacteria in these environments which secrete a water-holding exopolymer slime have been shown to exhibit enhanced survival (Boyle & Reade, 1983).
EPS AS AN ADSORPTIVE SPONGE: FOR SEQUESTERING DOM, METALS, AND TOXINS
Exopolymers are very ‘surface active’ molecules and possess high binding affinities for many dissolved compounds contained in sea water. In natural environments, rarely are all the compounds necessary for microbes present in concentrations sufficient to support maximal growth rates (Logan & Hunt, 1987). Exopolymers thus
MICROBIAL EXOPOLYMER SECRETIONS
79
represent an efficient way in which microbial cells can sequester and concentrate nutrients extracellularly, while keeping them in proximity to cell membranes and allowing easy access for exoenzymes. In slime-containing aggregates uptake of dissolved organic compounds by bacteria does occur (Paerl, 1975) and can be up to 60% greater than uptake by dispersed bacteria (Logan & Hunt, 1987). These adsorptive properties may prove to represent a most important interactive aspect of exopolymers in marine systems. Binding mechanisms of exopolymers The binding mechanisms of exopolymers which allow high adsorptive affinities relate closely to their compositions and physical properties. Because exopolymers are highly hydrated molecules (approx. 99% water), they effectively act as a ‘sponge’. Most binding occurs through cation exchange processes with water resulting in loss of ‘bound water’ for organics or metals (Rees, 1976; Rendelman, 1978a, b). The physical structure of EPS resembles a highly dispersed matrix of fibrils (see p. 93 ). Bacterial cells are more compact by comparison and estimated to be 60% water (Bratbak, 1985). This implies that exopolymers possess a large surface area for exchange reactions to occur (Sutherland, 1977a). Most studies directly examining the binding processes of exopolymers have involved metals. The literature is quite extensive and largely the result of sewage treatment studies. This has provided detailed data on the mechanisms of these adsorptive processes. The polysaccharide moieties of EPS are especially important in binding reactions because they possess abundant carboxyl and hydroxyl groups, which act as binding ligands for dissolved compounds (Aspinall, 1982a). The hydroxyl groups of exopolymer polysaccharides form relatively weak associations in the binding of some metals (Brown & Lester, 1979). Comparatively stronger binding of metal cations, however, can occur via carboxyl groups on carboxylated polysaccharides, called uronic acids. The adsorptive affinities of certain metals have been correlated with the content of uronic acids in the exopolymer (Kaplan et al., 1987). A survey of a wide variety of marine and freshwater bacteria by Kennedy & Sutherland (1987) has shown that bacterial exopolymers typically contained 20–50% of their polysaccharides as uronic acids. Recently, Smith & Geesey (1989) have developed HPLC methods to quantify ketal-linked pyruvates present on exopolymers. These pyruvates contain free carboxyl groups which are free to react with positivecharged molecules such as certain metals. Preliminary results suggested potentially high complexation capacities of exopolymers for metals (32 µg polymeric pyruvate·g dry sediment -1 ) under natural conditions. Metal-binding to exopolymers Exopolymers bind a wide variety of metals such as Pb, Sr, Zn, Cd, Co, Cu, Mn, Mg, Fe, Ag, and Ni (Dugan & Pickrum, 1972; Corpe, 1975; Brown & Lester, 1982; and others). Theoretical predictions of exopolymer-polysaccharide binding capacities, based on estimated numbers of available carboxyl and hydroxyl groups, suggest a very high capacity, especially for acidic polysaccharides (Rees, 1976).
80
ALAN W.DECHO
This means that a small amount of exopolymer could theoretically bind a large amount of a given metal. How do these theoretical values compare with observed estimates? The binding capacity of specific organic materials is difficult to quantify in natural sediments (Luoma & Davis, 1983). Because exopolymers are composed of a matrix of fibrils with high-molecular weight (MW), binding capacities of exopolymers cannot easily be expressed in terms of surface area, but instead must be expressed in terms of weight-specific binding (Harvey & Luoma, 1985). Most empirical measurements thus far have indicated high weight-specific binding capacities of exopolymers for many metals. The affinities of exopolymers vary depending on the specific metal involved (Harvey & Luoma, 1985). Harvey (1981) found a binding capacity for lead of 0.13 µmoles Pb·mg exopolymer -1 (using stationary-phase exopolymer derived from the marine bacterium Pseudomonas atlantica). He calculated that if exopolymers represented only a very small portion (approx. 3%) of the organic matter in sediments, the exopolymer could still complex all available Pb in the surface layer sediments of a Palo Alto salt marsh (Harvey, 1981). Adsorption densities as high as 22 ng metal·µg exopolymer -1 have been found for copper (Kaplan et al., 1987). Scott & Palmer (1988) found that cadmium adsorbs 3.28 ng metal·µg exopolymer -1 , while Brown & Lester (1982) observed that cobalt adsorption=5 ng metal·µg exopolymer -1 . In some studies cell floc exopolymers were shown to accumulate up to 25% of their weight as metal ions (Dugan & Pickrum, 1972). Microalgal exopolymers similarly show high complexing capacities for certain metals, such as copper (20 ng metal·µg polymer -1) (Vieira & Nascimento, 1988). Exopolymers can effectively remove metal ions from solution depending on their speciation, even at relatively high or low metal concentrations. For example, more than 95% of most metals are removed from solution by bacterial exopolymers, even at high (1 mg·l -1 ) metal concentrations. This reflects their tremendous potential to sequester and concentrate ions (Brown & Lester, 1982; Harvey & Luoma, 1985). Metal binding to exopolymer is strongly influenced by pH. This further suggests the involvement of H + ions in this binding (Cheng, Patterson & Minear, 1975; Rudd, Sterritt & Lester, 1983). It is both interesting and highly relevant to note that the greatest binding affinities occur at or near the pH of ambient sea water, approx. pH 8.0 (which is also the normal pH of sewage treatment processes) (Cheng et al., 1975; Rudd et al., 1983). At ambient sea water pH, Harvey & Luoma (1985) found >99% removal of Zn and Ag by exopolymer. Brown & Lester (1982) found 96% removal of Co while manganese showed less than 1% removal via exopolymer. In studies of freshwater lakes, microbial biofilms under nearneutral pH scavenged metals up to 12 orders of magnitude higher than biofilms under lower pH (acidic) conditions (Ferris et al., 1989). This is because at low pHs (i.e. acidic conditions) the availability of negatively charged sites such as carboxylates is greatly reduced so fewer metal cations can be adsorbed. At higher pHs (i.e. near those of sea water) metal binding is enhanced by a proportional increase in the number of ionised acidic groups which are free to bind ions (Ferris et al., 1989). Not all association of metals with exopolymers may, however, be due to adsorption. Because the solubility of the metal itself depends on pH, it is probable that the metals associated with exopolymers under natural conditions are the result of both ion-exchange binding processes and the precipitation and later physical entrapment of the metal by the polymer (Brown & Lester, 1979).
MICROBIAL EXOPOLYMER SECRETIONS
81
Exopolymer binding processes can be important in the downward transport of metals in ocean environments. Close associations between bacterial exopolymers and a variety of metals have been found in both sediments (Nealson, 1983) and the water column (Cowen & Silver, 1984; Cowen & Bruland, 1985). Open-ocean bacterial aggregates below 100 metres often have been found with extracellular capsules containing metal precipitates. Their frequency increased with depth and implies the downward accumulation of metals on EPS aggregates. Similar associations have been found in freshwater lakes (Mittelman & Geesey, 1985).
Binding of organic compounds to EPS Comparatively few studies have directly examined the binding of organic compounds to exopolymers. The binding mechanisms of DOM and metals to exopolymers, however, are thought to be similar because DOM competes with trace metals for binding sites on organic ligands (Luoma & Davis, 1983). Exopolymers are often in close association with microbial cells so they can also potentially bind exudation and cell lysis products of algae and bacteria. One might initially predict that exopolymers should preferentially bind only compounds with high MW such as proteins and large peptides (which will be later hydrolysed by exoenzymes and taken up by the cell). Components with lower MW (such as amino acids, simple sugars, etc.), would not readily bind to exopolymers because they can be directly taken up by the cell without substantial enzymatic modification prior to crossing the cell membrane. Surface chemistry studies also predict that, in general, high-MW compounds adsorb to a given surface in greater abundance than compounds of lower MW (Aveyard & Haydon, 1973). Examinations of adsorption to “marine detritus” give partial support to such predictions (Khaylov & Finenko, 1968). The limited available evidence from studies specifically examining exopolymers, however, does not support the predictions that exopolymers only bind large-MW DOM. In fact, small-MW compounds such as the amino acids alanine and arginine (Joyce & Dugan, 1970), and a variety of phosphates (Dudman, 1977) readily bind to exopolymers. Also, simple sugars such as glucose are significantly retarded (from 2–100% of the equivalent diffusion coefficient in water) when diffusing through an exopolymer matrix (Matson & Characklis, 1976; La Motta, 1976). These studies suggest that exopolymers readily bind at least some low-MW compounds. The binding of relatively large compounds such as proteins to bacterial EPS may provide an efficient mechanism to allow hydrolysis (via exoenzymes) of larger proteins into smaller peptides and free amino acids. These smaller components can then be directly taken up by the cell. The relative importance of these small peptides as bacterial substrates has recently been discussed (Coffin, 1989). As microbial cells change their physiological state, the composition of their secreted exopolymers (and hence their ability to bind DOM) may also change. Vasse, Dazzo & Truchet (1984) observed that the lectin-binding ability of Rhizobium exopolymer decreased with age of culture. The implications of these changes in the adsorptive properties of exopolymers, however, are not known.
82
ALAN W.DECHO
Adsorption of DOM by exopolymers can be especially important to microbial communities in nutrient-poor environments. For example, in freshwater streams, more than 90% of the bacteria are enclosed within epilithic biofilms (i.e., on the surfaces of rocks, etc.) (Geesey, Mutch, Costerton & Green, 1978). The adsorptive nature of the EPS-biofilms allows the microorganisms to concentrate nutrients from the relatively nutrient-poor passing water (Lock et al., 1984). This allows high growth rates for these bacteria, and the subsequent development of diverse grazer communities. Protective effects of exopolymers against toxic compounds While the binding affinities of exopolymers can sequester favourable nutrients, these same affinities may serve protective roles for the bacterial cell against metals and other toxins. Bacteria often can adapt to survive and grow in the presence of growth-inhibiting concentrations of metals. These adaptations can be intracellular, through methylation of the metals (Summers & Silver, 1978), as well as extracellular through the secretions of EPS. EPS polysaccharides, which surround cells readily bind metallic ions and other toxic substances. Certain extracellular proteins have also been shown to bind metals. These secretions act as a protective barrier against the entry of these compounds into cells (Bitton & Friehofer, 1978). In doing so, they are thought to serve as a general de-toxifying mechanism for both bacteria (Christensen, Kjosbakken & Smidsrod, 1985) and microalgae (Daniel & Chamberlain, 1981; Kaplan, Christiaen & Arad, 1987; and others), although the cell wall itself may also bind metals (Beveridge & Murray, 1980). It has been shown that bacteria which colonised surfaces coated with antifouling paint (Cu O) avoid direct contact with 2 the toxic surface by the secretion of mucilaginous sheets (Dempsey, 1981). This enables cells to escape the highest concentration of copper, which occurs at the immediate surface. Not all metals are toxic so the sequestering of certain essential metals, in low concentrations, is necessary to microbial cells for growth. In certain ironbacteria (Ridgeway, Means & Olson, 1981) and algae (Murphy, Lean & Nalewajko, 1976), the Fe ++ is sequestered from the surrounding water by exopolymer binding. Similar scavenging and deposition of iron (and manganese) has been associated with deep-sea hydrothermal vent bacteria (Jannasch & Wirsen, 1981; Cowen, Massoth & Baker, 1986) and in certain budding bacteria (Sly, Hodgkinson & Arunpairojana, 1988). These binding properties can be of great importance in the sequestering and concentrations of nutrients from the surrounding media (i.e. water). The adsorption of both metals and dissolved organic compounds to exopolymers appears to serve functions which both enhance uptake of favourable compounds, and also serves to protect microbial cells against unfavourable compounds.
ATTACHMENT TO SURFACES: EPS AS A GENERAL ADHESIVE FOR MICROBIAL CELLS
The general attachment of marine bacteria to surfaces such as sediment or detrital particles is closely linked to exopolymer secretions. In order to understand the role
MICROBIAL EXOPOLYMER SECRETIONS
83
of EPS in the attachment of bacteria to surfaces, the physical properties of surfaces and bacterial cells must be briefly mentioned. ZoBell (1943) first posited the idea that surfaces quickly adsorb dissolved organics compounds (DOM) present in sea water, and provide a localised concentration of DOM which can then be utilised by the bacterium. Attachment to surfaces thus enables the bacteria to grow in solutions where substrate concentrations are otherwise too dilute to support growth. Since that time, many studies have supported the idea that DOM adsorbs and concentrates on particulate matter in nature (Paerl, 1973; Balistrieri, Brewer & Murray, 1981). Charged substrates such as certain amino acids and sugars, and hydrophobic surface-active organic compounds such as fatty acids and glycoproteins, are often the first to be found concentrated on surfaces (Marshall, 1980). The presence of this organic film on surfaces facilitates the first step in attachment of bacteria on a surface (Kefford & Marshall, 1984) because it leads to an apparent change in the charge and free energy of the surface (Fletcher & Marshall, 1982b). Most surfaces, even in turbulent flow, are surrounded by ‘viscous sublayer’. Bacteria in the bulk phase must penetrate this viscous layer (usually 30–40 µm) in order to come into contact with the surface (Marshall, 1985). Although attachment is a highly complex process, it is thought to occur in a series of steps. These steps have been reviewed in detail by Fletcher & Marshall (1982b), Fletcher & McEldowney (1984), Characklis & Cooksey (1983), and Marshall (1985, 1986). The first step in bacterial adhesion is the initial contact (or at least the close association) between the bacterial cell and the surface. This step is reversible and has been termed “Initial Reversible Sorption” (Marshall, Stout & Mitchell, 1971). When cells are reversibly attached they may still exhibit Brownian motion, and are removed by moderate shear forces (Marshall et al., 1971). Their adsorption is largely controlled by the interrelationships of electrostatic forces between the bacterial cell and the surface, Van der Waals forces, temperature, surface charge and the wetability of the surface, and the presence and concentration of electrolytes. Most bacteria are so small that they behave as colloidal particles (Marshall & Bitton, 1980) and, in general have a negative charge at pH values higher than 2 to 3 (Harris & Mitchell, 1973). Sea water is approximately pH 8.0 hence both bacterial cells and surfaces tend to have overall negative charges. Therefore, the presence of positively charged ions (e.g. Ca ++ ) can be used to overcome the barrier caused by the similar charges, and facilitate the initial attachment. A recent study by Fletcher (1988) using interference reflection microscopy (IRM) indicated that few, if any, cells directly attach to the substratum surface and there is almost always a thin (nm) aqueous layer. This separation distance is often bridged by adhesive polymers separating the two surfaces. This secretion of adhesive polymers can allow firm attachment of cells even at relatively large distances (about 100 nm) from the surface. The concentration of electrolytes appears to affect this separation distance, which is balanced by attractive forces (i.e. Van der Waals forces) and repulsive forces (i.e. due to electrostatic repulsion). For example, high concentrations of certain electrolytes reduced the repulsion and distance between the bacterial cell and the surface. This suggests that fundamental differences in the charge characteristics of surface polymers may operate between freshwater and marine bacteria.
84
ALAN W.DECHO
Indeed a general preference for hydrophobic surfaces can be found in most microbial flora (Fletcher & Marshall, 1982a). Many marine and freshwater bacteria possess capsules prior to initial attachment. Heteropolysaccharide capsules, which contain uronic acids, confer an overall negative charge to the cell (Sutherland, 1980). The presence of the capsular polysaccharides and proteins at the bacterial surface, however, allow it the capability for a range of polar and electrostatic interactions as well as hydrogen bonding (Fletcher & Marshall, 1982a) which may also facilitate the initial attachment. Some EPS capsules are produced around the entire bacterial cell, while others are produced just at one pole. This can result in a random or perpendicular orientation, respectively, of the microbial cell to the surface (Marshall, 1980). The second step in bacterial adhesion (i.e. once on the surface) is timedependent and involves the bacterium secreting a copious exopolymer matrix (i.e. EPS-slime). This fibrous polysaccharide matrix can irreversibly bind the bacterium to the surface (Costerton, 1984). The anionic nature of the matrix further acts as an ion-exchange resin for continued concentration of charged nutrients (Costerton, Irvin & Cheng, 1981). Tosteson (1985) using specific antigens found that specific molecules within the EPS can be involved in attachment processes to surfaces. Several studies using electron microscopy have since provided evidence that continued attachment is indeed dependent on cell-surface polysaccharides (Fletcher & Floodgate, 1973; Marshall & Cruickshank, 1973; Corpe, 1980; Costerton, 1980; and others). Some proteases, however, are able to remove attached bacteria suggesting that proteins (i.e. probably in the form of EPS glycoproteins) may also be involved (Danielsson, Norkrans & Bjornsson, 1977; Fletcher & Marshall, 1982b). It has also been suggested that the crosslinking of adjacent exopolysaccharide chains may provide the permanent adhesive mechanism (Marshall, 1980). In addition, it has been suggested that the EPS, in acting as an ion-exchange resin, provides a reservoir of protons available to drive chemostatic uptake and ATP-generating systems. This could account for increased growth and metabolism seen in surface-associated films (Wardell, Brown & Flannigan, 1983). Indeed, not all exopolymers are involved in the adhesive process. Several polymers may be produced by a given bacterium, perhaps with different functions. For example, several “non-adhesive mutants” strains are known to produce copious amounts of exopolymer. It is postulated that in such mutants, the non-adhesive polymers may block the effects of adhesive polymers (K.C.Marshall, pers. comm.). Different types of exopolymers (each with different properties and compositions) may be secreted either simultaneously or in sequence by a given bacterium (see p. 111 ). The interactions of these exopolymers in the attachment process are highly complex and only partially understood. The question of whether initial attachment of bacteria to surfaces is an active or passive process is also not entirely certain. It appears that several mechanisms may be used depending on the substratum, conditions, and bacterium in question (Fletcher, 1980b).
EPS AS A DISPERSANT AND FOR TEMPORARY ATTACHMENT
In contrast to the above-mentioned, some bacteria are capable of reversible attachment (Kefford, Kjelleberg & Marshall, 1982; Hermansson & Marshall, 1985).
MICROBIAL EXOPOLYMER SECRETIONS
85
These bacteria initially secrete a ‘sticky’ exopolymer which enables the bacterium to attach and utilise surface-associated nutrients. Once the nutrients have been utilised, a second polymer is secreted which releases the attached bacterium. Fattom & Shilo (1984) using cyanobacteria found that initially a hydrophobic (i.e. adhesive) exopolymer was secreted. Later, a more hydrophilic exopolymer was secreted which released the cells from the surface. Some of the most fascinating evidence for such processes comes from the examination of EPS produced under conditions of complete nutrient and energy starvation. This EPS causes detachment of the cell from a surface. The process appears to begin when a bacterial cell enters starvation phase. Initially, cellular metabolism is very active (Kjelleberg, Humphrey & Marshall, 1983; Kjelleberg, Hermansson, Marden & Jones, 1987). This energy expenditure coincides with the production of extracellular polymers which decrease adhesiveness to hydrophobic surfaces (Rosenberg, Gottlieb & Rosenberg, 1983; Wrangstadh, Conway & Kjelleberg, 1986). In the marine environment this is thought to be an adaptation which enables cells under starvation conditions to detach from a surface and disperse, perhaps to areas of higher nutrient concentrations (Fattom & Shilo, 1985). These exopolymers show very different properties from those produced in the presence of nutrients. Certain gliding bacteria, which are able to move across a surface while attached, produce adhesive exopolymers which are temporary in nature. These polymers are of different composition (i.e. mainly glycoproteins and lipopolysaccharide) than the more permanent adhesive exopolymers (which are primarily polysaccharide) (Humphrey, Dickson & Marshall, 1979). Many benthic diatoms produce extracellular polymer used for locomotion (Chamberlain, 1976; Edgar & PickettHeaps, 1984; Webster, Cooksey & Rubin, 1985). This polymer is often more soluble than the mucilaginous capsule polymers produced by the same diatom (Edgar & Pickett-Heaps, 1984; Paterson, 1989). Whatever the mechanisms, it is now apparent that different types of extracellular polymers are secreted by microbial cells for different functions (i.e. use in the attachment, detachment and the movement of certain cells on surfaces).
SPECIFIC BINDING TO EXUDING SURFACES
Some bacterial cells attach to specific animal or plant surfaces. Because these surfaces often release nutrients they are referred to as “exuding surfaces”. The attachment of bacteria to such surfaces can be a highly specific process that operates through the action of bacterial pili structures and/or exopolysaccharides which attach via specific lectins (see below) located on the exuding (tissue) surface. This permits bacteria to attach only at specific sites where the proper receptors are present (Costerton, 1980; Sutherland, 1980). The gastrointestinal tract of many vertebrates (for general review see Savage, 1977), such as fish (Horsely, 1977) are colonised by monospecies of bacteria enclosed in EPS biofilms. In some cases attachment is mediated by specific polysaccharides in the bacterial EPS. These polysaccharides bind to special proteins called lectins (Goldstein & Hayes, 1978) which are present on the host cell. Lectins are typically very specific in their binding. A given lectin may complex with only a certain arrangement of sugar molecules within a polysaccharide, somewhat
86
ALAN W.DECHO
analogous to antigen-antibody binding (Sharon, 1977). This binding mechanism allows the host plant (or animal) to select specific bacteria from the wide range of types normally encountered. For example, the marine sponge Halichondria panicea produces a lectin which binds to the cell envelope of the symbiotic bacterium Pseudomonas insolita, and later may act as an extracellular trigger of nucleic acid synthesis for the bacterium (Muller et al., 1981). Similar symbiotic relationships have been studied in detail using the soybean plant (Rhizobium japonicum) bacterial nitrogen-fixing symbiosis (Vasse, Dazzo & Truchet, 1984). Even subtle changes in the non-carbohydrate constituents of the EPSpolysaccharides, which occur during the bacterial growth, are recognised by the host (Sherwood, Vasse, Dazzo & Truchet, 1984). The mechanisms of exuding systems are very different from hard-substratum biofilm surfaces such as sediment particles because microbial communities closest to the exuding surface receive (and often depend on) nutrients released from the surface. Odham et al. (1986) and Gilbert et al. (1989) experimentally mimicked these systems using permeable membranes as surfaces through which nutrient solutions could be pumped in a single direction. The exciting intricacies controlling these relationships are just beginning to be elucidated with the refinement of molecular techniques.
ROLE IN SYMBIOSIS AND SYNTROPHIC RELATIONSHIPS
Symbiotic relationships exist between bacteria (and microalgae) and a variety of animal hosts such as sponges, corals, squid, thaliceans, echinoderms, bryozoans, polychaetes, turbellarians, etc. In vertebrate animals, there is strong proof that the EPS capsule surrounding a bacterial cell provides a mechanism for symbiotic bacteria to avoid phagocytosis by certain host cells (i.e. recognition as a foreign body) (Schwarzmann & Boring, 1971). This is by the presence of specific antigens located within the EPS capsule and lipopolysaccharide. This identifies the symbiotic cell as a ‘part of the host’ and not as a ‘foreign body’ by effectively masking cell surface components. Such mechanisms are generally thought to mediate the access and continued presence of symbiotic microflora within animal tissues (Müller et al., 1981). It has even been suggested that as the microbial cells reach their later stages of growth, the capsules lose their configuration and phagocytosis by host cells occurs thus regulating the microbial populations within the tissues. Similarly, in pathogenic bacterial cells living within animal tissues, the presence of an EPS capsule around a bacterial cell is an important mechanism to prevent phagocytosis by host cells (Jann & Jann, 1985). Specific areas of cyanobacteria (i.e. heterocysts), where nitrogen fixation is occurring, are often colonised by bacteria (Paerl, 1976). The colonisation is mediated by the specific adhesion of bacteria to the EPS polysaccharides of the heterocysts (Lupton & Marshall, 1984). These close associations may reflect a highly complex mutalism, and are also believed to facilitate the efficient transfer of nutrients from one organism to the other (Paerl, 1976). The EPS secretions here may further modify local environmental conditions around the heterocysts. For example, exopolymers have been shown to slow the diffusion of oxygen and other molecules, and a relatively thin biofilm of exopolymer can create steep biogeochemical microzones (Sanders, 1966; Mueller, Boyle & Lightfoot, 1968).
MICROBIAL EXOPOLYMER SECRETIONS
87
Microzones around individual cells, or groups of cells, can increase their maximal metabolic efficiency (Jørgensen & Revsbech, 1983). In other nitrogen-fixing bacteria (Derxia sp. and others) the slime coatings appear to protect the bacterial cells from oxygen (Hill, 1971) thus allowing fixation of nitrogen in otherwise aerobic conditions (Paerl, 1978; Paerl & Kellar, 1978a, b). In many luminescent deep-sea fish, symbiotic luminescent bacteria typically inhabit the light organs (and often the gut) of the fish (Hastings & Nealson, 1982). These light-producing bacteria may be selected from the plethora of other bacteria present in sea water by their selective ability to bind to the specific glycocalyx of the cells lining the organ (Costerton, Geesey & Cheng, 1978). This allows the fish to concentrate selectively (in some cases monocultures of) luminescent bacteria (Stanier, Doudoroff & Adelberg, 1976). The mucous slime of many fishes has a great capacity to reduce frictional drag (Rosen & Cornford, 1971). The vast majority of this slime is produced by the fish itself. In fish which are adapted to swimming for prolonged periods at high speeds, specific bacteria are, however, found colonising the fish skin. These bacteria may assist in fish locomotion by changing the surface properties of the fish skin (through the production of drag-reducing exopolymers) (Sar & Rosenberg, 1987). These polymers reduced frictional drag by up to 22% at ambient skin concentrations (Sar & Rosenberg, 1989). The mechanics of these polymers is at present under investigation.
PROTECTION FROM GRAZING AND DIGESTION BY CONSUMER ANIMALS
In a physical sense, the slime exopolymer found in aggregates and on surfaces may act as a barrier to prevent grazing protozoans from gaining access to bacterial cells. Caron (1987) noted that bacteria (either attached or aggregated) were grazed to a lesser extent by microflagellates than freely suspended bacteria. The microflagellates were only able to graze bacterial cells close to the surface of an aggregate, suggesting that the mucilage of the aggregate afforded protection to cells deeper within the EPS. Other studies have shown that certain heterotrophic microflagellates may selectively graze aggregates (Sibbald & Albright, 1988). As physical degradation and dissolution of the aggregate occurs with time, grazing protozoa are able to penetrate throughout the aggregate, until finally disaggregation occurs (Biddanda & Pomeroy, 1988). In a more chemical sense, the capsular secretions around bacteria and diatoms may act as a barrier which slows the penetration of digestive enzymes to microbial cells. Such barriers may play a role in the selective digestion processes of recently grazed microbial cells (Porter, 1976; Fenchel & Jørgensen, 1977) which have been suggested to occur in a variety of animals (Chua & Brinkhurst, 1973; Tietjen & Lee, 1973; Porter, 1976; Decho & Castenholz, 1986; and others). Diatoms are often observed to pass through consumer guts, still intact and viable in the faecal pellets of certain polychaetes such as Streblospio benedicti (G.Lopez, pers. obs.). Absorption experiments using this same polychaete showed that diatom capsular exopolymers are less labile than slime exopolymers of the same diatom (Decho & Lopez, in prep.). The capsular coatings may enhance the survival of these diatoms once ingested, especially when gut passage times are relatively short. A longer retention time in the gut
88
ALAN W.DECHO
may result in partial or complete hydrolysis. It has been suggested that some microalgae may even benefit during passage through the herbivore gut. The microalgal cells may take up nutrients (Porter, 1976) and even photosynthesise (Epp & Lewis, 1981) during gut passage. The mechanism of resisting enzymatic digestion, however, is still uncertain but probably resides in either the EPS capsule, the cell wall itself, or both. Tight capsular coatings are often produced during the active growth stage of many microbial cells. For example, many bacterial and diatom cells produce a tight capsule during their log phase of growth, but subsequently produce a very loosely dissociated slime during later stages (i.e. stationary phase) (Sutherland, 1977a). Capsular EPS is often of different composition and tertiary structure than the loose slime EPS from the same microbial strain (Sutherland, 1977a; Vasse et al., 1984; Christensen, Kjosbakken & Smidsrod, 1985). Such compositional and structural differences can potentially affect the degradability of the EPS to enzymes. The digestion of exopolymer coatings on microbial cells (or lack of it) may be further dependent on the tertiary structure of the exopolymer. In exopolymer capsules, the long polysaccharide fibrils are more tightly wound around the cell than the loosely associated fibrils often found in later-stage exopolymers. The tightly wound fibrils (and their associated tertiary interactions) may reduce the ability of consumer digestive enzymes to hydrolyse them (Powell, 1979), and the microbial cell within. The gut pH of the consumer animal may be important here. High pHs observed in some animals’ guts may solubilise exopolymer by ‘unwrapping’ the tightly wound fibrils of a capsule (i.e. disrupting the tertiary structure of the exopolymer). This will allow enzymes to access more easily and hydrolyse the polymer (Powell, 1979). Such processes require further study. Microbial flora which inhabit the guts of consumer animals must possess protective adaptations to prevent their own digestion by these enzymes if they are to exist and proliferate in such an environment. Many marine animals are now known to possess resident gut flora for nutritional purposes (Plante, Jumars & Barross, 1989; and others). These bacteria may similarly resist digestion by the presence of exopolymer capsules. Such adaptations have been best studied using the bacteria which live within the rumen of cattle. The rumen bacteria are protected from the local harsh conditions by the presence of an exopolymer capsule (Costerton, Damgaard & Cheng, 1974). The microbial capsule appears to provide a natural protective barrier against a variety of agents which are potentially detrimental to microbial cells. Gelatinous sheaths surrounding microalgal and bacterial cells have been shown to provide protection against other lytic agents, such as bacteriophages, Bdellovibrio sp. (Venosa, 1975) and antibiotics (Costerton & Cheng, 1975). The full significance of microbial capsules in terms of food webs and on microbial survival, however, is not yet understood.
OTHER FUNCTIONS
EPS can function as a storage reserve for certain nitrogen-fixing bacteria (Patel & Gerson, 1974). In general, however, EPS is not likely to serve as a reserve source of carbon (energy) because most EPS-producing bacteria surveyed appear unable to
MICROBIAL EXOPOLYMER SECRETIONS
89
utilise their own EPS (Dudman, 1977). The possibility exists, however, that bacteria can utilise the EPS produced by other bacteria. For example, some marine Pseudomonas sp., and other bacterial strains can utilise the EPS of other bacterial species as a carbon source (Mitchell & Nevo, 1965; Tago & Aida, 1977), and a wide variety of enzymes capable of degrading EPS have since been isolated from bacteria (Sutherland, 1977c).
COMPOSITION, REGULATION AND STRUCTURAL ASPECTS OF EPS BACTERIAL EPS: COMPOSITION
The vast majority of compositional studies of EPS have examined laboratory isolates. These studies have indicated that most EPS is composed of polymer chains with high molecular weight (100000 to 300000 daltons). These polymers have been characterised as being predominantly polysaccharide (i.e. carbon), with lesser amounts of other components such as amino acids, amino sugars, phosphate, pyruvate, and acyl groups, uronic acids, and glycoproteins. Compositional differences of EPS, especially their polysaccharides, occur within a given species (or even within a strain). The structural diversity of EPS arises from the broad arrangement of monosaccharides (within a polysaccharide) and additional non-carbohydrate substituents (Kenne & Lindberg, 1983). A variety of factors affect the composition and production of exopolymer: (1) the physiological state (nutrient-poor compared with nutrient-rich) or growth stage (log phase compared with stationary phase) of the cell in which the EPS is secreted (Uhlinger & White, 1983; Christensen et al., 1985); (2) the composition of the nutrient media in which the culture is grown (Buckmire, 1984); and (3) the ionic (Annison & Couperwhite, 1986) and physical conditions of the media (i.e. solid compared with liquid, temperature) (Fletcher & Floodgate, 1973). Many bacteria in culture can be induced to yield large quantities of EPS when grown in a high-carbon: low-nitrogen growth medium. For many marine bacteria, a glucose (C) concentration of 1.0–2.0% (w/v) yields the greatest EPS production, with up to 73% conversion efficiency of the glucose into EPS during the stationary phase (Williams & Wimpenny, 1978). Yields of 100–300 mg dry EPS·100 ml culture -1 are common for a range of bacteria (Corpe, 1972; Harvey & Luoma, 1984; Anton, Meseguer & Rodriguez-Valera, 1988; and others). It is interesting, however, that while excess carbon in the media increases EPS production, it is not a necessity for EPS production. Marine bacteria can produce EPS using only sea water as a growth medium (pers. obs.). Furthermore, carbon limitation (in the media) does not completely inhibit EPS production. Many bacterial species can synthesise EPS in the absence of utilisable carbohydrate in the media (Sutherland, 1979) via utilisation of amino acids as a carbon source (Sutherland, 1982). Such capsular formation under low carbon conditions has also been found in Azotobacter (Jarman, Deavin, Slocombe & Righelato, 1978). In some genera, such as Bacillus, capsules composed of polypeptides are formed under growth conditions having excess nitrogen present (Wicken, 1985). Other bacterial isolates, however, suppress EPS production in the presence of excess
90
ALAN W.DECHO
nitrogen (Williams, 1974). The ability of bacteria to produce exopolymers under varying conditions is thought to reflect the important functions of these secretions under fluctuating nutrient and environmental conditions, and/or byproducts of metabolic pathways under these same conditions (Sutherland, 1977b). Under laboratory conditions most bacterial strains release largest quantities of exopolymer during the stationary phase of growth. The growth phases of bacteria, which we often call log or exponential phase, stationary phase, etc., generally reflect both the ambient nutrient conditions in proximity to the cell and the physiological state of the cell. Exopolymers produced by cells in log phase (i.e. when cells are actively growing and dividing) are different in composition from the exopolymer produced by the same strain of cells in stationary phase (Abe, Sherwood, Hollingsworth & Dazzo, 1984; Sherwood et al., 1984; Christensen et al., 1985). In laboratory cultures, cells in stationary phase can often revert back to an actively growing state (i.e. log phase) by simply replacing old (nutrient-depleted) media with fresh growth media. Such shifts in the physiological state of cells probably occur with frequency under natural conditions. It can therefore be expected that exopolymer compositions under natural conditions will be quite variable (Geesey, 1982), and perhaps more nitrogen-rich. Carbohydrate components Polysaccharides form a large portion of most EPS. These polysaccharides have been separated into two major groups depending on their simple sugar (monosaccharide) composition: (1) homopolysaccharides, which are composed entirely of a single type of simple sugar; and (2) heteropolysaccharides, which are composed of repeating units of several types of sugars, with added uronic acids and pyruvates or other ketals). Homopolysaccharides are found in bacterial cellulose, levans, dextrans, and some glucans (EPS composed solely of glucose) and occur in Agrobacterium, Streptococcus, Leuconostoc, and others. In marine systems heteropolysaccharides are perhaps more common, and contain two to four monosaccharides and often uronic acids. They are found in a variety of bacteria such as Klebsiella, Aerobacter, Salmonella, Pseudomonas, Xanthomonas, Azotobacter, and the archebacteria (Anton et al., 1988). While most EPS polysaccharides have high molecular weights, the sizes of these polysaccharides can vary greatly between and within strains (Sutherland, 1982). In most marine bacteria examined, the EPS polysaccharides are comprised of simple six-carbon sugars such as glucose, galactose, mannose, fucose, and rhamnose (Sutherland, 1977a). Pentoses (i.e. five-carbon sugars) such as fructose and ribose are comparatively less common (Powell, 1979). It is difficult, however, to predict the composition of an EPS polysaccharide for a given bacterial strain, and some strains produce several polysaccharides simultaneously. Many EPS polysaccharides have a general structure composed of repeating units of two to six monosaccharides, which are often accompanied by acyl or ketal substituents. Most polymers are usually linear and of varying lengths, to which side chains of one or more monosaccharides can be regularly attached (Sutherland, 1977a).
MICROBIAL EXOPOLYMER SECRETIONS
91
Other components and residues A variety of non-carbohydrate components (e.g. amino acids, amino sugars, proteins, uronic acids, acyl and phosphate groups, pyruvate, or other ketals, nucleotides, etc.), are also found associated with EPS. While these noncarbohydrate components make up a relatively smaller portion of the EPS on a per-weight basis (Sutherland, 1979), they can be extremely important to the tertiary structure and physical properties of the EPS. These components are most often in the form of residues and side groups on the polysaccharide chains, and contain a variety of reactive carboxyl, amino and sulphate groups (Aspinall, 1982c). Uronic acids are, in the simplest sense, carboxylated forms of sugars on a polysaccharide. The presence of uronic acids confer an overall negative charge and acidic properties to the EPS (Corpe, 1970). The proportional abundance and absolute amounts of uronic acids in EPS increase with age and metabolic stress (Uhlinger & White, 1983). Uronic acids such as glucuronic acid, N-acetyl-Dglucosamine, and N-acetyl-D-galactosamine are common in a large number of bacterial exopolysaccharides, while galacturonic acid and mannuronic acid may also be present. Kennedy & Sutherland (1987) surveyed a range of marine bacteria and found that most EPS polysaccharides contain about 20–50% of their polysaccharides as uronic acids. The significance of uronic acids in the adsorption process has already been discussed (see p. 79 ). Proteinaceous materials, in the form of exoenzymes, glycoproteins, and amino sugars are secreted or often found associated with the capsules of numerous bacteria (Usui, Yoshida & San Clemente, 1981; Orr, Koepp & Bartell, 1982; Rubinovitz, Gutnick & Rosenberg, 1982; and others), a large portion of which are in the form of glycoproteins (Corpe, Matsuuchi & Armbruster, 1976; Humphrey, Dickson & Marshall, 1979; Corpe, 1980; Fletcher, 1980c; Sutherland, 1980, 1983). In purified exopolymer, after removal of adsorbed compounds, concentrations of nitrogenous compounds such as proteins are generally less than 10%. Both DNA and RNA are often found closely associated with exopolymer (Nishikawa & Kuriyama, 1968; Pavoni, Tenny & Echelberger, 1972). Such exogenous DNA which binds to exopolymer may originate from active secretion by cells or cell lysis (see p. 116 ). Phosphate, pyruvate and acyl groups can also attach to sugar residues, and are now recognised as integral components of EPS (Sutherland, 1979). Many exopolysaccharides contain acyl groups (most frequently as o-acetyl groups and pyruvate ketals). These groups appear regularly on the repeating units of the monosaccharide components (Sutherland, 1982). It has been postulated that their presence is essential to protect uronic acid residues from epimerisation, and thus assures a high uronic acid content of the final polymer. This would have a considerable effect on the properties (i.e. negative charge and acidic nature) of the polymer (Smidsrod, 1974). The process of o-acetylation typically occurs early in EPS synthesis (Sutherland, 1979, 1982). Acyl groups, however, are removed by weak alkaline treatment (Sutherland, 1977a) which is used during many isolation and purification processes. Other ionic residues such as pyruvates have been commonly found (i.e. generally less than 9%) in both bacterial and algal EPS (Corpe, 1970; Moorehouse, Winter, Arnott & Bayer, 1977; Kennedy & Sutherland, 1987; Smith & Geesey, 1989). These pyruvates are often ketal-linked (i.e. found attached to glucose, galactose, and other sugars) (Sutherland, 1972) and contribute to the water-binding properties of the exopolysaccharides (Rees & Scott, 1971).
92
ALAN W.DECHO
Specific compositions of EPS from various bacterial strains The specific composition of EPS has been determined for a wide variety of bacteria. Detailed reviews on compositions and structure are given by Powell (1979), Aspinall (1982c), Sutherland (1985), and Kennedy & Sutherland (1987). As alluded to earlier, the composition of EPS not only varies between bacterial strains but can also vary within a given bacterial strain, depending on the growth phase. Christensen et al. (1985) found that different extracellular polysaccharides were produced by a marine Pseudomonas sp. during log phase and stationary phase of growth. The first polysaccharide (from log phase) contained glucose, galactose, glucuronic acid, and galacturonic acids, and formed ‘gels’ at high concentrations (> 1% w/v). This EPS was strongly involved in biofilm formation. The second polysaccharide was released at the end of the log phase and during the stationary phase. It contained N-acetyl glucosamine, deoxyoctulosonic acids, and deoxyhexoses, and formed aqueous solutions with low viscosity (i.e. a ‘loose slime’ consistency). This study showed that both the composition and structural consistency (ability to form gels) can vary depending on the growth phase in which the bacterium secretes the polymer. Kennedy & Sutherland (1987) surveyed a wide range of both marine and freshwater bacteria. They found that while the specific compositions differed between isolates, all isolates contained uronic acids and several neutral polysaccharides, with some of the marine strains having a high acetyl content. Gliding bacteria appear to produce a characteristically different type of EPS than attached bacteria. Humphrey et al. (1979) characterised the EPS of the gliding bacterium (Flexibacter BH3), and found it to be a glycoprotein containing glucose, fucose, galactose, and some uronic acid. The slime released by this gliding bacteria acted as a temporary adhesive and was not a highly acidic polysaccharide which is typically found in EPS used in permanent adhesion (Fletcher & Floodgate, 1973). It is important to note that compositional studies of EPS have generally involved strains of bacteria grown under laboratory conditions (i.e. controlled temperature, nutrients, etc.). It must be expected that EPS compositions under natural conditions will be considerably more variable. This will be the result of several factors: (1) the large diversity of microbial flora producing exopolymer; (2) that EPS-secreting bacteria under natural conditions experience a variety of physiological states resulting from the more heterogeneous and fluctuating conditions than those found in laboratory cultures; and (3) EPS compositions will be significantly modified by the adsorption of dissolved organic compounds. Such differences in composition can potentially affect their lability as a food source for animals. Unfortunately there are few data on the chemical composition of exopolymer under natural conditions. As laboratory studies continue, varying environmental conditions (nutrients, temperature, salinity, ions, etc.), and monitoring the corresponding changes in EPS composition will give us a better understanding of EPS composition under natural conditions. Such studies will be important in determining their tropic role. Role of adsorbed components on composition While the composition of purified exopolymer grown in the laboratory is largely carbohydrate, the compositions of exopolymers under natural conditions (which
MICROBIAL EXOPOLYMER SECRETIONS
93
consumer animals encounter) may be further influenced by the adsorption of dissolved and colloidal compounds. These adsorbed compounds can include a variety of dissolved compounds found in sea water such as amino acids, as well as compounds derived from recently lysed cells (i.e. DNA, RNA, fatty acids, etc.), and a variety of metals. Exopolymer is known to adsorb and concentrate nitrogenous compounds such as proteins and amino acids (Dugan, MacMillan & Pfister, 1970; Joyce & Dugan, 1970), and metals (Dugan & Pickrum, 1972; Brown & Lester, 1979). These binding processes have been discussed elsewhere (see p. 79 ). General enrichments of mucous aggregates contained in dialysis bags by dissolved organics have been noted by Paerl (1975). Coles & Strathmann (1973) found similar enrichment of mucous aggregates (derived from corals) with nitrogen over time by adsorptive processes. EPS, in addition to containing DOM from sea water, will also contain certain adsorbed excretion, secretion, and lysis products of the bacterium itself. These can include membrane lipids, proteins, cell wall turnover products, ATP, DNA and RNA, etc. The generalisation that exopolymer is just carbohydrate (and therefore could represent only an energy source for consumer animals) is much too simplistic for natural conditions and may be largely an artifact of compositional analyses of exopolymer derived from laboratory conditions. The extent to which adsorptive processes influence the composition of EPS requires further investigation. This is important from both a trophic standpoint and in the understanding of flux processes. Perhaps the use of membrane filter chambers, similar to those of McFeters & Stuart (1972) or Crumpton & Wetzel (1982), can be used to examine adsorptive processes of EPS under natural conditions (by isolating EPS within the chambers and excluding microbial cells, thus allowing only DOM to interact with the EPS within). The role of adsorptive processes in determining EPS compositions is ultimately important in understanding EPS as a nutritional resource for animals. Physical structure of capsular and slime EPS Bacterial EPS is a highly hydrated polymer matrix, approximately 99% water by weight (Sutherland, 1972, 1977a). The EPS produced ranges from discrete tight capsules closely surrounding the bacterial cell (Platt, Geesey, Davis & White, 1985) to loose slime which is not in close association with any given cell. When these capsule and slime matrices are observed in closer detail, the fibrous nature of the large polysaccharides becomes readily apparent (Marshall, Stout & Mitchell, 1971; Fletcher & Floodgate, 1973; Costerton, 1980). In bacterial capsules these fibres are arranged in a tightly-wound matrix at the cell surface. This was confirmed only after special techniques were developed for electron microscopy (EM) (see p. 106 ). In many bacteria, capsules are formed only during the exponential (i.e. log) phase of growth (Sutherland, 1977a; Christensen, Kjosbakken & Smidsrod, 1985). The size and thickness of the capsule varies depending on the species (Costerton, Irvin & Cheng, 1981), culture conditions (Baker & Kasper, 1976), and age (Costerton, Damgaard & Cheng, 1974). Tight capsules can range in thickness from 10 2 to 10 4 nm beyond the cell wall (Sutherland, 1977a). The distinction between capsule-EPS and other cell-surface polysaccharides is not
94
ALAN W.DECHO
always clear. The capsule may change in its consistency and other properties from the inner (i.e. near cell portions) to outer portions (Neu & Poralla, 1988). These differences may reflect gradual compositional changes in polymer further from the cell surface. Some bacteria secrete EPS capsules early in growth and loose slime later on, while other bacteria produce only slime. In bacteria which secrete tight capsules, a slow dissolution of the capsule may occur as the cell proceeds from log to stationary phase. The capsule becomes more loosely associated, eventually becoming slime. Not all bacterial cells will possess a capsule by the late senescent phase (Sutherland, 1977a). It has been speculated that if capsules (during exponential phase) serve protective functions to the cell (i.e. against digestion, desiccation, or micro-environmental changes), these protective effects should diminish as the cell reaches later (i.e. stationary and senescent) growth phases. Such processes may be of trophic significance to both microbial and grazer populations (see p. 128 ). Role of ions in the structural integrity of EPS The structural integrity which gives mucous-exopolymer its gel-like consistency is largely governed by the tertiary interactions of adjacent polysaccharide chains. Divalent cations such as Ca ++ and/or Mg ++, commonly found in sea water, are thought to act as ionic bridges which form cross-links between adjacent sugars on different chains (Rees, 1969, 1972a, b; Fletcher, 1980a). A high degree of cross-linking can result in the tight fibrous matrix observed in bacterial capsules. If bacteria are transferred to cation-deficient media, a rapid disruption of these secondary polymers results (Fletcher & Floodgate, 1976). Additions of Ca ++ and other divalent cations will restore the gel-like consistency of extracted EPS in diatoms (Lewin, 1956), and in some bacterial EPS (Smidsrod, 1974; Williams, Wimpenny & Lawson, 1979; Decho & Moriarty, in press). This suggests that conformational changes which cause gel formation are mediated by cations (Dea, McKinnon & Rees, 1972; Rees, 1972b). Mg ++ appears to have a similar role in EPS structure (and synthesis), as determined using cell free extracts in Streptococcus pneumoniae (Smith, Mills & Bernheimer, 1961). Also, the general addition of salts (which contain Ca and Mg ions) at extreme pHs resulted in the gelling of EPS extracted from intertidal bacteria (Boyle & Reade, 1983). Ca ++ ions are necessary for the adhesion of both marine bacteria (Marshall et al., 1971; Fletcher & Floodgate, 1973) and diatoms (Cooksey, 1981). In diatoms grown in Ca-deficient media, attachment to surfaces (via EPS) does not occur (Cooksey, 1981). This is because Ca ++ is used both intracellularly, in the transport and secretion of EPS-containing vesicles (as evidenced using Ca-specific transport inhibitors), and extracellularly, as a cross-linking agent. The latter occurs between localised negative charges in the EPS chains (as evidenced by addition of a Caspecific chelant ethylene-bis(oxyethylenenitrilo)tetraacetic acid EGTA) which specifically removes Ca ++ and causes some dissolution of diatom biofilms (Turakhia, Cooksey & Characklis, 1983; Cooksey & Cooksey, 1986). Lanthanum, which inhibits Ca ++ transport into cells, also inhibits diatom adhesion (Cooksey & Cooksey, 1980). While divalent cations (i.e. Ca++ and Mg++) are typically abundant in natural sea water, they can be limiting in freshwater systems. Fletcher (1988) has recently
MICROBIAL EXOPOLYMER SECRETIONS
95
suggested that the attachment mechanisms of bacteria in fresh-water compared with marine systems may differ due to the inherent presence or absence of specific cations in these systems. How the structural integrity of freshwater EPS is maintained (with very low levels of these cations) will provide an interesting comparison with marine systems. Attachment of EPS capsule to bacterial cell How the EPS capsule is attached to the bacterial cell has remained somewhat of a paradox. Some earlier studies have suggested that linkage of capsular material to cells is accomplished via lipopolysaccharides (LPS) in gram-negatives and techoic acids in gram-positives. LPS are highly branched, complex polysaccharides linked to a glucosamine-containing lipid (Osborn, 1963). The small amounts of LPS often found in bacterial slime have been presumed, by some, to represent contaminating material which has been ripped off the cell surface during extraction of the capsule. LPS, however, is also known to be lost during exponential growth by various bacteria (Rothfield & Pearlman-Kothencz, 1969). Also, removal of capsules in Escherichia coli requires phenol extraction, and is alkali labile (Jann et al., 1968). Such evidence suggests that the linkage of the EPS capsule to the bacterial cell is between the carboxyl groups of EPS uronic acids and the hydroxyl groups of LPS monosaccharides anchored in the cell itself (Sutherland, 1977a). A second possibility involves the covalent attachment of the capsule to the cell wall via specific proteins (Brautigam et al., 1988). Both hydrolysis of the peptidoglycan (i.e. cell wall) by muramidase or hydrolysis of protein by pronase removes the bacterial capsule. Glycoproteins have also been suggested in this regard. The glycocalyx capsule can be divided into two types: (1) an S-layer which is composed of a regular array of glycoprotein subunits immediately at the cell surface; and (2) the exopolymer capsule itself (Costerton et al., 1981). The linkage of S-layer glycoproteins to the cell wall by divalent cations (Chester & Murray, 1978) has been suggested to constitute a general mechanism by which capsules are attached (Costerton et al., 1981). A third possibility, based on studies of E. coli, suggests membrane phospholipids as the component which bind exopolymers to the cell surface (Gotschlich et al., 1981; Schmidt & Jann, 1982). Finally, Bayer & Thurow (1977) have observed knob-like structures (in electron micrographs) of unknown origin in E. coli capsules and have suggested their role in the attachment of the capsule to the cell. The exact attachment mechanism(s) of the capsule to the cell is still under investigation. While much of the available evidence supports the LPS-mediated mechanism, attachment mechanisms may differ depending on the organism under study.
MOLECULAR REGULATION
Mucoid colonies of bacteria can give rise to non-mucoid colonies (i.e. phase variation) and the reverse phenomenon is also possible. This suggests that the biosynthesis of EPS can be regulated and altered by the environment in which the cells exist (Markovitz, 1977). Genetic regulation, however, does play a role in the ability (or inability) of a bacterium to produce EPS capsules (Avery,
96
ALAN W.DECHO
MacLeod & McCarty, 1944; McCarty, 1946) and the amount of EPS produced (Whitfield, 1988). Very early, it was demonstrated that a non-encapsulated form of a bacterium could be transformed to a capsulated form via an unknown transforming agent (i.e. DNA) transferred from the capsulated form. Nonencapsulated mutants of many strains of bacteria have since been isolated and have demonstrated the role of the bacterial genome in capsular production (Hacking, Taylor, Jarman & Govan, 1983). The direct genetic control under which many proteins are synthesised, however, is not typically found for exopolysaccharide synthesis. Therefore, variations in the composition of EPS occur from molecule to molecule (Aspinall, 1982b). Very basically, genetic control is through DNA coding for enzymes used in various stages of the synthesis and assembly of EPS; the mechanisms vary depending on the strain (Markovitz, 1977). Whether these groups of genes are located close together in the genome and function as an operon, is still under investigation. In E. coli K1, the EPS genes are clustered at one locus of 15 kb which codes for up to 12 gene products (Silver, Vann & Aaronson, 1984). In Pseudomonas aeruginosa, which causes cystic fibrosis in humans, the ability to produce mucoid colonies appears to be controlled by a regulator gene (Deretic et al., 1989). This regulator gene positively controls a biosynthetic gene for EPS production. Furthermore, it is responsive to certain ‘environmental’ conditions such as specific compounds in the media, osmotic pressure, phosphate limitations, etc. Under stressed conditions certain EPS genes are amplified resulting in EPS production. Thus, the production of mucous-EPS by this bacterium may relate to specific environmental conditions to which regulator genes respond and begin transcription of biosynthetic genes for EPS production. Other molecular mechanisms, however, may be used in controlling EPS production. The genes which code for EPS production may be carried by special movable structures of DNA called transposons. The presence of small DNA sequences, called insertion elements, enables the gene to move readily between the bacterial chromosome and plasmid DNA when they attach at either end of the gene. It has recently been shown that the ability of the common marine bacterium P. atlantica to produce EPS may be controlled by insertion elements (Bartlett, Wright & Silverman, 1988). The insertion of such elements into a specific portion of an EPS gene turns off the ability of the bacterium to produce EPS. Removal of this same element once again activates EPS production (Bartlett & Silverman, 1989). Such molecular mechanisms may be important in the attachment and survival of marine bacteria in changing environments. The genes involved in the production of several capsular polysaccharides have been cloned in Escherichia coli (Roberts et al., 1986) and techniques using recombinant DNA technology are now cloning polysaccharide adhesive viscous exopolymer (PAVE) genes from marine bacteria in order to increase EPS yields for industrial processes (Weiner et al., 1985).
BIO-SYNTHESIS OF EPS
Understanding how EPS is synthesised is important to our later comprehension of how its composition varies under natural conditions. Production of EPS appears to be regulated at several levels such as the genetic level (see above), the physiological level, the precursor and lipid-intermediate level (see Whitfield, 1988; for review).
MICROBIAL EXOPOLYMER SECRETIONS
97
Influence of physiological conditions The first site at which control of synthesis can take place is that of nutrient uptake (Sutherland, 1979). In general, optimal yields of EPS are obtained in the presence of a high carbohydrate substrate (i.e. usually glucose, to a lesser extent fructose, sucrose) (Sutherland, 1972). Optimal yields occur at 2% (w/v) glucose, but the efficiency of conversion of substrate to polymer is best at slightly lower concentrations for some bacterial species (Sutherland, 1979). Conversion efficiency can be an important consideration when labelling EPS using 14C-glucose, and when obtaining a high specific activity of the polymer is a priority. Carbohydrate (used as a carbon substrate to synthesise EPS) enters the cell primarily through (1) active transport systems (where the substrate enters the cell unaltered) or (2) group translocation systems (where phosphorylation of the substrate occurs). Both of these processes require energy (Kornberg, 1976). Several uptake mechanisms can exist for each substrate (Sutherland, 1977b). Therefore, in some bacteria the rate of EPS production can be influenced by the source of the carbon substrate used (i.e. glucose, fructose, mannose, sucrose, succinate, gluconate, xylose, glycerol, ethanol, etc.). For example, highest rates for Zoogloea (Parsons & Dugan, 1971) occur using a glucose substrate. EPS synthesis occurs through all growth phases in many bacteria (Sutherland, 1977b). Highest EPS production for most strains of Pseudomonas begins, however, during the late log phase and continues through the stationary phase (Williams & Wimpenny, 1977, 1978). This excess late-stage production is typical of many marine bacteria. For bacterial-EPS synthesis, two distinct modes of polysaccharide synthesis can be distinguished: (1) they may be produced entirely by extracellular formation from specific precursors in the extracellular environment, or (2) they may be produced by intracellular-extracellular formation utilising precursors formed intracellularly and being assembled largely near the cytoplasmic membrane. In the first group (extracellular formation), EPS is synthesised essentially outside of the cell from precursor disaccharide sugars (mainly sucrose). The EPS produced are characteristically homopolysaccharides such as dextrans and levans. This type of EPS synthesis involves extracellular transferase enzymes but does not require activated precursor molecules (such as nucleoside diphosphate sugars) or lipid intermediates. The formation of extracellular EPS, however, is dependent on the presence of specific substrates such as sucrose and other oligosaccharides (Sutherland, 1977b). Because this type of EPS synthesis is of very limited occurrence in marine bacteria (mainly grampositive cocci) it will not be considered any further here. The second group (intracellular-extracellular formation) occurs in a wide variety of bacteria and produces heteropolysaccharides with specific chemical compositions confined to prokaryotes. This type of EPS is synthesised at the cytoplasmic membrane utilising activated precursor and carrier molecules (nucleotide diphosphate sugars and isoprenoid lipid intermediates) which are formed intracellularly. After formation and partial assembly, the EPS chains are extruded into the extracellular environment where further elongation may occur. In this type of synthesis, the polymers synthesised are structurally independent of the growth substrate employed, although their actual production is dependent on the physiological conditions. This mechanism, although more generally distributed than the first, requires a significant amount of energy expenditure by the bacterium (Jarman & Pace, 1984).
98
ALAN W.DECHO
The second level at which EPS synthesis can be regulated occurs at the immediate precursor level (i.e. sugar nucleotides). In order to produce EPS, of the second type (i.e. heteropolysaccharides) certain precursors called sugar nucleotides play an important role in synthesis (Norval & Sutherland, 1969). These precursors, which act as monosaccharide donors, include nucleoside diphosphate sugars such as UDPglucose, UDP-galactose, and UDP-glucuronic acid. The membrane functions as the site of synthesis for three distinct precursor macromolecules: UDP-N-acetylglucosamine, used in synthesis of peptidoglycan (cell wall), lipopolysaccharide and EPS. Because glucose and galactose are found in lipopolysaccharides and EPS is derived from UDP-glucose and UDP-galactose, respectively, there is probably a system of priorities within bacterial cells to ensure that peptidoglycan synthesis (for cell walls) occurs first, then lipopolysaccharide and finally exopolysaccharide synthesis. Regulation at the level of enzyme activity (i.e. control over enzyme synthesis) can also occur (Sutherland, 1979). Isoprenoid alcohols (IP) are another important group of precursors. These molecules play a role in the synthesis of EPS polysaccharide and other polymers in which there is a regular repeating oligosaccharide structure (i.e. as cell wall components or components external to the bacterial membrane). IP act as glycosyl carrier lipids and are important intermediates interacting with the nucleoside diphosphate sugars. The IP act as a transferase in the movement of monosaccharides from nucleoside diphosphates (Norval & Sutherland, 1969; Troy, Frerman & Heath, 1971).
Site of EPS synthesis In gram-negative bacteria, synthesis of lipopolysaccharides occurs at the inner membrane. Once the polysaccharide portion is located near the outer membrane, no further monosaccharides are added, even if the polysaccharide is incomplete (Osborn, Gander, Parisi & Carson, 1972). A majority of the available evidence suggests that synthesis of EPS also occurs at the inner membrane because isoprenoid alcohols are located there, and nucleoside diphosphate sugars (NDS) are required there (some NDS are produced in the cytoplasm and others by membrane bound enzymes) (Sutherland, 1977b). Export of EPS out of the cell (at least in Escherichia coli) may occur by porin proteins, such as protein K (Sutcliffe, Blumenthal, Walter & Foulds, 1983). These proteins allow the diffusion of hydrophilic molecules across the outer membrane barrier. Their presence is correlated with capsular EPS. Why some bacterial cells tend to produce increased amounts of EPS at the end of the exponential growth phase (and at lower temperatures) is not fully understood, but is likely to result via regulatory mechanisms controlling precursors rather than altered enzymatic activities (Sutherland, 1977b).
DIATOM AND MICROALGAL MUCILAGE
Composition The specific compositions of diatom and algal EPS have been characterised to a much lesser extent than bacterial EPS. Compositional studies have been conducted on
MICROBIAL EXOPOLYMER SECRETIONS
99
several types of diatoms, micro- and macroalgal mucilages, for a comprehensive review on compositions of both microalgal and macroalgal EPS, see Painter (1983). In diatoms the EPS polysaccharides consist of heteropolymers. These contain a wide variety of simple sugars such as galactose, mannose, arabinose, glucose, fucose, ribose, xylose, and rhamnose (Lewin, 1956; Allan, Lewin & Johnson, 1972). Uronic acids (such as glucuronic acid) can also be found (Huntsman & Sloneker, 1971; Allan et al., 1972; Chamberlain, 1976). Sulphate groups (Huntsman & Sloneker, 1971; Allan et al., 1972; Myklestad, Haug & Larsen, 1972; Crayton, 1982) and phosphate groups (Daniel, Chamberlain & Jones, 1980) are present in some diatom EPS. Protein may be present in some diatom EPS (Lewin, 1958; Paulsen, Haug & Larsen, 1978) but conspicuously absent in others (Chamberlain, 1976; Daniel et al., 1980). In addition to the capsule immediately surrounding the diatom cell (Lewin, 1955; Handa, 1969; Yokote, Honjo & Asakawa, 1985), many diatoms secrete further EPS mucilage for movement (Characklis & Cooksey, 1983; Edgar & Pickett-Heaps, 1984; Paterson, 1989), adhesion (Chamberlain, 1976; Daniel et al., 1980; Round, 1981; Vos, De Boer & Misdrop, 1988), tubes (Paulsen et al., 1978), etc. The composition of the EPS may vary somewhat depending on their function (Characklis & Cooksey, 1983). In general, diatom EPS production appears to increase during the stationary phase and under media conditions with limiting nutrients such as nitrogen or phosphate (Myklestad, 1974; Kroen & Rayburn, 1984). In various species of Chaetoceros, extra-cellular production of mucilage can be 40 mg·l -1 of growth medium (Myklestad & Haug, 1972) and up to 1.25 times greater than intracellular carbohydrate (Myklestad, 1974). The salinity of the media may also affect the composition and properties of the resulting EPS (Allan et al., 1972).
Synthesis In diatoms, the synthesis of EPS has been summarised by Cooksey & Cooksey (1986). In diatoms and microalgae, mucilaginous (EPS) substances have long been implicated in their attachment. Only recently, however, have the fine structural mechanisms been studied. Adhesive EPS are internally synthesised and contained in vesicles. These vesicles are produced in the dictyosome of the Golgi apparatus and contain polysaccharide-like material (Daniel et al., 1980). They are transported to the cell membrane and secreted through longitudinal channels in the diatom frustule called raphe (Daniel et al. , 1980). The mechanism of transport is still uncertain but perhaps occurs by microtubules (Webster, Cooksey & Rubin, 1985). The secretion of EPS-containing vesicles allow attachment of the diatom to surfaces (Webster et al., 1985), and also facilitates movement of the frustule. In diatoms, exudation of EPS is also a function of the physiological state of the algae, nutrient levels of the surrounding water, and various environmental factors (i.e. light, temperature, turbulence, etc.). Generally, net growth is dependent on the availability of limiting nutrients, generally nitrogen (Goldman, 1984). Cells can, however, be photosynthetically active even under low nutrient conditions if carbohydrates are being produced in excess of the structural demands of the cells. Excess carbohydrates are converted to reserve substances until cell storage depots are filled, after which they are respired or excreted as EPS (Smetacek & Pollehne, 1986).
100
ALAN W.DECHO
It has been suggested that in terms of ecosystems, a fundamental role of microbes is to burn excess energy contained in carbohydrates that would otherwise accumulate and tie up essential elements (Smetacek & Pollehne, 1986). This excess energy needs to be consumed in order to re-cycle the limiting resource.
METHODOLOGIES FOR ANALYSIS OF EXOPOLYMERS
ANALYSIS OF EPS FROM NATURAL SYSTEMS
The isolation and quantification of exopolymers from natural systems represents a most important step in accessing their potential availability, composition, and relevance to natural systems. There is, however, no single quantitative method which can accurately and precisely estimate exopolymer biomass under all situations. The most precise method available so far, is based on quantifying the uronic acid content (Fazio, Uhlinger, Parker & White, 1982), a component of most marine microbial exopolymers. This method measures amounts of each uronic acid in each carbohydrate with high sensitivity. While it is difficult to recover uronic acids quantitatively from polysaccharides, this method overcomes many of the previous technical problems (Fazio et al., 1982). It is, however, lengthy and requires substantial technical expertise. Under certain conditions, this method may slightly overestimate (or under-estimate) amounts of EPS because uronic acids are also found in polysaccharide polymers of higher plant cell walls, in gram-positive microbes grown under phosphate limitation, and in some gram-negative microbial lipopolysaccharides (Fazio et al., 1982). Using this method, Uhlinger & White (1983) conservatively estimated the EPS content to equal or exceed the biomass of the resident microbial flora in sediments. They also found that the uronic acid content of EPS increased with its age. This may have been due to the persistence of uronic acids relative to other (more degradable) components. The carbon portion of EPS of bacteria is known to be degraded relatively quickly in sediments (Henrichs & Doyle, 1986). Exopolymers are thought to be largely carbohydrate, so methods for measuring carbohydrates can potentially be used to estimate exopolymer concentrations. An example of such techniques is the anthrone test (Spiro, 1966) (which analyses carbohydrate concentrations). This method, however, only detects carbohydrates composed of six-carbon sugars (Paerl, 1975) and some exopolymers may contain significant amounts of ribose and pentose (i.e. five-carbon) sugars. Under such conditions, this method will under-estimate EPS concentrations. Also, the EPS must be quantitatively separated from other carbohydrate-containing material prior to analysis. Otherwise, cellular, dissolved and detrital debris, which also contain carbohydrates, may act as ‘contaminants’ and lead to over-estimates of EPS concentrations. The phenolsulphuric acid method (Dubois et al., 1956), generally considered more sensitive than the anthrone method, measures exopolymer in glucose equivalents. This method measures most sugars, including methylated sugars, pentoses, and structural carbohydrates (i.e. cellulose) and sugar storage compounds (i.e. starch). Similarly, however, it requires the prior
MICROBIAL EXOPOLYMER SECRETIONS
101
quantitative separation of EPS from cellular and detrital material (Brown & Lester, 1982). Grant, Bathmann & Mills (1986), using this method, estimated that diatom-EPS in surface sediments represented about 20% of the microalgal carbon present. While the quantitation of exopolymers is an important aspect in accessing their role in natural systems, it is also of interest to quantify the potential capacities of exopolymers to adsorb DOM and metals. The binding capacity of specific organic materials in natural sediments is difficult to quantify (Luoma & Davis, 1983). Recently, Smith & Geesey (1989) have been developing a method to measure polymeric pyruvate concentrations quantitatively in sediments using high-pressure liquid chromatography (HPLC). This is based on analysing ketallinked pyruvates, which commonly occur in bacterial and microalgal exopolysaccharides. Because the free carboxyl group on the a-keto acid is free to react with positive-charged molecules, the method potentially provides a means for measuring the adsorptive capabilities of exopolymers for certain metals (and organic compounds) in natural systems. In general, techniques for quantitatively measuring exopolymer under natural conditions are difficult to develop from both a theoretical and practical standpoint. In both theory and practice, the composition of EPS is variable. This makes it difficult to assay for a particular “signature molecule” (sensu White, 1986) which is present in constant amounts in all EPS, but is not found in other organic material. Perhaps the application of non-invasive techniques such as magnetic resonance imaging (MRI), and infrared spectroscopy (see below) may circumvent some of these problems.
ISOLATION OF BACTERIAL EPS FROM LABORATORY CULTURES
For the study of EPS as a food resource for consumers, the EPS produced by laboratory-grown strains can provide much information about the mechanics of EPS utilisation by consumer animals. While conditions (nutrient concentrations, the age of the cells producing EPS, and other factors) can be closely controlled, it is important to realise that EPS produced under natural conditions will be considerably variable in its composition and properties. Ideally, procedures for the isolation of EPS from microbial cultures should separate the cellular portion from the EPS portion without disruption or lysis of the microbial cells or denaturing the EPS. Procedures for isolation of EPS from bacterial cells in culture vary slightly depending on the purpose of the subsequent analyses (i.e. isolation of loose slime compared with capsules; characterisation of chemical composition, structure, etc.) (Corpe, 1970; Parsons & Dugan, 1971; Pavoni, Tenny & Echelberger, 1972; Evans & Linker, 1973; Tago & Aida, 1977; Williams & Wimpenny, 1978; Sutherland, 1979; Brown & Lester, 1982; Novak & Haugan, 1981; Aspinall, 1982b; Norberg & Enfors, 1982; Rudd, Sterritt & Lester, 1982; Boyle & Reade, 1983; Platt et al., 1985; Tosteson, 1985; Kennedy & Sutherland, 1987; and others). Analysis of the specific chemical structure of exopolysaccharides often require highly purified forms of EPS. Additional steps in extraction procedures must be followed to avoid contamination or alteration of the polymer. For most purposes, however, these additional steps are not necessary. While they are briefly noted here, more detailed explanations have been provided by Aspinall (1983).
102
ALAN W.DECHO
To begin EPS extractions, bacterial cultures are harvested in the appropriate growth phase (i.e. usually the stationary phase) in which the EPS is to be studied. The addition of 0.5% formalin (final concentration) to the culture will reduce leakage of intracellular contents (Sutherland & Wilkinson, 1971). Exopolymers are highly hydrated molecules, so their density will be close to that of the surrounding media. Therefore, centrifugation can be used to separate the EPS which will remain in the supernatant, from the denser cells and debris which will collect in the pellet. Centrifugation at 30 000 plus g for 30 min or longer will generally provide shear forces sufficient to remove most exopolymer from cells (Brown & Lester, 1982). Strains which produce a very viscous slime may, however, require more prolonged (i.e. for 2–3 h) or multiple centrifugations (Sutherland & Wilkinson, 1971; Kennedy & Sutherland, 1987). Multiple centrifugations, resuspending the original pellet each time, will increase the shear forces on the cells (Rudd et al., 1982). Ultrasonification (Norberg & Enfors, 1982) can also be used to separate EPS from the cellular fraction (prior to centrifugation), if cell lysis is not a concern. The supernatant containing EPS is then collected, and the pelleted cells and debris removed. Further centrifugation of the supernatant for prolonged periods (3 h) can be used to remove small cellular debris, if extreme purity is required for later analyses. The collected supernatant will also contain residual media components and various low-MW dissolved compounds excreted by the bacterial cells. Subsequent purification steps can be used to remove these components. Tight capsular EPS To remove firmly bound EPS-capsules, centrifugation alone, even at high shear forces, is often not sufficient (Pazur & Forsberg, 1980). Addition of ethylenediaminetetraacetic acid (EDTA) followed by blending and centrifugation is most effective. EDTA complexes with the divalent (metal) cations (Ca++ and Mg++) which are thought to bridge adjacent polysaccharide polymer chains in the formation of tight capsules (Mian, Jarman & Righelato, 1978). EDTA, however, has been shown to rupture cell membranes at high concentrations (Cheng, Ingram & Costerton, 1970), and to remove lipopolysaccharides from gram-negative bacterial cell envelopes (Gray & Wilkinson, 1965). Platt et al. (1985), in examining a freshwater bacterial strain, used EDTA (10 mM; final concentration) and found minimal cell lysis and contamination of EPS from cellular components. They monitored cellular leakage by measuring the intracellular enzyme glucose-6-phosphate dehydrogenase activity in the supernatant containing the EPS (Lessie & Vander Wyk, 1972). In marine bacteria, higher concentrations of EDTA must be used to overcome the binding of EDTA to metal ions naturally present in sea water. Decho & Moriarty (in press) found minimal (<4.0%) cell leakage using concentrations not greater than 0.04 M EDTA. If intracellular contamination is a concern, however, then leakage should be monitored periodically and certainly with each new extraction procedure. Isolation of polysaccharide The large polysaccharides, which characteristically make up EPS, and molecules closely associated with them (such as glycoproteins, certain lipids, etc.), can be
MICROBIAL EXOPOLYMER SECRETIONS
103
precipitated in cold alcohols. Subsequent purification involves multiple extractions using cold (0°C) ethanol (or methanol, or propanol) approximately 70–80%, alternately washing with distilled water (i.e. dissolving in distilled water or a suitable buffer, for 1–2 h). This will remove low-MW components such as the many adsorbed compounds, amino acids, free glucose, small lipids, nucleosides, and much of the salt and EDTA (if present from previous extraction steps). Quantitative precipitation of EPS in cold alcohols takes several (8–12) hours. Shorter amounts of time may significantly reduce the final yield of EPS. A precipitate is produced which is white to light brown in colour. This can be pelleted by light centrifugation. It is important to note that degradation of polysaccharides (via cleavage of glycosidic bonds) occurs in acidic conditions (Aspinall, 1982b) and should therefore be avoided. Dilute alkaline conditions may also cause some structural modifications (Aspinall, 1982b) which may or may not be pertinent to the investigator. Other compounds, such as ammonium sulphate (60%), have been used to precipitate polysaccharides (Sar & Rosenberg, 1989). These and other procedures of extraction have been reviewed by Troy (1979). Removal of protein Proteins in EPS can exist in a variety of forms. For example, extracellular enzymes in various stages of degradation, glycoproteins, and adsorbed polypeptides are often found associated with EPS. Adsorbed low-MW polypeptides are generally removed in the previous ethanol extraction step. Large forms of protein can be removed by successive extractions with chloroform: butanol: water (25:5:1) (Sevag, Lackman & Smolens, 1938), hot phenol (Rubinovitz, Gutnick & Rosenberg, 1982), or protease digestion (Spiro, 1976). In order to extract protein without destruction of its activity (i.e. for further analysis of the protein), hot phenol extraction is recommended (Rubinovitz et al., 1982). The extent of protein removal from the EPS can be quickly monitored by absorbance profiles at 280 nm (Evans & Linker, 1973; Platt et al., 1985). Other, more quantitative methods using chemical-spectrophotometic procedures, include: the bicinchoninic acid (BCA) assay (Sigma Chem. Co.) of Smith, Cabot & Foreman (1985); the Lowry method (Lowry, Rosebrough, Farr & Randall, 1951); and the Coomassie Brilliant Blue dye-binding method (Bio-Rad. Lab.) according to Bradford (1976). It should be noted that complete removal of protein from bacterial EPS is often difficult without substantial losses of polysaccharide components (Humphrey, Dickson & Marshall, 1979; Platt et al., 1985). This is also the case for microalgal EPS (Kieras, Roden & Chapman, 1977). Incomplete removal of protein probably results because a portion of the protein (i.e. glycoprotein) consists of protein segments covalently bonded to the numerous polysaccharide branches tightly wound about the protein (Kieras et al., 1977; Platt et al., 1985). In all the procedures listed above which utilise organic solvents, dialysis should be subsequently used to remove trace residues of the organic solvent (Platt et al., 1985). The purified EPS can then be concentrated by lyophilisation or rotary evaporation at low temperatures (i.e. 40°C). Removal of lipid
104
ALAN W.DECHO
While ethanol extractions will remove a variety of small lipids from EPS, additional extractions using an equal volume of ether can be used for more complete removal of lipid from exopolymer solutions (Platt et al., 1985). Similarly, chloroform: methanol extractions can be used (Bligh & Dyer, 1959). Labelling and Isolation of
14
C-labelled EPS
Optimal incorporation of labelled substrates, such as U- 14C-glucose, into bacterial EPS can be accomplished by first growing the bacterial cells in high-C: low-N media (0.5–1.0% w/v glucose; 0.5 g·1 peptone -1; 0.1 g·1 yeast extract -1) to their late log phase or early stationary phase of growth. At this time 14C-glucose (100 µCi to 5 mCi·100 ml culture -1 depending on the specific activity one needs to attain) is added. The culture is harvested at the stationary phase and extracted. While optimal yields of EPS occur at 1–2% (w/v) glucose, the efficiency of conversion of substrate to polymer is best at slightly lower concentrations for some bacterial species (Sutherland, 1979). By reducing the free glucose content of the fresh media to 0.5%, a high conversion efficiency of 14 C-glucose can occur while still attaining a high polymer production. Because the 14C-glucose is added when the cells have already reached the stationary phase, no significant increase in cell numbers should occur and incorporation of 14 C-label into extracellular components should be most efficient. Conversation efficiency is an important consideration when obtaining a high specific activity of the polymer is a priority. The 14C-EPS can then be isolated and extracted with a high specific activity. 14Clysine may be used in a similar manner specifically to label EPS proteins (Rubinovitz et al., 1982). The specificity of the labelling can be checked by examining the label present in subsamples of the EPS after hot phenol extraction (which removes protein). The use of other radiolabels such as 3H-tracers can provide a higher specific activity of the EPS; much of the label will, however, be lost by simple desorption of the 3 H-ion during ionic and pH changes used in subsequent extraction and purification steps.
ISOLATION OF DIATOM EPS
For extraction of diatom and microalgal exopolymer, slightly different methods have been used, depending on the purpose of the extraction. Most of these methods initially extract both intracellular and extracellular components (Lewin, 1955; Lewin, 1958; Lewin, Lewin & Philpott, 1958; Huntsman & Slonecker, 1971; Allan, Lewin & Johnson, 1972; Evans, Callow, Percival & Fareed, 1974). Cells are first centrifuged (23000 g, 15 min.), to remove culture media and water soluble components. This supernatant will also contain ‘dissolved’ EPS-slime which is highly water-soluble. This can be easily precipitated with cold alcohols after concentration by freeze drying or rotary evaporation (40°C). Mucilaginous capsules and coatings on the diatoms, due to their ‘gel-like’ state, are more difficult to remove and will be retained with the pelleted cells. These capsules have been subsequently water-solubilised using potassium chloride (Huntsman & Sloneker, 1971) or EDTA, then removed using hot water (Evans et al., 1974) or dissolution in 20% (w/v) NaOH (Lewin, 1955). The success of a given method for the removal
MICROBIAL EXOPOLYMER SECRETIONS
105
of a mucilaginous capsule appears dependent on the species of diatom from which the polymer is being extracted. Highest yields of EPS are generally found in stationary phase culture, therefore, labelled substrates (i.e. NaH 14CO ) should be 3 added at the late log or early stationary phase to ensure maximal incorporation of the radiolabel into the exopolymer. It should be realised that the method(s) used to isolate and purify the EPS should ultimately depend on the purpose(s) of the study. For example, if examination of EPS as an energy (i.e. carbon) source is required, then removal of protein (i.e. nitrogen-containing) components from EPS might be warranted. If examination of only high-MW components is needed, then ethanol extraction (to remove low-MW components) followed by dialysis using a suitable pore size might be used. If one wishes to examine EPS (complete with adsorbed components) then simple centrifugation (which provides the least modification of the polymer) can be used. The methods used to isolate EPS for later feeding experiments or analysis should be carefully considered a priori because they will ultimately influence its purity and composition.
FEEDING EXPERIMENTS USING EXOPOLYMERS
To examine ingestion and assimilation of EPS in feeding experiments, 14C-labelled EPS have been precipitated around a variety of particles depending on the size of the animals and the manner is which it feeds. For example, labelled EPS was precipitated around sand grains (Baird & Thistle, 1986) to mimic the EPS slime coatings which often cover sediments. This was then used in feeding experiments with large deposit-feeding holothurians, which typically ingest large amounts of sediment. For feeding experiments using smaller meiofauna-sized animals (harpacticoid copepods) which may ingest individual diatoms or groups of bacteria, labelled bacterial EPS was precipitated around bacterium-sized beads (Decho & Moriarty, in press) to mimic the extracellular capsule material surrounding a bacterial cell. Harvey & Luoma (1984) examined ingestion and incorporation of both dissolved and sediment-bound forms of exopolymer by the suspension-feeding clam Macoma balthica. To verify the ingestion visually and to measure gut retention times of mucus-EPS by grazer organisms, stains such as Neutral red (Fleming & Coughlan, 1978) have been used to label mucus (secreted by reef corals) and follow its subsequent ingestion by zooplankton (Gottfried & Roman, 1983). Also, fluorescently labelled EPS (i.e. dextran) has been directly added to water containing protozoan grazers. Subsequent observations of the protozoans nicely demonstrated their uptake of the fluorescently labelled polymer (Sherr, 1988).
USE OF LIGHT AND ELECTRON MICROSCOPY TO EXAMINE EPS
The use of scanning (SEM) and transmission electron microscopy (TEM) has greatly increased our resolution for examining microbial processes in the marine environment. Exopolymers have been observed using both TEM (Marshall, Stout & Mitchell, 1971; Fletcher & Floodgate, 1973; Marshall, 1976b; Corpe, Matsuuchi & Armbruster, 1976; Moriarty & Hayward, 1982) and SEM (DiSalvo & Daniels, 1975; Paterson, 1989). Most preparative techniques for EM,
106
ALAN W.DECHO
however, involved the dehydration of the material to be observed. Bacterial cell walls, diatom frustules, and chitin- or cellulose-containing material are not greatly altered by these preparations. Because EPS is highly hydrated significant deformation occurs during preparation for EM with much of its three-dimensional structure being lost (Chang & Rittman, 1986). Special adjustments in preparation must be made such as antibody stabilisation and lectin-binding (see Costerton, 1980) and these have been discussed in detail by Roth (1977). These special techniques overcome the major collapsing, physical deformation and other artifacts which typically occur due to the dehydration procedures necessary for most EM preparations (Bayer & Thurow, 1977; Mackie, Brown, Lam & Costerton, 1979; Chan, Acres & Costerton, 1982). Recently, low-temperature SEM has been used to observe diatom EPS relatively intact (Paterson, 1989). Samples are kept frozen (using liquid nitrogen), so they can be observed in a vacuum using SEM while in a partially hydrated state. Such methods can be very useful for observing exopolymers in natural sediments and aggregates because a more realistic representation of their true three dimensional nature is observed. EM stains such as Ruthenium Red, are specific for polyanions and will readily stain mucopolysaccharides, polysaccharides, hyaluronic acid, glycoprotein, and proteoglycans (cited within Costerton, Damgaard & Cheng, 1974). These stains have revealed an abundance of extracellular material produced by marine bacteria under natural conditions (Jones, Roth & Sanders, 1969; Fletcher & Floodgate, 1973). Tetrazolium redox indicator salts, micro-autoradiography, and micro-electrodes have been used to analyse micro-environments created by EPS-bound microbial aggregates within sediments (Paerl, 1984a). Also, silver methanamine and silver proteinate, have been used to characterise microzones in sediments and the processes which occur within them (Foster, 1981). For light microscopy, the exopolymer capsules around bacteria can be easily observed using India ink (Duguid, 1951). This stain will allow the capsule size and thickness to be determined without deformation (Roth, 1977). Alcian blue (pH 2.5) is another useful stain because it will not distort the general structure of the capsules (Roth, 1977) and is specific to mucopolysaccharides with carboxyl groups (Chamberlain, 1976).
TECHNIQUES FOR FUTURE WORK
As new techniques are developed, increased resolution of EPS composition, structure, and interactions under natural conditions will be realised. For example, EPS composition can be examined with great detail using HPLC (Kennedy & Sutherland, 1987). The tertiary structure of EPS can now be examined using specific antibodies and other molecular markers (i.e. fluorescent lectins) against extracellular polysaccharides (Larson, Vreeland & Laetsch, 1985; Tosteson, 1985; Vreeland, Zablackis, Doboszewski & Laetsch, 1987). A variety of non-destructive techniques have been developed and employed in other areas of research which may prove very useful in future microbial research in marine systems, especially in the analysis of EPS under natural conditions. For example, laser light scattering methods can provide information on the physiochemical properties of EPS capsules (Tanaka, 1981), Fourier transforming infrared spectroscopy (Griffiths, 1977) techniques have been used to provide information about micro-environments within EPS biofilms (Nichols et al., 1985).
MICROBIAL EXOPOLYMER SECRETIONS
107
Nuclear magnetic resonance (NMR), now called MRI (i.e. magnetic resonance imaging) characterise EPS molecules and can follow chemical reactions as they occur within an EPS matrix (techniques reviewed by Jennings & Smith, 1978; Perlin & Casu, 1982; McFeters et al., 1984; Lahaye, Yaphe & Rochas, 1985; Nath & Chakraborty, 1987). These techniques have been used extensively in the chemical characterisation of microbial extracellular polysaccharides. MRI may prove to be a very useful tool in the future analysis of microbial communities and the chemical composition of their by-products. Other techniques, such as electron para-magnetic resonance, have been used to analyse the binding of copper to exopolymer capsular material secreted by microalgae (Vieira & Nascimento, 1988). Further advantages of these techniques are that they require only very small amounts of sample and are non-destructive, so intact samples can be examined and recovered for further analyses. In addition to these techniques, heterologous and monoclonal antibodies have been prepared for bacterial EPS and other polysaccharides (see Bishop & Jennings, 1982, for review; Zaidi, Bard & Tosteson, 1984; Zambon et al., 1984). Many of the above techniques are now being used extensively in other areas of research. Integrating these techniques into our analyses of marine systems will provide enhanced resolution in quantifying not only EPS-related processes, but also a variety of other microbial processes under natural conditions.
OCCURRENCE OF EXOPOLYMERS IN NATURAL SYSTEMS AND THEIR INTERACTIVE ROLES IN OCEANIC PROCESSES While EPS serves many important functions to microbial cells, their presence in large abundances also imparts substantial effects on local environments. Examination of bacteria growing in a wide variety of natural environments (especially marine sediments, detrital particles, and aggregates) (Paerl, 1973; Sieburth, 1975; Moriarty & Hay ward, 1982) has shown that a large portion of the cells are surrounded by extracellular secretions (Costerton, 1984). The fundamental importance of exopolymers in a wide variety of marine processes, is just being recognised. Their study is important to our understanding of several marine habitats (benthic systems on soft and hard substrata, water column, deep-sea hydrothermal vent systems, etc.), and is discussed below.
OCCURRENCE AND EFFECT OF EXOPOLYMERS ON SEDIMENTS
In marine sediments, most microbial flora are attached or in some way associated with sediment and detrital particles. While bacteria themselves may only represent a small part of the total organic carbon (TOC) in sediments (Moriarty, 1980; Cammen, 1980) their extracellular secretions may be considerably more extensive (DeFlaun & Mayer, 1983; Uhlinger & White, 1983). Quantitative estimates of exopolymer biomass in natural sediments are difficult to measure because of analytical limitations (see p. 100). Their concentrations can vary widely depending on the area sampled and the method of analysis used. Biomass estimations of
108
ALAN W.DECHO
exopolymers from certain marine sediments (Fazio et al., 1982) show their concentrations to at least equal and probably exceed the biomass of the microbial flora producing them (Uhlinger & White, 1983). Qualitative examination indicates that the presence of mucous coatings derived from bacteria and diatoms on intertidal sediments appear to vary seasonally, with increased concentrations during warmer months (DeFlaun & Mayer, 1983). When the intact structure of marine sediments has been preserved, observations have revealed an extensive matrix of “amorphous organic material” between sediment and detrital particles (Wiese & Rheinheimer, 1978; Watling, 1988). Such matrix material had been previously noted in sediments by geologists (Neumann, Gebelein & Scoffin, 1970; Frankel & Mead, 1973) and is presumed to be of microbial origin (Watling, 1988). This slime-enclosed matrix, however, is not typically seen by biological investigators because it is easily destroyed during conventional sediment processing techniques. Electron microscopic examinations of the microbial flora from seagrass sediments and coral reefs showed that most cells were encapsulated, and existed enveloped within a mucous exopolymer slime layer attached to the sediment or detrital surfaces (Moriarty & Hayward, 1982). The slime appeared much more abundant in surface sediments than in sediments collected from 20-cm depth. Microbial secretions produced by both bacteria and diatoms affect sediment systems through their binding processes (Frankel & Mead, 1973; Holland, Zingmark & Dean, 1974; Rhoads, Yingst & Ullman, 1978; Vos, De Boer & Misdrop, 1988), especially on silt-sized particles (DeFlaun & Mayer, 1983; Grant, Boyer & Sanford, 1982). This can greatly affect sediment stability (Neumann et al., 1970; Robert & Gouleau, 1977; Paterson, 1989), and sediment resuspension (Grant et al., 1982; Grant, Bathmann & Mills, 1986). Paterson (1989) found that EPS released by diatoms for locomotion formed an extensive extracellular matrix throughout surface sediments. In other systems such diatom mucous films were often found to be patchy over cm scales (Grant & Bathmann, 1987; Hicks, 1988). Hicks (1988) found the cementing together of sandy sediments at low tide by such diatom EPS. With the incoming tide, the cemented surface sediments were then peeled off, forming rafts which transported meiofauna-sized animals. At a microscale, EPS can further affect the exchange of nutrients within sediment and at the sediment-water interface (sensu Grant et al., 1986; Grant & Bathmann, 1987). Some types of diatom EPS appeared to be highly persistent. Mucilages produced for locomotion were, however, found to be highly soluble (Webster, Cooksey & Rubin, 1985; Edgar & Pickett-Heaps, 1984) and their effect on sediment stability was short lived, significantly diminishing within a tidal cycle (Paterson, 1989). In other, more specialised, environments EPS secretions of both algae and bacteria are strongly linked to the cohesive structure of microbial mats (Nicholson, Stolz & Pierson, 1987) and stromatolites. Moriarty (1983) studied the stromatolites of Shark Bay in Australia, and found that most of the heterotrophic bacteria associated with them were embedded in abundant exopolymer slime layers. Stromatolites, which represent some of the earliest life forms known, are composed of blue-green cyanobacteria which cement sediment (via exopolymers) into layered mounds. Finally, in sediments and at sediment-water interfaces, the binding of smaller particles (i.e. silt-sized) by EPS into larger aggregates can effectively change their functional size category. Because particle size is often of importance to deposit- and
MICROBIAL EXOPOLYMER SECRETIONS
109
filter-feeding animals, such aggregation can affect feeding processes in these animals. While the existence of such aggregates within sediments has recently been questioned (Watling, 1988), continuing studies are in progress to understand better sediment microstructure in situ.
EXOPOLYMERS IN THE WATER COLUMN: THEIR ROLE IN AGGREGATE FORMATION AND BIOLOGICAL FLOCCULATION
Exopolymers occur in water-column systems as: (1) dispersed high-MW secretions which are operationally considered as DOM, and (2) particulateslime components of aggregates. The latter are more observable, occurring during the later stages of phytoplankton blooms, as well as other forms of microbially produced marine snow. Examination of open ocean aggregates shows a complex range of size classes, originating from a variety of sources (for review, see Lee & Wekeham, 1988). Observations using electron microscopy, indicate that many aggregates possess abundant filaments linking the particles together (Pomeroy, 1984). Such filaments (EPS) are produced by bacteria utilising DOM (Busch & Stumm, 1968; Paerl, 1974, 1978). In considering the formation of microbial aggregates, however, let us first ask: Why do bacterial aggregates form and how does the secretion of EPS relate to this aggregation? To understand this, we must first picture the environment of a bacterial cell which is free floating in the water column. A typical stationary bacterium, because of its small size (approx. 1 µm) and mass, is limited to diffusion in its ability to gather dissolved nutrients. A 10– 30 µm diffusion gradient exists immediately surrounding the cell in any direction. Water and new nutrients do not flow by the cell even if the medium or water is stirred. Rather, the cell is carried in a relatively stagnant pool of water and nutrients (White, 1986). To gain access to further nutrients, the bacterium can use one of several general possibilities (White, 1986). One is that it can swim 30 µm in any direction (expending energy), to escape this stagnant pool and possibly find better nutrient conditions. Some studies show, however, that under natural conditions a swimming bacterium cannot increase its nutrient supply by more than 10% by swimming (Purcell, 1977). A second possibility is to attach to a large (relative to the size of the bacterium) surface. The bacterium can then remain stationary while nutrients are adsorbed and concentrated as water flows by the surface. In open ocean environments, however, such surfaces are limited. A third possibility (i.e. aggregate formation) is to secrete an exopolymer slime. This sticky polymer will increase the effective size of the bacterium, and enable it to aggregate with other passing particles, further increasing its size. Eventually, this aggregate will itself behave like a large surface. Water (containing nutrients) will then flow by the aggregate as it sinks or is carried by currents. Nutrients can then be gathered and concentrated. Active aggregation has also been suggested for diatoms (for review see Smetacek, 1985) which are known to aggregate in a wide range of marine and freshwater environments (Bodungen, Smetacek, Tilzer & Zeitzchel, 1986; Kranck & Milligan, 1988). This represents an important consideration in understanding the later stages of phytoplankton blooms. While growing cells maintain themselves at close to neutral buoyancy, increased sinking rates have
110
ALAN W.DECHO
been noted in stationary-phase cells and under nutrient-depleted conditions (which are present in later stages of a phytoplankton bloom) (Bodungen, Brockel, Smetacek & Zeitzschel, 1981; Beinfang, Szyper & Laws, 1983). It is known that diatom cells form sticky flocs more frequently in later stages of growth than in early stages (Kranck & Milligan, 1988). This coincides with nutrient-depleted conditions and maximum production of EPS mucilage (Lewin, 1956; Myklestad & Haug, 1972; Eppley, Renger & Betzer, 1983; Kroen & Rayburn, 1984). Extracellular polymer production by Chaetoceros sp., can reach 40 mg·l -1 of growth medium during the stationary phase (Myklestad & Haug, 1972). During descent these sticky cell flocs further scavenge other particles, which if heavy, further accelerate sinking rates (Smetacek, 1985). As sinking cells reach deeper, more nutrient-rich water, sinking rates can be once again reduced (Bienfang et al., 1983). This has been shown to be physiologically regulated, at least in one diatom species, by the exchange of heavier ions for lighter ions (Anderson & Sweeney, 1978). Also, many diatoms are known to produce resting stages, which sink to the sediments and can later be resuspended to ‘seed’ the next bloom. This sinking behaviour may therefore have an adaptive value to such diatom cells in shallow-water environments (Smetacek, 1985). The sinking of these aggregates can be quite rapid, allowing phytoplankton cells and detritus to reach considerable depths (Silver & Alldredge, 1981). Large amounts of mucous aggregated material derived from phytoplankton blooms have been found on the sediment surface at 4500 m depth (Riemann, 1989). The previous entangling of these mucous flocs with faecal pellets and other cellular debris is thought to be an important factor in the formation of these fast sinking aggregates. The specific mechanisms and involvement of exopolymers in the flocculation process, however, have been most closely studied in activated sludge research. Flocculation occurs when bacteria convert C (in the sewage) to EPS (Busch & Stumm, 1968; Friedman, Dugan, Pfister & Remsen, 1969; Tago & Aida, 1977; Sheintuch, Lev, Einav & Rubin, 1986). These studies show that aggregate formation begins when polymer (EPS) bridges are formed between adjacent cells. This traps further material and increases the size of the aggregate (Busch & Stumm, 1968). The flocculation properties of the particles are largely due to the ionogenic materials present in the EPS (Horan & Eccles, 1986). These properties allow the EPS to behave as a polyelectrolyte and to form flocculent particles. The uronic acid residues of EPS polysaccharides act as the principle ionogenic agent, conferring an overall negative charge at pHs near those of sea water. The absence of certain ions may deter the aggregation process. For example, Fletcher & Floodgate (1976) reported the disaggregation of EPS substances when marine bacterial flocs were transferred to media deficient in calcium and magnesium. Specific polysaccharides can be linked to the flocculation-deflocculation process in activated sludge. Tago & Aida (1977) isolated two polysaccharides from nonfloc forming bacteria in activated sludge. Three polysaccharides could be isolated from floc-forming cells in the same system. The third polysaccharide (i.e. a mucopolysaccharide) caused floc formation. This mucopolysaccharide could be degraded by an extracellular enzyme secreted in non-floc-forming cells, and caused deflocculation in already existing flocs. This demonstrated the importance of specific polysaccharides in the formation of aggregate flocs. In some aggregates polymeric fibres can extend up to 50 µm from the cells and function to trap other cells and debris from surrounding water. This increases the size
MICROBIAL EXOPOLYMER SECRETIONS
111
of the aggregate and hastens flocculation (Geesey, 1982). Recent studies (Biddanda, 1988; Biddanda & Pomeroy, 1988) indicate that as aggregation proceeds, a well defined pattern of microbial succession occurs. Selective removal of bacterial cells by microflagellates close to the surface of an aggregate has been found and can influence the density of cells near the surface of the aggregate (Caron, 1987). Later, the development of this aggregate community, referred to as the “detritosphere”, will ultimately degrade the aggregate with time (Biddanda, 1988). In open-ocean water bacteria attached to particles are more metabolically active than free bacteria (Kirchman & Mitchell, 1982). Overall uptake by attached bacteria can be up to 60% greater than uptake by dispersed bacteria (Moriarty, 1979; Hodson, Maccubin & Pomeroy, 1981; Logan & Hunt, 1987; and others). This is because attachment to organic materials increases the availability and mass transfer of organic nutrients over time (Alldredge, 1979). In the water column, attached bacteria secrete EPS derived from DOM (Paerl, 1974) which can increase their particulate size. A large number of investigators have recognised the important role which microbially produced secretions play in aggregate formation and/or the attachment of bacteria (Leppard, Massalski & Lean, 1977; Tago & Aida, 1977; Alldredge, 1979; Newell, Lucas & Linley, 1981; Biddanda, 1985; and others). Because EPS concentrates dissolved nutrients (even recently fixed nitrogen) their flocculation from surface waters represents a pathway of transport for DOM (Paerl, 1975; Paerl, Richards, Leonard & Goldman, 1975) and metals, such as iron and manganese (Cowen & Silver, 1984), to sediments. This transport may be conservatively estimated because amounts of marine snow are considered, by some, to be seriously under-estimated using conventional water sampling techniques (Silver, Shanks & Trent, 1978; Knauer, Hebel & Cipriano, 1982). The aggregation process and its adsorptive exopolymer can therefore profoundly affect the mass transfer of nutrients and metals from water column to sediments.
EXPOLYMERS AS DON OR POM
In marine systems, the distinction between dissolved (DOM) and particulate (POM) organic matter is often operationally defined (Sharp, 1973). For most studies the DOM fraction is defined as the organic material passing through a 0.5-µm filter and typically includes colloidal material (Sharp, 1973). Colloids are high-MW compounds, and in a physiochemical sense act as “micro-particulate” matter (sensu Means & Wijayaratne, 1984). Colloidal forms may bind low-MW DOM and may later precipitate or coagulate to form larger particulate matter (Morel & Gschwend, 1987). Exopolymers can exist in both colloidal and particulate form, depending on whether or not they are particle-associated. A large portion of colloidal slime exopolymers under natural conditions (i.e. from the water column or pore-water) pass through filters and are operationally defined as DOM. Other portions of colloidal exopolymers may associate to already existing particulate material such as detrital and sediment surfaces and be considered as POM. In addition, the binding of low-MW DOM to exopolymers tends to dehydrate the exopolymer (via water exchange reactions) causing their precipitation into particulate form. Such processes have been suggested for macroalgal DOM to reach consumer animals (Mann, 1988).
112
ALAN W.DECHO
While much of the DOM in aquatic systems consists of high-MW compounds such as humic and fulvic acids, lignin, and protein, these compounds are relatively resistant to microbial breakdown. Exopolymers may be unusual in that they represent a potentially labile form of high-MW material (Sherr, 1988). Other labile components of DOM are the relatively smaller fraction of low-MW sugars, amino acids, fatty acids, peptides, etc., which readily adsorb to exopolymers. For these reasons exopolymers may represent a transition state between potentially labile pools of DOM and POM in marine systems. Their relative importance in flux processes, however, will be dependent on their concentrations and geochemical interactions in situ.
SETTLEMENT AND METAMORPHOSIS OF MARINE LARVAE
It is now known that a variety of factors, especially passive ones such as hydrodynamics, may affect the initial contact of a larva with a settlement substratum (see Butman, 1987, for review). Once contact has been made, however, the mechanisms which determine whether a larva will remain (i.e. settle) or move elsewhere appear to be an active choice process. With the limited data available, such choice processes are difficult to generalise and appear to vary depending on the specific larva involved. Many settlement studies, however, have indicated the importance of microbial films in these processes. A variety of laboratory studies have shown that the settlement and metamorphosis of certain marine larvae can be closely linked to specific biofilms which bacteria secrete. It was suggested long ago that the presence or absence of certain bacterial species and their biofilms might influence the settlement of certain marine larvae (ZoBell & Allen, 1935). Subsequently, only a limited number of studies have specifically addressed such settlement processes. These studies, mostly in environments with hard substrata, have demonstrated that the settlement of many different larvae on surfaces can be stimulated by specific bacterial films (Mihm, Banta & Loeb, 1981; Brancato & Woollacott, 1982; Weiner & Colwell, 1982; Mitchell & Kirchman, 1984; Weiner et al., 1985). Further detailed studies of Kirchman, Graham, Reish & Mitchell (1982a,b) demonstrated that both the settlement and subsequent metamorphosis of the polychaete larvae Janua brasiliensis on surfaces can be induced by a bacterially produced EPS film. They showed that the larva binds to the bacterial EPS using a highly specific lectin-binding mechanism. Lectins are proteins which will bind only to a specific arrangement of sugars within a polysaccharide (Sharon, 1977). The lectin proteins on the larval surface bind to the polysaccharide portion of the EPS. The addition of free glucose inhibits larval settlement because it interferes with the lectinbinding mechanism (Sharon & Lis, 1972). In other laboratory studies, the settlement response depends on the age of the larva, and the age of the bacterial film (Müller, 1973; Maki, Rittschof, Costlow & Mitchell, 1988). Once a larva has settled, secretion of a proteinaceous cement by the larva often occurs. If this cement does not bind strongly to the exopolymer (of the bacterial film), the larva may break free and leave to search for a more suitable substratum for metamorphosis (Maki et al., 1988). In some larvae bacterial films are not required for settlement (Miller, Rapean & Whedon, 1948), and certain bacterial films can even inhibit settlement (Maki et al., 1988). This suggests that a specific EPS released by certain bacteria may be necessary for the settlement of some larvae.
MICROBIAL EXOPOLYMER SECRETIONS
113
The larvae themselves, however, may have some role in controlling the bacterial film on which they live. In bryozoan larvae which are about to metamorphose, the release of specific bacteria (contained within their pallial sinus) inoculate the surface upon which they are attached (Zimmer & Woollacott, 1983). These bacteria perhaps play a role in successful completion of metamorphosis or in conditioning the substratum to affect further settlement of larvae (Woollacott, 1981). Bacteria and their films also promote the attachment of unicellular algae (Tosteson & Corpe, 1975; Mitchell & Kirchman, 1984) and the swarmer cells (i.e. reproductive spores) of larger algae such as Enteromorpha sp. (Dillon, Maki & Mitchell, 1989). This is thought to occur by the modification of the surface energy of the substratum by the bacterial films. Of fundamental interest here are the questions: Why do certain larvae choose areas with specific biofilms, i.e. for food or sturdy attachment? Also: How does the attachment of a larva trigger its subsequent metamorphosis? It is of applied importance to biotechnology to be able to manipulate microbial communities so as to reduce biofouling or promote the settlement of economically important fisheries resources, i.e. oysters, abalone, etc. (Bonar, Weiner & Colwell, 1986). The mechanisms of attachment to these biofilms and how such biofilms interact with larvae under natural conditions is not well understood at present. The nature of these interactions represents an area of both ecological and applied importance.
EFFECTS ON MICROBIOGEOCHEMICAL PROCESSES AND THE DEGRADATION OF DETRITAL PARTICLES
EPS secretions, owing to their diffusive characteristics, sediment-binding ability and adsorptive properties, can significantly alter many biogeochemical processes taking place in sediments, biofilms, and water-column aggregates. As EPS layers increase in thickness, the diffusion of nutrients (Kornegay & Andrews, 1968; Saunders & Bazin, 1973), gases (Mueller, Boyle & Lightfoot, 1968; Matson & Characklis, 1976), and toxic by-products to and from underlying layers is restricted. Such processes can result in the formation of steep physical and chemical gradients over very small spatial scales. The presence of micro-anaerobic zones within well oxygenated waters and sediments are examples of these processes (Paerl, 1984a; White, 1986). A variety of microgradients have been observed in sediments (Revsbech & Jørgensen, 1986) as well as water-column aggregates (Alldredge & Cohen, 1987; Paerl & Prufert, 1987; Paerl & BeBout, 1988; Richardson, Aguilar & Nealson, 1988) by the use of microprobes. The application of tetrazolium salts (Oren, 1987) to aggregates is another such technique which has been used to examine these microprocesses (Paerl, 1984a). The diffusion of O (and nutrients 2 such as , , , and ) through exopolymer slime are thought to control metabolic reactions within them (La Motta, 1976). An exhaustive study by Sanders (1966) indicated that exopolymer slime need only be about 21 µm thick in order to reduce significantly the diffusion of O2 to the interior. Aerobic bacteria close to the surface layer will consume much of the O . Deeper layers will develop 2 anoxic conditions allowing anaerobic bacteria to metabolise. Such microanaerobic zones within biofilms and ‘aerobic’ sediments can allow a variety of geochemical processes (which are normally inhibited by the presence of O ) to 2
114
ALAN W.DECHO
occur (White, 1986). For example, denitrification processes have been observed within biofilms located in aerobic waters (Nakajima, 1979; Ventullo & Rowe, 1982). The above-mentioned microprocesses can further influence trophic interactions by promoting diverse microhabitats for a variety of microorganisms and invertebrates (Paerl, 1984a). The degradation of detrital particles may be regulated, in part, by EPS biofilms. The formation of biofilms on surfaces, such as a sediment or detrital particles, is a common event (Floodgate, 1972) and can be regarded as a universal bacterial behaviour for survival, and for optimal positioning with regard to available nutrients (Costerton et al., 1987). The importance of EPS in regulating the degradative processes of “refractory particles” has been best studied in rumen microflora which degrade cellulose (Costerton, Marrie & Cheng, 1985; and citations therein). Many bacteria, capable of digesting insoluble organic nutrients (i.e. cellulose) have the specific ability to attach to the nutritive substrate by means of EPS instead (Akin & Amos, 1975). For example, EPS is necessary for the initial attachment and digestion by cellulytic bacteria (Kudo, Cheng & Costerton, 1987) although direct contact between the cell and cellulose substrate is not necessary (Kauri & Kushner, 1985). These primary colonisers attack the insoluble substrate and produce soluble nutrients that stimulate the growth of other adjacent heterotrophic organisms until a ‘digestive consortium’ is formed. Such a consortium can efficiently degrade the cellulose particle (see below). In marine systems, the biofilm community on the surface of a detrital particle may be similarly highly structured over microscale distances (i.e. µm). This would allow the utilisation of substrata and by-products (from other microbial flora within the biofilm) in a most efficient manner (Wimpenny, 1981). In marine systems, however, few data are available at present on the overall role of EPS in detrital degradation and other microbiogeochemical processes. These processes, although potentially important, have yet to be examined closely.
ROLE OF EPS IN THE DEVELOPMENT OF BIOFILMS AND MICROBIAL CONSORTIA
Biofilms readily form on most submerged surfaces such as rocks, detritus, and a variety of man-made surfaces (ship hulls, water pipes, etc.). Within these surface microenvironments are located structured populations of microorganisms which are quite different from those observed in the water column. Biofilm communities are embedded within an exopolymer slime matrix produced mainly by bacteria and microalgae (when present) which alters the physiochemical, nutrient, and hydrodynamic conditions present. At present, as the resolution of methodologies and the analysis of data increases, we must now address microbes, not singly, but in terms of their interactive effects on environment and each other. There is a growing idea in microbial ecology that microbial flora within certain surface biofilm communities exist as groups of physiological units, rather than as a random assortment of species or strains. These groups of microbial strains are embedded and spatially segregated within an exopolymer matrix. This idea, called the “microbial consortium hypothesis”, has recently gained attention in the study of other surface-associated systems (intestinal flora, dental plaque, cellulose digestion, metal corrosion, methane digestion, etc.) (Costerton et al., 1985).
MICROBIAL EXOPOLYMER SECRETIONS
115
Biofilm communities are often highly efficient systems. In energetic terms, the production of EPS used in a biofilm requires an expenditure of energy in the form of reduced organic structural components (Paerl, 1975). It is thought, however, that the energy required to produce EPS (and attach to a surface) may well be less than that expended during movement of a bacterial cell seeking nutrients (Wardell, Brown & Flannigan, 1983). The biofilm sequesters and concentrates nutrients from the bulk fluid passing by. In addition, the retention of enzymes bound to EPS from previous generations of microbial flora increase these benefits. Within the biofilm community the expenditures of energy and benefits will be shared by the community (consortium). The method of biofilm formation is advantageous because it allows the cells to remain in a nutritionally favourable niche where nutrients can be sequestered and utilised, and at the same time provides a measure of protection from chemicals, bacteriophages, surfactants, heavy metals, etc. Research involving the inactivation of biofilm bacteria has yielded much information on transfer processes which occur within biofilms. For example, the majority of viable bacteria in chlorinated drinking water are enclosed within biofilms on the surfaces of pipes (LeChevallier, Cawthon & Lee, 1988). The effectiveness of certain biocides, such as free chlorine, is greatly reduced because it reacts with EPS polysaccharides. Other biocides, such as monochloramine, are more effective because they are less reactive and can penetrate the biofilm exopolymer. In artificial water systems such processes account for the depletion of organic and metallic compounds due to adsorption by exopolymer-containing biofilms present (Costerton, 1984). The sequestering of other toxic compounds by the EPS components within biofilms may allow the persistence of viable microbial cells under otherwise lethal concentrations of that toxin. Close investigations of certain microbial communities have shown a definite microspatial organisation suggesting close physiological relationships and interdependencies (Wimpenny, 1981). Studies using radiolabelled substrates indicate that cells located deeper within the matrix are still able actively to take up some, but not all, nutrients by diffusion (Ladd, Costerton & Geesey, 1979). These cells may rely on specific metabolites produced by the type of surface layer. Such close interdependencies imply that microbial strains within a group must be well adapted to their micro-environments and must possess the proper metabolic machinery. In the development of spatially segregated groups the exchange of genes between bacteria cells may be especially important. The bacteria are able to metabolise more efficiently in their micro-environments through the enrichment of ‘visiting’ genes from neighbouring cells which already possess these metabolic capabilities. This may occur through ‘transformation processes’ (i.e. a bacteria takes up free exogenous DNA and incorporates it into its own genome) and ‘plasmid-transfer’ (i.e. the exchange of DNA through the direct contact of two adjacent bacteria), the latter being more common in natural systems. Transformation processes may have evolved from the utilisation of DNA as a nutrient source, because many transformable bacteria can use DNA as carbon, nitrogen, and energy sources (Stewart & Carlson, 1986). In transformation processes, exopolymers may enhance gene exchange by binding exogenous DNA and subsequently protecting it from degradation until it can be taken up by another microbial cell. Exogenous DNA has been found in fresh water and sea water up to concentrations of 88 µg·l -1 (see Karl & Bailiff,
116
ALAN W.DECHO
1989; and citations therein), and detrital organic matter (HolmHansen, Sutcliffe & Sharp, 1968). Exogenous DNA is also often found associated with exopolymer (Nishikawa & Kuriyama, 1968; Pavoni, Tenny & Echelberger, 1972). This exogenous DNA may be taken up by cells and incorporated into their genome. Such exogenous DNA is sufficiently large to encode for gene sequences (approx. 0.1 to 36 kb) (DeFlaun, Paul & Davis, 1986). This exogenous DNA may result from grazing, cell lysis or active excretion (Stewart & Carlson, 1986). It is often rapidly hydrolysed by both extracellular and cellassociated enzymes (Paul, Jefferey & DeFlaun, 1987). In the water-column turnover times as short as 6.5 h have been found (Paul et al., 1987). In sediments, however, turnover times are much slower (Novitsky, 1986). This is surprising because there is an ubiquitous presence of DNA-hydrolysing bacteria and DNAase activity in sea water (Paul et al., 1987). It is thought that DNA may be protected from nuclease digestion by binding to the sediment (Aardema, Lorenz & Krumbein, 1983). DNA is often found associated with exopolymer, and the exopolymers are closely associated with cells thus it is suggested that exopolymers may enhance the survival of exogenous DNA and its ability to transform other microbial cells. Such transformation processes would ultimately allow the local bacterial community to exchange “favorable metabolic genes” and therefore develop as a single metabolic unit which operates most efficiently for the given nutrient conditions (Sonea, 1988). Indeed many bacterial processes in natural ecosystems may be carried out by consortia (i.e. groups of physiologically related types), which can potentially coexist and interact as a single physiological unit (Wimpenny, 1981) . These consortia are anchored within an exopolymer matrix. Experimental manipulation here will be difficult. The concept of microbial consortia needs, however, to be addressed when examining the microbial flora in natural environments. It will provide new insights into detrital degradation and micronutrient processes under natural conditions.
HYDROTHERMAL VENTS
In hydrothermal vent systems, there are abundant mucous secretions. For example, bacteria secrete exopolymer capsules which sequester minerals from the surrounding sea water (Cowen & Silver, 1984; Cowen, Massoth & Baker, 1986). Other vent-associated bacteria form thick microbial mats which are similarly laden with EPS secretions (Jannasch & Wirsen, 1981). These mats are grazed upon by high densities of shrimp living in proximity (Van Dover et al., 1988). Such systems, conspicuously lacking in photosynthetic microflora (and their associated essential nutrients such as certain fatty acids) provide an interesting set-up to examine the role of exopolymers and the use of alternate food resources in order to obtain essential nutrients. General secretions of mucus produced by polychaetes living in proximity to the vents, accumulate minerals and trace metals (Juniper, Thompson & Calvert, 1986). These mucous aggregates contributed to the mass of sulphide deposits forming at the vents, and may represent a deoxification mechanism for accumulating metals.
OTHER SYSTEMS
MICROBIAL EXOPOLYMER SECRETIONS
117
In coral reefs, corals form the base of the reef food web. In this environment much can be learned regarding the role of mucus in trophic interactions. These coral secretions of mucus although not microbial in origin, may represent a significant pathway for the conversion of coral primary productivity to higher trophic levels (Ducklow & Mitchell, 1979b; Gottfried & Roman, 1983). Aggregates of mucus originating from corals represent a potential food resource for reef zooplankton and dominate the particulate matter in reef waters (Ducklow & Mitchell, 1979a). These aggregates become subsequently enriched with nitrogen over time (Coles & Strathmann, 1973) and are readily assimilated by reef zooplankton such as copepods and mysids (Richman, Loya & Slobodkin, 1975; Gottfried & Roman, 1983). Coral mucus (and its adsorbed components) may account for up to 70–80% of the organism’s carbon weight per day (Gottfried & Roman, 1983). Reef fish, shrimp and crabs are also known to ingest coral mucus (Preston, 1971; Daumas & Thomassin, 1977). In fresh water, similar mechanisms may operate. For example, a great majority of the physical, chemical, and biological activities occur in microzones of particles or surfaces (Paerl, 1980). It has been recognised for a long time that in flowing aquatic systems, more than 99% of the microbial organisms grow in adherent biofilms (Geesey et al., 1978; Costerton & Colwell, 1979). EPS plays a major role in the attachment of microbes to surfaces in streams (Brown, Ellwood & Hunter, 1977; Rounick & Winterbourn, 1983) thus allowing a biomass of microbial flora many times greater than that of the overlying water (Costerton, Geesey & Cheng, 1978). The organic slime films (EPS) allow attachment and resistance against the flowing water, and trap nutrients for the bacteria and diatoms which secrete them. These films, and their microbial flora have been suggested as a major food resource for a variety of common stream invertebrates (Madsen, 1974; Rounick & Winterbourn, 1983) but as yet, no studies specifically addressing this have been conducted. The importance of microbial slime in freshwater systems have been reviewed by Lock et al. (1984).
POTENTIAL ROLES OF EXOPOLYMERS IN FOOD WEBS UTILISATION AS A DIRECT FOOD RESOURCE: AVAILABLE EVIDENCE
Food value of exopolymer The potentially labile nature of exopolymers had previously prompted a number of investigators to propose that these secretions represent a significant source of carbon for microbial consumer animals (e.g. Hobbie & Lee, 1980; Moriarty, 1980; Cammen, 1980; and others). Microbial exopolymers are ubiquitous under most natural conditions, being closely associated with microbial flora, detritus and sediment. As consumer animals feed on bacteria, sediment and detrital particles, they will coincidentally ingest exopolymers (and their adsorbed DOM) which are closely associated. It is likely that such EPS secretions may supplement both benthic and pelagic consumer food resources. The relative importance of
118
ALAN W.DECHO
exopolymers as a food source, however, will ultimately depend on two factors: (1) how labile they are to a given consumer animal, and (2) their quantities under various natural conditions. What is the nutritional value of EPS as a food resource to benthic consumers? Most exopolymers examined so far have contained large amounts of easily degradable polysaccharides; it can be expected therefore that most exopolymers will represent a highly labile carbon resource for benthic and pelagic animals. Indeed, a wide range of indirect evidence has supported this assertion. Further adsorption of labile DOM (amino acids, sugars, etc.), to exopolymers will provide additional C and N pools which can be easily utilised once ingested by animals. Studies examining the uptake and utilisation of exopolymers by consumer animals are, however, relatively few. In one of the first studies directly addressing exopolymer as a food resource, Harvey & Luoma (1984) examined the clam Macoma balthica and found that bacterial exopolymer dissolved in sea water or associated with sediment was not incorporated to a great extent, even after prolonged feeding periods (i.e. more than 6 days). A subsequent study by Baird & Thistle (1986) examined a different animal, the sea cucumber Stichopus, and demonstrated the rapid uptake and utilisation of bacterial exopolymer. Assimilation was demonstrated via incorporation of 14Clabelled EPS into the rete mirabala organ of the animal. The apparent contrasting results of these two studies are interesting because both investigations used the same bacterial exopolymer (i.e. Pseudomonas atlantica) isolated from the same growth stage (i.e. the stationary phase). The two studies suggest that not all animals may be capable of assimilating a given type of exopolymer. Similarly, not all exopolymers may be labile to a given animal. Compositional analyses of exopolymers and analysis of digestive enzymes of consumer animals may help elucidate such processes. Recent studies by Decho & Moriarty (in press) found that bacterial exopolymer, isolated from a Pseudomonas sp., in the stationary phase was highly labile to a meiobenthic harpacticoid copepod, Laophonte sp. They coated “bacterium-sized beads” with 14C-exopolymer to examine their consumption and utilisation by this animal. A surprising aspect of this study was that the exopolymer was assimilated with a very high (80–85%) efficiency, suggesting that it represents an easily digestible carbon source for this animal. In other studies, Sherr (1988) demonstrated the ingestion of fluorescently labelled exopolymer (i.e. dextran) by both freshwater and marine protozoans. She suggested that exopolymers and other high molecular weight polysaccharide material can represent potential energy sources for microbial consumers. The dextran, used in the above study, was an exopolymer homopolysaccharide isolated from Lactobacillus in the stationary phase of growth (Sigma Chem. Co.). It is not known what role exopolymers may serve as a nitrogen source. Laboratory studies suggest it should be minimal. Conditions in situ may, however, produce EPS which is different in composition than that observed in the laboratory. For example, it is probable that exopolymer produced under natural conditions may be considerably more nitrogen-enriched. The natural media (i.e. sediment pore-water) has relatively higher N concentrations (in the forms of dissolved amino acids) which are quickly utilised by bacteria. In practice we have few data concerning the compositions of exopolymers under natural conditions. Such studies, however, are necessary before firm generalisations can be made.
MICROBIAL EXOPOLYMER SECRETIONS
119
A plethora of evidence in the literature indirectly suggest that utilisation of EPS may occur and will be examined below. These evidences do not themselves directly demonstrate utilisation; they are mentioned but must be viewed with proper restrictive interference. This indirect evidence comes from two major areas: (1) feeding studies of consumer animals, and (2) studies of digestive enzymes (to be discussed later, see p. 121 ), in both bacteria and animals, which are capable of EPS degradation. In feeding studies, the passage of the heavy metal chromium through several trophic levels (bacteria ? oligochaete ? fish) has been shown. This resulted from the uptake of metal by bacteria and its subsequent ingestion by tubificid oligochaetes (Patrick & Loutit, 1976a, b). Subsequent studies have indicated that the chromium adsorbed to bacterial exopolysaccharide can be transferred to higher consumers (i.e. polychaete and the mudsnail Amphibola) (Bremer & Loutit, 1986). Utilisation of the exopolymer itself, however, was not examined. In studies of microbial biofilm communities, White & Findlay (1988) examined the effects of grazing by detrital-feeding amphipods. They found a shift in the structure, nutritional status, and metabolic activities of the microbial community within the biofilm. Other indirect indications of ingestion of mucus were found by Stein (1984), who examined utilisation of microbial mat communities around shallowwater hydrothermal vents by grazing gastropods. The bacterium Beggiatoa sp., was conspicuously consumed by the gastropods and is known to secrete large amounts of exopolymer mucus in these systems. Direct utilisation of these exopolymers was not examined. In sediment environments, numerous studies have shown that the cellular biomass of bacteria is not sufficient to support local grazer populations (Tunnicliffe & Risk, 1977; Wetzel, 1977; Jensen & Siegismund, 1980; Cammen, 1980; and others). Also, studies examining the nutritional requirements of benthic consumers have revealed that only a small percentage (<10– 25%) of their carbon requirements can be derived from the consumption of bacterial cells directly (Cammen, 1980; Moriarty, 1982; Newell & Field, 1983; Juniper, 1987a,b). These data clearly show that microbial cells are simply not ingested in sufficient quantities to comprise the bulk of the carbon resources for these animals. Therefore, another major carbon source must be utilised to account for this deficiency. Enter exopolymers: investigators have previously suggested EPS to make up a large portion of this unaccounted for carbon resource, especially if they are highly labile (Cammen, 1980; Moriarty, 1982; & others). For example, Moriarty (1982) concluded that detrital slime (i.e. the slime layers on sediment, mucus, and extracellular exopolymers secreted by microbial flora) may comprise the bulk (more than 50%) of the carbon assimilated by a sea cucumber. In studies of freshwater lotic detrital systems, Findlay & Meyer (1984) have similarly found that bacteria (i.e. cellular carbon) comprised a small portion of the organic carbon in sediments, and a small portion of the carbon requirements for consumer animals (Findlay, Meyer & Smith, 1984). They concluded, however, that unless extracellular carbon secretions are in the order often times the cellular biomass, the overall role of bacteria as a carbon source for higher trophic levels in these systems would be minimal. In order to assess accurately the relevance of EPS production to the flow of energy and nutrients to benthic consumers, several fundamental aspects regarding both exopolymers and the microbial cells themselves must first be addressed. First
120
ALAN W.DECHO
it must be known how much EPS is present in natural systems, such as sediments, the water column, and its variability on a seasonal scale. Secondly, it must be known what portion of this EPS is highly labile, because some EPS (i.e. capsular EPS) may be relatively refractory. A third point relates to our analytical limitations in measuring microbial production itself. Estimates can vary considerably depending on the method used (Riemann et al., 1984). Much of the variation associated with microbial production estimates has stemmed from the use of conversion factors, which show a wide range of empirically derived values. This range is due partly to intrinsic variation and partly to the difficulty of accurately and precisely measuring such parameters. The conversion factor used can substantially affect the final production estimates, and ultimately the amount of C derived from bacterial cells and consumed by a bacteria-feeding animal. Examples of such conversion factors are carbon to wet weight ratios, and wet weight to dry weight ratios (Bratbak, 1985), and cell size (biovolume) estimates for bacteria (Novitsky & Morita, 1976; Albright & McCrae, 1987). Rates of bacterial production and turnover are still not entirely understood (Fallon, Newell & Hopkinson, 1983) and represent an area of intensive study. Because conversion factors ultimately affect bacterial production estimates, they represent a potential source for over- or under-estimation of bacterial production and the relative importance of EPS in a given system. In terms of nitrogen, numbers of living bacteria on particles have been shown to account for only 5% of the total detrital particulate nitrogen (Marsh & Odum, 1979). Nitrogen-rich exudation products of bacteria, however, may accumulate by chemical and/or physical associations with the decay-resistant components of aging detritus (Rice & Hansen, 1984). Estimates of EPS production based on these nitrogen excretions have been calculated. Exudation rates of 8 mg N·g -1 bacteria·day -1 as measured by Rice & Hansen (1984) would correspond to about 115 mg mucopolysaccharide·g -1 bacteria·day -1 (assuming mucopolysaccharides are 7% nitrogen). This implies a daily expenditure of about 5% of the cellular biomass for processing substrate extracellularly. If the biomass of EPS conservatively equals that of the microbial flora, as estimated by Uhlinger & White (1983), then approximate turnover rates for exopolymer should be in the range of 5 days. While the above approximations represent the only available information, they illustrate that caution must be used in drawing general conclusions from limited data. Empirical testing awaits to refine these estimates. In the only studies of EPS decomposition in marine sediments, Henrichs & Doyle (1986) examined EPS derived from the terrestrial bacterium Arthrobacter viscosus. This EPS also contained bacterial cellular material and was known from previous studies to be relatively refractory in terrestrial systems (Martin, Haider, Farmer & Fustec-Mathon, 1974). In marine sediments, however, they observed substantial decomposition after several days suggesting that it is much more degradable under marine conditions. Further studies, directly examining the decomposition and turnover rates of marine exopolymers, will be necessary, however, before further extrapolations regarding exopolymer turnover can be made. Enzymes which degrade EPS A second area of studies which suggest that EPS utilisation may occur comes from the presence of EPS-degrading enzymes in consumer animals. Understanding which enzymes degrade EPS is an important step in documenting their absorption
MICROBIAL EXOPOLYMER SECRETIONS
121
and utilisation by consumer animals. Many marine animals harbour resident gut bacteria. The role of these bacteria in the digestion process, however, is poorly understood. Many isolated bacteria produce extracellular enzymes capable of degrading exopolymers, so it is of interest to know whether the microbial flora present in many consumer guts produce similar enzymes. Such enzymes may be important in the digestion of consumer food resources (including exopolymers) or the consumer animals themselves produce such enzymes. Enzymes in animals Several enzymes, which can potentially digest EPS, show actively in animal homogenates. Once such example is ß-glucuronidase, an enzyme which indicates the potential ability to digest cell envelopes (Ghuysen, Tripper & Strominger, 1966), capsules and mucopolysaccharide slime of bacteria and diatoms (O’Colla, 1962). The nematode Monhystera denticulata ingests both bacteria and diatoms (Tietjen & Lee, 1977) and possesses the enzyme ß-glucuronidase (Deutsch, 1978). Similar enzymes have been found in the polychaetes Histriobdella homari (Jennings & Gelder, 1976) and Ctenodrilus serratus (Gelder, 1978), the parasitic copepods Mytilicola intestinalis (Moore, Lowe & Gee, 1978), the brown shrimp Penaeus sp. (Chambers, Heitz, McCorkle & Yarbrough, 1978) and many other marine animals. It is reasonable to assume, however, given the variability in the composition of exopolymers, that a variety of enzymes (rather than a single enzyme) act in concert to degrade the EPS sequentially (Bacon, 1979). It has been suggested that the weak carbohydrase activity found in many depositfeeders function in detachment of microbes from sediment (perhaps via dissolution of EPS) and preliminary digestion (i.e. removal of capsules and cell walls) of microbes (Lopez & Levinton, 1987). Changes in gut pH may also serve to dissolve exopolymers because acidic conditions are known to degrade exopolysaccharides (Aspinall, 1982c), and strong basic conditions cause many exopolymers to lose their tertiary structure and gel consistency (Lewin, 1955).
EPS-degrading enzymes isolated from bacteria A large number of enzymes, capable of degrading EPS have also been isolated from bacteria. While most of these have yet to be assayed in consumer animals, they may suggest a role of gut-flora in the digestion of EPS as well as other potential food resources, i.e. chitin, and various forms of detritus etc. Enzymes which degrade EPS can be separated into several general groups, depending on their mode and location of action (1)
(2)
Glycanohydrolases act on glycosidic (i.e. sugar-containing) material to yield different types of oligosaccharides (i.e. short-chain sugars). In general, they must be capable of hydrolysing the ß-1, 4 residues which occur in most exopolymers (Ikeda et al., 1982). These are often highly specific and depend on the monosaccharide residues present in the glycan and the anomeric nature of the glycosidic linkage which is hydrolysed. Eliminases (lyases) are also specific and produce unsaturated uronic acids at the non-reducing terminal ends. Examples of this group are hyaluronidases and ßglucanases. Hyaluronidases of animal origin produce tetrasaccharides with either uronic acid or amino sugar as the terminal reducing sugar. Hyaluronidases of bacterial origin are lyases and yield a disaccharide or larger fragments (Sutherland, 1977b).
122
ALAN W.DECHO
(3)
(4)
A third group of enzymes modifies the polysaccharide without actually hydrolysing it into monomeric constitutents. Deacetylases (which remove acyl groups from EPS) are an example of such enzymes (Sutherland, 1977b). These are important in the degradation of alginate (an algal polymer, also produced by certain pseudomonad bacteria) (Linker & Jones, 1966). In alginases produced by pseudomonads acetylated polysaccharides were poorly hydrolysed; the absence of acetylation, however, allows hydrolysis to occur readily (Linker & Jones, 1966). The apparent role of acetylation in the susceptibility of a substrate to hydrolysis may be related to how close the acetyl groups are to the glycosidic bonds to be hydrolysed. For example, de-acetylation does not have an inhibitory effect on enzyme action when acetyl groups are further from the glycosidic bond being hydrolysed (Sutherland, 1977b). Exoglycosidases (glycoside hydrolases) act on glycosidic bonds and, in general, have low specificity. They will hydrolyse any oligosaccharide or glycoside provided the aglycone residue and anomeric configuration of the linkage are correct (Sutherland, 1977b). Glycosidases are designed to open the ring structure of a sugar (i.e. break the glycosidic bond). These are often highly specific to the configuration of the sugar which they hydrolyse.
EPS polysaccharides are often very large and complex macromolecules, with complex tertiary interactions affecting their configuration (Rees, Morris, Thorn & Madden, 1982). It is possible that a large number of enzymes must act in concert to degrade sequentially EPS. It has been suggested that the major function of the weak carbohydrase activity in many deposit-feeders may be for detachment and preliminary digestion of microbes (perhaps to remove EPS coatings and cell walls) (Lopez & Levinton, 1987). A wide variety of enzymes have been found which are capable of partially degrading EPS components into simpler and more easily utilisable fractions. Other, more specific, enzymes bind to specific portions of EPS molecules, attacking them at specified linkages. For example, most marine exopolymers contain uronic acids (Kennedy & Sutherland, 1985). In enzymes (derived from bacteria) which attack polysaccharide substrates containing uronic acid, the heteropolysaccharide backbone is split without hydrolysing the o-ester or N-acyl linkages (Sutherland, 1977b). This generates oligosaccharides of different sizes which have a reducing end and a non-reducing end containing uronic acid (Shoham & Rosenberg, 1983). The actions of such enzymes have been reviewed in detail by Sutherland (1977b) and Bacon (1979). Factors which affect EPS degradability by enzymes The degree of hydration affects the susceptibility of a substrate to enzyme attack. The structural polysaccharides of refractory detritus (mainly derived from plants) are not made with any thought for their dismantling and, in fact, introduce many kinds of complexities into their structure which protect it against invasion and digestion (Bacon, 1979). For example, in cellulose, water is squeezed out of the crystalline structure making hydrolytic enzyme reactions very unlikely. In contrast, EPS is highly hydrated (Sutherland, 1977a) with water molecules forming an essential part of its ordered structure (Bacon, 1979). Therefore, EPS is potentially composed of easily hydrolysable polysaccharides. While EPS is composed of long, hydrated polymer chains, these polymer chains are often tightly interwoven to form a complex matrix (i.e. bacterial capsule)
MICROBIAL EXOPOLYMER SECRETIONS
123
surrounding the microbial cell. Ionic interactions between adjacent polymer chains hold this matrix intact. These interactions (and the presence of branching side chains), can reduce the ability of enzymes (i.e. especially endopolysaccharases) to hydrolyse them (Bacon, 1979). Other enzymes, such as exopolysaccharases, may first need to access these polymer chains. Exopolysaccharases are enzymes which attack the non-reducing end (i.e. the free end) of a polysaccharide chains. Many exopolysaccharases show multiple binding sites (in addition to the catalytic site). That is the enzyme must bind to the polysaccharide at several residues for maximum catalytic effect (Bacon, 1979). Under these conditions longer chain oligosaccharide substrates are preferred. The action of an exo-enzyme will often, but not alwas, be halted at or near a branching point in the polysaccharide chain. Therefore, the presence of branching points and side chains on the EPS can reduce the ability of these enzymes to hydrolyse it. Endopolysaccharases act on the internal portions of a chain and often close to a branch point. They are usually very specific in their mode of binding. Endopolysaccharases may therefore have limited action on EPS initially, because tertiary interactions can hold inner portions of polysaccharide chains in close proximity to other parts of the molecular structure (Bacon, 1979). Many EPS exopolysaccharides consist of sugar residues which have noncarbohydrate substituents attached to them (see p. 91 ). These are always one or more hydroxyl groups available for substitution on each residue. When small ester groups, such as acetyl groups, are present, they can interfere with intermolecular interactions of polysaccharide molecules and increase their solubility in water (Bacon, 1979). Substituents, such as acetyls, may also interfere with enzymesubstrate binding and protect regions of the polysaccharide chain from attack (Morris & Bacon, 1977). A certain polysaccharide, capable of being degraded by a given enzyme, can be protected from attack by binding with another polysaccharide which occupies many of the enzyme-binding sites (Bacon, 1979). The above information illustrates two points which should be noted regarding the action of enzymes on EPS. First, that barriers to enzyme action can be constructed at the molecular level. Secondly, the inhibition of digestion is not an all or none process. It can be better described as a slow dissolution of intermolecular associations and not an impermeable barrier (Bacon, 1979), and is therefore “time-dependent”. In attempting to digest a food substrate such as EPS, the gut-passage time of the animal may be important because it is approximately the length of time which enzymes have to hydrolyse the substrate. Ambient temperatures will also certainly affect the ability of enzymes to act on the food substrate. It should be noted that when preparing EPS substrates for enzymatic studies, heating and drying (i.e. lyophilising) has been found to alter the resistance of the EPS to polysaccharases (Scherrer, Berlin & Gerhardt, 1977). Substrates should therefore be used in a “never dried state”. The composition, structural interactions and tertiary arrangements of exopolymer varies depending on the nutrient conditions and growth phase of the bacterium. This can potentially affect the ability and efficiency of animal enzymes to degrade the EPS. A substrate may be conservative in its primary structure, but highly heterogeneous in its secondary and tertiary structures, which may conceal its resistance to attack by the enzyme preparations (Bacon, 1979). It is therefore
124
ALAN W.DECHO
difficult to generalise on the digestibility of EPS under natural conditions because the bacterial cells which secrete the EPS are living under a wide variety of growth and nutrient conditions. Also, non-enzymatic pre-digestion of EPS may occur (i.e. alkaline mid-gut) by transforming the EPS tertiary structure into a more readily degradable form (sensu Lopez & Levinton, 1987). The enzymatic degradation of EPS can be complex. Therefore, while the presence of certain groups of enzymes in consumer animal homogenates may suggest the ability to digest EPS, this evidence can only be considered as supportive evidence because other factors (described above) affect the action of these enzymes. Exopolymers in relation to other food resources Ultimately, however, to assess the nutritional quality of EPS as a food source for consumer animals, future studies must examine: (1) the general composition (i.e. C: N ratio); (2) the specific composition, such as essential nutrients (i.e. amino acids, essential fatty acid, etc.) of EPS under natural conditions; and (3) must take into account the role of adsorptive processes in altering these compositions such as the relative amounts of C and N, and essential nutrients gained via adsorption of DOM. In the past 40 years remarkable changes have taken place in the methodologies used in oceanic ecology. These changes have shifted (several times) our understanding and resulting paradigms concerning lower marine food webs. As new and more precise methods are used, we find ourseves rethinking fundamental processes. Where does exopolymer fit in with other potential food resources present in the marine environment? Non-cellular organic matter in sediments exists in different pools (Berner, 1980), the vast majority of which is thought to be relatively refractory (i.e. humic acids, fulvic acids, lignins, etc.). EPS, especially slime-EPS, may represent a highly labile form of non-cellular organic matter (Henrichs & Doyle, 1986; Decho & Moriarty, in press). Many animals which ingest sediment, detritus, and microalgae, also ingest bacterial cells closely associated with those other food resources. Most recently, the hypotheses regarding food resources of benthic deposit-feeders understate the role of bacteria, and suggest that these other components, such as diatoms, DOM, certain plant detritus, and EPS, make up the bulk.
Bacteria As a general food source bacterial cells contain a wide variety of proteins, carbohydrates, lipids, nucleic acids (i.e. phosphates), etc. In studies of consumer animals ingested bacteria can represent a large portion (70%) of the nitrogen requirements (Siebers, 1982; Newell & Field, 1983; Seiderer, Davis, Robb & Newell, 1984; Rice, Bianchi & Roper, 1986). In terms of specific nutrients, bacterial cells represent a source of certain essential nutrients such as the amino acid methionine (Morita, 1979) and B-complex vitamins (Phillips, 1984). Other essential nutrients such as polyunsaturated fatty acids (PUFA) and sterols, however, are characteristically lacking in bacteria. Therefore, bacterial cells by themselves do not contain all the essential nutrients for animals (Phillips, 1984) and in general are not ingested in sufficient quantities to satisfy general C requirements of animals (Cammen,
MICROBIAL EXOPOLYMER SECRETIONS
125
1980). Their importance to benthic animals as a food resource may be rather in their role as a general nitrogen source (Rice et al., 1986), and to supply certain supplemental nutrients. Diatoms and microalgae Diatoms represent a source of essential fatty acids (i.e. polyunsaturated fatty acids) for most marine invertebrates (Phillips, 1984), and hence represent a good source of essential nutrients. As a general source of carbon, diatoms and microalgae may represent a substantial portion of the carbon requirements for certain consumers (Newell & Field, 1983). Diatoms are known to be consumed by a variety of meiobenthic (see Hicks & Coull, 1983, for review) and macrobenthic animals (see Lopez & Levinton, 1987, for review). Cellular detritus The labile nature of various types of detritus as a food resource has been shown to vary depending on its origin and age (Tenore et al., 1984; and others). Even ‘refractory’ detritus has now been found to be assimilated at very low efficiencies (Kemp, 1986). Ingestion of large amounts of such detritus can cumulatively add up to an appreciable amount of carbon assimilated, even at low assimilation efficiencies. Also, the presence of specialised gut-flora which are capable of utilising the recalcitrant polysaccharides is now being recognised (Poole & Wildish, 1979) and may contribute to the ability of a consumer to digest cellulose, chitin, and other refractory compounds.
OTHER POTENTIAL ROLES OF EXOPOLYMERS IN FOOD WEBS
Role as a vehicle to transfer adsorbed-DOM and metals directly to higher trophic levels By virtue of their physical properties exopolymers are capable of adsorbing and concentrating many other organic molecules (Joyce & Dugan, 1970; Dugan, MacMillan & Pfister, 1970; Rees, 1976) and metals (Corpe, 1975; Brown & Lester, 1982; Rudd, Sterritt & Lester, 1983; Cowen & Silver, 1984; Cowen & Bruland, 1985). They are also in close association with microbial cells so they can potentially bind exudation and cell lysis products of algae and bacteria. This binding of DOM (and metals) to exopolymer may represent an important trophic process and the role of exopolymers in marine systems. The implication is that microbial consumer animals which ingest exopolymers under natural conditions, also ingest this additional adsorbed-DOM pool. LabileDOM (i.e. amino acids, fatty acids, etc.), adsorbed on exopolymer, can significantly enhance its nutritional value to consumer animals. EPS (especially their polysaccharide moieties) are known to bind and concentrate both low- and high-MW compounds (Rees, 1976). Although the quantitative effects of DOM-adsorption on the subsequent composition of EPS under natural conditions is not known, these processes suggest that the role of EPS in food webs may not be restricted to being a carbon source. Once the exopolymer (and its adsorbed-DOM) is in the gut of consumer animals, the DOM portion could theoretically be ‘desorbed’ from exopolymers by a simple pH change, because the binding affinities of exopolymers are dependent on pH (see p. 80 ). This could provide a non-enzymatic and relatively simple mechanism by which consumer animals can acquire DOM which is concentrated on the exopolymer. Gut pH changes of consumer animals, however, and the depuration of
126
ALAN W.DECHO
adsorbed compounds from particulate material while in the gut of consumers has not generally been investigated. The adsorptive processes of exopolymers can be potentially important in food webs in several ways. Exopolymers can sequester and concentrate DOM (and toxic metals) from sea water. The ingestion of this exopolymer-bound DOM by animals could represent a vehicle for DOM (and metals) to reach directly higher trophic levels (Fig 2). The binding of DOM to exopolymers may place the DOM into a more ‘bio-available’ state for animals to ingest (i.e. bound to particulate exopolymer). It has been shown, for example, that metals become more ‘bioavailable’ when they are adsorbed to exopolymers. They are more readily taken up and incorporated by sediment-feeding animals than the same metals which are in “free solution” or bound to acid-washed sediment particles (Harvey & Luoma, 1985). The binding abilities of exopolymers for metals and organic compounds have already been discussed (see p. 79 ). This may be especially important in the study of consumer animals which ingest particulate material such as water-column aggregates, sediment, detritus, and associated microbial cells. The investigation of such processes could be potentially applicable to nutrient fluxes processes. For example, it has been generally assumed that DOM (both low and high-MW compounds) are utilised primarily by bacteria. This pathway would bypass microbial cellular metabolism of the DOM and its associated losses via respiration of carbon dioxide. There are few data on the study of these adsorptive processes to exopolymer-mucus and their role in transferring DOM directly to higher trophic levels. These processes, however, must be examined closely as they may prove to be the most important aspect of exopolymers in food webs and flux processes. In their purified form, exopolymers are primarly carbon in composition (Kennedy & Sutherland, 1987). Adsorption of DOM can potentially enrich exopolymer particulates with nitrogenous compounds (i.e. amino acids, small polypeptides, etc.), and specific nutrients such as essential amino acids, fatty acids, and vitamins (i.e. derived from cell lysis). Such nitrogen-enrichment has been observed in coral mucus (Coles & Strathmann, 1973) and was shown to enrich the nutritive value of the exopolymer to consumer animals. Bowen (1980) found that “non-protein” amino acids, associated with microalgal and particulate matter derived from bacteria, were important in the diet and growth of Tilapia. These amino acids were presumably adsorbed to the aggregate-floc material (derived from microalgae and bacteria) upon which the fish fed. Joyce & Dugan (1970) found rapid adsorption of the amino acids arginine and alanine by exopolymer. The general adsorption of carbohydrates and amino acids to colloidal forms of biogenic polymeric material has also been observed (Means & Wijayaratne, 1984). Such studies support the idea that adsorption of “dissolved” organics onto “particulate” organic material is a commonly-occurring process (Balistrieri, Brewer & Murray, 1981). Microbial exopolymer films may represent labile adsorptive sponges, and may act as an efficient transfer mechanism for DOM to reach higher trophic levels. These processes warrant closer examination in marine systems. Exopolymer-capsules: a mechanism which may influence consumer utilisation of microbial cells as food Not all exopolymers may be similarly labile to consumer animals. Exopolymers exist as both capsules (immediately surrounding cells) as well as amorphous slime (on
MICROBIAL EXOPOLYMER SECRETIONS
127
aggregates and surfaces) (Fig 1a, p.75). While it appears that slime exopolymers are easily digested, there are indications which suggest that capsular exopolymers may be relatively refractory to consumer animals (Decho, pers. obs.). These capsules may actually protect the microbial cells from digestion during passage through the gut of consumer animals, and thus influence the ability of a consumer to utilise microbial cells as food. Evidence for the differential utilisation of microbial cells has been observed in a range of marine animals (see p. 87 ). In the digestion of a microbial cell by consumer enzymes, the exopolymer capsule (if present) represents a first line of resistance against lysis. EPS capsules are known to have many different ‘protective’ functions for microbial cells against lytic agents, bacteriophages, etc. It is therefore not unreasonable to speculate that the presence of a capsule may reduce the digestibility of the microbial cell enclosed within. Numerous studies have observed the viable passage of microbial cells through consumer guts. The exact means by which microbial cells survive digestion are not known for certain. Possible mechanisms by which capsular exopolymers may slow the digestion of a microbial cell and evidence supporting these ideas has already been discussed (see p. 123 ). In the relationship of exopolymer-capsules to animalmicrobial feeding processes it is not implied that encapsulated cells are nondigestible per se. Rather, it is suggested, that cells with capsules may survive gut passage with a greater frequency than other non-encapsulated cells, especially in animals with relatively short gut passage times. It is hoped that further experimentation will elucidate the mechanisms underlying the differential utilisation of microbial cells by consumer animals and the relative importance of capsular secretions in this process. One primary role of both microalgal and bacterial exopolymers may be to represent a labile source of carbon (and to a lesser extent nitrogen) supplements to the diet of microbial-feeding consumer animals. The quantities, compositions,
Fig 2. —Diagram showing conceptual role of microbial exopolymers in food webs. DOM is adsorbed and concentrated on exopolymers, and can then be directly transferred to consumer animals via ingestion of the exopolymers bypassing microbial metabolism of the DOM; consumer animals can therefore directly utilise DOM.
128
ALAN W.DECHO
and labile nature of exopolymers under natural conditions are not well understood. It is thought, however, that exopolymers under natural conditions may be higher in nitrogen content than laboratory studies have indicated. A major role of exopolymers may be to adsorb and efficiently transfer DOM directly to higher trophic levels. Exopolymers may acquire a variety of nutritionally important compounds through adsorption processes. Small amounts of exopolymer can potentially bind relatively large amounts of dissolved compounds. Their binding and concentration of labile low-MW DOM from sea water, and the adsorption of microbial exudates and cell lysis products may significantly enhance their composition as a food resource for consumer animals. Closer examination of their quantities and adsorptive processes under natural conditions is needed before their relative importance as a food resource can be ascertained. Ultimately, in assessing the functional importance of exopolymers in food webs and organic fluxes, the question of: How much exopolymer is present? may not be as important as: What kinds of exopolymers are present?
SUMMARY AND FUTURE DIRECTIONS FOR RESEARCH Exopolymer secretions are a ubiquitous component of marine systems. They serve many functions which enhance the survival and competitive success of microorganisms in a variety of aquatic, terrestrial, and host-pathogen environments. While their functional roles and intrinsic importance have been well demonstrated in many different systems, their functional importance in the marine environment has remained largely unexplored. In many aquatic systems, encapsulated bacteria and slime-producing bacteria comprise a numerically predominant part. Light microscopic observations of detrital material do not reveal the complex networks of extracellular fibrils and mucilage attributable to previous and current microbial growth periods. An undetermined portion of the carbon metabolised by microbial cells resides in extracellular form (i.e. as EPS). Just how important this potentially large carbon pool is as a food resource, and in the binding and transfer of nutrients and toxic compounds to higher trophic levels remains to be evaluated. Ultimately the significance of EPS in oceanic environments must be assessed not only in terms of its quantity, but also in terms of its quality (i.e. specific adsorptive capabilities and labile nature). Relatively small amounts of EPS can bind relatively large quantities of metals (and DOM), can induce aggregation processes, and affect the utilisation of microbial cells by animals. If exopolymers are highly labile, then relatively small amounts of exopolymer can contribute appreciably to the carbon requirements of a given consumer animal. The recognised presence of EPS has several potentially important implications which must be addressed for understanding marine processes. They are outlined below. (1) What portion of microbially-produced carbon resides in extracellular high-MW form (i.e. EPS)? This extracellular production is not typically included in microbial productivity estimates, but is directly available to higher trophic levels. Quantification
MICROBIAL EXOPOLYMER SECRETIONS
129
of bacterial and microalgal EPS concentrations in natural sediments and watercolumn aggregates, in different environments, and at different times of the year, represents a central point in assessing the availability of EPS to consumer animals. Conversion efficiencies of C into bacterial biomass generally range from 10 to 60% (see Williams, 1984; Cole, Findlay & Pace, 1988 for reviews). Therefore much of the carbon assimilated by bacteria is thought to be lost through respiration (rather than incorporated into cellular biomass). Under certain conditions, especially in sediments and aggregates, a significant portion of ‘non-cellular’ bacterial production may, however, be secreted in the form of EPS (Uhlinger & White, 1983). Labelled dissolved substrates are quickly metabolised by bacteria and converted into EPS material (Paerl, 1974). A large portion (62%) of the energy utilised by bacteria may be funnelled into EPS production (Jarman & Pace, 1984). Such extracellular material is typically not considered in bacterial productivity estimates (Paerl, 1980) but is potentially available to higher trophic levels because it is consumed along with microbial cells during grazing. Similarly, microalgae, especially during later stages of phytoplankton blooms, produce excessive amounts of extracellular slime (Smetacek, 1985). Such slime adsorbs and concentrates nutrients which are then available to both water-column and sediment consumers. The magnitude of this extracellular production and its effect on nutrient fluxes under these conditions is not known. (2) What are the turnover rates of microbial exopolymers under natural conditions? In addition to biomass estimations of exopolymer, it is also necessary to measure exopolymer turnover rates directly under natural conditions. Such estimates, however, have been conspicuously few. Future studies which directly measure turnover rates of exopolymer under natural conditions are a necessary step in assessing the fate, lability and persistence of this extracellular production in marine systems. (3) Do EPS secretions serve as a highly labile supplement for consumer animal food resources? Several studies have already demonstrated the utilisation of EPS by consumer animals. It is not known whether all animals which ingest sediment, detritus, and microbial cells, are capable of utilising the microbial EPS closely associated with them. The role of EPS as a source of labile carbon, nitrogen, and specific nutrients, relative to other potential foods (bacteria, microalgae, detritus) under natural conditions, requires further investigation. EPS secretions of both bacteria and microalgae appear to be ubiquitously distributed in the marine systems, especially in sediment environments. If exopolymers are highly labile, their role as a general carbon source can be potentially substantial in the diet of consumer animals. (4) Adsorption of DOM to EPS can occur and then be directly consumed by higher trophic levels. What is the relative importance of these adsorption process in both trophic and nutrient fluxes? By virtue of their physical nature, exopolymers have great adsorptive capabilities. This may represent an efficient mechanism for DOM (adsorbed onto the exopolymers) to be ingested and directly available to consumer animals: DOM → Adsorb to EPS → Consumer-Animal Ingestion. It has been suggested, that a significant portion of the turnover of DOM in nature (presumed to be via bacterial mineralisation) may be mediated by adsorption and concentration of these dissolved compounds to the mucus exopolymers (Paerl, 1974).
130
ALAN W.DECHO
(5)
(6)
(7)
(8)
(9)
The adsorptive properties of EPS, and their role in enhancing the nutritional quality of mucus exopolymers, must be examined in detail, as it may prove to be a most important aspect of EPS in marine systems. Certain EPS-capsular coatings may affect the digestibility of microbial cells by consumer animals. What is the overall significance of this process to microbial consumer animals? Is all exopolymer utilised similarly by animals? The answer is probably not. While some slime-EPS appears to be highly labile, other EPS in the form of capsules surrounding microbial cells appears to be relatively refractory. Exopolymer composition and tertiary structure is known to vary considerably between capsular and slime-exopolymer. These differences may affect the relative digestibility of certain EPS by consumer animals. Such EPScapsules may actually ‘protect’ some microbial cells from digestion by consumer animals. The full significance of this, in relation to digestibility of EPS by consumer animals, is not yet understood. Does the binding of small particles (i.e. silt-size), coated by EPS, affect the feeding processes of consumer animals which key on particle size for feeding? The ‘sticky’ nature of microbial mucous secretions can have important effects on the aggregation of particles. Aggregation processes have been shown to increase the efficiency of filter-feeders (Seki, 1972) in gathering particles. Robertson, Mills & Zieman (1982) observed that aggregates were formed via bacterial uptake of DOC released by seagrasses. These aggregates rapidly attained a size that could be ingested by macroconsumers. Similar EPS-mediated aggregation processes can occur in sediments and influence particle-selective deposit-feeders. What is the significance of EPS on detrital degradation and the formation of microgeochemical zones within sediments and aggregates? EPS-biofilms are known to occur within sediments, on the surfaces of detrital particles, and within open-water aggregates. The presence of EPS deposits throughout aggregates and on the surfaces of detrital particles can create microzones, with steep chemical and redox gradients. The gradients develop because of microbial activity and the effect of EPS on diffusion O2 and other compounds. This eventually results in anaerobic patches within aerobic sediments or waters. Within such micro-environments a variety of nutrient transformation processes can occur, such as cellulose digestion, N 2-fixation, ammonification, and denitrification. The development of diverse microbial and eukaryote communities within a small localised area concomitantly occurs. The dynamic nature of detrital microzones, and the crucial role they may play in nutrient availability and cycling in aquatic systems is now being realised. The regulating role of EPS in these microbiogeochemical processes requires closer examination. What is the relative importance of EPS in the transfer of metals and other toxins into food webs? Microbial exopolymers readily bind and concentrate a variety of metals. This binding enhances the bio-availability of metals to animals. Exopolymers may therefore represent an efficient vehicle for the entry and transfer of metals and other potentially toxic compounds through food webs. What is the role of EPS in the transformation and development of microbial communities on surfaces? Exogenous DNA is often found associated with EPS. This DNA can potentially transform microbial cells within the EPS matrix. Such transformation processes are thought to be important mechanisms in the survival and adaptation of microbial communities to changing and toxic environments.
MICROBIAL EXOPOLYMER SECRETIONS
131
Exogenous DNA which binds to EPS may be less prone to degradation by natural processes. This may increase its chances of being taken up and incorporated into the genome of competent microbial cells. These transformation processes are thought to foster the development of microbial consortia (i.e. groups of microbial cells which act as efficient metabolic units). Such processes may be important in the understanding the efficiency of detrital degradation and microbiogeochemical processes in marine environments. The above provides examples of the gaps and inadequacies of our current knowledge concerning the trophic role of exopolymers in marine (and fresh-water) environments and, it is hoped, will provide directions for future research.
ACKNOWLEDGEMENTS I thank J.W.Fleeger, C.Lee, G.R.Lopez, K.C.Marshall, and D.J.W. Moriarty for helpful conversations which sparked interest and appreciation of the potential interactions of exopolymers in marine systems. Parts of this review were assembled during and supported by a National Science Foundation Dissertation Improvement Grant (No. OCE 8313109) and a Fulbright-Hays Post-Doctoral Fellowship (CSIRO Marine Laboratories, Australia).
REFERENCES Aardema, B.W., Lorenz, M.G. & Krumbein, W.E., 1983. Protection of sedimentadsorbed transforming DNA against enzymatic inactivation. Appl. Environ. Microbiol., 46, 417–420. Abe, M., Sherwood, J.E., Hollingsworth, R.I. & Dazzo, F.B., 1984. Stimulation of clover root hair infection by lectin-binding oligosaccharides from the capsule and extracellular polysaccharides of Rhizobium trifolii. J. Bacteriol., 160, 517–520. Akin, D.E. & Amos, H.E., 1975. Rumen bacterial degradation of forage cell walls investigated by electron microscopy. Appl. Microbiol., 29, 692–701. Albright, L.J. & McCrae, S.K., 1987. Annual cycle of bacterial specific biovolumes in Howe Sound, a Canadian west coast fjord sound. Appl. Environ. Microbiol., 53, 2739–2744. Allan, G.G., Lewin, J. & Johnson, P.G., 1972. Marine polymers. IV. Diatom polysaccharides. Bot. Mar., 15, 102–108. Alldredge, A.L., 1979. The chemical composition of macroscopic aggregates in two neretic seas. Limnol. Oceanogr., 24, 855–866. Alldredge, A.L. & Cohen, Y., 1987. Can microscale chemical patches persist in the sea? Microelectrode study of marine snow, fecal pellets. Science, 235, 689–691. Alldredge, A.L., Cole, J.J. & Caron, D.A., 1986. Production of heterotrophic bacteria inhabiting macroscopic organic aggregates (marine snow) from surface waters. Limnol. Oceanogr., 31, 68–78. Anderson, L.W.J. & Sweeney, B.M., 1978. Role of inorganic ions in controlling sedimentation rate of a marine centric diatom Ditylum brightwelli. J. Phycol., 14, 204–214.
132
ALAN W.DECHO
Annison, G. & Couperwhite, I., 1986. Influence of calcium on alginate production and composition in continuous cultures of Azotobacter vinelandii. Appl. Microbiol. Biotechnol, 25, 55–61. Anton, J., Meseguer, I. & Rodriguez-Valera, F., 1988. Production of an extracellular polysaccharide by Haloferax mediterranei. Appl. Environ. Microbiol., 54, 2381– 2386. Aspinall, G.O., 1982a. General introduction. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 1–18. Aspinall, G.O., 1982b. Isolation and fractionation of polysaccharides. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 19–35. Aspinall, G.O., 1982c. Chemical characterization and structure determination of polysaccharides. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 36–132. Aspinall, G.O., 1983. Classification of polysaccharides. In, The Polysaccharides, Vol. 2, edited by G.O.Aspinall, Academic Press, New York, pp. 1–11. Avery, O.T., MacLeod, C.M. & McCarty, M., 1944. Studies on the chemical nature of the substance including transformation of pneumococcal types. Induction of transformation by deoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med., 79, 137–158. Aveyard, R. & Haydon, D.A., 1973. An Introduction to the Principles of Surface Chemistry. Cambridge University Press, Cambridge, UK, 232 pp. Bacon, J.S.D., 1979. Factors limiting the action of polysaccharide degrading enzymes. In, Microbial Polysaccharides and Polysaccharases, edited by R.C.W.Berkeley et al., Academic Press, New York, pp. 269–284. Baird, B.H. & Thistle, D., 1986. Uptake of bacterial extracellular polysaccharides by a deposit-feeding holothurian (Isostichopus badionotus). Mar. Biol., 92, 183– 187. Baker, C.J. & Kasper, D.L., 1976. Microcapsule of type III strains of group B Streptococcus: production and morphology. Infect. Immun., 13, 189–194. Balistrieri, L., Brewer, P.G. & Murray, J.W., 1981. Scavenging residence times of trace metals and surface chemistry of sinking particles in the deep ocean. DeepSea Res., 28A, 101–121. Bartlett, D.H. & Silverman, M., 1989. Nucleotide sequence of IS492, a novel insertion sequence causing variation in extracellular polysaccharide production in the marine bacterium Pseudomonas atlantica. J. Bacteriol., 171, 1763–1766. Bartlett, D.H., Wright, M.E. & Silverman, M., 1988. Variable expression of extracellular polysaccharide in the marine bacterium Pseudomonas atlantica is controlled by genome rearrangement. Proc. Natl. Acad. Sci. USA, 85, 3923– 3927. Bayer, M.E. & Thurow, H., 1977. Polysaccharide capsule of Escherichia coli: micro scopic study of its size, structure and site of synthesis. J. Bacteriol., 130, 911– 936. Berner, R.A., 1980. A rate model for organic matter decomposition during bacterial sulfate reduction in marine sediments. Colloq. Int. CNRS, 293, 35–44. Beveridge, T.J. & Murray, R.G.E., 1980. Sites of metal deposition in the cell wall of Bacillus subtilus. J. Bacteriol., 141, 876–887. Biddanda, B.A., 1985. Microbial synthesis of macroparticulate matter. Mar. Ecol. Prog. Ser., 20, 241–251. Biddanda, B.A., 1988. Microbial aggregation and degradation of phytoplanktonderived detritus in seawater . II. Microbial metabolism. Mar. Ecol. Prog. Ser., 42, 89–95. Biddanda, B.A. & Pomeroy, L.R., 1988. Microbial aggregation and degradation of phytoplankton-derived detritus in seawater . I. Microbial succession. Mar. Ecol. Prog. Ser., 42, 79–88.
MICROBIAL EXOPOLYMER SECRETIONS
133
Bienfang, P.K., Szyper, J. & Laws, E., 1983. Sinking rate and pigment responses to light-limitation of a marine diatom: implications to dynamics of chlorophyll maximum layers. Oceanol. Acta, 6, 55–62. Bishop, C.T. & Jennings, H.J., 1982. Immunology of polysaccharides. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 292–330. Bitton, G. & Friehofer, V., 1978. Influence of extracellular polysaccharides on the toxicity of copper and cadmium toward Klebsiella aerogenes. Microb. Ecol., 4, 119–125. Bligh, E.G. & Dyer, W.J., 1959. A rapid method of lipid extraction and purification. Can. J. Biochem. Physiol., 35, 911–917. Bodungen, B. von, Brockel, K.V., Smetacek, V. & Zeitzschel, B., 1981. Growth and sedimentation of the phytoplankton spring bloom in the Bornholm Sea (Baltic Sea). Kieler Meeresforsch. Sonderh., No. 5, 49–60 . Bodungen, B. von, Smetacek, V., Tilzer, M.M. & Zeitzschel, B., 1986. Primary production and sedimentation during spring in the Antarctic Peninsula region. Deep-Sea Res., 33A, 177–194. Bonar, D.B., Weiner, R.M. & Colwell, R.R., 1986. Microbial-invertebrate interactions and potential for biotechnology. Microb. Ecol., 12, 101–110. Bowen, S.H., 1980. Detrital nonprotein amino acids are the key to rapid growth of Tilapia in Lake Valencia, Venezuala. Science, 207, 1216–1218. Boyle, C.D. & Reade, A.E., 1983. Characterization of two extracellular polysaccharides from marine bacteria. Appl. Environ. Microbiol., 46, 392–399. Bradford, M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye-binding. Anal. Biochem., 72, 248–254. Brancato, M.S. & Woollacott, R.M., 1982. Effect of microbial films on settlement of bryozoan larvae (Bugula simplex, B. stolonifera, and B. turrita). Mar. Biol., 71, 51–56. Bratbak, G., 1985. Bacterial biovolume and biomass estimations. Appl. Environ. Microbiol., 49, 1488–1493. Brautigam, E., Fiedler, F., Woitzik, D., Flammann, H.T. & Weckesser, J., 1988. Capsule polysaccharide-protein-peptidoglycan complex in the cell envelope of Rhodobacter capsulatus. Arch. Microbiol., 150, 567–573. Bremer, P.J. & Loutit, M.W., 1986. Bacterial polysaccharide as a vehicle for entry of Cr (III) to a food chain. Mar. Environ. Res., 20, 235–248. Brown, C.M., Ellwood, D.C. & Hunter, J.R., 1977. Growth of bacteria at surfaces. FEMS Lett., 1, 163–166. Brown, M.J. & Lester, J.N., 1979. Metal removal in activated sludge: the role of bacterial extracellular polymers. Water Res., 13, 817–837. Brown, M.J. & Lester, J.N., 1982. Role of bacterial extracellular polymers in metal uptake in pure bacterial culture and activated sludge. I. Effects of metal concentration. Water Res., 16, 1539–1548. Buckmire, F.L.A., 1984. Influence of nutrient media on the characteristics of the exopolysaccharide produced by three mucoid Pseudomonas aeruginosa strains. Microbios, 41, 49–63. Burney, C.M., 1986. Bacterial utilization of total in situ dissolved carbohydrate in offshore waters. Limnol. Oceanogr., 31, 427–431. Busch, P.L. & Stumm, W., 1968. Chemical interactions in the aggregation of bacteria: bioflocculation in waste treatment. Environ. Sci. Technol., 2, 49–53. Butman, C.A., 1987. Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanogr. Mar. Biol. Annu. Rev., 25, 113–165. Cammen, L., 1980. The significance of microbial carbon in the nutrition of the deposit-feeding polychaete Nereis succinea. Mar. Biol., 61, 9–20.
134
ALAN W.DECHO
Carlsson, J., 1967. Dental plaque as a source of salivary streptococci. Odont. Rev., 18, 173–180. Caron, D.A., 1987. Grazing of attached bacteria by heterotrophic microflagellates. Microb. Ecol., 13, 203–218. Chamberlain, A.H.L., 1976. Algal settlement and secretion of adhesive materials. In, Proc. 3rd Int. Biodegrad. Symp., edited by J.M.Sharpley & A.M.Kaplan, Applied Science Publishers, London, pp. 417–432. Chambers, J.E., Heitz, J.R., McCorkle, F.M. & Yarbrough, J.D., 1978. The effects of crude oil on enzymes in the brown shrimp (Penaeus sp.). Comp. Biochem. Physiol, 61C, 29–32. Chan, R., Acres, S.D. & Costerton, J.D., 1982. The use of specific antibody to demonstrate glycocalyx, K99 pili, and the spatial relationships of K99 + enterotoxigenic E. coli in the ileum of colostrum-fed calves. Infect. Immun., 37, 1170–1180. Chang, H.T. & Rittman, B.E., 1986. Biofilm loss during sample preparation for scanning electron microscopy. Water Res., 20, 1451–1456. Characklis, W.G. & Cooksey, K.E., 1983. Biofilms and microbial biofouling. Adv. Appl. Microbiol, 29, 93–138. Characklis, W.G., Nimmons, M.J. & Picologlou, B.F., 1981. Influence of fouling biofilms on heat transfer. J. Heat Transfer Eng., 3, 23–37. Cheng, K.G., Ingram, J.M. & Costerton, J.M., 1970. Release of alkaline phosphatase from cells of Pseudomonas aeruginosa by manipulation of cation concentration and of pH. J. Bacteriol., 104, 748–753. Cheng, M.H., Patterson, J.W. & Minear, R.A., 1975. Heavy metals uptake by activated sludge. J. Wat. Pollut. Control Fed., 47, 362–376. Chester, I.R. & Murray, R.G.E., 1978. Protein-lipid-lipopolysaccharide association in the superficial layer of Spirillum serpens cell walls. J. Bacteriol., 133, 932– 941. Christensen, B.E., Kjosbakken, J. & Smidsrod, O., 1985. Partial chemical and physical characterization of two extracellular polysaccharides produced by marine periphytic Pseudomonas sp. strain NCMB 2021. Appl. Environ. Microbiol., 50, 837–845. Chua, K.E. & Brinkhurst, R.O., 1973. Bacteria as potential nutritional resources for three sympatric species of tubificid oligochaetes. In, Estuarine Microbial Ecology, edited by L.H.Stevenson & R.R.Colwell, University of South Carolina Press, Columbia, pp. 513–517. Coffin, R.B., 1989. Bacterial uptake of dissolved free and combined amino acids in estuarine waters. Limnol. Oceanogr., 34, 531–542. Cole, J.J., Findlay, S. & Pace, M.L., 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar. Ecol. Prog. Ser., 43, 1–10. Coles, S.L. & Strathmann, R., 1973. Observations on coral mucus “flocs” and their potential trophic significance. Limnol. Oceanogr., 18, 673–678. Cooksey, B. & Cooksey, K.E., 1980. Calcium is necessary for motility in the diatom Amphora coffeaeformis. Plant Physiol., 65, 129–131. Cooksey, K.E., 1981. Requirement for calcium in adhesion of a fouling diatom to glass. Appl. Environ. Microbiol., 41, 1378–1382. Cooksey, K.E. & Cooksey, B., 1986. Adhesion of fouling diatoms to surfaces: some biochemistry. In, Algal Biofouling, edited by L.V.Evans & K.D.Hoagland, Elsevier Science Publ., Amsterdam, pp. 41–53. Corpe, W.A., 1970. An acid polysaccharide produced by primary film forming bacteria. Develop. Ind. Microbiol., 11, 402–412. Corpe, W.A., 1972. Periphytic marine bacteria and the formation of microbial films on solid surfaces. In, Effect of Ocean Environment on Microbial Activities, edited by R.Colwell & R.Morita, University Park Press, Baltimore, USA, pp. 397–417.
MICROBIAL EXOPOLYMER SECRETIONS
135
Corpe, W.A., 1975. Metal-binding properties of surface materials from marine bacteria. Dev. Ind. Microbiol., 16, 249–255. Corpe, W.A., 1980. Microbial surface components involved in adsorption of microorganisms onto surfaces. In, Adsorption of Microorganisms to Surfaces, edited by G.Bitton & K.C.Marshall, John Wiley & Sons, New York, pp. 105–144. Corpe, W.A., Matsuuchi, L. & Armbruster, B., 1976. Secretion of adhesive polymers of marine bacteria to surfaces. In, Proc. 3rd Int. Biodegrad. Symp., edited by Applied Science Publishers, London, pp. 433–442. Costerton, J.W., 1974. Structure and function of the cell envelope of gram-negative bacteria. Bacteriol. Rev., 38, 87–110. Costerton, J.W., 1980. Some techniques involved in study of adsorption of microorganisms to surfaces. In, Adsorption of Microorganisms to Surfaces, edited by G.Britton & K.C.Marshall, John Wiley & Sons, New York, pp. 403– 423. Costerton, J.W., 1984. Mechanisms of microbial adhesion to surfaces. Direct ultrastructural examination of adherent bacterial populations in natural and pathogenic ecosystems. In, Current Perspectives in Microbial Ecology, Proc. 3rd Int. Symp. Microbial Ecol., edited by M.J.Klug & C.A.Reddy, pp. 115–123. Costerton, J.W. & Cheng, K.J., 1975. The role of the bacterial cell envelope in antibiotic resistance. J. Antimicrob. Chemotherapy, 1, 363–377. Costerton, J.W., Cheng, K.J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M. & Marrie, T.J., 1987. Bacterial biofilms in nature and disease. Ann. Rev. Microbiol., 41, 435–464. Costerton, J.W. & Colwell, R.R., 1979. Native Aquatic Bacteria: Enumeration, Activity and Ecology. ASTM Press, Philadelphia, 214 pp. Costerton, J.W., Damgaard, H.N. & Cheng, K.J., 1974. Cell envelope morphology of rumen bacteria. J. Bacteriol., 118, 1132–1143. Costerton, J.W., Geesey, G.G. & Cheng, K.J., 1978. How bacteria stick. Sci. Am., 238, 86–95. Costerton, J.W., Irvin, R.T. & Cheng, K.J., 1981. The bacterial glycocalyx in nature and disease. Annu. Rev. Microbiol., 35, 299–324. Costerton, J.W., Marrie, T.J. & Cheng, K.J., 1985. Phenomenon of bacterial adhesion. In, Bacterial Adhesion, edited by D.C.Savage & M.Fletcher, Plenum Press, New York, pp. 3–43. Cowen, J.P. & Bruland, K.W., 1985. Metal deposits associated with bacteria: implications for Fe and Mn marine biogeochemistry. Deep-Sea Res., 32A, 253– 272. Cowen, J.P., Massoth, G.J. & Baker, E.T., 1986. Bacterial scavenging of Mn and Fe in a mid- to far-field hydrothermal particle flume. Nature (London), 322, 169– 171. Cowen, J.P. & Silver, M.W., 1984. The association of iron and manganese with bacteria on marine macro participate material. Science, 224, 1340–1342. Crayton, M.A., 1982. A comparative cytochemical study of volvocacean matrix polysaccharides. J. Phycol., 18, 336–344. Crumpton, W.G. & Wetzel, R.G., 1982. Effects of differential growth and mortality in the seasonal succession of phytoplankton populations in Lawrence Lake, Michigan. Ecology, 63, 1729–1739. Daniel, G.F. & Chamberlain, A.H.L., 1981. Copper immobilization in fouling diatoms. Bot. Mar., 24, 229–243. Daniel, G.F., Chamberlain, A.H.L. & Jones, E.B.G., 1980. Ultrastructural observations on the fouling diatom Amphora. Helgol. Meeresunters., 34, 123– 149. Danielsson, A., Norkrans, B. & Bjornsson, A., 1977. On bacterial adhesion and the effect of certain enzymes on adhered cells of a marine Pseudomonas sp. Bot. Mar., 20, 13–17.
136
ALAN W.DECHO
Darbyshire, B., 1974. The function of the carbohydrate units of three fungal enzymes in their resistance to dehydration. Plant Physiol., 54, 717–721. Daumas, R. & Thomassin, B.A., 1977. Protein fractions in coral and zoantharian mucus: possible evolution in coral reef environments. In, Proc. 3rd Int. Symp. Coral Reefs, edited by D.L.Taylor, University of Miami, Florida, pp. 517–523. Dea, I.C.M., McKinnon, A.A. & Rees, D.A., 1972. Tertiary and quaternary structure in aqueous polysaccharide systems which model cell wall cohesion: reversible changes in conformation and association of agarose, carogeenan, and galactomannans. J. Mol. Biol., 58, 153–172. Decho, A.W. & Castenholz, R.W., 1986. Spatial patterns and feeding of meiobenthic harpacticoid copepods in relation to resident microbial flora. Hydrobiologia, 131, 87–96. Decho, A.W. & Moriarty, D.J.W., in press. Investigation of bacterial mucusexopolymer utilization by marine animals. Methodology and results using harpacticoid copepods. Limnol. Oceanogr. DeFlaun, M.F. & Mayer, L.M., 1983. Relationships between bacteria and grain surfaces in intertidal sediments. Limnol. Oceanogr., 28, 873–881. DeFlaun, M.F., Paul, J.H. & Davis, D., 1986. A simplified method for dissolved DNA determination in aquatic environments. Appl. Environ. Microbiol., 52, 654–659. Dempsey, M.J., 1981. Marine bacterial fouling: a scanning electron microscope study. Mar. Biol., 61, 305–315. Deretic, V., Dikshit, R., Konyecsni, W.M., Chakrabarty, A.M. & Misra, T.K., 1989. The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J. Bacteriol., 171, 1278–1283. Deutsch, A., 1978. Gut structure and digestive physiology of two marine nematodes Chromadorina germanica (Butschli, 1847) and Diplolaimella sp. Biol. Bull. (Woods Hole, Mass.), 155, 317–335. Dillon, P.S., Maki, J.S. & Mitchell, R., 1989. Adhesion of Enteromorpha swarms to microbial films. Microb. Ecol., 17, 39–47. DiSlavo, L.H. & Daniels, W.G., 1975. Observations on estuarine microfouling using the scanning electron microscope. Microb. Ecol., 2, 234–240. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. & Smith, F., 1956. Colorimetric methods for determination of sugars and related substances. Anal. Chem., 28, 350–356. Ducklow, H. & Mitchell, R., 1979a. Composition of mucus released by coral reef coelenterates. Limnol. Oceanogr., 24, 706–714. Ducklow, H. & Mitchell, R., 1979b. Bacterial populations and adaptations in the mucus layers on living corals. Limnol. Oceanogr., 24, 715–725. Dudman, W.F., 1977. The role of surface polysaccharides in natural environments. In, Surface Carbohydrates of the Prokaryote Cell, edited by I.W.Sutherland, Academic Press, New York, pp. 357–414. Dugan, P.R., MacMillan, C.B. & Pfister, R.M., 1970. Aerobic heterotrophic bacteria indigenous to pH 2.8 acid mine water: microscopic examination of acid streamers. J. Bacteriol., 101, 973–981. Dugan, P.R. & Pickrum, H.M., 1972. Removal of mineral ions from water by microbially produced polymers. Proc. 27th Ind. Waste Conf. Purdue Univ. Engng. Ext. Ser. No. 141, 1019–1038. Duguid, J.P., 1951. The demonstration of bacterial capsules and slime. J. Pathol. Bacteriol., 63, 673–685. Edgar, L.A. & Pickett-Heaps, J.D., 1984. Diatom locomotion. In, Progress in Phycological Research, Vol. 3, edited by F.E.Round & D.J.Chapman, Biopress Ltd., Bristol, UK, pp. 47–88. Epp, R.W. & Lewis, W.M., 1981. Photosynthesis in copepods. Science, 214, 1349– 1350.
MICROBIAL EXOPOLYMER SECRETIONS
137
Eppley, R.W., Renger, E.H. & Betzer, P.R., 1983. The residence time of particulate organic carbon in the surface layer of the ocean. Deep-Sea Res., 30A, 311–323. Evans, L.R., Callow, M.E., Percival, E. & Fareed, V., 1974. Studies on the synthesis and composition of extracellular mucilage in the unicellular red alga Rhodella. J. Cell Sci., 16, 1–21. Evans, L.R. & Linker, A., 1973. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J. Bacteriol., 116, 915–924. Fallon, R.D., Newell, S.Y. & Hopkinson, C.S., 1983. Bacterial production in marine sediments: will cell-specific measures agree with whole system metabolism. Mar. Ecol. Prog. Ser., 11, 119–127. Fattom, A. & Shilo, M., 1985. Production of emulcyan by Phormidium J-1: its activity and function. FEMS Microb. Ecol, 31, 3–9. Fattom, S.R. & Shilo, M., 1984. Hydrophobicity as an adhesion mechanism of benthic cyanobacteria. Appl. Environ. Microbiol., 47, 135–143. Fazio, S.A., Uhlinger, D.J., Parker, J.H. & White, D.C., 1982. Estimations of uronic acids as quantitative measures of extracellular and cell wall polysaccharide polymers from environmental samples. Appl. Environ. Microbiol., 43, 1151– 1159. Fenchel, T. & Jørgensen, B.B., 1977. Detritus food chains of aquatic ecosystems: the role of bacteria. In, Advances in Microbial Ecology, Vol. 1, edited by M. Alexander, Plenum Press, New York, pp. 3–37. Ferris, F.G., Schultze, S., Witten, T.C., Fyfe, W.S. & Beveridge, T.J., 1989. Metal interactions with microbial biofilms in acidic and neutral pH environments. Appl. Environ. Microbiol., 55, 1249–1257. Findlay, S. & Meyer, J.L., 1984. Significance of bacterial biomass and production as an organic carbon source in lotic detrital systems. Bull. Mar. Sci., 35, 318– 325. Findlay, S., Meyer, J.L. & Smith, P.J., 1984. Significance of bacterial biomass in the nutrition of a freshwater isopod (Lirceus sp.), Oecologia (Berlin), 63, 38– 42. Fleming, J.M. & Coughlan, J., 1978. Preservation of vitally stained zooplankton for live dead sorting.. Estuaries, 1, 135–137. Fletcher, M., 1980a. The characteristics of interfaces and their role in microbial attachment. In, Microbial Adhesion to Surfaces, edited by R.C.W.Berkeley, et al., Ellis Horwood Limited, Chichester, pp. 67–78. Fletcher, M., 1980b. The question of passive versus active attachment mechanisms in non-specific bacterial adhesion. In, Microbial Adhesion to Surfaces, edited by R.C.W.Berkeley et al., Ellis Horwood Limited, Chichester, pp. 197–210. Fletcher, M., 1980c. Adherence of marine microorganisms to smooth surfaces. In, Bacterial Adherence, edited by E.H.Beachey, Chapman & Hall, London, pp. 347–374. Fletcher, M., 1988. Effects of electrolytes on attachment of aquatic bacteria to solid surfaces. Estuaries, 11, 226–230. Fletcher, M. & Floodgate, G.D., 1973. An electron microscope demonstration of an acid polysaccharide involved in adhesion of a marine bacterium to solid surfaces. J. Gen. Microbiol., 74, 325–334. Fletcher, M. & Floodgate, G.D., 1976. The adhesion of bacteria to solid surfaces. In, Ultrastructure: the Use of the Electron Microscope, edited by R.Fuller & D. W.Lovelock, Academic Press, New York, pp. 101–107. Fletcher, M. & Marshall, K.C., 1982a. Are solid surfaces of ecological significance to aquatic bacteria? In, Advances in Microbial Ecology, edited by K.C.Marshall, Plenum Press, New York, pp. 199–236. Fletcher, M. & Marshall, K.C., 1982b. A bubble contact angle method for evaluating substratum interfacial characteristics and its relevance to bacterial attachment. Appl. Environ. Microbiol., 44, 184–192.
138
ALAN W.DECHO
Fletcher, M. & McEldowney, S., 1984. Microbial attachment to non-biological surfaces. In, Current Perspectives in Microbial Ecology, edited by M.J.Klug & C.A.Reddy, American Society of Microbiology, pp. 124–129. Floodgate, G.D., 1972. The mechanism of bacterial attachment to detritus in aquatic systems. Mem. Ist Ital. Idrobiol. Suppl., 29, 309–323. Foster, R.C., 1981. Polysaccharides in soil fabrics. Science, 214, 665–667. Frankel, L. & Mead, D.J., 1973. Mucilaginous matrix of some estuarine sands in Connecticut. J. Sediment. Petrol., 43, 1090–1095. Friedman, B.A., Dugan, P.R., Pfister, R.M. & Remsen, C.C., 1969. Structure of exocellular polymers and their relationship to bacterial flocculation. J. Bacteriol., 98, 1328–1334. Geesey, G.G., 1982. Microbial exopolymers: ecological and economic considerations. Am. Soc. Microbiol. News, 48, 9–14. Geesey, G.G., Mutch, R., Costerton, J.W. & Green, R.B., 1978. Sessile bacteria: an important component of the microbial population in small mountain streams. Limnol. Oceanogr., 23, 1214–1223. Gelder, S.R., 1978. Observations in selected free-living and symbiotic polychaetes and oligochaetes (Annelida). Ph.D. thesis, University of Leeds, Leeds. Ghuysen, J.M., Tripper, D.J. & Strominger, J.L., 1966. Enzymes that degrade bacterial cell walls. In, Methods in Enzymology: Complex Carbohydrates, Vol. 8, edited by E.F.Neufeld & V.Ginsberg, Academic Press, New York, pp. 685– 699. Gilbert, P., Allison, D.G., Evans, D.J., Handley, P.S. & Brown, M.R.W., 1989. Growth rate control of adherent bacterial populations. Appl. Environ. Microbiol., 55, 1308–1311. Goldman, J.C., 1984. Conceptual role for microaggregates in pelagic waters. Bull. Mar. Sci., 35, 462–476. Goldstein, I.J. & Hayes, C.E., 1978. The lectins: carbohydrate-binding proteins of plants and animals. Adv. Carbohydr. Chem. Biochem., 35, 127–340. Gotschlich, E.C., Fraser, B.A., Nishimura, O., Robbins, J.B. & Liu, T.Y., 1981. Lipid on capsular polysaccharides of gram-negative bacteria. J. Biol. Chem., 256, 8915–8921. Gottfried, M. & Roman, M.R., 1983. Ingestion and incorporation of coral-mucus detritus by reef zooplankton. Mar. Biol., 72, 211–218. Grant, J. & Bathmann, U.V., 1987. Swept away: resuspension of bacterial mats regulates benthic-pelagic exchange of sulfur. Science, 236, 1472–1474. Grant, J., Bathmann, U.V. & Mills, E.L., 1986. The interactions between benthic diatom films and sediment transport. Estuarine Coastal Shelf Sci., 23, 225– 238. Grant, W.D., Boyer, L.F. & Sanford, L.P., 1982. The effects of bioturbation on the initiation of motion of intertidal sands. J. Mar. Res., 40, 659–677. Gray, G.W. & Wilkinson, S.G., 1965. The effect of ethylene diaminetetraacetic acid on the cell walls of some gram-negative bacteria. J. Gen. Microbioi, 39, 385–399. Griffiths, P.R., 1977. Chemical Infrared Fourier Transforming Spectroscopy. John Wiley & Sons, New York, 340 pp. Hacking, A.J., Taylor, I.W.F., Jarman, T.R. & Govan, J.R.W., 1983. Alginate biosynthesis by Pseudomonas mendocina. J. Gen. Microbiol., 129, 3473–3480. Hamilton, W.A., 1985. Sulphate-reducing bacteria and anaerobic corrosion. Ann. Rev. Microbioi., 39, 195–217. Handa, N., 1969. Carbohydrate metabolism in the marine diatom Skeletonema costatum. Mar. Biol., 4, 208–214. Harris, R.H. & Mitchell, R., 1973. The role of polymers in microbial aggregation. Annu. Rev. Microbiol., 27, 27–50.
MICROBIAL EXOPOLYMER SECRETIONS
139
Harvey, R.W., 1981. Lead-bacterial interactions in an estuarine salt marsh microlayer. Ph.D. thesis, Stanford University, Stanford, 161 pp. Harvey, R.W. & Luoma, S.N., 1984. The role of bacterial exopolymer and suspended bacteria in the nutrition of the deposit-feeding clam, Macoma balthica. J. Mar. Res., 42, 957–968. Harvey, R.W. & Luoma, S.N., 1985. Effect of adherent bacteria and bacterial extracellular polymers upon assimilation by Macoma balthica of sedimentbound Cd, Zn and Ag. Mar. Ecol Prog. Ser., 22, 281–289. Hastings, J.W. & Nealson, K.H., 1982. The symbiotic luminous bacteria. In, The Prokaryotes, edited by M.P.Starr et al., Springer-Verlag, Berlin, pp. 1332– 1346. Henrichs, S.M. & Doyle, A.P., 1986. Decomposition of 14C-labeled organic substances in marine sediments. Limnol. Oceanogr., 31, 765–778. Hermansson, M. & Marshall, K.C., 1985. Utilization of surface localized substrate by non-adhesive marine bacteria. Microb. Ecol., 11, 91–105. Hicks, G.R.F., 1988. Sediment rafting: a novel mechanism for the small-scale dispersal of intertidal estuarine meiofauna. Mar. Ecol. Prog. Ser., 48, 69–80. Hicks, G.R.F. & Coull, B.C., 1983. The ecology of marine meiobenthic harpacticoid copepods. Oceanogr. Mar. Biol. Annu. Rev., 21, 67–175. Hill, S., 1971. Influence of oxygen concentration on the colony type of Derxia gummosa grown on nitrogen-free media. J. Gen. Microbiol., 67, 77–83. Hobbie, J. & Lee, C., 1980. Microbial production of extracellular material: importance in benthic ecology. In, Marine Benthic Dynamics, edited by K.R.Tenore & B. C.Coull, University of South Carolina Press, Columbia, pp. 341–346. Hodson, R.E., Maccubin, A.E. & Pomeroy, L.R., 1981. Dissolved adenosine triphosphate utilization by free-living and attached bacterioplankton. Mar. Biol., 64, 43–51. Holland, A.F., Zingmark, R.G. & Dean, J.M., 1974. Quantitative evidence concerning the stabilization of sediments by marine benthic diatoms. Mar. Biol., 27, 191–196. Holm-Hansen, O., Sutcliffe, W.H. & Sharp, J., 1968. Measurement of deoxyribonucleic acid in the ocean and its ecological significance. Limnol. Oceanogr., 13, 507–514. Horan, N.J. & Eccles, C.R., 1986. Purification and characterization of extracellular polysaccharide from activated sludges. Water Res., 11, 1427– 1432. Horsley, R.W., 1977. A review of the bacterial flora of teleosts and elasmobranchs, including methods for its analysis. J. Fish Biol., 10, 529– 553. Humphrey, B.A., Dickson, M.R. & Marshall, K.C., 1979. Physiochemical and in situ observations on the adhesion of gliding bacteria to surfaces. Arch. Microbiol., 120, 231–238. Huntsman, S.A. & Sloneker, J.H., 1971. An exocellular polysaccharide from the diatom Gomphonema olivaceum. J. Phycol., 7, 261–264. Ikeda, F., Shuto, H., Sato, T., Fukui, T. & Tomita, K., 1982. An extracellular polysaccharide produced by Zoogloea ramigera 115. Eur. J. Biochem., 123, 33–40. Jann, K. & Jann, B., 1985. Cell surface components and virulence: Escherichia coli O and K antigens in relation to virulence and pathogenicity. In, The Virulence of Escherichia coli, edited by M.Sussman, Academic Press, New York, pp. 156–176. Jann, K., Jann, B., Schneider, K.F., Orskov, F. & Orskov, I., 1968. Immunochemistry of K antigens of Escherichia coli. Eur. J. Biochem., 5, 456–465.
140
ALAN W.DECHO
Jannasch, H.W. & Wirsen, C.O., 1981. Microbiological survey of microbial mats near deep sea thermal vents. Appl. Environ. Microbiol., 41, 528–538. Jarman, T.R., Deavin, L., Slocombe, S. & Righelato, R.C., 1978. Investigation of the effect of environmental conditions on the rate of exopolysaccharide synthesis in Azotobacter vinelandii. J. Gen. Microbiol., 107, 59–64. Jarman, T.R. & Pace, G.W., 1984. Energy requirements for microbial exopolysaccharide synthesis. Arch. Microbiol., 137, 231–235. Jennings, H.J. & Smith, I.C.P., 1978. Polysaccharide structures using Carbon-13 Nuclear Magnetic Resonance. Methods Enzymol., 50, 39–50. Jennings, J.B. & Gelder, S.R., 1976. Observations on the feeding mechanism, diet, and digestive physiology of Histriobdella homari van Beneden 1858: an aberrant polychaete symbiotic with North American and European lobsters. Biol. Bull. (Woods Hole, Mass.), 151, 489–517. Jenson, K.T. & Siegismund, H.R., 1980. The importance of diatoms and bacteria in the diet of Hydrobia sp. Ophelia, 17 (Suppl.), 193–199. Jones, H.C., Roth, I.L. & Sanders, W.M., 1969. Electron microscopic study of a slime layer. J. Bacteriol., 99, 316–325. Jørgensen, B.B. & Revsbech, N.P., 1983. Colorless sulfur bacteria, Beggiatoa spp., in O and H S microgradients. Appl. Environ. Microbiol., 45, 1261– 2 2 1270. Joyce, G.H. & Dugan, P.R., 1970. The role of floc-forming bacteria in BOD removal from waste water. Dev. Ind. Microbiol., 11, 377–386. Juniper, S.K., 1987a. Deposit-feeding ecology of Amphibola crenata. I. Longterm effects of deposit feeding on sediment microorganisms. N. Z. J. Mar. Fresw. Res., 21, 235–246. Juniper, S.K., 1987b. Deposit-feeding ecology of Amphibola crenata. II. Contribution of microbial carbon to Amphibola’s carbon requirements. N. Z. J. Mar. Fresh-water Res., 21, 247–251. Juniper, S.K., Thompson, J.A.J. & Calvert, S.E., 1986. Accumulation of minerals and trace elements in biogenic mucus at hydro thermal vents. Deep-Sea Res., 33A, 339–347. Kaplan, D., Christiaen, D. & Arad, S., 1987. Chelating properties of extracellular polysaccharide from Chlorella spp. Appl. Environ. Microbiol., 53, 2953– 2956. Karl, D.M. & Bailiff, M.D., 1989. The measurement and distribution of dissolved nucleic acids in aquatic environments. Limnol. Oceanogr., 34, 543– 558. Kauri, T. & Kushner, D.J., 1985. Role of contact in bacterial degradation of cellulose. FEMS Microbiol. Ecol., 31, 301–306. Kefford, B., Kjelleberg, S. & Marshall, K.C., 1982. Bacterial scavenging: utilization of fatty acids localized at a solid-liquid interface. Arch. Microbiol., 133, 257–260. Kefford, B. & Marshall, K.C., 1984. Adhesion of Leptospira at a solid-liquid interface: a model. Arch. Microbiol., 138, 84–88. Kemp, P.F., 1986. Direct uptake of detrital carbon by the deposit-feeding polychaete Euzonus mucronata (Treadwell). J. Exp. Mar. Biol. Ecol., 99, 49– 61. Kenne, L. & Lindberg, B., 1983. Bacterial polysaccharides. In, The Polysaccharides, Vol. 2, edited by G.O.Aspinall, Academic Press, New York, pp. 287–363. Kennedy, A.F.D. & Sutherland, I.W., 1987. Analysis of bacterial exopolysaccharides. Biotechnol. Appl. Biochem., 9, 12–19. Khaylov, K.M. & Finenko, Z.Z., 1968. Interaction of detritus with higher molecularweight components of dissolved organic matter in seawater. Oceanology, 8, 776–785.
MICROBIAL EXOPOLYMER SECRETIONS
141
Kieras, J.H., Roden, L. & Chapman, D.J., 1977. The covalent linkage of protein to carbohydrate in the extracellular protein-polysaccharide from the red alga Porphyridium cruentum. Biochem. J., 165, 1–9. Kirchman, D., Graham, S., Reish, D. & Mitchell, R., 1982a. Lectins may mediate in the settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). Mar. Biol. Lett., 3, 131–142. Kirchman, D., Graham, S., Reish, D. & Mitchell, R., 1982b. Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). J. Exp. Mar. Biol. Ecol., 56, 153–163. Kirchman, D. & Mitchell, R., 1982. Contributions of particle-bound bacteria to total microheterotrophic activity in five ponds and two marshes. Appl. Environ. Microbiol., 43, 200–209. Kjelleberg, S., Hermansson, M., Marden, P. & Jones, G.W., 1987. The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment. Annu. Rev. Microbiol., 41, 25–49. Kjelleberg, S., Humphrey, B.A. & Marshall, K.C., 1983. Initial phases of starvation and activity of bacteria at surfaces. Appl. Environ. Microbiol., 46, 978–984. Knauer, G.A., Hebel, D. & Cipriano, F., 1982. Marine snow: major site of primary production in coastal waters. Nature (London), 300, 630–631. Kornberg, H.L., 1976. Genetics in the study of carbohydrate transport by bacteria. J. Gen. Microbiol., 96, 1–16. Kornegay, B.H. & Andrews, J.F., 1968. Kinetics of fixed-film biological reactors. J. Water Pollut. Control Fed., 40, R460–R468. Kranck, K. & Milligan, T.G., 1988. Macroflocs from diatoms: in situ photography of particles in Bedford Basin, Nova Scotia. Mar. Ecol. Prog. Ser., 44, 183–189. Kroen, W.K. & Rayburn, W.R., 1984. Influence of growth status and nutrients on extracellular polysaccharide synthesis by the soil alga Chlamydomonas mexicana (Chlorophyceae). J. Phycol., 20, 253–257. Kudo, H., Cheng, K.J. & Costerton, J.W., 1987. Electron microscopic study of the methyl cellulose-mediated detachment of cellulolytic rumen bacteria from cellulose fibers. Can. J. Microbiol., 33, 267–272. Ladd, J.N. & Butler, J.H. S., 1975. Humus-enzyme systems and synthetic organic polymer analogs. In, Soil Biochemistry, Vol. 4, edited by E.A.Paul & A.D. McLaren, Marcel Dekker, New York, 277 pp. Ladd, T.I., Costerton, J.W. & Geesey, G.G., 1979. Determination of the heterotrophic activity of epilithic microbial populations. In, Native Aquatic Bacteria: Enumeration, Activity and Ecology, edited by J.W.Costerton & R.R.Colwell, ASTM STP 695, ASTM Press, Philadelphia, pp. 180–195. Lahaye, M., Yaphe, W. & Rochas, C., 1985. 13C-N.M.R. spectral analysis of sulfated and desulfated polysaccharides of the agar type. Carbohydr. Res., 143, 240–245. La Motta, E.J., 1976. Internal diffusion and reaction in biological films. Environ. Sci. Technol., 10, 765–769. Larson, B., Vreeland, V. & Laetsch, W.M., 1985. Assay-dependent specificity of a monoclonal antibody with alginate. Carbohydr. Res., 143, 221–227. LeChevallier, M.W., Cawthon, C.D. & Lee, R.G. 1988. Inactivation of biofilm bacteria. Appl. Environ. Microbiol., 54, 2492–2499. Lee, C. & Wakeham, S.G., 1988. Organic matter in seawater: biogeochemical processes. In, Chemical Oceanography, Vol. 9, edited by J.P.Riley & R.Chester, Academic Press, New York, pp. 1–51. Leppard, G.G., Massalski, A. & Lean, D.R.S., 1977. Electron-opaque microscopic fibers in lakes: their demonstration, their biological derivation, and their potential significance in the redistribution of cations. Protoplasma, 92, 289– 309.
142
ALAN W.DECHO
Lessie, T.G. & Vander Wyk, J.C., 1972. Multiple forms of Pseudomonas multivorans glucose-6-phosphate and 6-phosphogluconate dehydrogenases: differences in size, pyridine nucleotide specificity, and susceptibility to inhibition by adenosine 5 '-triphosphate. J. Bacteriol., 110, 1107–1117. Lewin, J.C, 1955. The capsule of the diatom Navicula pelliculosa. J. Gen. Microbiol., 13, 162–169. Lewin, J.C., 1956. Extracellular polysaccharides of green algae. Can. J. Microbiol., 2, 665–672. Lewin, J.C., Lewin, R.A. & Philpott, D.E., 1958. Observations on Phaeodactylum tricornutum. J. Gen. Microbiol., 18, 418–426. Lewin, R.A., 1958. The mucilaginous tubes of Amphipleura rutilans. Liminol Oceanogr., 3, 111–113. Linker, A. & Jones, R.S., 1966. A new polysaccharide resembling alginic acid isolated from pseudomonads. J. Biol. Chem., 241, 3845–3851. Lock, M.A., Wallace, R.R., Costerton, J.W., Ventullo, R.M. & Charlton, S.E., 1984. River epilithon: toward a structural-functional model. Oikos, 42, 10– 22. Logan, B.E. & Hunt, J.R., 1987. Advantages to microbes of growth in permeable aggregates in marine systems. Limnol. Oceanogr., 32, 1034–1048. Lopez, G.R. & Levinton, J.S., 1987. Ecology of deposit-feeding animals in marine sediments. Q. Rev. Biol., 62, 235–260. Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J., 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem., 193, 265–275. Luoma, S.N. & Davis, J.A., 1983. Requirements for modeling trace metal partitioning in oxidized estuarine sediments. Mar. Chem., 12, 159–181. Lupton, F.S. & Marshall, K.C., 1984. Mechanisms of specific bacterial adhesion to cyanobacteria heterocysts. In, Current Perspectives in Microbial Ecology, edited by M.J.Klug & C.A.Reddy, Am. Soc. Microbiol., Washington, DC, pp. 144– 150. Mackie, E.B., Brown, K.N., Lam, J. & Costerton, J.W., 1979. Morphological stabilization of capsules of group B Streptococci, Types Ia, Ib, II, and III, with specific antibody. J. Bacteriol., 138, 609–617. Madsen, B.L., 1974. A note on the food of Amphinemura sulcicollis (Plecoptera), Hydrobiologia, 45, 169–175. Maki, J.S., Rittschof, D., Costlow, J.D. & Mitchell, R., 1988. Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface films. Mar. Biol., 97, 199–206. Mann, K.H., 1988. Production and use of detritus in various freshwater, estuarine and coastal marine ecosystems. Limnol. Oceanogr., 33, 910–930. Markovitz, A., 1977. Genetics and regulation of bacterial capsular polysaccharide biosynthesis and radiation sensitivity. In, Surface Carbohydrates of the Prokaryote Cell, edited by I.W.Sutherland, Academic Press, New York, pp. 415– 446. Marsh, D.H. & Odum, W.E., 1979. The effect of resuspension and sedimentation on the amount of microbial colonization of salt marsh detritus. Estuaries, 2, 184–188. Marshall, K.C., 1976a. Interfaces in Microbial Ecology. Harvard University Press, Cambridge, 156 pp. Marshall, K.C., 1976b. Mechanism of adhesion of marine bacteria to surfaces. In, Proc. 3rd Int. Congr. on Marine Corrosion and Biofouling, edited by R.F.Acker, et al., Northwestern University Press, Evanston, Illinois, pp. 625– 632. Marshall, K.C., 1980. Bacterial adhesion in natural environments. In, Microbial Adhesion to Surfaces, edited by R.C.W.Berkeley et al., Ellis Horwood Limited, Chichester, pp. 187–196.
MICROBIAL EXOPOLYMER SECRETIONS
143
Marshall, K.C., 1985. Mechanisms of bacterial adhesion at solid-water interfaces. In, Bacterial Adhesion, edited by D.C.Savage & M.Fletcher, Plenum Press, New York, pp. 133–161. Marshall, K.C., 1986. Adsorption and adhesion processes in microbial growth at interfaces. Adv. Colloid Interface Sci., 25, 59–86. Marshall, K.C. & Bitton, G., 1980. Microbial adhesion in perspective. In, Adsorption of Microorganisms to Surfaces, edited by G.Bitton & K.C.Marshall, John Wiley & Sons, New York, pp. 1–5. Marshall, K.C. & Cruickshank, R.H., 1973. Cell surface hydrophobicity and the orientation of certain bacteria at interfaces. Arch. Microbiol., 91, 29–40. Marshall, K.C., Stout, R. & Mitchell, R., 1971. Mechanism of the initial events in the sorption of marine bacteria to surfaces. J. Gen. Microbiol., 68, 337–348. Martin, J., Haider, K., Farmer, W. & Fustec-Mathon, E., 1974. Decomposition and distribution of residual activity of some 14 C-microbial polysaccharides and cells, glucose, cellulose, and wheat-straw in soil. Soil Biol. Biochem., 6, 221– 230. Matson, J.V. & Characklis, W.G., 1976. Diffusion into microbial aggregates. Water Res., 10, 877–881. McCarty, M., 1946. Chemical nature and biological specificity of the substance inducing transformation of pneumococcal types. Bacteriol. Rev., 10, 63–71. McFeters, G.A., Bazin, M.J., Bryers, J.D., Caldwell, E., Characklis, W.G., Lund, D.B., Mirelman, D., Mitchell, R., Schubert, R.H.W., Tanaka, T. & White, D. C., 1984. Biofilm development and its consequences. In, Microbial Adhesion and Aggregation, edited by K.C.Marshall, Springer Verlag, New York, pp. 109– 124. McFeters, G.A. & Stuart, D.G., 1972. Survival of coliform bacteria in natural waters: field and laboratory studies with membrane-filter chambers. Appl. Environ. Microbiol., 24, 805–811. Means, J.C. & Wijayaratne, R.D., 1984. Chemical characterization of estuarine colloidal organic matter: implications for adsorptive processes. Bull. Mat. Sci., 35, 449–461. Mian, F.A., Jarman, T.R. & Righelato, R.C., 1978. Biosynthesis of exopolymer by Pseudomonas aeruginosa. J. Bacteriol., 134, 418–422. Mihm, J.W., Banta, W.C. & Loeb, G.I., 1981. Effects of adsorbed organic and primary fouling films on bryozoan settlement. J. Exp. Mar. Biol. Ecol, 54, 167– 179. Miller, M.A., Rapean, J.C. & Whedon, W.F., 1948. The role of slime film in the attachment of fouling organisms. Biol. Bull. (Woods Hole, Mass.), 94, 143–157. Mitchell, R. & Kirchman, D., 1984. The microbial ecology of marine surfaces. In, Marine Biodeterioration: An Interdisciplinary Study, edited by J.D.Costlow & R.C.Tripper, Naval Institute Press, Anapolis, pp. 49–56. Mitchell, R. & Nevo, Z., 1965. Decomposition of structural polysaccharides of bacteria by marine microorganisms. Nature (London), 205, 1007–1008. Mittelman, M.W. & Geesey, G.G., 1985. Copper-binding characteristics of exopolymers from a freshwater-sediment bacterium. Appl. Environ. Microbiol., 49, 846–851. Moore, M.N., Lowe, D.M. & Gee, J.M., 1978. Histopathological effects induced in Mytilus edulis by Mytilicola intestinalis and the histochemistry of the copepod intestinal cells. J. Cons., Cons. Int. Explor. Mer, 38, 6–11. Moorehouse, R., Winter, W.T., Arnott, S. & Bayer, M.A., 1977. Conformation and molecular organization in fibers of capsular polysaccharide from Escherichia coli M41 mutants. J. Mol. Biol., 109, 373–391. Morel, F.M.M. & Gschwend, P.M., 1987. The role of colloids in the partitioning of solutes in natural waters. In, Aquatic Surface Chemistry, edited by W.Stumm, Wiley Interscience, New York, pp. 405–422.
144
ALAN W.DECHO
Moriarty, D.J.W., 1979. Biomass of suspended bacteria over coral reefs. Mar. Biol., 53, 193–200. Moriarty, D.J.W., 1980. Measurement of bacterial biomass in sandy sediments. In, Biogeochemistry of Ancient and Modern Environments, edited by P.A Trudinger, et al., Australian Academy of Science, Canberra, pp. 131–138. Moriarty, D.J.W., 1982. Feeding of the holothurians on bacteria and organic matter. Aust. J. Mar. Freshwater Res., 33, 255–263. Moriarty, D.J.W., 1983. Bacterial biomass and productivity in sediment, stromatolites, and water of Hamelin Pool, Shark Bay, Western Australia. Geomicrobiol. J., 3, 121–133. Moriarty, D.J.W. & Hayward, A.C., 1982. Ultrastructure of bacteria and the proportion of gram-negative bacteria in marine sediments. Microb. Ecol., 8, 1–14. Morita, R.Y., 1979. Deep-sea microbial energetics. Sarsia, 64, 9–12. Morris, E.J. & Bacon, J.S.D., 1977. The fate of acetyl groups and sugar components during the digestion of grass cell walls in sheep. J. Agric. Sci., 89, 327–340. Mueller, J.A., Boyle, W.C. & Lightfoot, E.N., 1968. Oxygen diffusion through Zoogloea flocs. Biotechnol. Bioeng., 10, 331–358. Müller, W.E.G., 1973. Metamorphose-induktion bei Planulalarven. I. Der bakterielle Induktor. Wilhelm Roux’ Arch., 173, 107–121. Müller, W.E.G., Zahn, R.K., Kurelec, B., Lucu, C., Müller, I. & Uhlenbruck, G., 1981. Lectin, a possible basis for symbiosis between bacteria and sponges. J. Bacteriol., 145, 548–558. Murphy, T.P., Lean, D.R.S. & Nalewajko, C., 1976. Blue-green algae: their excretion of iron-selective chelator enables them to dominate other algae. Science, 192, 900–902. Myklestad, S., 1974. Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture. J. Exp. Mar. Biol. Ecol., 15, 261–274. Myklestad, S. & Haug, A., 1972. Production of carbohydrates by the marine diatom Chaetoceros affinis var. willei Gran) Hustedt. I. Effect of the concentration of nutrients in the culture medium. J. Exp. Mar. Biol. Ecol., 9, 125–136. Myklestad, S., Haug, A. & Larsen, B., 1972. Production of carbohydrates by the marine diatom Chaetoceros affinis var. willei (Gran) Hustedt. II. Preliminary investigation of the extracellular polysaccharide. J. Exp. Mar. Biol. Ecol., 9, 137–144. Nakajima, T., 1979. Dentrification by the sessile microbial community of a polluted river. Hydrobiologia, 66, 57–64. Nath, R.K. & Chakraborty, A.K., 1987. Structural studies on the capsular polysaccharide of Klebsiella serotype K40. Eur. J. Biochem., 162, 439–443. Nealson, N.H., 1983. The microbial manganese cycle. In, Microbial Geochemistry: Studies in Microbiology, Vol. 3, edited by W.E.Krumbein, Black well Sci. Publ., Oxford, U.K., pp. 191–221. Neu, T.R. & Poralla, K., 1988. An amphiphilic polysaccharide from an adhesive Rhodococcus strain. FEMS Microbiol. Lett., 49, 389–392. Neumann, A.C., Gebelein, C.D. & Scoffin, G.P., 1970. The composition, structure, and erodability of subtidal mats, Abaco, Bahamas. J. Sediment Petrol., 40, 274–279. Newell, R.C. & Field, J.G., 1983. The contribution of bacteria and detritus to carbon and nitrogen flow in a benthic community. Mar. Biol. Lett., 4, 23–36. Newell, R.C., Lucas, M.I. & Linley, E.A.S., 1981. Rate of degradation and efficiency of conversion of phytoplankton debris by marine microorganisms. Mar. Ecol. Prog. Ser., 6, 123–136.
MICROBIAL EXOPOLYMER SECRETIONS
145
Nichols, P.D., Henson, J.M., Guckert, J.D., Nivens, D.E. & White, D.C., 1985. Fourier transform infrared spectroscopic methods for microbial ecology: analysis of bacteria, bacteria-polymer mixtures and biofilms. J. Microbiol. Meth., 4, 79–94. Nicholson, J.A.M., Stolz, J.F. & Pierson, B.F., 1987. Structure of a microbial mat at Great Sippewissett Marsh, Cape Cod, Massachusetts. FEMS Microbiol. Ecol., 45, 343–364. Nishikawa, S. & Kuriyama, M., 1968. Nucleic acid as a component of mucilage in activated sludge. Water Res., 2, 811–812. Norberg, A.B. & Enfors, S., 1982. Production of extracellular polysaccharide by Zoogloea ramigera. Appl. Environ. Microbiol., 44, 1231–1237. Norval, M. & Sutherland, I.W., 1969. A group of Klebsiella mutants showing temperature-dependent polysaccharide synthesis. J. Gen. Microbiol., 57, 369– 377. Novak, J.T. & Haugan, B., 1981. Polymer extraction from activated sludge. J. Water Pollut. Control Fed., 9, 1420–1424. Novitsky, J.A., 1986. Degradation of dead microbial biomass in a marine sediment. Appl. Environ. Microbiol., 52, 504–509. Novitsky, J.A. & Morita, R.Y., 1976. Morphological characteristics of small cells resulting from nutrient starvation of a psychrophilic marine vibrio. Appl. Environ. Microbiol., 32, 617–662. O’Colla, P., 1962. Mucilages. In, Physiology and Biochemistry of Algae, edited by R. A.Lewin, Academic Press, New York, pp. 337–356. Odham, G., Tunlid, A., Valeur, A., Sundin, P. & White, D.C., 1986. Model system for studies of microbial dynamics at exuding surfaces such as the rhizosphere. Appl. Environ. Microbiol., 52, 191–196. Oren, A., 1987. On the use of tetrazolium salts for the measurement of microbial activity in sediments. FEMS Microbiol. Ecol., 45, 127–133. Orr, T., Koepp, L.H. & Bartell, P.F., 1982. Carbohydrate mediation of the biological activities of the glycoprotein of Pseudomonas aeruginosa. J. Gen. Microbiol., 128, 2631–2638. Osborn, M.J., 1963. Studies on the gram-negative cell wall, I. Evidence for the role of 2-keto-3-deoxyoctonate in the lipopolysaccharide of Salmonella typhimurium. Proc. Natl. Acad. Sci., USA, 50, 499–506. Osborn, M.J., Gander, J.E., Parisi, E. & Carson, J., 1972. Mechanisms of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membranes. J. Biol. Chem., 247, 3962–3972. Paerl, H.W., 1973. Detritus in Lake Tahoe: structural modification by attached microflora. Science, 180, 496–498. Paerl, H.W., 1974. Bacterial uptake of dissolved organic matter in relation to detrital aggregation in marine and freshwater systems. Limnol. Oceanogr., 19, 966–972. Paerl, H.W., 1975. Microbial attachment to particles in marine and freshwater ecosystems. Microb. Ecol., 2, 73–83. Paerl, H.W., 1976. Specific associations of the blue-green algae Anabaena and Aphanizomenon with bacteria in freshwater blooms. J. Phycol., 12, 431–435. Paerl, H.W., 1978. Role of heterotrophic bacteria promoting N fixation by 2 Anabaena in aquatic habitats. Microb. Ecol., 4, 215–231. Paerl, H.W., 1980. Attachment of microorganisms to living and detrital surfaces in freshwater systems. In, Adsorption of Microorganisms to Surfaces, edited by G. Bitton & K.C.Marshall, John Wiley & Sons, New York, pp. 375–402. Paerl, H.W., 1984a. Alteration of microbial metabolic activities in association with detritus. Bull. Mar. Sci., 35, 393–408.
146
ALAN W.DECHO
Paerl, H.W., 1984b. Transfer of N and CO fixation products from Anabaena 2 2 oscillarioides to associated bacteria during inorganic carbon sufficiency and deficiency. J. Phycol., 20, 600–608. Paerl, H.W. & BeBout, B.M., 1988. Direct measurement of O -depleted microzones in marine Oscillatoria: relation to N fixation. Science,2 241, 442–445. 2 Paerl, H.W. & Kellar, P.E., 1978a. Optimization of N fixation in O -rich waters. 2 2 In, Microbial Ecology, edited by M.W.Loutit & J.A.R.Miles, Springer-Verlag, Berlin, pp. 68–75. Paerl, H.W. & Kellar, P.E., 1978b. Significance of bacterial Anabaena (Cyanophyceae) associations with respect to N -fixation in freshwater. J. 2 Phycol., 14, 254–260. Paerl, H.W. & Prufert, L.E., 1987. Oxygen-poor microzones as potential sites of N fixation in nitrogen-depleted aerobic marine waters. Appl. Environ. 2 Microbiol., 53, 1078–1087. Paerl, H.W., Richards, R.C., Leonard, R.L. & Goldman, C.P., 1975. Seasonal nitrate cycling as evidence for complete vertical mixing in Lake Tahoe, CaliforniaNevada. Limnol. Oceanogr., 20, 1–8. Painter, R.J., 1983. Algal polysaccharides. In, The Polysaccharides, Vol. 2, edited by G.O. Aspinall, Academic Press, New York, pp. 196–286. Parsons, A.B. & Dugan, P.R., 1971. Production of extracellular polysaccharide matrix by Zoogloea ramigera. Appl. Microbiol., 21, 657–661. Patel, J.J. & Gerson, T., 1974. Formation and utilization of carbon reserves by Rhizobium. Arch. Microbiol., 101, 211–220. Paterson, D.M., 1989. Short-term changes in the erodibility of intertidal cohesive sediments related to the migratory behavior of epipelic diatoms. Limnol. Oceanogr., 34, 223–234. Patrick, F.M. & Loutit, M.W., 1976a. Passage of metals in effluents, through bacteria to higher organisms. Water Res., 10, 333–335. Patrick, F.M. & Loutit, M.W., 1976b. Passage of metals to freshwater fish from their food. Water Res., 12, 395–398. Paul, J.H., Jefferey, W.H. & DeFlaun, M.F., 1987. The dynamics of extracellular DNA in the marine environment. Appl. Environ. Microbiol., 53, 170–179. Paulsen, B.S., Haug, A. & Larsen, B., 1978. Structural studies of a carbohydrate containing polymer present in the mucilage tubes of the diatom Berkeleya rutilans (Trent). Grun. Carbohydr. Res., 66, 103–111. Pavoni, J.L., Tenny, M.W. & Echelberger, W.F., 1972. Bacterial exocellular polymers and biological flocculation. J. Water Pollut. Control Fed., 44, 414– 431. Pazur, J.H. & Forsberg, L.S., 1980. Isolation and purification of carbohydrate antigens. In, Methods in Carbohydrate Chemistry, Vol. 8, edited by R.L.Whistler & J.N.BeMiller, Academic Press, New York, pp. 211–217. Perlin, A.S. & Casu, B., 1982. Spectroscopic methods. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 133–195. Phillips, N.W., 1984. Role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bull. Mar. Sci., 35, 283– 298. Plante, C.J., Jumars, P.A. & Barross, J.A., 1989. Rapid bacterial growth in the hindgut of a marine deposit feeder. Microb. Ecol. (in press). Platt, R.M., Geesey, G.G., Davis, J.D. & White, D.C., 1985. Isolation and partial chemical analysis of firmly bound exopolysaccharide from adherent cells of a freshwater sediment bacterium. Can. J. Microbiol., 31, 675–680. Pomeroy, L.R., 1974. The ocean’s food web, a changing paradigm. Bioscience, 24, 499–504.
MICROBIAL EXOPOLYMER SECRETIONS
147
Pomeroy, L.R., 1984. Significance of microorganisms in carbon and energy flow in aquatic ecosystems. In, Current Perspectives in Microbial Ecology, edited by M. J.Klug & C.A.Reddy, Am. Soc. Microbiol., Washington, DC, pp. 405– 411. Poole, N.J. & Wildish, D.J., 1979. Polysaccharide degradation in estuaries. In, Microbial Polysaccharides and Polysaccharases, edited by R.C.W.Berkeley et al., Academic Press, New York, pp. 399–416. Porter, K.G., 1976. Enhancement of algal growth and productivity by grazing zooplankton. Science, 192, 1332–1334. Powell, D.A., 1979. Structure, solution properties and biological interactions of some microbial extracellular polysaccharides. In, Polysaccharides and Polysaccharases, edited by R.C.W.Berkeley et al., Academic Press, New York, pp. 117–160. Preston, E., 1971. Niche overlap and competition among five sympatric species of xanthid crabs. Ph.D. thesis, University of Hawaii, Honolulu, 125 pp. Purcell, E.M., 1977. Life at low Reynolds numbers. Am. J. Phys., 45, 3–11. Rees, D.A., 1969. Structure, conformation and mechanism in the formation of polysaccharide gels and network. Adv. Carbohydr. Chem. Biochem., 24, 267– 332. Rees, D.A., 1972a. Polysaccharide gels. Chem. Ind. (London), 16, 630–636. Rees, D.A., 1972b. Shapely polysaccharides, the eighth Colworth Medal Lecture. Biochem. J., 126, 257–273. Rees, D.A., 1976. Stereochemistry and binding behavior of carbohydrate chains. In, Biochemistry of Carbohydrates, Vol. 5, edited by W.J.Whelan, University Park Press, Baltimore, pp. 1–42. Rees, D.A., Morris, E.R., Thorn, D. & Madden, J.K., 1982. Shapes and interactions of carbohydrate chains. In, The Polysaccharides, Vol. 1, edited by G.O.Aspinall, Academic Press, New York, pp. 196–291. Rees, D.A. & Scott, W.E., 1971. Polysaccharide conformation. Part VI. J. Chem. Soc. (B), 469–479. Rendelman, J.A., 1978a. Metal-polysaccharide complexes, Part I. Food Chem., 3, 47–79. Rendelman, J.A., 1978b. Metal-polysaccharide complexes. Part II. Food Chem., 3, 127–162. Revsbech, N.P. & Jørgensen, B.B., 1986. Microelectrodes: their use in microbial ecology. Adv. Microb. Ecol., 9, 293–352. Rhoads, D.C., Yingst, J.L. & Ullman, W.J., 1978. Seafloor stability in central Long Island Sound. Part I. Temporal changes in erodability of fine-grained sediments. In, Estuarine Interactions, edited by M.L.Wiley, Academic Press, New York, pp. 221–224. Rice, D.L., Bianchi, T.S. & Roper, E.H., 1986. Experimental studies of sediment reworking and growth of Scoloplos spp. (Orbiniidae: Polychaeta). Mar. Ecol. Prog. Ser., 30, 9–19. Rice, D.L. & Hanson, R.B., 1984. A kinetic model for detrital nitrogen: role of the associated bacteria in nitrogen accumulation. Bull. Mar. Sci., 35, 326–340. Richardson, L.L., Aguilar, C. & Nealson, K.H., 1988. Manganese oxidation in pH and O microenvironments produced by phytoplankton. Limnol. Oceanogr., 2 33, 352–363. Richman, S., Loya, Y. & Slobodkin, L.B., 1975. The rate of mucus production by corals and its assimilation by the coral reef copepod Acartia negligens. Limnol. Oceaogr., 20, 918–923. Ridgeway, H.F., Means, E.G. & Olson, B.H., 1981. Iron bacteria in drinkingwater distribution systems: elemental analysis of Gallionella stalks, using Xray energy-dispersive microanalysis. Appl. Environ. Microbiol., 41, 288–297.
148
ALAN W.DECHO
Riemann, B., Nielsen, P., Jeppesen, M., Marcussen, B. & Fuhrman, J.A., 1984. Diel changes in bacterial biomass and growth rates in coastal environments, determined by means of thymidine incorporation into DNA, frequency of dividing cells (FDC), and microautoradiography. Mar. Ecol. Prog. Ser., 17, 227–235. Riemann, F., 1989. Gelatinous phytoplankton detritus aggregates on the Atlantic deep-sea bed. Structure and mode of formation. Mar. Biol., 100, 533–540. Robert, J.M. & Gouleau, D., 1977. Experimental confirmation of the role of the benthic diatom Navicula ramosissima (Agarh) Cleve in the secretion of mucoidal materials which stabilize muddy marine littoral flats. C.R. Acad. Sci. Ser. D., 284, 1915–1918. Roberts, I., Mountford, R., High, N., Bitter-Suermann, D., Jann, K., Timmis, K. & Boulnois, G., 1986. Molecular cloning and analysis of genes for production of K5, K7, K12, K92 capsular polysaccharides in Escherichia coli. J. Bacteriol., 168, 1228–1233. Robertson, M.L., Mills, A.L. & Zieman, J.C., 1982. Microbial synthesis of detritus-like particles from dissolved organic carbon released by tropical seagrass. Mar. Ecol Prog. Ser., 7, 279–285. Rosen, M.W. & Cornford, N.E., 1971. Fluid friction of fish slimes. Nature (London), 234, 49–51. Rosenberg, E., Gottlieb, A. & Rosenberg, M., 1983. Inhibition of bacterial adherence to hydrocarbon and epithelial cells by emulsan. Infect. Immun., 39, 1024–1028. Roth, I.L., 1977. Physical structure of surface carbohydrates. In, Surface Carbohydrates of the Prokaryote Cell, edited by I.W.Sutherland, Academic Press, New York, pp. 5–26. Rothfield, L. & Pearlman-Kothencz, M., 1969. Synthesis and assembly of bacterial membrane components. A lipopolysaccharide-phospholipid-protein complex excreted by living bacteria. J. Mol. Biol., 44, 477–492. Round, F.E., 1981. The Ecology of the Algae. Cambridge University Press, Cambridge, 653 pp. Rounick, J.S. & Winterbourn, M.J., 1983. The formation, structure and utilization of stone surface layers in two New Zealand streams. Freshwater Biol., 13, 57– 72. Rubinovitz, C., Gutnick, D.L. & Rosenberg, E., 1982. Emulsan production by Acinetobacter calcoaceticus in the presence of chloramphenicol. J. Bacteriol., 152, 126–132. Rudd, T., Sterritt, R.M. & Lester, J.N., 1982. The use of extraction methods for the quantification of extracellular polymer production by Klebsiella aerogenes under varying cultural conditions. Eur. J. Appl. Microbiol. Biotechnol., 16, 23–27. Rudd, T., Sterritt, R.M. & Lester, J.N., 1983. Mass balance of heavy metal uptake by encapsulated cultures of Klebsiella aerogenes. Microb. Ecol., 9, 261–272. Sanders, W.M., 1966. Oxygen utilization by slime organisms in continuous culture. J. Air Water Pollut., 10, 253–276. Sar, N. & Rosenberg, E., 1987. Fish skin bacteria: colonial and cellular hydrophobicity. Microb. Ecol., 13, 193–202. Sar, N. & Rosenberg, E., 1989. Fish-skin bacteria: production of frictionreducing polymers. Microb. Ecol., 17, 27–38. Saunders, P.T. & Bazin, M.J., 1973. Attachment of microorganisms in a packed column: metabolite diffusion through the microbial flora as a limiting factor. J. Appl. Chem. Biotechnol., 23, 847–853. Savage, D.C., 1977. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol., 31, 107–133.
MICROBIAL EXOPOLYMER SECRETIONS
149
Scherrer, R., Berlin, E. & Gerhardt, P., 1977. Density, porosity, and structure of dried cell walls isolated from Bacillus megaterium and Saccharomyces cerevisiae. J. Bacteriol., 129, 1162–1164. Schmidt, M.A. & Jann, K., 1982. Phospholipid substitution of capsular (K) polysaccharide antigens from Escherichia coli causing extra-intestinal infections. FEMS Microbiol. Lett., 14, 69–74. Schwarzmann, S. & Boring, J.R., 1971. Antiphagocytic effect from a mucoid strain of Pseudomonas aeruginosa. Infect. Immun., 3, 762–767. Scott, J.A. & Palmer, S.J., 1988. Cadmium bio-sorption by bacterial exopolysaccharide. Biotechnol. Lett., 10, 21–24. Seiderer, L.J., Davis, C.L., Robb, F.T. & Newell, R.C., 1984. Utilization of bacteria as nitrogen resource by kelp-bed mussel Choromytilus meridionalis. Mar. Ecol. Prog. Ser., 15, 109–116. Seki, H., 1972. The role of microorganisms in the marine food chain with reference to organic aggregates. Mem. Ist. Ital. Idrobiol., 29 (Suppl.), 245 only. Sevag, M.G., Lackman, D.B. & Smolens, J., 1938. The isolation of the components of streptococcal nucleoproteins in serologically active form. J. Biol. Chem., 124, 425–436. Sharon, N., 1977. Lectins. Sci. Am., 236, 108–119. Sharon, N. & Lis, H., 1972. Lectins: cell agglutinating and sugar-specific proteins. Science, 177, 949–959. Sharp, J.H., 1973. Size classes of organic carbon in seawater. Limnol. Oceanogr., 18, 441–456. Sheintuch, M., Lev, O., Einav, P. & Rubin, E., 1986. Role of exocellular polymer in the design of activated sludge. Biotechnol. Bioengin., 28, 1564– 1576. Sherr, E.B., 1988. Direct use of high molecular weight polysaccharides by heterotrophic flagellates. Nature (London), 335, 348–351. Sherwood, J.E., Vasse, J.M., Dazzo, F.B. & Truchet, G.L., 1984. Development and trifoliin A-binding ability of the capsule of Rhizobium trifolii. J. Bacterial., 159, 145–152. Shoham, Y. & Rosenberg, E., 1983. Enzymatic depolymerization of emulsan. J. Bacteriol., 156, 161–167. Sibbald, M.J. & Albright, L.J., 1988. Aggregated and free bacteria as food sources for heterotrophic microflagellates. Appl. Environ. Microbiol., 54, 613– 616. Siebers, D., 1982. Bacterial-invertebrate interactions in uptake of dissolved organic matter. Am. Zool., 22, 723–733. Sieburth, J.McN., 1975. Microbial Seascapes. University Park Press, London, 200 pp. Silver, M.W. & Alldredge, A.L., 1981. Bathypelagic marine snow: deep-sea algal and detrital community. J. Mar. Res., 39, 501–530. Silver, M.W., Shanks, A.L. & Trent, J.D., 1978. Marine snow: microplankton habitat and source of small-scale patchiness in pelagic populations. Science, 201, 371–373. Silver, R.P., Vann, W.F. & Aaronson, W., 1984. Genetic and molecular analysis of Escherichia coli K1 antigen genes. J. Bacteriol., 157, 568–575. Sly, L. L, Hodgkinson, M.C. & Arunpairojana, V., 1988. Effect of water velocity on the early development of manganese depositing biofilm in a drinking-water distribution system. FEMS Microbiol. Ecol, 53, 175–186. Smetacek, V. & Pollehne, F., 1986. Nutrient cycling in pelagic systems: a reappraisal of the conceptual framework. Ophelia, 26, 401–428. Smetacek, V.S., 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar. Biol., 84, 239–251.
150
ALAN W.DECHO
Smidsrod, O., 1974. Molecular basis for some physical properties of alginate in the gel state. Faraday Discuss. Chem. Soc., 37, 263–274. Smith, B.D., Cabot, E.L. & Foreman, R.E., 1985. Seaweed detritus versus benthic diatoms as important food resources for two dominant subtidal gastropods. J. Exp. Mar. Biol. Ecol., 92, 143–156. Smith, E.E.B., Mills, G.T. & Bernheimer, H.P., 1961. Biosynthesis of pneumococcal capsular polysaccharides. J. Biol. Chem., 236, 2179–2187. Smith, J.J. & Geesey, G.G., 1989. Detection and quantitation of polymeric pyruvate in bacterial exopolymers and aquatic sediments. Abstr. Am. Soc. Microbiol., New Orleans, p. 287 only. Sonea, S. 1988. A bacterial way of life. Nature (London), 331, 216 only. Spiro, R.G., 1966. Analysis of sugars found in glycoproteins. In, Methods in Enzymology, VIII, edited by E.F.Neufeld & V.Ginsburg, Academic Press, New York, pp. 4–5. Spiro, R.G., 1976. Isolation of glycopeptides from glycoproteins by proteolytic digestion. In, Methods in Carbohydrate Chemistry, edited by R.L.Whistler & J.N.BeMiller, Academic Press, New York, pp. 185–190. Stanier, R.Y., Doudoroff, M. & Adelberg, E.A., 1976. The Microbial World. Prentice Hall, Englewood Cliffs, 4th Edition, 871 pp. Stein, J.L., 1984. Subtidal gastropods consume sulfur-oxidizing bacteria: evidence from coastal hydrothermal vents. Science, 223, 696–698. Stewart, G.S. & Carlson, C.A., 1986. The biology of natural transformation. Ann. Rev. Microbiol., 40, 211–235. Summers, A.O. & Silver, S., 1978. Microbial transformations of metals. Annu. Rev. Microbiol., 32, 637–672. Sutcliffe, J., Blumenthal, R., Walter, A. & Foulds, J., 1983. Escherichia coli outer membrane protein K is a porin. J. Bacteriol., 156, 867–872. Sutherland, I.W., 1972. Bacterial exopolysaccharides. Adv. Microbiol. Physiol., 8, 143–213. Sutherland, I.W., 1977a. Microbial exopolysaccharide synthesis. In, Extracellular Microbial Polysaccharides, edited by P.A.Sanford & A.Laskin, Am. Chem. Soc., Washington, DC, pp. 40–57. Sutherland, I.W., 1977b. Bacterial exopolysaccharides—their nature and production. In, Surface Carbohydrates of the Prokaryote Cell, edited by I.W.Sutherland, Academic Press, New York, pp. 27–96. Sutherland, I.W., 1977c. Enzymes acting on bacterial surface carbohydrates. In, Surface Carbohydrates of the Prokaryote Cell, edited by I.W.Sutherland, Academic Press, New York, pp. 209–245. Sutherland, I.W., 1979. Microbial exopolysaccharides: control of synthesis and acylation. In, Microbial Polysaccharides and Polysaccharases, edited by R.C. W.Berkeley et al., Academic Press, New York, pp. 1–34. Sutherland, I.W., 1980. Polysaccharides in the adhesion of marine and freshwater bacteria. In, Microbial Adhesion to Surfaces, edited by R.C.W.Berkeley et al., Ellis Horwood Limited, Chichester, pp. 329–338. Sutherland, I.W., 1982. Biosynthesis of microbial exopolysaccharides. Adv. Microb. Physiol., 23, 79–150. Sutherland, I.W., 1983. Microbial exopolysaccharides—their role in microbial adhesion in aqueous systems. Crit. Rev. Microbiol., 10, 173–200. Sutherland, I.W., 1985. Biosynthesis and composition of gram-negative bacterial extracellular and wall polysaccharides. Annu. Rev. Microbiol., 39, 243–270. Sutherland, I.W. & Wilkinson, J.F., 1971. Chemical extraction methods of microbial cells. Meth. Microbiol., 5, 345–380. Tago, Y. & Aida, K., 1977. Exocellular mucopolysaccharide closely related to bacterial floc formation. Appl. Environ. Microbiol., 34, 308–314. Tanaka, T., 1981. Gels. Sci. Am., 244, 124–138.
MICROBIAL EXOPOLYMER SECRETIONS
151
Tenore, K.R., Hanson, R.B., McClain, J., Maccubin, A.E. & Hodson, R.E., 1984. Changes in composition and nutritional value to a benthic deposit feeder of decomposing detritus pools. Bull. Mar. Sci., 35, 299–311. Tietjen, J.H. & Lee, J.J., 1973. Life history and feeding habits of the marine nematode, Chromadora macrolaimoides Steiner. Oecologia (Berlin), 12, 303– 314. Tietjen, J.H. & Lee, J.J., 1977. Feeding behavior of marine nematodes. In, Ecology of Marine Benthos, edited by B.C.Coull, University of South Carolina Press, Columbia, pp. 22–36. Tonn, S.J. & Gander, J.E., 1979. Biosynthesis of polysaccharides by procaryotes. Annu. Rev. Microbiol., 33, 169–199. Tosteson, T.R., 1985. The regulation and specificity of marine microbial surface interactions. In, Biotechnology of Marine Polysaccharides, edited by R.R. Colwell, McGraw-Hill, New York, pp. 77–114. Tosteson, T.R. & Corpe, W.A., 1975. Enhancement of adhesion of the marine Chlorella vulgaris to glass. Can. J. Microbiol., 21, 1025–1031. Troy, F.A., 1979. The chemistry and biosynthesis of selected bacterial capsular polymers. Annu. Rev. Microbiol., 33, 519–560. Troy, F.A., Frerman, F.A. & Heath, E.C., 1971. The biosynthesis of capsular polysaccharide in Aerobacter aerogenes. J. Biol. Chem., 246, 156–163. Tunnicliffe, V. & Risk, M.J., 1977. Relationships between the bivalve Macoma balthica and bacteria in intertidal sediments: Minas Basin, Bay of Fundy. J. Mar. Res., 35, 499–507. Turakhia, M.H., Cooksey, K.E. & Characklis, W.G., 1983. Influence of a calciumspecific chelant on biofilm removal. Appl. Environ. Microbiol., 46, 1236– 1238. Uhlinger, D.J. & White, D.C., 1983. Relationship between physiological status and formation of extracellular polysaccharide glycocalyx in Pseudomonas alantica. Appl. Environ. Microbiol., 45, 64–70. Usui, Y., Yoshida, K. & San Clemente, C.L., 1981. Hydroxyproline-rich protein in the capsule of a strain of Staphylococcus aureus. Can. J. Microbiol., 27, 955–958. Van Dover, C.L., Fry, B., Grassle, J.F., Humphris, S. & Rona, P.A., 1988. Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar. Biol., 98, 209–216. Vasse, J.M., Dazzo, F.B. & Truchet, G.L., 1984. Re-examination of capsule development and lectin-binding sites on Rhizobium japonicum 3I1B110 by the glutaraldehyde/ruthenium red/uranyl acetate staining method. J. Gen. Microbiol., 130, 3037–3047. Venosa, A.D., 1975. Lysis of Sphaerotilus natans swarms cells by Bdellovibrio bacteriovirus. Appl. Environ. Microbiol., 29, 702–705. Ventullo, R.M. & Rowe, J.J., 1982. Dentrification potential of epilithic communities in a lotic environment. Curr. Microbiol., 7, 29–34. Vieira, A.A.H. & Nascimento, O.R., 1988. An EPR determination of copper complexation by excreted high molecular weight compounds of Ankistrodesmus densus (Chlorophyceae). J. Plankt. Res., 10, 1313–1315. Vos, P.C., De Boer, P.L. & Misdrop, R., 1988. Sediment stabilization by benthic diatoms in intertidal sandy shoals: qualitative observations. In, Tideinfluences, Sedimentary Environments and Facies, edited by P.L.De Boer et al., Reidel, Dordrecht, Holland, pp. 511–526. Vreeland, V., Zablackis, E., Doboszewski, B. & Laetsch, W.M., 1987. Molecular markers for marine algal polysaccharides. Hydrobiologia, 151/152, 155–160. Wardell, J.N., Brown, C.M. & Flannigan, B., 1983. Microbes and surfaces. In, Microbes in Their Natural Environment, edited by J.H.Slater et al., Cambridge University Press, Cambridge, pp. 351–378.
152
ALAN W.DECHO
Watling, L., 1988. Small-scale features of marine sediments and their importance to the study of deposit-feeding. Mar. Ecol. Prog. Ser., 47, 135–144. Webster, D.R., Cooksey, K.E. & Rubin, R.W., 1985. An investigation of the involvement of cytochemical structures and secretions in gliding motility of the marine diatom Amphora coffeaeformis. Cell Motility, 5, 103–122. Weiner, R.M. & Colwell, R.R., 1982. Induction of settlement and metamorphosis in Crassostrea virginica by a melanin-synthesizing bacterium. Technical Report, Maryland Sea Grant, No. UM-SG-TS-82–05, 44 pp. Weiner, R.M., Colwell, R.R., Jarman, R.N., Stein, D.C., Somerville, C.C. & Bonar, D.B., 1985. Applications of biotechnology to the production, recovery and use of marine polysaccharides. Biotechnology, 3, 899–902. Wetzel, R.L., 1977. Carbon resources of a benthic salt marsh invertebrate Nassarius obseletus Say (Mollusca Nassadiidae). In, Estuarine Processes, Vol. 2, edited by M.Wiley, Academic Press, New York, pp. 293–308. White, D.C., 1986. Quantitative physiochemical characterization of bacterial habitats. In, Bacteria in Nature, Vol. 2. Methods and Special Applications in Bacterial Ecology, edited by J.S.Poindexter & E.R.Leadbetter, Plenum Press, New York, pp. 177–203. White, D.C. & Findlay, R.H., 1988. Biochemical markers for measurement of predation effects on the biomass community structure, nutritional status, and metabolic activity of microbial biofilms. Hydrobiologia, 159, 119–132. Whitfield, C., 1988. Bacterial extracellular polysaccharides. Can. J. Microbiol., 34, 415–420. Wicken, A.J., 1985. Bacterial cell walls and surfaces. In, Bacterial Adhesion, edited by D.C.Savage & M.Fletcher, Plenum Press, New York, pp. 45–70. Wiese, W. & Rheinheimer, G., 1978. Scanning electron microscopy and epifluorescence investigation of bacterial colonization of marine sand sediments. Microb. Ecol., 4, 175–188. Williams, A., 1974. Extracellular polysaccharide production by a gram-negative bacterial isolate. Ph.D. thesis, University College, Cardiff. Williams, A.G. & Wimpenny, J.W.T., 1977. Exopolysaccharide production by Pseudomonas NCIB 11264 grown in batch culture. J. Gen. Micribiol., 102, 13–21. Williams, A.G. & Wimpenny, J.W.T., 1978. Exopolysaccharide production by Pseudomonas NCIB 11264 grown in continuous culture. J. Gen. Microbiol., 104, 47–57. Williams, A.G., Wimpenny, J.W.T. & Lawson, C.J., 1979. Preliminary studies on the composition and rheological properties of extracellular polysaccharide synthesized by Pseudomonas PB1 (NCIB 11264). Biochim. Biophys. Acta, 585, 611–619. Williams, P.J., leB., 1984. Bacterial production in the marine food chain: the emperor’s new suit of clothes? In, Flows of Energy and Materials in Marine Ecosystems, Theory and Practice, edited by J.M.R.Fasham, NATO Conf. Ser., Series 4, Marine Sci., Vol. 13, Plenum Publ. Corp., New York, pp. 271–299. Wimpenny, J.W.T., 1981. Spatial order in microbial ecosystems. Biol. Rev., 56, 295– 342. Woollacott, R.M., 1981. Association of bacteria with bryozoan larvae. Mar. Biol., 65, 155–158. Wrangstadh, M., Conway, P.L. & Kjelleberg, S., 1986. The production and release of an extracellular polysaccharide during starvation of a marine Pseudomonas sp. and the effect thereof on adhesion. Arch. Microbiol., 145, 220–227. Yokote, M., Honjo, T. & Asakawa, M., 1985. Histochemical demonstration of a glycocalyx on the cell surface of Heterosigma akashiwo. Mar. Biol., 88, 295– 299.
MICROBIAL EXOPOLYMER SECRETIONS
153
Zaidi, R., Bard, F. & Tosteson, T.R., 1984. Microbial specificity of metallic surfaces exposed to ambient seawater. Appl. Environ. Microbiol., 48, 519–524. Zambon, J.S., Huber, P.S., Myer, A.E., Slots, J., Fornalik, M.S. & Baier, R.E., 1984. In situ identification of bacteria species in marine microfouling films using an immunofluorescence technique. Appl. Environ. Microbiol., 48, 1214– 1220. Zimmer, R.L. & Woollacott, R.M., 1983. Mycoplasma-like organisms: occurrence with the larvae and adults of a marine bryozoan. Science, 220, 208–210. ZoBell, C.E., 1943. The effect of solid surfaces upon bacterial activity. J. Bacteriol., 46, 75–82. ZoBell, C.E. & Allen, E.C., 1935. The significance of bacteria in the fouling of submerged surfaces. J. Bacteriol., 29, 239–251.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 155–175 Margaret Barnes, Ed. Aberdeen University Press
A REVIEW OF THE ECOLOGY OF SURF-ZONE DIATOMS, WITH SPECIAL REFERENCE TO ANAULUS AUSTRALIS M.M.B.TALBOT, G.C.BATE and E.E.CAMPBELL Department of Botany, Institute for Coastal Research, University of Port Elizabeth, P.O. Box 1600, Port Elizabeth, 6000 Republic of South Africa
ABSTRACT Phytoplankton studies in shallow coastal regions have been restricted largely to a select group of species, collectively known as surf-zone diatoms, that accumulate into dense patches along exposed sandy coastlines. Field-work has concentrated on establishing the distribution of these populations, the dynamics of population movement, and the causal factors. The dynamics of population movement include (a) an endogenously controlled vertical migration between the water surface during the day and the sediment at night and (b) a horizontal movement between the surf zone during medium to high energy conditions and the nearshore during calm periods. Much of the work, however, has been restricted to Anaulus australis, and it remains to be shown whether these behaviour patterns are characteristic of surf-zone diatoms as a whole.
INTRODUCTION An increasing number of exposed sandy beaches along temperate and warmtemperate latitudes are now considered exceptions to the opinion that sandy beaches are usually without much life (Pearse, Humm & Wharton, 1942; Hedgpeth, 1957; Brown, 1964; Eltringham, 1971), merely forming a boundary between terrestrial and marine systems. These so-called consumer-dominated environments were recognised as being subsidised by both oceanic and terrestrial organic material (Brown, 1964; McLachlan, 1980). While this is recognisably true for many sandy beaches, the presence of high phyto-plankton cell concentrations along many medium to high energy beaches is contrary to the opinion that sandy beaches support mainly a heterotrophic population of organisms. Ecological studies of surf-zone flora have been restricted to those beaches which are characterised by persistently dense populations of phytoplankton species, clearly visible as patches of discoloured water. The species responsible for these accumulations are diatoms and are known collectively as surf-zone diatoms. These diatoms, when present on sandy beaches, develop dense, localised accumulations known as cell patches. These patches are clearly visible as dark brown stains which result from large numbers of the cells floating on the surface where they are maintained by relatively stable foam.
156
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
Ecological studies go back to the work of Becking et al. (1927) and Thayer (1935), whose investigations on patches of Aulacodiscus kittonii along the Washington coast, USA, were aimed at evaluating oil production by these organisms. Apart from the work of Cassie & Cassie (1960) on primary productivity of Chaetoceros armatum and Asterionella glacialis (=japonica) along the New Zealand coast, little attention was given to surf-zone diatoms until the initiation of extensive studies on Chaetoceros armatum and Asterionella socialis along the Washington coast (reviewed by Lewin & Schaefer, 1983). The only other system to have received extensive attention is the Sundays River Beach along the southeast coast of South Africa (Mc-Lachlan & Lewin, 1981; Sloff, McLachlan & Bate, 1984; Campbell & Bate, 1988a; Talbot & Bate, 1988a). This system is dominated by Anaulus australis (=birostratus). In addition, two other studies of note are those of Eagle & Hennig (1984) in False Bay, South Africa and the ecophysiological work of Kindley (1983) in New Zealand. Other reports refer to sigh tings (Grindley & Taylor, 1964, 1970; Gunter, 1979; Gunter & Lyles, 1979; McLachlan & Hesp, 1984) or relate specifically to faunal studies (Rapson, 1954; Gianuca, 1983). Lewin & Schaefer (1983) reviewed much of the literature on surf-zone diatoms up to the early 1980s. We review the more recent literature pertaining to their ecology and propose updated models of cell patch formation, environmental determinants, and trophic significance. Most of these models have only been tested for A. australis, reflecting an almost complete lack of recent work on other surfzone diatoms.
SPECIES DIVERSITY OF SURF-ZONE DIATOMS The dominant taxonomic feature of surf-zone diatoms is their low species diversity (H’). All reported occurrences of large accumulations of these diatoms involve only one, or at the most, two species. The numerically dominant surf-zone diatoms form a discrete taxonomic group, with only six species having been reported, belonging to the four genera; Anaulus, Asterionella, Aulacodiscus, and Chaetoceros. There is no taxonomic lineage among these species, other than belonging to the division Bacillariophyta. Certain species tend to coexist, such as Anaulus australis and Asterionella glacialis, which cooccur along the Sundays River Beach (Campbell, 1987) and on a few beaches along the Australian coastline (McLachlan & Hesp, 1984). Working at the Sundays River Beach, Campbell (1987) showed that, within the surf zone, Anaulus australis made up 96.8% of the phytoplankton numbers in the surface layers. The remainder of the species assemblage consisted of Asterionella glacialis (1.3%), Navicula spp. (0.7%), and Aulacodiscus johnsonii (0.3%). Species of Campylosira, Hemiaulus, Leptocylindrus, Nitzschia, and Rhizosolenia made up the bulk of the rest. Anaulus australis loses its dominance seaward of the inner surf zone or beach terrace (see Fig 1 for geomorphologic terms) and often does not feature in the top 10 or 20 species. Transient dominance in sandy surf zone by non-surf-zone diatom species include the red tide organism, e.g., Gonyaulax spp. and Noctiluca spp. (Grindley & Taylor, 1970; Pérès, Laborde, Romano & Souza-Lima, 1986), while a number of non-red tide flagellates are occasional blooming species in other surf zones
ECOLOGY OF SURF-ZONE DIATOMS
157
Fig 1. —The morphology and hydrology of a two-bar, intermediate type sandy beach. Arrows indicate the characteristic onshore-offshore current patterns of rip systems.
(R.Carter cited in Eagle & Hennig, 1984; Hobson, 1985). These, however, fill entirely different ecological niches to surf-zone diatoms and will not be discussed further in this review.
ANATOMICAL CONSIDERATIONS Anatomical work on species of surf-zone diatoms has been restricted to the descriptive work of Lewin & Norris (1970) on Chaetoceros armatum and Asterionella socialis; the definitive work of Kruger & Wilson (1984) and Drebes & Schulz (1989) on Anaulus australis; and the work of Holmes & Mahood (1980) on Aulacodiscus kittonii. These studies indicate no common morphological traits among the various species of surf-zone diatoms. Both pennate and centric forms occur. They range from pillow-shape with no appendages as in Anaulus australis to cylindrical in Chaetoceros armatum, with an elaborate system of setae. There is also a wide variation in size, ranging from a volume of 65 µm 3 for Asterionella glacialis cells, to >6000 µm 3 for Aulacodiscus kittonii (Talbot & Bate, 1986). One common anatomical feature is the presence of an outer mucilaginous covering on the frustules. Lewin & Mackas (1972), Lewin, Chen & Hruby (1979), Lewin, Colvin & McDonald (1980), and Talbot & Bate (1988a) have shown Chaetoceros armatum and Anaulus australis to possess a system of platelets on the outer surfaces of the frustules. In Chaetoceros armatum Lewin et al. (1980) found the platelets to contain the clay species, montmorillinite and illite. In this species, the outer coat appears ‘rough’ with inorganic platelets embedded in the mucilage. In Anaulus australis, we also suspect these platelets to be of marine
158
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
sedimentary origin because they disappear diurnally (see p. 163 ). We have noted a similar outer layer of mucilage on the cells of Asterionella glacialis along the Sundays River Beach. BIOGEOGRAPHY Figure 2 illustrates the areas where patches of surf-zone diatoms have been observed around the world. In the Southern Hemisphere these sightings have been restricted to a belt between latitudes 29°S and 34°S. In the Northern Hemisphere patches have been sighted as far north as 49°N. The South African and Washington coasts are the only two coastlines to have been extensively studied with a view to establishing large-scale distribution features. Garver & Lewin (1981) recorded cell concentrations of surf-zone diatoms on 13 exposed sandy beaches of the Oregon and Washington coasts, USA, covering a distance of some 600 km of shoreline. Surfzone diatom cells were present along much of the coastline, extending as far south as Cape Blanco, Oregon. A major sampling exercise that covered the entire South African and Namibian coasts, a coastline of almost 5000 km, indicated that Anaulus australis is restricted to an ‘active area’ of some 1000 km. Here cell patches are common and background cell numbers are generally high. Outside this area, the species is almost entirely absent. A. australis has not been reported in the southwestern Indian Ocean (Taylor, 1966) or the southeastern Atlantic (Austin, 1980; Kruger, 1980). These observations are in accordance with those of Drebes & Schulz (1989) who found this species to have a restricted global distribution. This 1000-km stretch on the south coast coincides with that portion of the coastline which has a generally southerly aspect (Fig 2). The significance of aspect is considered important in South Africa although all the factors responsible have not been fully determined.
Fig 2. —Distribution map of surf-zone diatoms indicating recorded sites and active areas.
ECOLOGY OF SURF-ZONE DIATOMS
159
Sharp boundaries exist at the eastern and western limits of A. australis distribution. These coincide with the inflection points of the southern African continent and indicate that the environmental determinant for A. australis is linked in some way to the coastline configuration. The south coast has a unique configuration and aspect, being made up of a series of log-spiral (or half-heart) bays with eastward jutting promontories. Most of these bays are backed by transgressive or fixed dunefields (Tinley, 1985) and there are patches of A. australis on most of these exposed sandy beaches within the log-spiral bays. At the Cape of Good Hope in the west and Cape Padronne in the east the coast becomes relatively linear with only occasional embayments. On the east coast, one such embayment, Cintsa Bay, situated 30 km north of East London, has recently been shown to have dense patches of A. australis. This was the first sighting in an area previously considered to be free of patch-forming surf-zone diatoms. The distribution of A. australis along the south coast of South Africa and of Chaetoceros armatum and Asterionella socialis along the Oregon and Washington coasts have distinct similarities. In both cases the distribution is spatially variable, appears to have distinct boundaries which are related to coastal features and show no large-scale distribution patterns within the active area. Studies are at present underway to determine whether similar distribution features are present along the east coast of South America (N.M. Gianuca, pers. comm.). Cells of A. glacialis, which occasionally are co-dominant with Anaulus australis, do not share a similar ‘active area’ along the south coast of the Cape, but are more evenly distributed along the 5000 km of southern African coastline.
FREQUENCY OF PATCH OCCURRENCE Cell patches are not a permanent feature of the surf zone they occupy. Talbot & Bate (1988b) identified four major temporal features. The first is a diel periodicity, whereby cell patches form in the morning and wane at dusk before disappearing by nightfall. This has been reported for Chaetoceros armatum, Asterionella socialis (Lewin & Hruby, 1973; Lewin & Rao, 1975), Aulacodiscus kittonii (Kindley, 1983), and Anaulus australis (McLachlan & Lewin, 1981; Eagle & Hennig, 1984; Sloff, 1984). This diel periodicity is the most conspicuous temporal feature and has received the most attention. Both the morning increase and the late afternoon decrease in patch intensity are sudden (Fig 3). Kindley (1983) found that cells disappeared from the inner surf zone at night. Lewin & Hruby (1973) and Sloff (1984) reported lowered, but none the less significant numbers. Talbot & Bate (1988c) found complete disappearance when day-time concentrations were not high enough for patch formation (<300 cells·ml -1). When cell patches are present during the day, cell numbers are reduced at night. Several other features of the population also show diel rhythms (Fig 3), but these will be discussed later. Superimposed on the regular periodicity of appearance-disappearance is a mesoscale variability comprising a sequence of presence-absence-presence. Along a stretch of beach A. australis and Asterionella glacialis patches may fail to form for days or even weeks at a time (Gianuca, 1983; Sloff, 1984). Such a sequence was
160
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
Fig 3. —Stylised diagram illustrating the diel changes in cell characteristics of numerous surf-zone diatom species. Data compiled from Lewin & Hruby (1973), Lewin & Rao (1975), and Talbot & Bate (1986, 1988c).
studied in detail by Talbot & Bate (1988c) (Fig 4). Closer attention to Anaulus australis indicated that most of the cells had left the surf-zone water altogether during these periods of absence (Talbot & Bate, 1988c).
Fig 4. —Temporal changes in the concentration of Anaulus australis cells and patch occurrence during a storm-calm-storm cycle (after Talbot & Bate, 1988c).
ECOLOGY OF SURF-ZONE DIATOMS
161
Seasonality can be regarded as a third temporal feature in only a few species. Lewin (1978) found that Chaetoceros armatum displayed symptoms of physiological stress during the late summer, while cell concentrations of Asterionella socialis along the Olympic Peninsula, Washington disappeared during summer (Garver & Lewin, 1981). Seasonality was also found in the occurrence of “blooms” of Asterionella glacialis in South America (Gianuca, 1983). In this case an increase was reported from late summer, throughout autumn and winter, tending to disappear during spring. No seasonality has ever been reported in the case of Anaulus australis (McLachlan & Lewin, 1981). This is strengthened by the fact that no physiological adaptation or adjustment to temperature has been found in A. australis (Campbell & Bate, 1988b). This could be attributed to the warm-temperate climate of the southern coast of South Africa. The fourth time-scale is one that has been recorded along both the Washington coast and the Sundays River Beach. Sporadic observations of populations of surf-zone diatoms along the coast of the Olympic Peninsula, Washington, between 1927 and the 1970s have indicated a species change from Aulacodiscus kittonii to a codominance of Chaetoceros armatum and Asterionella socialis (Lewin, 1978). While Anaulus australis has been present along the Sundays River Beach for the last 15 years, there have been complete but reversible changes to Asterionella glacialis (Bate & McLachlan, 1987). Occasional co-dominance of these two species has been reported by Talbot & Bate (1988b) and Du Preez, Campbell & Bate (in press). A lack of information regarding the prevailing environmental conditions during these species changes has thus far made them impossible to explain. A pulse in patch intensity with a frequency of several seconds to a few minutes has been reported (Talbot, 1986) but it has failed to receive any further scientific attention. This frequency appears to coincide with that of infragravity waves which have a period of about 2 min at the Sundays River Beach. Maximum patch intensity is achieved during the wave trough. This periodicity requires more attention in order to quantify its frequency and to determine the driving forces involved. PATCH DYNAMICS OF SURF-ZONE DIATOMS EARLY VIEWS
Assemblages of surf-zone diatoms were originally termed “epidemics” (Becking et al., 1927) but later were considered to be blooming phenomena (Thayer, 1935). Lewin & Hruby (1973) subsequently considered the patches to form by a concentration of cells from the underlying water column to the surface layers in response to a diel periodicity in cell buoyancy. The role of cell buoyancy, together with the involvement of a blooming event has formed the core of the numerous subsequent models of patch dynamics. Current models concentrate more on the role of cell advection. FLOATATION
Floatation has been at the centre of most models of patch dynamics. Lewin & Schaefer (1983) concluded that “The ability to float at the surface of the water either
162
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
as a stabilized foam or attached to larger surf bubbles constitutes a feature unique to the surf diatoms”. Such floatation would permit cells to experience an onshore shear stress by wave bores which would keep them from being washed out to sea. Using surface drogues to study the movement of surf-zone diatom cells, Talbot & Bate (1987b) conclusively showed that particles at the air-water interface describe entirely different advection patterns from the remainder of the water column. While there is extensive exchange of water between the surf zone and the rip-head zone, there is no exchange of neuston across the outer breaker line. This impermeability of the breaker line to floating cells is the key factor whereby cells can build up a concentration gradient leading to numbers inside the surf zone that are four to five orders of magnitude greater than those recorded immediately seaward of the breaker zone. More recent laboratory evidence supports the proposal of Lewin & Hruby (1973) that floatation does not involve a change in the inherent buoyancy of the cells but is acquired by attachment to air bubbles (Strydom, unpubl.; Talbot, 1986). Similar floatation phenomena, whereby cells rise to the surface through adherence to rising bubbles, has been demonstrated for a variety of bacteria and phytoplankton (Boyles & Lincoln, 1958; Wallace, Loeb & Wilson, 1972). Micro-electrophoretic studies of the interaction between organic coatings of the frustules and air-water interfaces are needed to explain the mechanisms of floatation of surf-zone diatoms.
DIEL PERIODICITY
Extensive demographic studies of Anaulus australis have indicated conclusively that floatation by itself is insufficient to account for patch formation and there is a need to import cells into the water of the inner surf zone. Cell division rate does not provide this increase in numbers because at best it contributed 21% of the observed increase in cell numbers during patch formation in the early morning (Talbot & Bate, 1986). Kindley (1983), Sloff (1984), and Talbot & Bate (1986) originally suggested that this cell influx may come from points seaward of the breaker line during the early morning. This was disproved by Talbot & Bate (1988a) who showed that patch formation and decay could occur without any changes in the number of offshore cells. The source of cells, therefore, had to come from within the surf zone. This was finally demonstrated when the study area was extended to include the sediment. In this way it was possible to show that cells enter the sediment in the late afternoon when patches disappear. In the morning, patch formation follows the elution of cells from the sediment and their migration to the air-water interface. The absence of obvious senescence (i.e., no increase in dead cells or endospore formation during a decline in patch intensity) provides further evidence that surf-zone diatoms do not bloom in the normally accepted sense (Talbot & Bate, 1988b). Studies of cell characteristics have revealed numerous endogenous rhythms in surf-zone diatoms and many of these rhythms have been linked to the formation and decay of cell patches. Anatomical studies have demonstrated that cell floatation, division and size, as well as nitrate reductase (Collos & Lewin, 1974) and the appearance of a mucous sheath (Talbot & Bate, 1988a) show rhythmic changes, with distinct phasing to dawn and dusk and with a relatively quiescent period in between (see Fig 3).
ECOLOGY OF SURF-ZONE DIATOMS
163
Fig 5. —Model of diel patch formation and decay.
From numerous observations, Talbot & Bate (1988a) have proposed the following model of patch formation and decay. In the early morning, cells begin to divide. At this time they lose their mucous sheath. The loss of mucus (by an unknown process) causes the cells to be released from the sediment by the scouring action of waves. The cells then enter the water column and become briefly planktonic by attaching to air bubbles that have been entrained by passing wave bores. Cells concentrate at the air-water interface and there they complete the process of division (Fig 5). By late afternoon, the recently divided cells once again develop the mucous sheath which provides them with an active surface and enables them to switch their attachment from air bubbles to sand grains. In this way the population becomes nocturnally epipsammic until cell division is again initiated just prior to dawn. Although division is initiated early in the day, these early division activities are restricted to cell enlargement along the pervalvar axis, a re-positioning of the chloroplasts so that they are aligned on either side of the nucleus and cytokinesis. The two daughter cells are only apparent towards mid-day. Formation of the mucous layer and the process of cell division were proposed as cues in the above model following numerous observations of the selective appearance of dividing, mucus-free cells in the morning (Fig 6) and the selective sedimentation by recently divided, mucus-coated cells in the late afternoon. The obvious question of how the mucus is formed and removed from the outer surface of the cells is, as yet, unanswered.
MESOSCALE VARIANCE
164
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
Fig 6. —Day-night differences in the vertical distribution of the Anaulus australis population within the inner surf-zone. The frequency of dividing and mucus-free cells in the various vertical habitats is indicated. A fully blackened pie = 100%. (After Talbot & Bate, 1988).
Although the model of vertical migration explains the diel periodicity, it does not account for the fact that there are times when cells disappear completely from the surf-zone sediment and water column. Kindley (1983) and Sloff (1984) were the first workers to consider seriously patch dynamics in terms of a larger population which extended beyond the breaker line. It was proposed that patch dynamics may be a function of an onshore-offshore movement of cells across the breaker line, but in both cases neither data nor a mechanism were advanced. Kindley (1983) was able to show considerable numbers of Chaetoceros armatum and Aulacodiscus kittonii cells behind the surf zone, occasionally encountering concentrations in excess of 2×10 3 cells·ml -1 . Lewin (1978) recorded a cell concentration of Asterionella socialis of 1.3×10 5 cells·ml - 1 behind the breaker line at the bottom (6 m) along the Washington coast, while Talbot & Bate (1988c) found a concentration of 448 cells·ml -1 at the bottom immediately seaward of the breaker line. The overriding influence of the surf-zone hydrology in this regard made any further attempts
ECOLOGY OF SURF-ZONE DIATOMS
165
at elucidating the mechanisms of mesoscale variance entirely futile without adequate consideration of wave action and water currents. For this reason, we include a resume of the hydrological work that has been carried out on beaches dominated by surf-zone diatoms. Attempts to couple cell advection with hydrodynamic features has been restricted to Anaulus australis at the Sundays River Beach. Longshore currents and rip currents are the two dominant advective processes in intermediate energy surf zones dominated by surf-zone diatoms. The surf zone of the Sundays River Beach is dominated by rip currents, with an alongshore frequency of 2.1 active rips per running km of coastline (Talbot & Bate, 1987a). This condition is probably similar to that encountered at the majority of other localities where surf-zone diatoms have been reported. Photogrammetric measurements of dye dispersion in the surf zone and extensive aerial and ground surveys of rip activity along the Sundays River Beach, demonstrated that rip systems have the potential to link the surf zone and the adjacent rip-head zone (Fig. 1, p. 157) through extensive water exchange across the breaker line (Talbot & Bate, 1987b). A flushing of 0.032 m 3 ·m -1·s 1 across the breaker line gives the surf-zone water a half-residence period of 220 min on average. At this rate the return (onshore) flow of the rip system would be capable of advecting 2.3×10 9 cells·h -1 ·m -1, enough to build up cell patches within 8 h as found to occur at the Sundays River Beach (Talbot & Bate, 1988b). Having entered the surf zone, surf-zone diatoms rise to the surface, thereby ensuring their retention in this zone. This allows the concentration build-up to take place. Although surf-zone hydrodynamics have been shown to have the potential for such advection, no direct evidence of any such population movements had been forwarded until the work carried out along the Sundays River Beach by Talbot & Bate (1988c). Evidence for an onshore-offshore movement was obtained during two of five exercises, confirming the contentions of Kindley (1983) and Sloff (1984) of the involvement of a nearshore population in the mechanism of patch dynamics. The most distinct case of an offshore movement was found to follow a 22 m·s-1 gale when the entire surf-zone population disappeared from the surf zone to accumulate in the nearshore by 1030 h. Offshore currents with a flux of 80 m3 ·s-1·rip -1 were recorded during this event. Mesoscale variance is, therefore, meteorologically determined while diel periodicity is induced by rhythmic changes in cell characteristics. In both cases the driving force stems from wave and wave-related hydrographic features. The extent to which all surf-zone diatoms display similar behaviour patterns and tendencies to accumulate in exposed surf zones needs to be established. HYPOTHESES CONCERNING GEOGRAPHICAL DISTRIBUTION Numerous environmental factors have been considered important for making a particular beach host to accumulations of surf-zone diatoms. Reviewing the work of the 1970s, Lewin & Schaefer (1983) listed beach topography, wind, nutrient supply, and rainfall as important determinants. Many of the problems encountered in establishing the major environmental determinants relate to a lack of understanding concerning patch dynamics and prevailing environmental conditions
166
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
associated with patches of surf-zone diatoms. This is particularly true of beach morphology and hydrology which had been neglected, with the exception of the work of Garver & Lewin (1981) and Talbot & Bate (1987a, b). There are as yet no reports of ecosystems dominated by surf-zone diatoms along non-sandy beaches. This absolute requirement is expected to result from their need for an epipsammic life-mode at night (Talbot & Bate, 1988a). It may, in addition, be through a need for a particular surf circulation pattern that is specific to sandy beaches. Garver & Lewin (1981) argued about the need for a beach of a minimum length. This is corroborated by the work of Campbell & Bate (1988a) which shows high potential losses of cells in the alongshore direction through longshore water currents. The reason for this minimum length requirement has been linked to cell losses from the surf zone across the lateral boundaries of the beach. Talbot (1986) measured longshore currents in excess of 1.5 m·s -1. From this it was suggested that, while surf-zone diatoms are capable of overcoming losses across the breaker line, there might not be a similar conservative behaviour at the lateral boundaries. From the spatial distribution of cell patches during 1984, 1985, and 1986, Campbell & Bate (1988a) estimated that up to 16% of the A. australis population could have been lost across the lateral limits of the Sundays River Beach. There appears to be a requirement for rip-current related surf circulation which would agree with the mechanisms of patch formation advanced by Talbot & Bate (1988a). All reported cases of diatom patches come from broad, shallow surf zones, generally where the three dimensional flow patterns generate a rip-current dominated coastline (McLachlan & Lewin, 1981; Lewin & Schaefer, 1983; McLachlan, 1983). McLachlan & Hesp (1984) speculated that patch occurrence in incipiently dissipative systems (e.g., Eagle & Hennig, 1984) may be explained in terms of shore-normal standing waves which would result in a quasi-discrete distribution of patches at the antinodes. Several reports have suggested a direct wind influence on patch dynamics (Rapson, 1954; Gianuca, 1983; Eagle & Hennig, 1984; Romer, unpubl.). The work of Kindley (1983), Sloff (1984), and Romer (1986) provided evidence of maximum patch development with onshore winds. This positive correlation was explained on the basis of onshore winds providing an added means of concentrating cells into the surf zone. These authors concluded that wind direction and not velocity was important. Talbot & Bate (1988b) have shown that offshore winds in excess of 22 m·s-1 can lead to the immediate and complete removal of A. australis from the surf zone to areas seaward of the breaker line. McLachlan (1983) has suggested that wind controls both wave action and surf circulation and it is these factors that create the conditions for patch development. The report of a 24-hour lag between the onset of wind and its major effect (Sloff, 1984) supports this suggestion. Conclusive evidence for this indirect or remote effect of wind came from the work of Talbot & Bate (1988b) who monitored an A. australis population over a storm-calm-storm cycle. Cell numbers decreased with decreasing wave energy until patches failed to form in the morning. This inactive period lasted for a few days, ending abruptly with the resumption of high wave energy. Patches were back in the surf zone less then eight hours after the wave event. Light and variable winds prevailed throughout the exercise. The high waves had been generated in the Roaring Forties by the passage of an Atlantic trough some 1000 km from the site being studied.
ECOLOGY OF SURF-ZONE DIATOMS
167
It is expected that the effect of wave height on patch occurrence is itself indirect. We have shown (unpubl. data) that numerous surf parameters vary with wave height during this period, including beach morphodynamic state, frequency of rip currents, wave break on the outer sand bar, and beachface accretion-erosion rates. The foregoing evidence clearly establishes that wind is the major factor and that its effect can be resolved into local and remote components. The local component is direct and immediate, while the remote effect is indirect. Rain is reportedly correlated with the development of cell accumulations (Becking et al., 1927; Gunter, 1979; Gunter & Lyles, 1979; Gianuca, 1983) The influence of rainfall, however, has not been demonstrated in all cases. Kindley (1983) found no correlation between rainfall and patch activity in New Zealand while a similar lack of response has been found in South Africa. McLachlan & Lewin (1981) have argued that in cases of no apparent correlation, there could still be a dependence on ground water seepage. The work of Campbell (1986) conclusively shows that reduced salinities do not enhance rates of primary production in A. australis. A beneficial effect of ground water flow, if present, could be due to the high nutrient levels of such water. Seepage of ground water may be especially important in the eastern Cape, South Africa, where the two major areas of surf-zone diatom patches, i.e., the Sundays River and Maitlands beaches are backed by large dunefields which provide a slow but continuous water flow of 1000 l·day -1 ·m -1 to the surf zone (McLachlan & Illenberger, 1986). Ground water seepage may play a bigger role than previously anticipated with the discovery that A. australis cells are nocturnally epipsammic. Talbot & Bate (1988a) argued that this positioning of the cells gives them direct and first access to the nutrient-rich water that percolates through the sediment before entering the surf zone. On the other hand, work on nitrate reductase activity in A. australis indicates that maximum activity occurs some hours after cells elute from the sand (unpubl. data). The geographical location of areas with surf-zone diatoms (called “active” areas) may be linked to mesoscale (10–100 km) geomorphologic and hydrographic features (Garver & Lewin, 1981; Shannon, Walters & Moldan, 1983). In Algoa Bay, South Africa, patches form along the northern sector of the log-spiral bay where sediments have been shown to be trapped by hydrodynamic features created by the aspect of the beach relative to the prevailing direction of approaching waves (Swart, 1986) and the beach configuration. Talbot & Bate (1988d) have argued that this same trapping mechanism may account for the high concentration of detrital organic matter in this part of the bay. It remains to be determined whether accumulations of surf-zone diatoms require some large scale hydrodynamic feature to provide the trapping device. Using discriminant analysis, Garver & Lewin (1981) found that a certain concentration of the clay mineral montmorillinite is a prerequisite for patch occurrence along the Washington coast. This is interesting in the light of the proposed involvement (Talbot & Bate, 1988a) of a clay coat in the process of patch formation in A. australis and in the presence of a high clay and silt load at the Sundays River Beach (Talbot, 1986). Using the foregoing observations we propose the following model of environmental requirements for active areas (Fig 7). Active areas occur, at least within the Southern Hemisphere, strictly between the latitudes 29°S and 34°S, at the northern limit of the Roaring Forties. This can be translated into some overriding climatic requirement. Temperature is ruled out, as indicated by the
168
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
Fig 7. —Model of environmental requirements for surf-zone diatom accumulations.
distribution of A. australis along the entire southern coast of South Africa. There is a 6°C difference between the two extremities of this coast. Furthermore, eurythermal responses have been reported for Chaetoceros armatum and Asterionella socialis (Lewin & Mackas, 1972) as well as for Anaulus australis (Campbell & Bate, 1988b). We propose that the meteorological requirement is for periodic high wave energy which accompanies the passage of atmospheric disturbances or east-moving low pressure cyclonic systems which develop in the circumpolar westerlies along the Southern Ocean (Tyson, 1986). Within these active areas, beach aspect, relative to the direction of wave approach, and sediment particle size, if conducive, will result in beach morphodynamics which range from transverse bar and rip to incipiently dissipative (see Short & Wright, 1983, for an explanation of terms relating to beach morphodynamics). With this given morphodynamic state, two more important requirements are an ample supply of freshwater run-off and a beach geomorphology which provides an uninterrupted beach length of more than 10 km and some headland by which cells are trapped on a large scale and not swept away from the area. Given favourable conditions for the above parameters, the model predicts the potential for accumulations of surf-zone diatoms. It must be stressed that the freshwater requirement does not imply a need for reduced salinities, but rather a requirement for nutrients. This aspect is at present receiving extensive attention.
SPATIAL FEATURES IN RELATION TO RIP CURRENTS With the exception of accumulations of Chaetoceros as reported by Gunter (1979) and Gunter & Lyles (1979), accumulations of surf-zone diatoms take the form of discrete patches which occur at intervals in the foam within the inner surf zone. McLachlan & Lewin (1981) claimed that cell patches occurred in conjunction with rip systems, coinciding spatially with the offshore flow. They argued that cells accumulate as a result of a counter balance of forces between
ECOLOGY OF SURF-ZONE DIATOMS
169
offshore flowing rip currents and onshore shear stress caused by wave bores. Using a mathematical model to describe the patterns of accumulation of surfzone diatoms, Winter (1983) found cell patches to occur over rip currents under conditions of rapid growth rate and high wave energy. Under medium energy and with a slower growth rate, patches were found to form immediately to the side of rip currents. Subsequent observations along False Bay, South Africa (Eagle & Hennig, 1984) and Algoa Bay (Talbot & Bate, 1987c) have confirmed this association between rips and diatom patches. At low tide, 94% of 176 cell patches studied in Algoa Bay were found within a few metres of a rip current. A reduced association between patches and rips at high tide was ascribed to the more indistinct current patterns which prevail. In these experiments patches were, however, never observed directly over the offshore current of rip systems. Instead they occurred 5–15 m from the edge of the current (Eagle & Hennig, 1984; Talbot & Bate, 1987c). Ground measurements, including fine-scale observations of cell distribution in relation to water currents, provided confirmation of the latter relationship between rip currents and diatom accumulations. Current speed and direction accounted for 50% of the observed variance in cell concentration (Talbot & Bate, 1987c). Diatom patches are juxtaposed because they are present in quiescent areas between the offshore flowing rip current and onshore return flow. Surface drogues released in rip systems, often remained stationary for prolonged periods in these quiescent areas, mimicking the movement of the diatom patches. Frequency of cell division has a spatial distribution which has been reported for Anaulus australis during numerous studies (Talbot & Bate, 1987c, 1988a,c,d). Within the surf zone maximum frequency of division (F ) varies max from more than 90% in patches, to 50% in the water column, to 13% in the sediment while no cells in the nearshore region have been found in the process of division. This indicates that the process of diatom accumulation may operate on dividing cells only. This means that the denser the patches, the greater the population growth and vice versa.
THE ECOLOGICAL ROLE OF SURF-ZONE DIATOMS McLachlan (1980) was one of the first workers to recognise the ecological significance of large populations of surf-zone diatoms within areas previously accepted as being low in primary production, particularly by comparison with intertidal zones covered with macrophytes. McLachlan (1980) envisaged a self sustained ecosystem which stretched across the beachface, the surf zone and part of the nearshore (see Fig 1). In this system, the surf-zone diatoms are the primary producers, with large bivalve populations forming the major consumers and the interstitial fauna the decomposers. The functional integrity of such a beach/surf ecosystem would be maintained by water circulation patterns within the surf zone. This opinion was shared by Kindley (1983) who found surf-zone diatoms representing the producer level in a discrete ecosystem along several beaches of New Zealand. In this case, zooplankton and molluscs were the consumers, with
170
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
meiofauna and bacteria the decomposers. Using a simulated in situ modelling approach to calculate the primary production of A. australis, Campbell & Bate (1988c) estimated that this species fixed 120 kg C·m-1·yr -1 in Algoa Bay. We have confirmed the beach/surf ecosystem concept by demonstrating that patterns of circulation in the surf zone characteristic of beaches with associated surf-zone diatoms, give the surf-zone water mass a high residence time which ensures the retention of surf-zone diatoms. Surf zones dominated by surf-zone diatoms coincide with beaches that carry a high faunal biomass (Rapson, 1954; McLachlan & Hesp, 1984). Accumulations of surf-zone diatoms are one of three major factors considered to result in high biomass along the South African coastline (Hutchings, Nelson, Horstman & Tarr, 1983; McLachlan, 1983; Bally, 1987). Attempts at a systems analysis of the Sundays River beach/surf have indicated that A. australis produces enough carbon to drive the major food chains (McLachlan, 1980; McLachlan et al., 1981; Romer, 1986) including the macroscopic, interstitial, and microbial chains (McLachlan, 1987). Several surf-zone consumers have been shown to ingest surf-zone diatoms at high rates. These include the bivalves Siliqua patula (Lewin, Eckman & Ware, 1979), Donax serra (Donn, 1987), the mysid Mesopodopsis slaberri (Webb, Perissinotto & Wooldridge, 1987), the mullet Liza richardsonii (McLachlan & Lewin, 1981), and the prawn Macropetasma africana (Cockcroft, 1982). Current work on the dominant mysid Gastrosaccus psammodytes indicates a spatial distribution that closely resembles that of Anaulus australis (T.H.Wooldridge, pers. comm.). The potential role of the mucus produced by A. australis has recently been recognised. It is at present estimated that approximately 50% of the bacterial carbon requirement is met by the mucous coat released from A. australis cells in the early morning (G.S.Romer, pers. comm.). If the diatoms, however, reabsorb the mucus, the amount of carbon released for microbial consumption would be over-estimated. The view of beach/surf ecosystems being driven by surf-zone diatoms has, however, been challenged after reference to the high detrital load of 3.5 kg C·m1 (calculated out to 500 m) in the beach/surf ecosystem at the Sundays River Beach by Talbot & Bate (1988d). Despite the conspicuousness of the diatom patches, A. australis makes up only 5% of the total carbon of the whole ecosystem. The origin and fluxes of the detrital carbon present in these beaches are an important feature of these ecosystems that remains to be investigated. Our preliminary studies (unpubl. data) implicate vegetation of terrestrial origin rather than macrophytes or phytoplankton of marine origin. Surf-zone diatoms assume a high trophic significance only when patches are present within the surf zone. Under these conditions the live fraction accounts for almost 50% of the carbon in this restricted portion (5% by volume). Romer (1986) has argued that during this period the A. australis patches are “disproportionately important as zones of feeding and serve as loci for energy transfer through the grazing macrofaunal food chain”. The observed correlation between surf-zone diatom patches and high faunal biomass may not be a cause-and-effect relationship. It is possible that the beachface fauna are responding to a ‘trapping’ of organic particles by existing beach geomorphologic features. The organic particles can be detrital, surf-zone diatoms or both.
ECOLOGY OF SURF-ZONE DIATOMS
171
CONCLUSIONS Two decades of ecological study on surf-zone diatoms have contributed greatly to our understanding of their dynamics, including the mechanics and forcing functions whereby such marked dominance is achieved in the inner surf zone of certain beaches. Originally regarded as blooms, these large concentrations of cells characteristic of surf-zone diatoms have been shown to be accumulations. The cells make selective use of surf-zone water movement which drives a number of vertical and horizontal movements of the population. Among the advective features characteristic of these organisms is a diel vertical migration between the sand and water column which is linked to endogenous changes in cell characteristics. Meteorological and surf conditions induce onshore-offshore changes in the position of the population, bringing about periods of activity and inactivity in the surf zone, each of which can last between a few days to weeks. Wave energy, beach sediment, aspect, and geomorphology, together with a source of nutrients are identified as primary environmental determinants for active areas of these surf-zone diatoms. Such complex requirements lead to the active areas being restricted to a few hundred kilometres in length scattered around the world. It is necessary to establish the biogeography of surf-zone diatoms with greater certainty if the trophic significance of this group of marine diatoms is to be assessed. We can expect further work to reveal other sandy beaches that are dominated by surf-zone diatoms. Bate & McLachlan (1987) appealed for information from around the world. So far, however, there have been no additional reports. Furthermore, ecological understanding will only follow when more widely related case studies are examined. At the time of writing, the eastern coast of South America appears one of the most appealing areas to study. Surf-zone diatom populations produce part of the fuel for numerous food chains in the surf zone which link beachfaces, surf zones and parts of the nearshore together to form a single and viable beach/surf ecosystem. Biogeographic studies have indicated that surf-zone diatoms may assume trophic significance, but only within strictly delineated areas. They are virtually absent outside these areas. Work on the ecology of surf-zone diatoms appears to have reached a stage where further understanding is stymied. This is because ecological understanding has outstripped physiological and anatomical considerations. Attention has also been focused too sharply on A. australis, and to a lesser extent on Chaetoceros armatum and Asterionella socialis. There is an urgent need to test the models of patch dynamics proposed for Anaulus australis on other species.
REFERENCES Austin, N.E.H., 1980. Plankton of the Benguela current—a preliminary survey. Vol 1.. M.Sc. thesis, University of Natal, Pietermaritzburg, South Africa, 126 pp. Bally, R., 1987. The ecology of sandy beaches of the Benguela ecosystem. In, The Benguela and Comparable Ecosystems, edited by A.I.L.Payne et al., S. Afr. J. Mar. Sci., 5, 759– 770.
172
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
Bate, G.C. & McLachlan, A., 1987. Surf-zone discoloration by phytoplankton: the consequence of pollution? Mar. Pollut. Bull, 18, 65–67. Becking, L.B., Tolman, C.F., McMillin, H.C., Field, J. & Hashimoto, T., 1927. Preliminary statement regarding the diatom “epidemics” at Copalis Beach, Washington, and an analysis of diatom oil. Econ. Geol., 22, 356–368. Boyles, W.A. & Lincoln, R.E., 1958. Separation and concentration of bacterial spores and vegetative cells by foam floatation. Appl. Microbiol., 6, 327 only. Brown, A.C., 1964. Food relations on the intertidal sandy beaches of the Cape peninsula. S. Afr. J. Sci., 60, 35–41. Campbell, E.E., 1986. The influence of abiotic variables on the photosynthetic rate of Anaulus birostratus (Grunow) Grunow from the Sundays River Beach surf zone. M.Sc. thesis, University of Port Elizabeth, South Africa, 151 pp. Campbell, E.E., 1987. The estimation of phytomass and primary production of a surfzone. Ph.D. thesis, University of Port Elizabeth, South Africa, 429 pp. Campbell, E.E. & Bate, G.C., 1988a. The influence of current direction on longshore distribution of surf phytoplankton. Bot. Mar., 31, 257–262. Campbell, E.E. & Bate, G.C., 1988b. The photosynthetic response of surf phytoplankton to temperature. Bot. Mar., 31, 251–255. Campbell, E.E. & Bate, G.C., 1988c. The estimation of annual primary production in a high energy surf-zone. Bot. Mar., 31, 337–343. Cassie, R.M. & Cassie, V., 1960. Primary production in a New Zealand west coast phytoplankton bloom. N. Z. J. Sci., 3, 173–199. Cockcroft, A.C., 1982. Aspects of the biology of the swimming prawn Macropetasma africanus (Balss). M.Sc. thesis, University of Port Elizabeth, South Africa, 218 pp. Collos, Y. & Lewin, J., 1974. Blooms of surf zone diatoms along the coast of the Olympic Peninsula, Washington. IV. Nitrate reductase activity in natural populations and laboratory cultures of Chaetoceros armatum and Asterionella socialis. Mar. Biol., 25, 213–221. Donn Jr, T.E., 1987. Longshore distribution of Donax serra in two log-spiral bays in the eastern Cape, South Africa. Mar. Ecol. Prog. Ser., 35, 217–222. Drebes, G. & Schulz, D., 1989. Anaulus australis sp. nov. (Centrales, Bacillariophyceae), a new marine surf zone diatom, previously assigned to A. birostratus (Grunow) Grunow. Bot. Mar., 32, 53–64. Du Preez, D.R., Campbell, E.E. & Bate, G.C., in press. First recorded bloom of the diatom Asterionella glacialis Castracane in the surf-zone of the Sundays River Beach, South Africa. Bot. Mar. Eagle, G.A. & Hennig, H.F.-K.O., 1984. Surfzone phytoplankton blooms in False Bay. A summary of available information. CSIR Report C/SEA 8420, Stellenbosch, South Africa, 27 pp. Eltringham, S.K., 1971. Life in Mud and Sand. The English Universities Press Ltd, London, 218 pp. Garver, J.L. & Lewin, J., 1981. Persistent blooms of surf diatoms along the Pacific coast, USA. 1. Physical characteristics of the coastal region in relation to the distribution and abundance of the species. Estuarine Coastal Shelf Sci., 12,217–229. Gianuca, N.M., 1983. A preliminary account of the ecology of sandy beaches in southern Brazil. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W.Junk Publishers, The Hague, pp. 413–419. Grindley, J.R. & Taylor, F.J.R., 1964. Red water and marine fauna mortality near Cape Town. Trans. R. Soc. S. Afr., 37, 111–130. Grindley, J.R. & Taylor, F.J.R., 1970. Factors affecting phytoplankton blooms in False Bay. Trans. R. Soc. S. Afr., 39, 201–210. Gunter, G., 1979. Notes on sea beach ecology. Food sources on sandy beaches and localized diatom blooms bordering Gulf beaches. Gulf Res. Rep., 6, 305–307. Gunter, G. & Lyles, C.H., 1979. Localized plankton blooms and jubilees on the Gulf Coast. Gulf Res. Rep., 6, 297–299.
ECOLOGY OF SURF-ZONE DIATOMS
173
Hedgpeth, J.W., 1957. Sandy beaches. In, Treatise on Marine Ecology and Paleoecology, Vol. 1, Ecology, edited by J.W.Hedgpeth. Geol. Soc. Am. Mem., 67, 587–608. Hobson, L.A., 1985. Surf eutrophication? Mar. Pollut. Bull, 16,499 only. Holmes, R.W. & Mahood, A., 1980. Aulacodiscus kittonii Arnott-distribution and morphology on the west coast of the United States. Br. Phycol. J., 15, 377–389. Hutchings, L., Nelson, G., Horstman, G.A. & Tarr, R., 1983. Interaction between coastal plankton and sand mussels along the Cape coast, South Africa. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W.Junk Publishers, The Hague, pp. 481–500. Kindley, M.J., 1983. Physiological ecology of surfzone diatoms. M.Sc. thesis, University of Auckland, New Zealand, 109 pp. Kruger, I., 1980. A checklist of South West African marine phytoplankton, with some phytogeographic relations. Fish. Bull. S. Afr., 13, 31–53. Kruger, I. & Wilson, E.G., 1984. Morphology and affiliation of the centric diatom Anaulus birostratus (Grunow) Grunow from South Africa. S. Afr. J. Mar. Sci., 2, 163– 194. Lewin, J., 1978. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. IX. Factors controlling the seasonal cycle of nitrate in the surf at Copalis Beach (1971–1975). Estuarine coastal Mar. Sci., 7, 173–183. Lewin, J., Chen, C. & Hruby, T., 1979. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. X. Chemical composition of the surf-zone diatom Chaetoceros armatum and its major herbivore, the Pacific razor-clam, Siliqua patula. Mar. Biol., 51, 259–265. Lewin, J., Colvin, J.R, & McDonald, K.L., 1980. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. XII. The clay coat of Chaetoceros armatum T. West. Biol. Mar., 23, 333–341. Lewin, J., Eckman, J.E. & Ware, G.N., 1979. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington, XI. Regeneration of ammonium in the surf environment by the Pacific razor clam Siliqua patula. Mar. Biol., 52, 1–9. Lewin, J. & Hruby, T., 1973. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. II. A diel periodicity in buoyancy shown by the surf-zone diatom species Chaetoceros armatum T. West. Estuarine coastal Mar. Sci., 1, 101– 105. Lewin, J. & Mackas, D., 1972. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. I. Physiological investigations of Chaetoceros armatum and Asterionella socialis in laboratory cultures. Mar. Biol., 16, 171–181. Lewin, J. & Norris, R.E., 1970. Surf-zone diatoms of the coasts of Washington and New Zealand Chaetoceros armatum T. West and Asterionella spp. Phycologia, 9, 143–149. Lewin, J. & Rao, V.N.R., 1975. Blooms of surf-zone diatoms along the coast of the Olympic Peninsula, Washington. VI. Daily periodicity phenomena associated with Chaetoceros armatum in its natural habitat. J. Phycol., 11, 330–338. Lewin, J. & Schaefer, C.T., 1983. The role of phytoplankton in surf ecosystems. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W. Junk Publishers, The Hague, pp. 381–389. McLachlan, A., 1980. Exposed sandy beaches as semi-closed ecosystems. Mar. Environ. Res., 4, 59–63. McLachlan, A., 1983. Sandy beach ecology—A review. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W.Junk Publishers, The Hague, pp. 321–380. McLachlan, A., 1987. Sandy beach research at the University of Port Elizabeth: 1975– 1986. Institute for Coastal Research, University of Port Elizabeth, South Africa, 111 pp McLachlan, A., Erasmus, T., Dye, A.H., Wooldridge, T., van der Horst, G., Lasiak, T.A. & McGwynne, L., 1981. Sand budget energetics: an ecosystem approach towards a high energy interface. Estuarine Coastal Shelf Sci., 13, 11–25.
174
M.M.B.TALBOT, G.C.BATE AND E.E.CAMPBELL
McLachlan, A. & Hesp, P.A., 1984. Surf zone diatom accumulations on the Australian coast. Search, 15, 230–231. McLachlan, A. & Illenberger, W.K., 1986. Significance of groundwater nitrogen input to a beach/surfzone ecosystem. Stygologia, 3, 291–296. McLachlan, A. & Lewin, J., 1981. Observations on surf phytoplankton blooms along the coast of South Africa. Bot. Mar., 24, 553–557. Pearse, A.S., Humm, J.H. & Wharton, G.W., 1942. Ecology of sand beaches at Beaufort, North Carolina. Ecol. Monogr., 12, 135–190. Pérès, J.-M., Laborde, P., Romano, J.-C. & Souza-Lima, Y., 1986. Eau rouge à Noctiluca sur la côte de Provence en Juin 1984. Essai d’interprétation dynamique. Ann. Inst. Océanogr. (Paris), 62, 85–116. Rapson, A.M., 1954. Feeding and control of Toheroa (Amphidesma ventricosum Grey) (Eulamellibranchiata) populations in New Zealand. Aust. J. Mar. Fresh-water Res., 5, 486–512. Romer, G.S., 1986. Faunal assemblages and food chains associated with surf-zone phytoplankton blooms. M.Sc. thesis, University of Port Elizabeth, South Africa, 194 pp. Shannon, L.V., Walters, N.M. & Moldan, A.G.S., 1983. Some features in two bays as deduced from satellite ocean colour imagery. S. Afr. J. Mar. Sci., 1, 111–122. Short, A.D. & Wright, L.D., 1983. Physical variability of sandy beaches. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W.Junk Publishers, The Hague, pp. 133–144. Sloff, D.S., 1984. Spatio-temporal biomass distribution of surf zone phytoplankton. M.Sc. thesis, University of Port Elizabeth, South Africa, 152 pp. Sloff, D.S., McLachlan, A. & Bate, G.C., 1984. Spatial distribution and diel periodicity of Anaulus birostratus Grunow in the surf zone of a sandy beach in Algoa Bay, South Africa. Bot. Mar., 27, 461–465. Swart, D.H., 1986. Physical environmental interactions in the Sundays River/ Schelmhoek area. CSIR Res. Rep. 568, Stellenbosch, South Africa, 44 pp. Talbot, M.M. B., 1986. The distribution of the surf diatom Anaulus birostratus in relation to the nearshore circulation in an exposed beach/surfzone ecosystem. Ph.D. thesis, University of Port Elizabeth, South Africa, 356 pp. Talbot, M.M.B. & Bate, G.C., 1986. Diel periodicities in cell characteristics of the surf diatom Anaulus birostratus: their role in the dynamics of cell patches. Mar. Ecol. Prog. Ser., 32, 81–89. Talbot, M.M.B. & Bate, G.C., 1987a. Distribution patterns of rip frequency and intensity in Algoa Bay, South Africa. Mar. Geol., 76, 319–324. Talbot, M.M.B. & Bate, G.C., 1987b. Rip current characteristics and their role in the exchange of water and surf diatoms between the surfzone and nearshore. Estuarine Coastal Shelf Sci., 25, 707–720. Talbot, M.M.B. & Bate, G.C., 1987c. The spatial dynamics of surf diatom patches in a medium energy, cuspate beach. Bot. Mar., 30, 459–465. Talbot, M.M.B. & Bate, G.C., 1988a. The use of false buoyancies by the surf diatom Anaulus birostratus in the formation and decay of cell patches. Estuarine Coastal Shelf Sci., 26, 155–167. Talbot, M.M.B. & Bate, G.C., 1988b. The response of diatom populations to environmental conditions. Changes in the extent of the planktonic fraction and surface patch activity. Bot. Mar., 31, 109–118. Talbot, M.M.B. & Bate, G.C., 1988c. Distribution patterns of the surf diatom Anaulus birostratus in an exposed surfzone. Estuarine Coastal Shelf Sci., 26, 137–153. Talbot, M.M.B. & Bate, G.C., 1988d. The relative quantities of live and detrital organic matter in a surf diatom-dominated surf-zone. J. Exp. Mar. Biol. Ecol., 121, 255– 264. Taylor, F.J.R., 1966. Phytoplankton of the South Western Indian Ocean. Nova Hedwigia, 12, 433–476.
ECOLOGY OF SURF-ZONE DIATOMS
175
Thayer, L.A., 1935. Diatom water-blooms on the coast of Washington. Proc. La. Acad. Sci., 2, 68–72. Tinley, K.L., 1985. Coastal dunes of South Africa. South African National Scientific Programmes, Rep. No. 109, FRD, CSIR, 300 pp. Tyson, P.D., 1986. Climatic Change and Variability in Southern Africa, Oxford University Press, Cape Town, 220 pp. Wallace, G.T., Loeb, G.I. & Wilson, D.F., 1972. On the floatation of particulates in seawater by rising bubbles. J. Geophys. Res., 77, 5293–5301. Webb, P., Perissinotto, R. & Wooldridge, T.H., 1987. Feeding of Mesopodopsis slabberi (Crustacea, Mysidacea) on naturally occurring phytoplankton. Mar. Ecol. Prog. Ser., 38, 115–123. Winter, D.F., 1983. A theoretical model of surf-zone circulation and diatom growth. In, Sandy Beaches as Ecosystems, edited by A.McLachlan & T.Erasmus, Dr W.Junk Publishers, The Hague, pp. 157–167.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 177–276 Margaret Barnes, Ed. Aberdeen University Press
PATTERNS OF REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS* BERNABÉ SANTELICES Departamento de Ecologia, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile
ABSTRACT Reproductive processes of seaweeds and patterns of propagule production and release, dispersal, settlement and recruitment are reviewed. Present interpretations of the adaptive values of life history aspects such as sexual and asexual reproduction, alternation of generations, isomorphic and heteromorphic cycles and relative allocation of resources to reproduction are discussed. The evidence concerning the abiotic control and the ontogenic, specific and seasonal patterns of propagule production and release are evaluated. The nature of the propagule releasing mechanisms, the morpho-physiological characteristics of the released propagules, their dispersability by biotic and abiotic agents and the factors influencing their settlement, attachment, germination and recruitment are analysed. Overall, the evidence indicates that concepts derived from studies with land plants do not completely explain the reproductive processes of seaweeds. Similarly, the ecophysiological responses of the free-floating propagules are also conspicuously different from the free living plankton to which they have been compared. The literature describes numerous processes that remain poorly understood. Examples are: the mechanisms of spore release; the biological basis for the reduced viability of algal spores; the roles of grazers on spore release and dispersal and the ecological importance of positive interspecific and intraspecific interactions on settlement and recruitment. In addition, numerous ecologically important phenomena have not been reported or studied. These include the nature and dynamics of the spore clouds, the turnover rates and ecological roles of the bank of microscopic forms, alternative ways of spore attachment and the adaptive significance of spore germination. A more realistic understanding of the reproduction, dispersal and recruitment processes of seaweeds will result if ecological concepts and methods are applied to them, with due consideration for their morphological, physiological and life-history characteristics.
INTRODUCTION From an estimated total of 9×10 9 spores released yearly by a macroscopic sporophyte of Laminaria longicruris, about 9×10 6 recruit to the microscopic gametophyte stage (Chapman, 1984), and of these, only one sporophyte×m-2 grows * Review of literature completed by March 30, 1989.
178
BERNABÉ SANTELICES
to reproductive size. Thus, the establishment of a new individual in a given area, either colonising a new habitat or replacing a previously established parental population, is a complex phenomenon which includes several stages and is characterised by enormous mortality. The various stages include propagule production and release, dispersal, settlement, recruitment and growth. Since at each stage of the process the individuals are affected by environmental stresses, which include abiotic extremes, grazing and disease, a fraction of the population is removed by mortality at each stage. The survivors deal with a different set of environmental constraints in each succeeding stage. Thus, individuals and populations observed in the field are the tiny minority that the environment has failed to eliminate. The hazards at each stage vary among species. Some species such as those in the genera Pelvetia and Iridaea, are susceptible to grazing of their reproductive tissues (Moore, 1977; Gaines, 1985; Gunnill, 1985). Others, such as Enteromorpha or Ulva, because of their larger dispersal shadows, are susceptible to consumption of their spores by plankton grazers. Germinating propagules of crustose species can be overgrown by other erect, fast-growing, frondose algae (Lubchenco & Cubit, 1980; Slocum, 1980) while spores settling in estuarine or high intertidal habitats are exposed to abiotic extremes. Since these hazards are different for different taxa, a variety of responses are often found when algal species assemblages are studied in a given place. These responses suggest that there are several alternative ways to produce, release, disperse and settle propagules. In seaweeds, the various life-history stages may exhibit different ploidy levels, may be of very different sizes and inhabit different environments. For example, the conditions affecting a macroscopic (1–2 m long), benthic, diploid sporophyte are very different from those affecting the microscopic (15–150 µm diameter) free-floating, propagules or the small-sized or microscopic, haploid gametophyte. Consequently, the processes of reproduction, dispersal and recruitment of seaweeds often involve different ecological scales and their study has to be approached from different perspectives and with different techniques. This diversity of approaches and techniques, the different spatial and temporal scales involved and the diversity of responses observed seemingly have only stimulated reviews on specific aspects of reproduction (e.g. Pedersen, 1981; West & Hommersand, 1981; Clayton, 1988) and dispersal (e.g. Hoek, 1987; Hoffmann, 1987) Comprehensive, integrated reviews are still lacking and the pertinent literture is both abundant and scattered. This study discusses the accumulated information on the processes of propagule production and release by seaweeds, their dispersal and their settlement and recruitment in intertidal and sub tidal communities. In order to understand these processes, an analysis of ecologically important patterns of reproduction in seaweeds is also provided. As Doherty & Williams (1988) have noted, the realisation by marine ecologists that variability in replenishment of spores can profoundly influence the local demography of species and the structure of multispecies assemblages, led to a renewed interest in studying patterns of reproduction, dispersal and recruitment. In seaweeds such processes are important, in addition, for both an understanding of patterns of geographic distribution and for the development of cultivation and farming techniques of economically important species.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
179
In this review, the various processes are approached from the perspective of field ecology, with special emphasis on those adaptations that increase the organism’s ability to cope with a given environment or maximise the chances of survival of offspring in the field. Since few studies on seaweed reproduction have been approached from this perspective, the body of evidence accumulated is likely to appear heterogeneous and fragmentary. In fact, most conclusions reached in a recent review (DeWreede & Klinger, 1988) on patterns of seaweed reproduction were mainly based on correlations because rigorous experiments are lacking. By approaching the problem from this perspective, however, areas in need of additional research should become evident. Identification of such areas is a primary goal of this review.
SOME GENERAL PATTERNS OF REPRODUCTION IN SEAWEEDS Seaweeds produce a variety of unicellular or multicellular agents or reproduction. They can be sexual or asexual, motile or non-motile, small or large. The following section is a selected précis of the large amount of lifehistory information that is available. It is presented to provide background for readers unfamiliar with these organisms. It is then followed by discussions of problems related to general patterns of seaweed reproduction. These discussions include: (1) an explanation for the adaptive value of alternation of generations and isomorphic and heteromorphic cycles; (2) explanations for the relative abundance of haploid and diploid thalli; (3) explanations for sexual and asexual reproduction; and (4) the application of the r- and k-selection concepts to seaweeds.
SEXUAL AND ASEXUAL REPRODUCTION
Most macroscopic Chlorophyta, Phaeophyta and Rhodophyta exhibit both sexual and asexual reproduction and the phenomenon of alternation of generations is widespread in all three groups. In the field, the most obvious examples of asexual reproduction are the stoloniferous outgrowths of creeping axes, which are to be found on almost all types of substrata that support seaweed growth. For example, this is a common way in which species of Gelidium and Pterocladia propagate on hard substrata (Yamada, 1976). Species of Caulerpa can colonise new, soft substrata by stoloniferous growth while the initiation and expansion of extensive beds of Gracilaria in several places is achieved by the establishment of thallus fragments partially buried in soft bottoms (Santelices & Doty, 1989). Several types of macroalgae, especially filamentous forms, but also species of Enteromorpha and Sargassum, propagate by various forms of fragmentation. Fragmentation may result from physical or chemical damage such as wave action or insolation. In a few species, such as Rhodochorton purpureum, fragmentation is even recognised as the principal mode of propagation (Knaggs, 1966, 1967; Pearlmutter & Vadas, 1978). After settlement, a fragment of this species forms one or more adhesive rhizoids and subsequently new filamentous shoots.
180
BERNABÉ SANTELICES
The production of vegetative offspring, however, often requires a high investment of resources per propagule (Fenner, 1985). An economic way of population increase is through asexual reproduction by small-sized, multi- or unicellular propagules. Being small in comparison with the parent plant, propagules can be produced in large numbers and their small size facilitates their dispersal to new habitats. Seaweeds produce both multicellular and unicellular, small-sized propagules. Examples of multicellular propagules are the buds or gemma-like branch-lets produced by Sphacelaria. They consist of triradiate or quadriradiate branches of up to 200 µm long, attached to a major axis by a short stalk (Boney, 1966). Once detached, the rayed structure floats easily and eventually becomes entangled on a given substratum. Any one of the arms can then germinate to produce a soft filament that then expands into a disc from which the erect filament of a new plant arises. Unicellular propagules, the spores, are produced by most seaweeds within ordinary vegetative cells or within special cells or groups of cells called sporangia. Even though many species produce these unicellular propagules by mitotic division, in seaweeds the term “spore” is also used for unicellular propagules resulting from meiotic divisions. Asexually formed propagules are expected to produce offspring that are genetically identical to the parent plants (Stebbins & Hill, 1980). The resulting population supposedly has less genetic flexibility than sexually produced populations and major environmental changes can seriously affect them. In stable environments, however, where the parental plants are already established, asexual propagules should exhibit survival rates at least as high as sexually-produced propagules. Meiotically produced spores have the potential for greatly enhanced genetic variability that is likely to increase the probabilities of survival of at least some individuals during environmental changes. Sexual reproduction, however, involves larger expenditures of resources than asexual reproduction, with greater risks of reproductive failures. For example, in the field, the density of gamete-producing individuals per unit area and the resulting distance between them might limit fertilisation. In fact, this has been one of the factors found to limit recolonisation of barren grounds by Macrocystis (North, 1971b). In other cases, as in the Australian populations of Scytosiphon lomentaria studied by Clayton (1981), not all gametes may be functional. The values found with that species could be as low as 0.4% or as high as 79%. Interestingly, they never reached 100%, suggesting that even though gametes might encounter each other in the field, this does not necessarily ensure successful sexual fusion. There is not enough information to judge the generality of the above situations, but perhaps it explains the necessity of both sexual and asexual reproduction in seaweeds. Below some critical gamete density, asexual reproduction may become more important; a situation likely to be common in many habitats, where vertical and horizontal currents may reduce the probabilities of gamete encounters. The relative importance of different types of reproduction in population maintenance seem to vary from one type of algae to another. The establishment of most kelp species, where sporophytes have rather reduced propagation capacities, seems to depend entirely on spores. Traditionally, the establishment
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
181
of populations of opportunistic species has also been thought to depend on sexual or asexual spores. Kennelly & Larkum (1983), however, found that the temporal patchiness in settlement of species of the genera Polysiphonia, Bangia, Ulva and Giffordia reflected not only changes in the release of spores from mature plants, but also the abundance of fragments of mature thalli landing on their experimental plates. For other species such as Gelidium, Iridaea or Gymnocongrus, spore release does not seem to lead to remarkable success in establishing new populations. The observations of Hansen (1977) with respect to Iridaea cordata in central California may be used to summarise our present understanding of this problem. At the end of the growing season, these Californian populations consist almost entirely of mature thalli, the majority of which are tetrasporangial. Therefore, the population should have a high potential for forming sexual plants. Despite this, gametangial thalli constitute only a minor component of the population. Moreover, new blades are primarily produced from perennating crusts. Hansen (1977) suggested that perhaps holdfasts are long-lived and stress-tolerant and survive better under field conditions where competition for space may limit sporeling development. If that is true, the basal structure would be an adaptation for successful vegetative production at the expense of sexual reproduction. As Hansen (1977) noted, however, the adaptive value of investing so much energy in the development of reproductive sori is not understood. Similar comments have more recently been repeated by several authors (e.g. May, 1986; D’Antonio, 1986). Apomeiosis has been suggested as a possible explanation because apomictic life histories have been described for species of Gigartinales (West & Polanshek, 1972; Polanshek & West, 1977). However, observations and comments on the reduced success of sexual or asexual propagules in establishing new populations, as compared with vegetative regeneration, include not only Gigartinales but several other groups of red and brown algae. Obviously this is an area in great need of additional research. It is not clear if spore production involves large amounts of resources in different types of seaweeds. If that is the case, it is not understood why so many seaweeds invest such resources in propagules that are rather ineffective in establishing new populations.
ALTERNATION OF GENERATIONS
Most species of Chlorophyta, Phaeophyta and Rhodophyta so far studied exhibit sexual and asexual reproduction with free living individuals that specialise in the production of asexual spores or of sexual gametes (Bold & Wynne, 1985). These are referred as sporophytes and gametophytes respectively. In most seaweeds, haploid gametophytes and diploid sporophytes alternate in a cyclic fashion linked by the events of syngamy and meiosis. The phenomenon is known as alternation of generations and the life histories exhibiting two karyologically different phases are known as diplohaplontic life histories. They are very well represented among green and brown seaweeds. It has long been recognised that alternation of generations in general, and the diplohaplontic life histories in particular, result in increased genetic variability during the production of a large number of propagules (Svedelius, 1929; Feldmann, 1952; Drew, 1955; Dixon, 1973; Searles, 1980; DeWreede & Klinger,
182
BERNABÉ SANTELICES
1988). In this type of life history, mitotic divisions of the zygote initiate the diploid sporophyte. Some or a majority of these diploid cells will later undergo meiosis during spore formation. Assuming outcrossing, resultant heterozygosity in the original zygote, and a reasonably large number of chromosomes, each of these spores will be a genetically different meiospore, likely to produce genetically distinct offspring. Therefore, a delay of meiosis until after a multitude of diploid cells has been produced from the zygote yields a potentially great diversity of genotypes from a single original zygote. Red seaweeds (Rhodophyta) exhibit slightly more complex life histories, generally recognised as triphasic because, in addition to the gametophytes, two very different sporophytic phases are produced. After gamete fusion, the zygote develops by mitosis into a diploid sporophyte which is retained and nurtured by the female gametophytic thallus. This parasitic plant eventually produces mitotically divided spores that, if settling in a safe and fertile place, will grow into a diploid, free-living sporophyte. As in Chlorophyta and Phaeophyta, this sporophyte will then divide meiotically, yielding a great quantity of genetically diverse meiospores. The adaptive significance of retaining and nurturing this second sporophyte has been interpreted as a mechanism compensating for the lack of motile gametes in the Rhodophyta (Searles, 1980). Fertilisation processes are thought to have been relatively inefficient in ancestral red algae compared with other algae, such as Chlorophyta and Phaeophyta, with specialised systems using flagellated gametes. The idea has remained largely untested due to the methodological difficulties involved in fertility studies with red algae and the problems of handling microscopic propagules in the field. The concept is consistent with the idea that the increased expenditures of resources and greater risks of reproductive failures involved in sexual reproduction could be somewhat compensated for by asexual replication. However, several basic assumptions in this hypothesis remain little understood. First, there seem to be no quantitative measurements comparing the fertilisation efficiency of red algae with green or brown seaweeds. Second, the scarcity of male plants, so commonly reported among red algae (e.g. Dixon, 1973) has not been considered. Third, it is unknown whether or not lack of motility in the reproductive elements of red algae have in fact contributed to the supposedly inefficient reproduction. Fourth, it is unknown if red algae might have adaptations other than motility that might increase fertilisation efficiency. Several species of red algae release their spermatia in slime strands (Fetter, 1977) of, as yet, unknown function.
HETEROMORPHIC AND ISOMORPHIC LIFE CYCLES
Since seaweeds produce both haploid and diploid thalli and spores, ideas explaining the origin of alternation of generations in land plants have been applied to them. In land plants, there is a correlation between DNA quantities and life style (Stebbins & Hill, 1980). Forms with relatively low DNA contents exhibit a tendency towards a more fugitive, weedy annual opportunistic life style, while those with high DNA contents tend towards a slower-growing, perennial, environmentally resistant style. Therefore, the occurrence of both phases in the life history of a species could be understood as an adaptation to
A sample of biological and chemical differences among reproductive phases of isomorphic species of seaweed.
TABLE I
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS 183
184
BERNABÉ SANTELICES
an environment that was seasonally variable (Stebbins & Hill, 1980), or that contained two niches differing chiefly with respect to certain environmental characteristics (Keddy, 1981). The above idea has been applied to seaweeds (Nakahara & Masuda, 1971; Hsiao & Druehl, 1973; Lubchenco & Cubit, 1980; Littler & Littler, 1980; Druehl, 1981, Clayton, 1988) and thought to explain the occurrence of species with heteromorphic alternation of generations (e.g. morphologically different gametophytes and sporophytes). The evidence indicates numerous ecological differences between reproductive phases. In such species this might include differential effects of ecological factors in relation to propagule production and release or interphase differences in the growth, reproduction and mortality of the propagules, germlings or mature thalli. Overall, these differences support the idea that heteromorphic alternation of generations could be understood as adaptations to exploit seasonally or spatially dissimilar niches. In fact, the morphological and ecological dissimilarities between some phases (e.g. Porphyra, Macrocystis, Scytosiphon) are so marked it has been suggested that they are under bimodal selection pressures with the two phases responding to completely different environmental constraints and evolving towards opposite life styles (Vadas, 1979). Many green, brown and red seaweed species are isomorphic, however, and they also occur in seasonally or temporally variable environments. As the reproductive phases show virtually identical forms, questions focus on whether or not there are adaptive advantages and concommitant costs associated with ploidy levels in these species. The data, summarised in Table I, also suggest numerous morphological, ecological and chemical differences between reproductive phases of isomorphic algae. Even though the differences seem to be more subtle than in heteromorphic species (Littler, Littler & Taylor, 1987a), they do exist and pose unanswered questions as to the adaptive value of the phenomenon of alternation of generations. Together with suggesting an adaptive explanation for the phenomenon of alternation of generations, Stebbins & Hill (1980) postulated that heteromorphic alternation of generations was derived from isomorphic alternation of generations by disruptive selection. This proposal is based on the assumption that complex life cycles are evolutionarily unstable because, as selection acts independently on each reproductive stage, one of them will be reduced or lost in favour of the other (Istock, 1966). The explanation has not been explicitly tested with seaweeds. However, not all experimental results fit the hypothesis. For example, experimental studies with the isomorphic red alga Iridaea laminarioides have shown that herbivores have a marked preference for the diploid phase (Luxoro & Santelices, 1989). In contrast, previous studies (Lubchenco & Cubit, 1980) have suggested that among heteromorphic species the haploid is the phase most preferred by herbivores. It is difficult to understand how disruptive selection could operate and one type of alternation be derived from the other, with these changes in importance of ecologically significant factors.
RELATIVE ABUNDANCE OF GAMETOPHYTES AND SPOROPHYTES
The question of the relative abundance of gametophytes and sporophytes is closely related to the adaptive value of the phenomenon of alternation of generations which
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
185
is supposed to lie in the adaptiveness of diploidy itself (Hansen & Doyle, 1976). A diploid genome is likely to have enhanced fitness as a result of heterosis and of the masking of deleterious recessive alleles. The testing of this idea in seaweeds has indicated that in general (e.g. see reviews by Dixon, 1965, 1973; DeWreede & Klinger, 1988; Clayton, 1988) many populations are dominated by sporophytes. The opposite is true, however, in several genera of the family Gigartinaceae of the Rhodophyta (see reviews by Hannach & Santelices, 1985 and Hannach & Waaland, 1986). Sporophytic dominance has been explained in several ways. As early as 1944, Johnstone & Feeney suggested differential mortality of one phase over the other or differential survival of one type of propagule over the other. Both explanations have later been repeated by several authors (Hansen & Doyle, 1976; Mshigeni, 1976; Hoyle, 1978; Kain, 1982). Apomeiosis as well as production of adventitious thalli by tetrasporophytes have also been suggested (Hansen & Doyle, 1976; Carter, 1985). Alternatively, differences in the sporophyte to gametophyte ratio could reflect differences in the duration of the respective reproductive processes rather than in the abundance of both phases. Since female plants of red algae are usually recognised by the presence of cystocarps, any difference in time required for gametogenesis, fertilisation and development of the cystocarp, as compared with that required for the initiation and maturation of sporangia, might significantly affect the recorded abundance of both phases (Kapraun, 1978). Furthermore, in many red algal species, each mature cystocarp releases the entire spore production within a period of only one to at most a few hours, and rapid decay of the fertile branchlets bearing the empty cystocarps are seen soon after (Ngan & Price, 1980). In contrast, the fertile branchlets of the tetrasporophytic plants release spores daily for up to 1 week, as maturation of tetrasporangia progresses from the base to the tip of the fertile branchlet. According to this last explanation, the observed differences are an artifact derived from the durations over which the spores are released rather than from real differences in the numerical abundance of both phases. So far, these alternative hypotheses have not been tested simultaneously with one or a few species. It should be noted that several of them challenge the general validity of statements about the enhanced adaptability of diploidy over haploidy in algae. This idea, together with the widespread dominance of gametophytic over sporophytic phases in some species of the Gigartinaceae, suggests the need for renewed studies on the subject.
RELATIVE ABUNDANCE OF SEXUAL AND ASEXUAL REPRODUCTION
As will be discussed later (p. 198), there is ample evidence suggesting that differentiation and release of several types of propagules by algae are controlled by environmental factors, especially photoperiod and temperature. As both factors change with latitude, it would be expected that the relative abundance of sexual and asexual reproduction also exhibit latitudinal patterns of change. For seaweeds this idea was first stated by Dixon (1965) while working with European populations of the red alga Pterocladia capillacea. The species is widely distributed, but vegetative, in England, Wales and Ireland. No traces of
186
BERNABÉ SANTELICES
germlings or vegetative propagation were found in several years of research, although individual clones of the species were observed to survive and remain in the same position for many years. Tetrasporic thalli of this species occur southward from the south of Finisterre (France), and cystocarpic thalli are present still farther south, in northern Spain. Based on this pattern, shown also by other species of red algae, Dixon (1965) hypothesised that the phenomenon may be explained in terms of physiological expression of some reproductive capacity. Both sexual and tetrasporic thalli are likely to be found in the centre of distribution of the species. Towards the limits of their distribution range, external conditions would inhibit the expression of the haploid sexual thalli although the diploid thalli would produce tetraspores. At the limits of their distribution, the reproductive potential of both haploid and diploid thalli would be completely inhibited. The spatial (geographic) relationship described by Dixon (1965) also applies on a seasonal scale for many species. Geographically widespread species (e.g. Pterocladia capillacea) have different portions of their life history under seasonal control. In the poleward limits of their distribution, the occurrence of a given thallus is likely to be seasonal. Towards the Equator seasonality is apparent only in growth and reproduction, and in many places a distinct growth cycle can be recognised. As latitude decreases further, seasonal regulation becomes restricted to reproduction, sexual reproduction being a more persistent seasonal phenomenon. The above hypothesis has received support from laboratory studies (e.g. Hoek, 1982) indicating that the environmental window for sexual reproduction is often narrower than the one for asexual spore production which, in turn, is narrower than the individual boundaries for growth. For example, Lüning (1980a,b, 1981a,b) reported the sporophytic (Trailiella) phase of Bonnemaisonia cannot form tetrasporangia at temperatures of 12°C or lower and under day lengths of 12 hours or more. In nature, the short-day requirements delay reproduction until after the autumn equinox. At latitudes higher than 80°N in Europe, temperature falls below 10°C before the daylength is short enough to initiate reproduction, so that the tetrasporophytes remain sterile and the gametophytes are absent. A somewhat similar case has been described for Gigartina acicularis (Guiry & Cunningham, 1984). Gametogenesis in this species is confined to a relatively narrow temperature (14–18°C) and photoperiodic range (=12 h). As one goes further north in the Atlantic, this reproductive window becomes progressively smaller, eventually reaching a point where reproduction in a population may take place only when higher than average autumn temperature allows induction. Guiry & Cunningham (1984) have suggested that the phenomenon might be general and that other species, currently maintaining populations by perennation and fragmentation may, with a change in ambient temperature, be able to reproduce. Some exceptions to the general pattern proposed by Dixon (1965) have also been noted. For example, female gametophytes of Laminaria saccharina and L. digitata have been produced in laboratory cultures closer to the uppermost temperature boundary for growth. In addition, and perhaps of more widespread occurrence, field modifications to the general climate expected for the area have been found to modify local patterns of reproduction. For example, in The Netherlands, the flooding with turbid estuarine waters and the heavy shading
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
187
by a fucoid canopy reduced the light reaching the mid-littoral Rhodochorton purpureum population to such an extent that it was “night” for the algae during part of the high water period (Breeman, Bos, van Essen & van Mulekom, 1984). In spring this caused an extension of the period with “effective” short days and the plants responded with continued production of tetrasporangia out of season. These field modifications seem to be common but difficult to document. They are most important for a general understanding of reproductive patterns in the algae.
RELATIVE ALLOCATION OF RESOURCES TO REPRODUCTION
During the course of its life, each organism has a finite amount of resources available to it in the form of energy and materials. The way in which the resources are used in the various vital activities (e.g. growth, defence, reproduction) will determine survival and growth of the individual and the probabilities of passing on its genes to the succeeding generation. The relative allocation of resources between the various vital demands observed today in each species is presumed to be an optimum compromise brought about by natural selection during the evolutionary history of the species. Therefore, relative resource allocation will vary between different species in different habitats. For example, species evolved under high risks of grazing will survive only if resources are allocated to defence mechanisms, such as distasteful chemicals and calcareous inclusions. Within this framework, it is generally held (Fenner, 1985) that reproduction imposes a cost on an organism, either in terms of slower growth or an increased chance of mortality. A relationship has therefore been described between the proportion of resources that a species uses in reproduction and the predictability of the environment (Pianka, 1970). Habitats with unstable conditions (e.g. those exposed to frequent and unpredictable abiotic changes) are often dominated by species with the ability to produce numerous offspring. This ability seems to be more important than that of competing with neighbouring organisms. In such environments, mortality of juveniles and adults tends to be high and is normally independent of density. Prolific and frequent propagule production allows the colonisation and survival of such species in those habitats. In contrast, organisms dominating more stable environments, devote relatively less energy and materials to reproduction and more to vegetative growth, competing for resources with neighbouring organisms. Here, mortality of juveniles tends to be high and density-dependent, but mortality of the adult is reduced. These two contrasting types of organisms are said to be respectively r-selected and kselected (Pianka, 1970). They typify extremes. Since there is a continuum of characteristics between these two extremes the classification of organisms into r- or k-selected is not always self-evident. That different species of seaweeds have different degrees of fertility and reproductive capacity has been recognised in early phenological and ecological studies. The application of the r- and k-selection concepts to these organisms, however, has been more recent. Studies on perennation (Dixon, 1965), colonisation (Connell, 1975), succession (Littler & Murray, 1975) and grazing (Vadas, 1977) led to a formal proposal (Vadas, 1979) that distinguished ephemeral from perennial algal forms. Ephemerals have high growth rates, high reproductive
188
BERNABÉ SANTELICES
capacities, relatively simple thalli and moderately high calorific values. Seemingly, energy is shunted primarily into reproduction and dispersal rather than into development. Perennials have slower growth rates and turnover times than ephemerals. Energy in these forms seems to be directed more into thallus structure than into reproduction. The idea that in seaweeds the above ecological attributes could be related to morphology and productivity was advanced and tested by Littler & Littler (1980). First, they listed the hypothetical survival strategies available to opportunistic and late successional forms and the cost and benefits of such strategies. Then they assessed the reliability of several of these predictions by directly measuring physiological, calorific, morphological, palatability and physical qualities of macroalgae from various successional seres. Reproductive capacity was not measured directly but inferred from successional and repopulation studies. Littler & Littler (1980) showed that early colonists in pioneer seral stages had morphologically simpler thalli, higher net productivity, higher calorific contents (and therefore higher nutritive content), suffered less per cent thallus losses to herbivores and had higher percentages of pigmented (structural) components than late successional macroalgae. Furthermore, they found macroalgal forms representative of intermediate successional stages, which showed intermediate values in the above measurements and morphologies intermediate in complexity and toughness. They could therefore relate algal morphology to algal adaptations and functions, distinguishing morphofunctional groups that would represent different ways of allocating resources to different biological functions. As the morpho-functional groups of algae can be recognised on most shores, the form-function hypothesis has received support and several classification systems of seaweed morphology (e.g. Steneck & Watling, 1982) have been proposed. A close study of the hypothesis has shown four types of problem, however, some of which were anticipated by Littler & Littler (1980). The first problem refers to heterogeneity within the group distinguished. Often a form-functional group includes species with very different phylogenetic and evolutionary histories and predictions on their adaptations do not always follow the expected pattern. Thus, much variation in reproductive capacities, life history and longevity patterns can be found among members of a similar morphofunctional group. For example, the longevity, reproductive capacity and dispersal of the annual kelp Postelsia palmaeformis in the west coast of North America is conspicuously different (Dayton, 1973; Paine, 1979) from equivalent responses of species of Macrocystis (North, 197la) or Pelagophycus (Foster & Schiel, 1985). In central Chile, the bull kelp Durvillaea antarctica exhibits a fugitive life history very different from the one exhibited in the same habitat by the kelp Lessonia nigrescens (Santelices, Castilla, Cancino & Schmiede, 1980). In California, Dayton (1975a,b) has also described life style differences between Hedophyllum and Lessoniopsis, which are considered to be similar (Dayton, 1984) to the relations described for Lessonia-Durvillaea in central Chile. Similar intra-group variations have been described among non-calcareous, encrusting forms (Slocum, 1980; Dethier, 1981; Littler & Littler, 1983), and are likely to be widespread within each major morphological group. These variations led Littler & Littler (1983) to recognise that the functional group ranking should be regarded as recognisable units along a continuum, each containing considerable variation of forms and concommitant functional responses.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
189
Attempts to apply the r- and k-selection concepts to the seaweeds have revealed additional complications. One of them is exemplified by species with morphologically and functionally dissimilar reproductive generations. As discussed previously, numerous species with heteromorphic alternate states are particularly suited to widely different seasons or habitats. Often one phase will be active in seasons or habitats that the other phase cannot survive. Pertinent examples, already noted by Vadas (1979) and Littler & Littler (1980) are those of Scytosiphon lomentaria or Petalonia fascia. In both species the gametophytic phase is a sheetlike or a tubular, short-lived frond exhibiting fast growth and early reproduction. Both species have a non-calcareous, encrusting, Ralfsia-like sporophyte, which exhibits slow growth and less reproductive output but which tolerates grazing and sand scouring. An analogous example in the Rhodophyta is represented by MastocarpusPetrocelis. The erect, fast growing, frequently reproducing fronds of Mastocarpus papillatus alternate (West, 1972) with an encrusting phase known under the name of Petrocelis middendorffii. In the field, P. middendorffii exhibits slow growth rates, low recruitment, low mortality rates and great longevity (Paine, Slocum & Duggins, 1979). Care should therefore be taken not to characterise the species’ life history based on one, often the most visible, phase of the life history. Perhaps the most common example is the characterisation of many species of Porphyra as ephemeral, based only on the foliose phase. For most species in this genus there is almost complete lack of information regarding the field longevity, persistence and resilience of the filamentous, often endozoic, Conchocelis phase. Additional complications have arisen from the direct count of propagules in the water column. Opportunistic forms are expected to produce large numbers of spores over extended periods, whereas late successionists are characterised by marked seasonal variability and release of small numbers of propagules. Incubation of samples from surface water and from water running off a rocky platform, however, yielded somewhat different results (Hoffmann & Ugarte, 1985). Sporelings of species classified as late successionists exhibited, as expected, marked spatial and temporal variations in numbers. Counting of sporelings of species characterised as opportunistic, on the other hand, showed two types of responses. One group of algae, including Scytosiphon-Petalonia, ectocarpoids and ulvoids developed large numbers (10 3 –10 4 ) of sporelings per sample (500 ml) of sea water. A second group of species, of the genera Bryopsis, Rhizoclonium, Porphyra, Centroceras and Ceramium, however, exhibited a remarkably lower number of propagules, two or three orders of magnitude less than the previous group. The algae traditionally considered opportunistic because of their morphological simplicity seem, therefore, to be a heterogeneous group concerning propagule production. Species lacking morphological differentiation might exhibit considerable plasticity of individual cells, complicating still further the application of the rand k-selection concepts to their life styles. For example, the almost “cosmopolitan” Ulva lactuca adapts efficiently to low light by increasing chlorophyll concentration and light absorption and continues to grow under irradiances corresponding to minimum light requirements of deep-living marine macroalgae and phytoplankton living under ice (Vermaat & Sand-Jensen, 1987). The species is able to live for 2 months in the dark and to resume growth immediately when transferred to light. Exposure to anoxia and sulphide
190
BERNABÉ SANTELICES
gradually reduces vitality, but does not affect survival over 2 months. Rapid deep freezing is detrimental to the survival of U. lactuca, while field samples show that more gradual, natural freezing is not. Thus, the authors concluded, U. lactuca combines rapid growth rates during favourable periods (r-life style) with high survival capacities in the same type of tissue during periods of stress (klife style). In summary, the accumulated evidence enables the life history cycles of numerous seaweed species to be understood but leaves unexplained several problems related to general patterns of seaweed reproduction. With few exceptions the energetic components of spore production and the relative importance of different types of reproduction to population maintenance in the field are little known. Various aspects related to the adaptive significance of isomorphic and heteromorphic cycles are unclear. Several hypotheses and observations, especially with red algae, challenge the general validity of statements on the enhanced adaptability of diploid over haploid thalli. Lifehistory characteristics, cellular plasticity and morphological convergences complicate the application to seaweeds of the r- and k-selection concepts. Overall, the evidence suggests the need for consideration of the biology of these organisms before applying these generalisations to them. With due allowances for their different biology, seaweeds should be a fertile ground for testing some of these general hypotheses, extending and modifying them as dictated by the evidence.
PATTERNS OF PROPAGULE PRODUCTION There are a large number of morphologically different kinds of reproductive bodies and a diversity of reproductive methods in seaweeds. A descriptive analysis of such diversity is beyond the scope of this review. Rather, this part focusses on patterns of spore production, both at the individual and the community level. Most of the experimental studies related to patterns of spore production in seaweeds can be arranged around two main subjects, resource-allocation theory and environmental control of spore production. Resource-allocation theory suggests that reproduction imposes a cost on an organism (Cody, 1966; Harper, 1977; Fenner, 1985). The idea has been implicit in much of the phycological literature related to the carposporophytic phase of the red algae, which develops on, and is nursed by, the female gametophytic thallus. The specialised literature is rife with concepts stressing energetic dependence of reproduction on growth. The supposed nutritive value of the auxiliary cells and nutritive filaments during sexual reproduction and carpospore formation has been central even to the classification systems in use and to the present understanding of phylogenetic relationships in the Rhodophyta. However, few if any quantitative data on energy dependence have been produced for this or any other group of seaweed. In fact, in a recent review, De Wreede & Klinger (1988) concluded that in seaweeds there was no indication of resource trade-off between growth and reproduction nor was there any demonstration that algal growth and reproduction could be limited by the same resources.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
191
Evidence for reproduction-associated costs has also been sought through more indirect relationships, including the time relationship between growth and reproduction; the relative amounts of algal tissue devoted to reproduction (considered to be reproductive effort), the existence of a minimum prereproductive age or size in different species and the relationships between size and number of spores produced. All of these subjects are reviewed in this section.
REPRODUCTIVE BODIES, FERTILE STRUCTURES AND REPRODUCTIVE EFFORTS
In order to measure the amount of energy devoted by the plant to reproduction, fertile structures need to be clearly distinguished in the field. This presents a major problem when trying to apply the concept to seaweeds. In a majority of the Chlorophyta, the gametangia and the sporangia are unicellular and indistinguishable from vegetative cells until the flagellated propagules are released. In the Phaeophyta, gametangia are more or less differentiated from vegetative cells and may be unicellular or pluricellular, but they are microscopic and, with the exception of the Fucales, generally they are not grouped in macroscopically visible structures. The sporangia, however are often grouped in more or less extensive fertile areas called sori. A sorus may be borne on a special fertile blade called a sporophyll and in many species these are readily visible structures that can be measured in the field. In the red algae, the male gamete and the spores (frequently in groups of four) may be borne superficially and scattered over the entire upper part of the thallus, or they may be grouped in various kinds of sori. When they occur in distinct sori, some accurate measurements on time of appearance, relative position in the plant and approximate measurements of the energy (in terms of biomass) devoted to reproduction by these algae can be made in the field. After fertilisation, the carposporophyte of the red algae may appear surrounded by gametophytic tissue forming a macroscopically visible reproductive structure, the cystocarp. Cystocarps may appear as small, dark spots (1 to 5 mm diameter) embedded in, or projecting from, the thallus as small domoid warts or papillae on the surface or margins of blades and branches. In many species, cystocarpic structures can be readily recognised in the field. The literature therefore generally contains data on the time-space distribution of this phase. Since it is parasitic, its formation seemingly imposes a cost to the gametophytic thalli, but such a cost has not been measured in terms of energy. Results of experimental harvesting in the field, however, strongly suggest such a relationship, at least for some Gigartinaceae. For example, on the eastern coast of the United States, maximum carpospore production of Mastocarpus stellatus occurs during October-November (Burns & Mathieson, 1972). Careful harvesting in December had little or no effect on the number of cystocarps produced the following season, while severe harvesting drastically reduced the reproductive potential the following season. Careful and moderate harvesting in August allowed control levels of reproduction after 1 year. However, the reproductive potential of these plants was sacrificed for the immediate season, even though they have already recovered 30–40% of the control biomass. Severe harvesting in August prevented the development of cystocarps for two seasons. Likewise, harvesting of Iridaea laminarioides in
192
BERNABÉ SANTELICES
central Chile reduced the production of cystocarps in the experimental populations (Santelices & Norambuena, 1987). The only equivalent experiments done with brown algae seem to be those of Reed (1987) with Macrocystis pyrifera. The results indicate that the vegetative biomass greatly influences zoospore production, because the removal of 75% of vegetative fronds led to a drastic decrease in sporophyll production. Sporophyll biomass was closely related to zoospore production. Measurements of the proportion of algal biomass allocated to reproductive tissues has yielded variable results. Estimated values are about 4% in Macrocystis pyrifera, 2 to 30% in two species of Laminaria (DeWreede & Klinger, 1988), 10–20% in Ecklonia radiata (Novaczek, 1984a) and 40–60% in Ascophyllum nodosum. In Lithophyllum incrustans, the only red alga where the measurements have been made, reproductive effort was calculated to be between 10–55% (Ford, Hardy & Edyvean, 1983; Edyvean & Ford, 1984a). In this last case the value was measured by the percentage of the year’s growth given over to reproductive structures (conceptacles). In Ulva lactuca, the only member of the Chlorophyta studied, the per cent reproductive biomass varied from 20% in late spring to 60% in late summer (Niesembaum, 1988). In this species the process of sporulation was estimated to limit the biomass of the alga and potentially supplement the standing crop of phytoplankton in the water column. Apart from interspecific variation, several other factors seem to modify reproductive effort. Some are related to ontogenic differences and reproductive phases. For example, in Lithophyllum incrustans, the reproductive effort increases with age, reaching a plateau value of 14–23% in 9 to 14-year old tetrasporic plants and 50–55% in 25 to 35-year old cystocarpic plants. Reproductive effort also changes with environmental conditions. The 7 m-deep plants of Ecklonia radiata studied by Novaczek (1984a) exhibited efforts of 20%, about double the value shown by a 15 m-deep population in the same locality. In the case of Ascophyllum nodosum, Cousens (1986) found no clear trend in reproductive effort with shore level. However, effort declined from 60% to about 38% from the most wave exposed to the most sheltered locality. The causes of these variations are not well understood. Factors could be affecting reproduction via changes in growth and energy requirements or directly through differentiation of reproductive tissues. In the case of Lithophyllum incrustans, both types of effects seem to be important as reproductive efforts vary according to the surface to volume ratios of the pools inhabited by the species (Edyvean & Ford, 1984a,b) as well as from north to south (North Scotland to South Devon) in Great Britain. The multiplicity of functions displayed by algal tissue that lacks morphophysiological differentiation seems to be an additional factor complicating the interpretation of results on reproductive efforts in many seaweeds. For example, Schiel (1985a) noted that growth increments followed by development of reproductive fronds and then by abrupt shedding of most of the thallus have been described in Cystoseira osmundacea and Sargassum muticum on the west coast of the United States (Norton, 1977a, 1981; DeWreede, 1978), S. muticum in the British Isles (Fletcher & Fletcher, 1975) and for S. sinclairii in New Zealand. For all of these species the fronds that are produced and shed annually are the main bulk of the plants, which develop reproductive structures along the entire length of this new growth. About 90% of plant biomass is invested in these deciduous fronds for large S. sinclairii plants, and over 80% for larger Cystoseira plants.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
193
The cost of reproduction in the above species, Schiel (1985a) suggested, should not be assessed in terms of sizes and numbers of eggs and sperms only, as was done by Vernet & Harper (1980), but should also take into account the annual growth of the vegetative structures that support these fertile materials. DeWreede & Klinger (1988) have argued that in organisms such as seaweeds in which blades constitute the primary photosynthetic organs and only occasionally (seasonally) bear reproductive structures, the cost of the blades should not be included in the cost of reproduction. The basis of the discrepancy, however, seems to lie in the application to seaweeds of the concept of reproductive effort, which has been primarily developed for the morphologically differentiated structures of land plants. Perhaps some of the measuring methods developed for land plants (Bazzaz & Reekie, 1985; Reekie & Bazzaz, 1987a,b,c) and which are based on carbon budgets could be applied successfully to seaweeds.
ONTOGENIC PATTERNS OF SPORE PRODUCTION
The question of whether or not an organism must attain a certain age before reproducing is important for an understanding of the population and community ecology of seaweeds and for projecting their conservative use as natural resources. If reproduction is energetically dependent on growth, a minimum age is expected. Furthermore, if reproduction incurs a cost in terms of survival, the organism is, perhaps, more likely to die after producing and releasing its reproductive propagules. The application of these ideas to seaweeds has revealed, once again, variable results. Pre-reproductive age can range from one or a few days as in microscopic gametophytes of Laminariales to 9 to 12 months in sporophytes of Macrocystis pyrifera, to 2 years in several species of Fucus (Mathieson, Shipman, O’Shea & Hasevlat, 1976; Niemeck & Mathieson, 1976), to 4 to 5 years in Ascophyllum nodosum (Sideman & Mathieson, 1983). It is not always clear that energetic requirements are the necessary cause for species with extended pre-reproductive ages, although in the case of Pterygophora californica, DeWreede (1984) found a significant positive correlation between age, sporophyll biomass and number of spores produced. Perhaps part of the above variability originates in the fact that age is a poor predictor of important demographic parameters in organisms with growth rates that can be suppressed by environmental variables (Harper, 1977). Under adverse conditions small individuals may reach old age without becoming reproductive. By following a cohort of Laminaria longicruris from recruitment in the macrobenthos through to extinction, Chapman (1986b) could separate the effects of chronological age and plant size on fecundity. Likewise he could also measure the cost of reproduction in terms of survival. His results indicated a clear trend of increasing reproductive output with size, regardless of age. Only larger plants reproduced, while smaller individuals, regardless of age, failed to become fertile. Among plants of more than 200cm length, there was a trend of increasing sorus area with increasing length, but the considerable variability in the data reduced the possibility of predicting sorus area from plant size with any confidence.
194
BERNABÉ SANTELICES
Data on other brown algae have both supported and contradicted Chapman’s (1986b) findings. For example, in some species of Landsburgia and Carpophyllum only the larger thalli reproduce in any given year (Schiel, 1985a). Similarly, larger individuals in populations of Laminaria ephemera, Ecklonia radiata, Sargassum johnstonii, S. herporhizum and S. sinicola, have been reported to start propagule production earlier in the season than small individuals (McCourt, 1984; Novaczek, 1984a). In contrast, intertidal populations of Sargassum polyceratium showed no indication that a certain threshold size had to be reached before fertility sets in, nor have the laterals to reach a certain age before they develop receptacles (De Ruyter van Steveninck & Breeman, 1987). The reason for these variations are not known.
SPECIFIC PATTERNS OF SPORE SIZES AND NUMBERS
In land plants, the way the reproductive materials are apportioned to the seeds has been found to be an ecologically important character (Fenner, 1985). Resources can be partitioned either into many small seeds or a few large ones. Within the constraints of a given reproductive allocation there is clearly an antagonism between seed size and numbers. The resulting size is understood to represent a compromise between the requirements of dispersal, which would favour small seeds, and the requirements for seed establishment, which would favour large seeds. Perhaps influenced by the above line of thinking, Van der Meer (1977) and Okuda & Neushul (1981) have suggested that large seaweed spores might be better for survival and germination under stressful environmental conditions. Spores sizes, at least in red algae, range from 15 µm to 120 µm in diameter (Coon, Neushul & Charters, 1972; Ngan & Price, 1979), but their variation in size has been related to buoyancy and dispersal rather than to settlement and recruitment (Coon et al., 1972). The reason for this is the general belief that, contrary to land plant seeds, seaweed spores carry very limited amounts of nutritional materials usable as food for the free-floating propagule or the early developmental stages. It is not surprising, therefore, that spore sizes in seaweeds range over only about one order of magnitude, while in land plants the variation extends for well over 10 orders of magnitude. Perhaps the most extensive study on sizes of seaweed spores has been carried out by Ngan & Price (1979) in 92 populations of carpospores and tetraspores representing tropical benthic algal taxa. Spore sizes are often used as taxonomic characters and their sizes were therefore expected to be genetically fixed. Contrary to this expectation, Ngan & Price (1979) found considerable variation in spore sizes in all populations of carpospores studied, perhaps due to the co-occurrence in the same sporangia of spores at different levels of maturation. In spite of the above variation, Ngan & Price (1979) found no obvious correlation between size and the effects of single or interacting ecological factors; nor did they find any direct relationship between spore size and the vertical distribution of the taxa on the shore. They could predict, but not explain, that taxa with large-sized spores (mean diameter=50–135 µm) were of common occurrence at lower tidal levels while taxa with small-sized spores (mean diameter=16–50 µm) were present at all tidal levels.
Diversity of units and methods used to measure spore production in seaweeds.
TABLE II
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS 195
196
BERNABÉ SANTELICES
Studies on spore sizes in red algae have shown, however, at least two other interesting correlations. Carpospores are generally larger than tetraspores (Ngan & Price, 1979), a trend that is consistent with the idea that cytoplasmic volume is related to ploidy levels. In addition, species of orders considered as advanced in the Florideophyceae produce larger spores than species of groups regarded as less advanced. Thus, although there seems to be considerable variability in spore sizes, some phylogenetic relationship seems to exist. How this pattern relates to adaptations either for settlement or dispersal is still unknown. Spore numbers have been quantified in a diversity of species (Table II). But while some have estimated spore output per plant, others have quantified the number of spores per g of fresh weight, per thallus per unit time, per area of fertile tissue, per cystocarp, per fertile branch or per cm2 or m2 of rocky surface. As Hoffmann (1987) has remarked, the diversity of units is such that meaningful comparisons among taxa are impossible. Therefore, although there seem to be some phylogenetically related trends in spore sizes, at least in the red algae, the inverse relationship between size and number described for land plants cannot be stated for seaweeds.
SEASONAL PATTERNS OF SPORE PRODUCTION
Numerous reports (reviewed by Hoffmann, 1987) have studied phenological events in benthic algae focussing on the time relationship between reproduction and growth. Many have concluded that the onset of reproduction generally follows a period of active vegetative growth. Furthermore, in several red algal species, such as Dumontia incrassata, the female plants initiate reproductive branches only after growth has stopped and in some, such as Gelidium or Pterocladia, the onset of reproduction means momentary detention of the growth activity of the apical cells (Hommersand & Fredericq, 1988). All of these observations tend to support the idea that, even though there might not necessarily be a trade-off between growth and reproduction in seaweeds, at least both functions seem to be temporally segregated. The pattern is, however, by no means general for all seaweeds. In Codium fragile and Mastocarpus stellatus maximum growth and maximum reproduction are achieved simultaneously, as seems to be the case for 57 common species of red algae studied by Ngan & Price (1980) in Australia. Both cystocarpic and tetrasporic phases were recorded during the period of active growth for most of the red algal taxa they studied. In addition, the modular construction of most seaweeds can introduce other complications when studying the time relationships between growth and reproduction. Unless previously tagged individuals or ramets are carefully followed through time, the observed field responses could correspond to the average of the population but not necessarily represent the changes in growth or reproduction of specific ramets or individuals. Thus, growth and reproduction could be simultaneous for the population but not for individual plants. Several of the phenological studies discussed by Hoffmann (1987) seem to relate to this problem. Spore production is followed by spore release. Together, the two phenomena determine the fertility schedule of the given species. Successful recruitment of juveniles does not depend only on spore production and release, but also on the
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
197
availability of resources for the settling of juveniles. Time of maximum resource availability might not necessarily overlap with the optimum time for growth. It would not be surprising, therefore, to find patterns of seasonal variation in spore production or even fertility schedules. They may best be understood as compromises between seasonality of growth in the plant and availability of energy and resources for the recruit. So far no one has looked for such a compromise in seaweeds. The accumulated evidence on seasonal patterns of spore production suggests latitudinal variations in seasonality (see review and references in Hoffmann, 1987). In cold-temperate regions, the fertility of many species tends to be restricted to summer and autumn (Conover, 1964; Zaneveld & Barnes, 1965). In these latitudes only occasionally has fertility been reported during winter or spring, as is the case in some of the species of Fucus in Nova Scotia (McLachlan, Chen & Edelstein, 1971). In temperate regions, the fertility of many species tends to be seasonal, with maximum fertility in spring and autumn (Hoffmann, 1987). A few species, though, are known to remain fertile throughout the year. Extended fertility is of common occurrence in the tropics, although at these latitudes also some species are only seasonally fertile. The consequences of these different fertility schedules on spore release and arrival at the shore are important. In the tropics there will be propagules arriving at coastal regions throughout the year, although the species composition probably varies. Whereas spores of many species may always be present, the presence of others will be seasonal (Hoffmann, 1987). In temperate latitudes, spore production, and increased competition for space and settlement, will be maximum in spring and autumn. As Kain (1975) has remarked, species such as Laminaria hyperborea, which produces most zoospores in early January, have obvious advantages in colonising rocky surfaces. Such refuges in time probably would also confer competitive advantages on species inhabiting cold-temperate regions. The more drastic climatic conditions in those regions would, however, probably decrease the possibilities of successfully advancing reproduction to times much earlier in the season. The above generalisations on reproductive periodicities are frequently based, however, on individual species and somewhat different results become apparent when groups of species are analysed. For example, Kain (1982) found that some subtidal red algae in England, such as Plocamium cartilagineum had highest fertility in summer, whereas others, such as Delesseria sanguinea, had a winter sporing season. On the temperate coast of Pacific South America, Santelices & Yera (1984) found that 20–30% of the red algal flora was fertile at any one season, with a gradual replacement of sporing species throughout the year. On the eastern coast of Sicily, Cormaci, Duro & Furnari (1984) found that, out of a total of 135 species of Ceramiales, 51% were reproductive in winter, 57% in spring, 65% in summer and 54.5% in autumn. All these findings suggest a more uniform partitioning of the time axis by the reproductive activities of benthic algae in temperate latitudes than previously thought. Such partitioning may imply a more or less uniform propagule distribution throughout the year, a condition that has important ecological consequences on competitive interactions during spore settlement and growth and on the predictability of spores as food for grazers. It is as yet unknown if a partitioning of the time axis also occurs at other latitudes. In cold areas, climatic conditions are perhaps too extreme during large parts of the year to allow spore viability or germination and growth. In tropical
198
BERNABÉ SANTELICES
waters, many species are fertile most of the year. In fact, Hay & Norris (1984) found that the seasonal patterns of reproduction of six species of Gracilaria in the Caribbean were inconsistent with the hypothesis that available attachment sites are being partitioned temporally, as all six species were reproductive throughout the year.
THE ENVIRONMENTAL CONTROL OF SPORE PRODUCTION
Three abiotic factors, light, temperature and nutrient concentrations have been found to stimulate spore production of seaweeds in laboratory studies (Table III). Three components of light, namely total radiation, light quality and photoperiodism play important roles in different species. Total radiation refers to the energy or the photons received at a surface over a given period of time (Dring, 1984). Light quality refers to the effects of specific wave lengths, represented in these cases by blue and red light. Photoperiodism means the control of some aspect of a life cycle, in this case spore production, by the timing of light and darkness in a 24-hour cycle and not by its total amount. The most commonly demonstrated factor in the above studies is photoperiodism. Photoperiodic regulation of gamete or spore production is by far best represented among the red algae, but Dring (1984) has suggested that this probably reflects the intense interest in recent years in life history studies on red algae, rather than any real difference between the red algae and other groups of seaweeds. Similarly, there is an increased representation of species sensitive to short day regimes. But this probably reflects the methodological criteria used to ensure that the observed phenomenon is truly a photoperiodic response. As Dring (1984) has recognised,
TABLE III A sample of field and laboratory studies as evidence for the effects of different environmental factors on spore production in seaweeds.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
199
there seems to be no reason to expect that algae would respond to short days more often than to long days. Most of the species exhibiting a genuine photoperiodic response have heteromorphic life cycles. An explanation advanced for this coincidence suggests that one of the two phases can only survive part of the year, so that the initiation of this phase has to be timed very accurately (Lüning, 1981a). In many cases the response involves spore formation from which, upon germination, originate gametophytes. As discussed previously (p. 184), the haploid generation has been supposed to have less environmental resilience, but in recent years, a number of experimental studies have also demonstrated photoperiodic control of reproduction in species with isomorphic phases. The rhodophyte Dumontia contorta (Rietema, 1982; Rietema & Breeman, 1982), Gigartina acicularis and Halymenia latifolia (Guiry, 1984; Guiry & Cunningham, 1984), and the phaeophyte Glossophora kunthii (Hoffmann, 1988) have all shown true photoperiodic control of spore production under laboratory conditions. The onset of sexual or asexual reproduction in microalgae has frequently been attributed to nutrient availability (De Boer, 1981). Although not as well documented, similar responses have been found in seaweeds and they are mainly of two types (Table III). One relates to the needs of specific seaweeds for particular nutrients in order to reproduce (e.g. iodine by Petalonia fascia). The other relates specifically to nitrogen perhaps because it is the nutrient most studied. The evidence suggests that both nitrogen enrichment and nitrogen depletion can induce the production of different types of reproductive cells. There are a number of problems related to physiological responses to controlled abiotic conditions when they are applied to field performance of seaweed reproduction. The first such complication arises because the many factors involved in propagule production may interact in the field. A number of such interactions have been reproduced under laboratory conditions, but the level of field complexity is likely to be higher. The importance of the interaction between temperature and photoperiod on the latitudinal determination of fertility and on fertility windows has been discussed previously. Another ecologically important complexity is represented by the photoperiodtemperature-irradiance-nutrient interaction which has been shown to control reproduction of some red algal species. For example, Lüning (1980b) found that plants of Bonnemaisonia incubated in sea water with normal quantities of Provasoli enrichment induced only 10–30% of the individuals to differentiate tetrasporangia under the most favourable daylength-temperature conditions. When the Provasoli enrichment was decreased to 5% of normal, however, 75% of the plants responded. This type of interaction is consistent with the expected simultaneous change of several abiotic factors in temperate latitudes after summer, when days become shorter, irradiance and temperature decrease and nutrients are very much reduced or depleted. To add to the complexity these factors interact not only at low concentrations but also at higher levels or even compensate one for the other. One such example is represented by Dumontia contorta. In this species, long (10 h) photoperiods inhibit the development of upright thalli (Rietema & Breeman, 1982) when grown in unenriched or depleted media. Frequent renewal of the culture medium or enrichment of sea water, however, permitted development of upright thalli under long photoperiods. In the field, nutrient availability is notoriously
200
BERNABÉ SANTELICES
modified by water movement, a factor not yet incorporated in the study of the above interaction. A second source of complexity and variation relates to the existence of physiological ecotypes, which do not necessarily respond to a given ecological factor in a similar way to other ecotypes in the species. Perhaps the most studied example of this situation is represented by the photoperiodic response of the brown alga Scytosiphon lomentaria. Lüning (1980b) found that the critical daylength for seven isolates of this species, collected at different geographic places between 32°N and 55°N, increased steadily with the latitude of origin of the isolate. In contrast, day length-neutral populations of Scytosiphon lomentaria have been found in Australia (Clayton, 1978), Denmark (Kristiansen & Pedersen 1979) and eastern Canada (Correa, Novaczek & McLachlan, 1986); A similar variation has been found among isolates of Audouinella (=Rhodochorton) purpureum (Dring & West, 1983). Perhaps some of the variability of these results has originated from the use in the laboratory of different levels of the factors involved in the photoperiod-irradiancetemperature-nutrients interaction. In any case, the existence of such variations certainly warns against blind extrapolation of these results to field situations and, as Dring (1984) has recognised, they certainly hinder the efforts to extract meaningful ecological information from laboratory experiments. Age-class may also influence the response to the environmental factors inducing propagule production. For example, Hasegawa (1962) found an earlier readiness for sorus formation in Laminaria digitata after the first year of life. Individuals during their first year were reproductive from October to March, with sporogenesis peaking in January. In 2- and 3-year old plants, sporogenesis started in June or July and extended to January or February, with sporogenesis peaking in October—November. An earlier readiness for sorus formation after the first year of life has also been observed by Kawashima (1983) in Laminaria angustata. Some of the experimental studies carried out on environmental control of reproduction in seaweeds have provided supporting evidence for the antagonistic nature of growth and reproduction, at least in short-day species. Several recent reports (e.g. Kain, 1987; Hoffmann, 1988; Lüning, 1988) have concluded that short days stimulate reproduction while long days inhibit reproduction and stimulate growth. The effects can be brought about by photoperiod either alone or interacting with irradiance, temperature or nutrients. Kelps are among the species most studied. Several species of Laminaria exhibit a marked seasonal development with maximum growth activity of the fronds in the first half (spring-early summer) of the year, subsequent reduction of growth rates in late summer, and formation of sori in autumn and winter. Experimental studies have shown that, at least in Laminaria saccharina, short day regimes allow, and long day regimes prevent sorus formation (Lüning, 1988). A period of slow or even zero growth precedes sorus formation. Lüning (1988) wondered whether or not the growth reduction observed in this species under short day conditions is a by-product of sorus formation in a way such that the correlated inhibition of growth will end as soon as the reproductive step of sorus formation has been passed. Even though experimental evidence is lacking, some previous observations seem to support the above possibility. For example, Sanbonsuga & Hasegawa (1969) showed that the sporophytes of Costaria costata exhibit a period of retarded growth
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
201
before sori appear. Growth rate is not reduced in immature individuals growing under the same experimental conditions. Antagonism between growth, represented by new blade formation, and reproductive structure initiation was also found in what seems to be the only field experiment that was concerned with factors controlling propagule production. The red alga Delesseria sanguinea is strongly seasonal in England. Gametangia and tetrasporangia are produced in early and mid winter, respectively. New blades appear in late winter. Kain (1987) installed an underwater lamp in a Delesseriadommated subtidal stand off the Isle of Man, illuminating about 40 plants for 1 hour in the night or day. In the sea the provision of light at night prevented fertility in the tetrasporophytes but stimulated production of new blades which arose about 6 weeks earlier than the control. Tetrasporangia were formed only after the night illumination ceased. It is as yet unknown if there is a similarly antagonistic relationship between growth and reproduction among long-day species of seaweeds and how the switching from one to another function could be achieved. In summary, experimental studies have been successful in identifying the single and interacting effects of biotic and abiotic factors that stimulate spore production and determine temporal patterns of reproduction in seaweeds. The application of resource-allocation concepts to these organisms has been less successful. Fertile structures are not always clearly distinguishable in the field. Algal tissues often display a multiplicity of functions and lack the specialisation of land plant tissues. Consequently it is often difficult to measure reproductive efforts which, in addition, seem to be highly variable, depending on the type, habitat and physiological state of the seaweed. Pre-reproductive ages or sizes seem to be a requirement for some species only. There seem to be phylogenetically-related trends in spore size, but ecologically-related trends are not evident. The inverse relationship between sizes and numbers described for seeds of land plants does not hold for spores of seaweeds. Perhaps a more realistic application of resourceallocation theory to seaweeds will result if concepts and methods are applied to them with due consideration for their morphological, physiological and lifehistory characteristics.
PATTERNS OF PROPAGULE RELEASE The number of spores produced by a seaweed and the precise timing of spore discharge depend on at least three variables: (1) the physiological state of the parent plant and especially of the reproductive tissues; (2) the degree of maturation of the developing spore; and (3) the modifying effects of the environmental factors triggering the process. Studies on propagule release by seaweeds have, however, rarely been approached from these perspectives. Many experiments have confounded patterns of spore production with patterns of spore release and most have restricted themselves to testing singlefactor effects on spore release under laboratory conditions. Spores have, however, been studied from several perspectives and a body of information has accumulated on the factors modifying the process of spore release and the ecophysiological responses of the released spore. The accumulated knowledge on all these processes is discussed in this section. First, the abiotic and
202
BERNABÉ SANTELICES
biotic control of spore release, then the nature of the releasing mechanisms followed by morphological and ecophysiological characteristics of the released propagules.
ENVIRONMENTAL CONTROL OF SPORE RELEASE
Irradiance, light quality and dosage, emersion, salinity, growth factors and digestive enzymes, all have been experimentally shown to influence spore release in the seaweeds (Table IV). The following analysis distinguishes abiotic from biotic factors for the purposes of clarity, but it is evident that both types of factors may interact under field conditions. Abiotic factors A number of studies suggest that propagules are released under low illumination conditions or that high irradiance seems to reduce the number of spores released. For example, Friedlander & Dawes (1984a) found that the number of carpospores released by Gracilaria foliifera was higher in darkness or under low (8 µE·m-2·s1 ) irradiances. Similarly, the number of tetraspores released by G. sjostedtii, G. corticata and G. textorii decreased when the irradiance used was raised from 1500 to 2000 lux (32 to 42 µE·m -2·s -1, Umamaheswara Rao & Subbarangaiah, 1981). Species of Hypnea, Gelidium, Pterocladia and Gelidiopsis also show increased spore release under low irradiance (Umamaheswara Rao & Kaliaperumal, 1983).
TABLE IV A sample of factors known to influence spore release in seaweeds.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
203
The adaptive value of this low light intensity response, however, has been scarcely explored. As will be discussed later (p. 239) there are several studies indicating that the already settled microscopic stages of benthic algae exhibit low light tolerance, a feature generally interpreted as showing an adaptation for survival under the canopy of adult or fully grown plants. Yet it is unknown if the newly released spores are generally sensitive to high irradiance. Even if this were the case, it remains unclear how dim light or darkness might affect the cell wall of the reproductive tissues, increasing the potential for spore release. A potential relationship between light effects and auxin metabolism in the process of spore production of Vaucheria sessilis has been suggested (Hellebust, 1970) and perhaps this could apply to other species as well. In V. sessilis, zoospore production was inhibited by high (above 3000 lux) irradiance while low light or darkness favoured gametangia formation. On the other hand, indoleacetic acid stimulated, while indolecarboxylic acid inhibited zoosporangia formation. Interestingly, Ogata (in Kim, 1970) reported that some specific concentrations of heteroauxins (0.1–10 ppm), naphtalene acetic acid (10 ppm) and gibberellins (0.1 ppm), could stimulate tetraspore release in species of Gracilaria, a response also described by Liu & Gordon (1986) when applying 3–8 ppm of kinetins. Even though a number of studies with flowering plant growth regulators have been conducted with the algae (see Buggeln, 1981, for a review) most of them have focussed on the effects of these substances on morphogenesis and growth but not on reproduction or their potential interaction with light on spore release. An alternative explanation for the damaging effects of light might be the stimulation of synthesis or release of sporulation-inhibitor substances. Such inhibitors are known to exist, to be produced by vegetative tissues and, therefore, their concentration might change in relation to growth activity. For example, the formation and release of zoospores and gametes of Ulva mutabilis can be blocked by some still unknown substance that can be extracted into fresh growth medium from a suspension of living thallus fragments (Nilsen & Nordby, 1975). The chemical nature of the inhibitory substance is unknown. It could be a low-molecular weight substance able to bind rather firmly to the highly negatively charged ulvin molecules or a volatile compound of unknown nature (Nilsen & Nordby, 1975). Contrary to the above, there is another group of seaweeds whose patterns of spore release are light dependent. For example, the sporulation of Enteromorpha intestinalis is inhibited (Christie & Evans, 1962) and the daily periodicity and spore release of Nitophyllum punctatum becomes aperiodic (Hellebust, 1970) under continuous darkness. In these cases, however, the light requirements relate more to the diurnal alternating periods of light and darkness than to irradiance requirements. That spore release in seaweeds can exhibit a daily rhythmicity has been known since Suto’s (1950a) early studies on spore shedding and attachment. Thereafter a number of studies (e.g. Katada, 1955; Dring, 1974; Umamaheswara Rao, 1974; Lüning, 198la; Umamaheswara Rao & Subbarangaiah, 1981; Ngan & Price, 1983) have repeated the observation for many other species. Furthermore, some species show a precise rhythm of spore release that can be maintained for a time under laboratory conditions. Thus, Indian populations of Gelidiella acerosa studied by Umamaheswara Rao (1974) shed most spores in the laboratory between 1400 and 1800. Indian and
204
BERNABÉ SANTELICES
Australian populations of Gracilaria exhibit maximum spore output between 0500 and 0900 (Umamaheswara Rao & Subbarangaiah, 1981; Ngan & Price, 1983). A major concern of researchers investigating these diel patterns of spore release has been to decide if they are regulated by endogenous factors such as circadian rhythms (see Dring, 1974 and Sweeney, 1983 for discussions) or exogenous factors, which represent diel fluctuations in the environment. Even though this is an interesting physiological problem, from the ecological point of view the question of endogenous versus exogenous control is not critical. Even if the rhythm is controlled by an endogenous clock, the setting of the clock will be provided by the environment. Thus, while the biological clock regulates the potential response, the actual response is determined largely by the environment. Apart from describing the phenomenon, little else is known about this observed pattern and no explanation seems to have been advanced as to the adaptive value of these daily periodicities. It is now known that circadian rhythms affect several aspects of cellular activities in the algae, including photosynthetic gas exchange, the patterns of activity of some enzymes and cell divisions (Lobban, Harrison & Duncan, 1985). Perhaps the daily rhythmicity of spore shedding results from the periodicity of one or several of the above cellular activities. Even if that were the case, the diversity found among different species in the timing of maximum spore release is still puzzling. Early on Suto (1950c) noted that species in the genera Sargassum and Caulerpa release their propagules early in the morning, those in the genera Undaria, Gelidium and Pterocladia shed in the afternoon, while in Porphyra spores are released at any time of the day. Timing maximum spore release at different times of the day might reduce interspecific competition for settling sites among spores. Precisely defined, simultaneous gamete release could improve the probabilities of gamete encounter (Pringle, 1986) while interspecific differences in daily release time could prevent hybridisation. It seems that none of these hypotheses has been tested in field populations of seaweeds. Daily periodicity of propagule release has been related to tidal oscillations by Ngan & Price (1983). Working with 48 tropical benthic taxa from 25 genera they found that the time of maximum spore output under laboratory conditions occurred when populations on the shore would be submerged in sea water and especially around the times of high tides. They view this as an adaptation to reduce desiccation of recently settled spores, as well as to promote spore dispersal. In their study with tropical benthic algae, Ngan & Price (1983) also related tidal oscillations to the time of spore release and spore sizes and suggested that the interaction might be expected to play a significant role in sorting small and large spores in relation to vertical height on the shore. They found that the species with small-sized spores release their propagules either early in the morning or in the evening or, in a few cases, during both periods. Spore output was highest in these cases during the lower of the two high waters which occur daily in their study region (Victoria, Australia). Taxa that have large-sized spores and which generally inhabit the lower intertidal levels, shed their spores only in the afternoon and high spore output occurs during either the lower or the higher of the two high waters. The authors suggested that these differences between taxa in the periodicity of spore discharge may play some part in reducing competition for the space available for spore settlement.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
205
In addition to, or instead of, daily periodicity, seaweeds may exhibit lunar or semilunar rhythms of propagule release. In these cases the rhythmic fluctuations in spore shedding run closely parallel to the lunar cycle. This type of response apparently was first described by Williams (1898, 1905) while working with Dictyota dichotoma in North Wales. Later it was found in populations of the same species for Jamaica (Hoyt, 1907), Naples (Lewis, 1910) and North Carolina (Hoyt, 1927). In his studies, Hoyt (1927) noted that the rhythmicity of Dictyota correlated closely with moonlight, and therefore suggested that the changing phase of the moon was the changing external condition most likely to regulate reproduction (both propagule production and release). Thirty-four years later, Bünning & Müller (1961) were able to test the hypothesis experimentally and concluded that, under laboratory conditions, artificial moonlight as low as 3 lux replacing the 10-hour dark period for 1 night could phase the rhythm and produce a maximum egg release 9 days later. Subsequently, Vielhaben (1963) showed that irradiance as low as 0.3 lux could induce a response. In the sea, lunar and semilunar rhythmicity also determines tidal rise and fall and several reports (Table IV) have correlated rhythms of spore or gamete release with tidal rhythms. Most of these studies have not experimented with artificial moonlight but some have provided experimental evidence suggesting that effectively, the tides are the external regulatory factor. For example, Ohno (1972) reported that in the wild crops of Monostroma the fruiting fronds released propagules periodically for several days on every neap tide. A similar periodicity in gamete liberation was observed in populations cultivated in nets which were air-exposed daily for 4 hours at low tide. Such periodicity was, however, not found where the fronds were cultivated constantly submerged in sea water. It seems that the observed effects of two other ecological factors, desiccation and salinity, could be related to the tidal-induced rhythmicity of spore shedding. In several species (Table IV) spore release can be stimulated by immersing the algae in sea water following a period of desiccation. This reponse is especially common among fertile cystocarps. Likewise, spore shedding, at least in species of Gracilaria and Lithophyllum, is stimulated by salinity changes. Both salinity changes and desiccation followed by re-immersion in sea water are common during a tidal cycle. Biotic factors Spore release can also be stimulated by biotic interactions. Grazing and grazers help to release propagules in at least two forms. One consists of tearing open cystocarps during the feeding process. This is done by Hyale media while consuming Iridaea laminarioides. Experimental studies by Buschmann & Santelices (1987) indicate that in this way the invertebrate releases large numbers of spores which exhibit, under laboratory conditions, similar rates of growth as control (no-grazer) spores. Field populations of I. laminarioides may have unopened cystocarps even in senescent, decaying fronds. At sites with higher amphipod densities, however, the total number of open cystocarps in mature and senescent fronds increases, suggesting a facilitation mechanism.
206
BERNABÉ SANTELICES
Specific consumption of reproductive tissues by benthic marine invertebrates has been described in a few species. Thus, Moore (1977) found that the amphipod Hyale nilsonni preferred fertile tips of Pelvetia canaliculata; the isopod Idotea wosnesenskii consumes preferentially the fertile tissues of Iridaea cordata (Gaines, 1985); several phytal organisms consume reproductive tissues of Pelvetia fastigiata (Gunnill, 1985); and Littorina littorea exhibits a preference for Fucus receptacles (Watson & Norton, 1985). Perhaps in these cases propagule release is also mediated by grazers. In fact, Moore (1986) suggested that the amphipod Hyale nilsonii could be transporting seaweed embryos after feeding in the fertile tips of Pelvetia. Incomplete digestion of seaweed tissues by their respective grazers stimulate both propagule differentiation and release in some species. In recent years, the cultivation of faecal pellets recovered from sea urchins, grazing molluscs, herbivorous fishes and filter-feeders (Santelices, Correa & Avila, 1983; Jernakoff, 1985a; Santelices & Correa, 1985; Buschmann & Santelices, 1987; Breeman & Hoeksema, 1987; Paya & Santelices, 1989) has resulted in the subsequent growth of a diversity of Chlorophyta, Phaeophyta and Rhodophyta. The process is more complex than just simple regeneration of algal fragments escaping digestion. In partially digested fragments of Chlorophyta and Bangiophycidae (Rhodophyta) the cytoplasm of the surviving cells condenses towards one side of the cell, then the wall disintegrates, the tissue loses integrity and protoplasts are set free in the culture medium. In green algal cells, the protoplasts develop flagella, behave like swarmers and settle down on the bottom of the culture vessels, originating new thalli. In red algal cells the protoplasts can develop a callus tissue or new individuals. Under laboratory conditions the new individuals grew at least as fast as control thalli arising from non-ingested propagules. The release of swarmers is a common response of some seaweeds to stressful situations (Vidaver, 1972) and protoplast release has also been reported after application of abalone gut enzymes to species of Porphyra (Polne-Fuller & Gibor, 1984). The fact that this release occurs naturally after digestion by invertebrates, however, adds an evolutionary perspective to these responses. Grazing has been a powerful and continuous selection factor in algal evolution. Since swarmer and protoplast production in these algae is often stimulated by the passage through the digestive tract of grazers, Santelices & Ugarte (1987) suggested that the process might be analogous to some dispersal mechanisms observed in land-plants, where seed germination is sometimes stimulated by passing through digestive tracts. However, the process is unique in the sense that incomplete digestion stimulates de novo formation and release of algal propagules. Experimental evidence indicates, in addition, that some grazers, such as species of Siphonaria, almost always stimulate protoplast release. Such grazers seemingly have important ecological roles not only in dispersing and redistributing propagules, but also increasing the number of macroalgal propagules being dispersed. Quantification of the ecological importance of this process indicates that the quantities of propagules so produced in some species compare well with the recorded abundance of propagules settling in experimental plots in the field (Santelices & Paya, 1990). This response is likely to be comparatively more important at times or seasons when the reproductive output of the seaweed is reduced and the grazing pressure is high.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
207
A second general group of biotic interactions leading to propagule release is the coordination of plasmogamy by hormone-like substances generically recognised as pheromones. Members of the Phaeophyta are the only cases in algae where the chemical identity of molecules involved in the process is known (Müller, 1981, 1986) and all of them are involved in the coordination of gametogenesis, synchronising the discharge of gametes. In brief, the released egg secretes into the surrounding medium a pheromone that induces release of spermatozoids in nearby male plants. Subsequently, the same substance attracts the sperm to the eggs. All major families or orders in the Phaeophyta produce their own attractants (Müller, 1981, 1986) which are generally simple, volatile hydrocarbons insoluble in water. All attractants identified in brown algae so far coordinate plasmogamy, which eventually results in a zygote and the development of a sporophyte. Therefore, in a strict sense, gamete rather than spore release has proved to be mediated by pheromones. The explanation is that in dioecious species with unisexual gametophytes, combination of gamete release and attraction of one gamete to the other increases the probabilities of reproduction (Müller, 1981; Lobban, Harrison & Duncan, 1985). Chemically mediated spore release could perhaps be expected, however, in species in which settlement and growth is enhanced when groups rather than single spores arrive together at a given area. As will be discussed in the section on positive interactions during recruitment (p. 249), there is some evidence suggesting that this might be the case in some species of Gigartinaceae. Based on numerous laboratory experiments, Müller (1981, 1986) has proposed some ecological considerations regarding the phenomenon of chemically-related gamete release in the Phaeophyta that perhaps have a general value for this type of phenomena among the seaweeds. All attractants so far identified are highly volatile and hydrophobic. These characteristics certainly help to avoid the build up of chronic concentrations which would decrease the efficiency of gradients around the releasing cells. Furthermore, the chemical effect is very clearly a shortdistance phenomenon because the chemical attraction is not effective more than 0.5 mm away from the source cells and the range may in some cases be much less. The accumulated evidence on brown algal pheromones indicates that within a given order or family there is little species-specific difference with respect to the chemical composition of the pheromone or in the response of the male gametophyte. Furthermore, there are substances, sometimes released together with the true attractant, of as yet unknown function. Müller (1981, 1986) has suggested that some of these substances would trigger the release and chemotaxis of a competitor’s spermatozoid that would eventually be “misguided” by the substance and fail to fertilise its own oogonium. Müller (1981, 1986) further suggested that “chemical warfare”, waged by interfering with a competitor’s sexual information system, cannot be ruled out entirely. The idea of a chemical warfare that either inhibits or stimulates the propagule release of a potential competitor out of season could also apply to spores, but the evidence has not yet been produced.
THE NATURE OF THE RELEASE MECHANISM
Traditionally (e.g. see Mshigeni, 1974 for review), the turgor pressures resulting from the wetting of desiccated thalli by the incoming waves have been thought to
208
BERNABÉ SANTELICES
stimulate spore discharge. The observation that changes in gradients of osmotic concentrations between the experimental culture medium and the algal cell can also stimulate spore release (Allsopp, 1966) lends support to this interpretation. More recent studies have shown, however, that algal reproductive structures may exhibit different release mechanisms and not all of them can be attributed to osmotic changes. The simplest example is the discharge of zooids in Dictyosphaeria. The propagules are released through liberation tubes in the cell wall (Hori & Enomoto, 1978a,b). These are openings that have a projecting peristome. The ultrastructural changes leading to the differentiation of this structure are unknown. In the case of the fucoids, such as Pelvetia, Fucus and Ascophyllum, the extrusion of gametangia follows a period of several hours of exposure to air (Boney, 1966). It results from shrinkage of the receptacles after uptake of water during the previous immersion period. Gametangia release thus results from a reduction, rather than an increase, in turgor pressure. Studies carried out with Chorda tomentosa have exemplified spore release by brown algae plurilocular sporangia (Toth, 1976). The mature sporangia contain 128 immature zoospores with the mass of spores being surrounded by a mucilaginous carbohydrate. Upon release, the entire contents of the sporangium are extruded from the apex. Initial release is observed as a slight momentary eruption as the spore mass bursts out. The mucilage that holds the embedded zoospores begins to swell and draws out the remaining mass in the sporangium. Upon release the mucilage continues to swell, separating the embedded zoospores. A most important role in the releasing mechanism is assigned by Toth (1976) to the mucilage around the spores and to presumed enzymatic digestion of the apical cap. The mucilage located around the spores, and identified as alginic acid, could exert a constant pressure on the sporangial wall and apical cap. Since the plants of Chorda tomentosa are normally submerged, it is supposed that the cap would remain hydrated and firm at all times. At the time of spore release, it is presumed that the spores secrete one or several enzymes which selectively digest away and weaken the apical cap. Enzymatic digestion has also been implied in the release of red algal monospores. The first account of the process was provided by McBride & Cole (1971, 1972) working with monospores of Smithora naiadum. They observed that during monospore formation, large dictyosomes with their maturing faces toward the centre of the cells produce irregular vesicles containing a compacted, fibrillar substance. Later these vesicles coalesce resulting in large membranebound deposits within the cell. Immediately preceding and during liberation of the spore, these vacuole-like structures migrated towards the periphery of the cell and subsequently expelled their fibrillar contents. The mechanism of release involved a fusion of the vacuole membrane with the plasmalemma. Prior to spore release the thickness of the cell wall is considerably thinner than in vegetative cells because cell wall production does not keep pace with the enlargement of the spore. The extrusion of the spore was observed to be achieved by a breakage in the cell wall on one or other side of the thallus. As illustrated by McBride & Cole (1971, Fig 16) this opening can be as small as 1/5 of the spore diameter and the spore seemingly is squeezed through the narrow passage in the cell wall. The fibrillar materials expelled prior to and during release are thought to function as a mucilaginous secretion that could aid
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
209
in spore release by acting as a lubricant (McBride & Cole, 1971). This could be critical to the success of the process, as liberation takes place through a very small opening in the cell wall. In addition, the mucilage would protect the fragile spore after release. The cell wall of the parent thallus undergoes extensive changes to allow the monospore to be released. The thickness of the cell wall is definitely reduced, but there must also be some loss of structural stability. McBride & Cole (1971) suggested that the cell walls in the vicinity of the monospore may undergo an actual decomposition or degradation, perhaps through enzymatic digestion or physical internal pressure. More recently, Hawkes (1980) reported that monospores are released in Porphyra gardneri following dissolution of the cell wall layers beneath the outer cuticle. The mechanisms involved in cystocarp opening and carpospore liberation seem to involve enzymatic digestion as well as changes in turgor pressure (Boney, 1978). The cystocarps of Rhodymenia pertusa have a pericarp composed of several layers of cells, a terminal ostiole and a canal leading from the internal cystocarpic cavity to the ostiole. Inside the cystocarpic cavity there are masses of carpospores which surround a central “core” of mucilaginous substances. Upon hydration this mucilage, as well as the mucilage sheath associated with each individual carpospore, swells and results in a sudden increase in volume of the spore mass. Since the turgid cells of the pericarp offer an effective resistance to the pressure of the spore mass, hydrostatic pressure on the pericarp wall directs the expanding spore mass towards the terminal canal leading to the ostiole. Interestingly, the apical region of the pericarp as well as the lining of both the ostiole and the short canal leading to it consist of small, and relatively thick-walled cells. Swelling of the mucilage propels the spore mass to the basal part of the canal leading to the ostiole and the lack of flexibility in this region together with the steady narrowing of the channel as it approaches the ostiole, leads to the jet-like ejection of the mucilaginous spore mass into the overlying water. Boney (1978) has stressed the crucial role played in the process by the toughened apical region of the pericarp. In his studies with Rhodymenia pertusa, Boney (1978) noted that there was no induction of mass release of spores unless the dark-light cycles applied to the algae were followed by slight prodding of the flexible pericarp wall with a blunt glass needle. It is unknown if in nature this mechanical aid is provided by the effects of changes in water pressure due to movement of the fronds. Equally unknown are the effects that these pressure changes might have on the spore mass and the mucilage so as to facilitate release. No detailed study seems to have focused on the releasing mechanisms from unicellular sporangia in Phaeophyta or tetrasporangia release in Rhodophyta. In this last case it is thought (Boney, 1966) that when sporangia remain immersed below the surface of the thallus, spores escape by squeezing between the covering cells. Rupture of the sporagium wall might be due both to enlargement of the spores and to swelling of mucilage.
SOME MORPHOLOGICAL CHARACTERISTICS OF THE RELEASED PROPAGULES
Almost 30 studies (Table V) have examined the ultrastructure of spore formation or have described recently released spores of various species of Chlorophyta,
210
BERNABÉ SANTELICES
Phaeophyta and Rhodophyta. In spite of the ultrastructural differences characteristic of the members of these different Divisions, some morphological features seem common to all types of released spores. Many of these common features might be especially important for understanding the ecological features of recently released propagules.
TABLE V Electron microscopy studies of seaweed propagules
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
211
All spores exhibit large number of Golgi-derived, electron dense, small-sized vesicles. These vesicles are distinguished from those described in the previous section by their smaller size and the electron-dense (cored) nature of their contents. In Ulva and Enteromorpha these vesicles are formed in the gametes shortly before the gametes are released from the gametangium (Christie, Evans & Shaw, 1970; Evans & Christie, 1970; Bråten, 1971; Callow & Evans, 1974). The newly settled zygote also has these vesicles, but they are secreted during the settling of the zygote. In spite of a systematic search, these vesicles have not been found in the cells of these species at any other stage of their life cycle. Experiments using specific enzymes indicate that the secreted substance is a glycoprotein made up of 1–4 a-linked glucose units combined with proteinaceous materials (Christie & Shaw, 1968; Christie, Evans & Shaw, 1970; Evans & Christie, 1970). The presence of numerous vesicles has been reported also in the zoospores of species of Ectocarpus and Chorda in the Phaeophyta (Baker & Evans, 1973a,b; Toth, 1974, 1976). Upon zoospore germination in these species also, the vesicles have been observed to deposit their contents to the outside of the germlings and their fibrous contents have been assumed to act as an adhesive substance. The released spores of the red alga Smithora naiadum also exhibit copious amounts of vesicular products (McBride & Cole, 1971). In fact, the organelles in the cells are crowded into the small spaces left between these vesicles. Abundant vesicles are also present in the released carpospores of Porphyra variegata. Two types of vesicles were distinguished in this last species, however, both with moderately electron-dense fibrils in an electron-transparent matrix (Pueschel & Cole, 1985). The smaller of these (about 0.3 µm in diameter) were abundant in mature, unattached spores but were absent in attached spores and sporelings. The whole surface of the recently attached spore appeared coated with a layer of moderately electron-dense material presumed to be adhesive mucilage. Thus, in the red algae also these vesicles are thought to be adhesive in function. It is interesting to note that prematurely released carpospores of Porphyra variegata also exhibit vesicles (Pueschel & Cole, 1985), but they are not otherwise differentiated with regard to shape, size and content. The abundance of reserve materials in the recently released spore may be ecologically important, but this importance has only infrequently been discussed. Floridean starch seems to be abundant in the spores of red algae and McBride & Cole (1971, 1972) and Pueschel & Cole (1985) have remarked on the decrease of starch after monospore settlement in Smithora, as well as in Porphyra variegata. There are a number of reports suggesting that the plastids are somewhat modified or not completely developed in the newly released spore. For example, in the phaeophyte Chorda tomentosa, the immature zoospore prior to release contains a disc shaped chloroplast, possessing an eyespot region (Toth, 1976). Released zoospores still embedded in mucilage contain chloroplasts which appear to be dividing into two equal sections. Upon settlement, the chloroplast is composed of two separate membrane systems and there is evidence of production of thylakoid membranes. Afterwards the plastid enlarges, filling an entire half of the germling. Later, the plastid not only keeps enlarging but also changes from a discoid to a flattened dumb-bell shape.
212
BERNABÉ SANTELICES
In the Rhodophyta, also, there are indications of significant changes in the structure of the spore plastid upon release. For example, the carpospore plastids of Lithothrix have fewer thylakoids, with fewer and less dense phycobilisomes, than the plastids of the vegetative cells (Borowitzka, 1978). The monospore of Smithora exhibits somewhat modified chloroplasts, with lamellae so closely appressed that they give the appearance of grana-like structure (McBride & Cole, 1971). As many as 20 lamellae could be involved in these formations. The structure of these plastids, however, rather than being associated with an altered plastid metabolism was thought to result from the accumulation of too many organelles inside the cell (McBride & Cole, 1971). In the case of the carpospores of Porphyra variegata, the recently released cell had a single pyrenoid with arms radiating from the region of the central pyrenoid (Pueschel & Cole, 1985). Thylakoids penetrated the pyrenoid either transversing it directly or forming a reticulum within the pyrenoid. Upon settlement new pyrenoids were formed in the same chloroplast and initially they were rarely penetrated by lamellae. Some authors (McBride & Cole, 1971) have noted the significant crowding of subcellular organelles in small spore volumes. At least in Smithora, mitochondria are often closely packed and confined to a small area. The nucleus is usually surrounded by a layer of cytoplasm containing only small amounts of endoplasmic reticulum. As already mentioned, chloroplast lamellae are closely appressed. McBride & Cole (1971) have suggested that this crowding of organelles and the noticeable lack of free cytoplasm presumably restricts circulation to metabolic precursors and to organelles themselves, resulting in decreased synthetic activity prior to attachment of the monospore and release of the vesicular materials. A mucilage layer is a common feature of propagules of red, brown and green algae. In red algal spores, the mucilage sheath occupies 50 to 80% of the combined spore plus mucilage volume, depending on the species (Boney, 1975, 1981; Ngan & Price, 1979). Immature spores are surrounded by relatively more mucilage than fully mature spores and both types progressively lose their mucilage while floating in the water after release. It is as yet unknown if the mucilage layer could be produced by the spore and regenerated after floating free for some time. If some of the vesicles secreting this mucilage layer persist in the release spore, however, regeneration of a mucilage layer is a possibility. Among other functions, the mucilage layer may protect the spore. Electron microscopy studies have concluded that the propagules appear to be very delicate (McBride & Cole, 1971). In many instances the pressure of the cellular contents in combination with outside stimuli causes the plasmalemma to rupture, resulting in a flow of vesicular contents out of the cell. These studies also have revealed that abnormal spore formation is frequent. For example, Hori & Enomoto (1978a) reported abnormal zooid formation in species of Ulva, Caulerpa, Valonia and Dictyosphaeria. Several causes for these failures have been noted. There may be defective development of flagellar roots, incomplete or incorrect orientation of the division furrows, incomplete separation of protoplast units or the dispositions of the organelles during cell division follow abnormal patterns. These failures during propagule differentiation are often over-looked in morphological studies and their consequences frequently ignored in ecological studies. Yet, they are probably most important when explaining reduced germination values of spores or decreased gamete efficiency during sexual fusion.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
213
ECOPHYSIOLOGICAL CHARACTERISTICS OF THE RELEASED PROPAGULE
So far, very few efforts have been devoted to studying the ecophysiological responses of released spores and most efforts have been orientated towards understanding how the spores sink to the bottom and attach to the substratum. We know little, therefore of how the released spores function while they are freefloating. Nevertheless, the accumulated information allows for the characterisation of a few general patterns. Spore viability The most commonly reported general character refers to the short viability of the free-floating spore (Suto, 1950a,c; Kain, 1964; Jones & Babb, 1968). The time that the spore remains viable after it is released normally does not exceed a few days and frequently it does not exceed 24 or 48 h. Only the spores of Enteromorpha have been found to be capable of living for up to 8 days (Jones & Babb, 1968). The reasons for the short viability of the free-floating, spore are unknown. Some authors (e.g. Reed, Laur & Ebeling, 1988) have suggested lack of protecting outer covering of the spores and susceptibility to grazing. However, spores have short viability even in protected environments or in grazer-free containers such as those used in laboratory experiments. The morpho-physiological data on free-floating propagules allow for the formulation of several alternative, often complementary hypotheses to explain the short viability of free-floating species. Both Kain (1964) and Amsler (in Reed, Lauer & Ebeling, 1988) measured photosynthesis in free-floating spores and found that even under saturation intensities, photosynthesis just balances respiration. On the other hand, Ohno & Arasaki (1967) found that in Ulva pertusa the ratios of chlorophylls to carotenoids and of chlorophyll a to chlorophyll b in gametes and spores were much reduced when compared with vegetative cells and that it increased in the course of development from spore to sporeling. These results, together with the previously discussed ultrastructural observations on chloroplast development in the recently released spore, tend to suggest that perhaps the photosynthetic apparatus of recently released spores is not fully functional. In the case of gametes, freeliving sperms and eggs of Fucus serratus are capable of photosynthesis (McLachlan & Bidwell, 1978). For unknown reasons the photosynthetic rate decreases with time, however, and increases only on fertilisation and embryo growth. An additional, complementary explanation emerges from the comparison of light intensity in planktonic and benthic habitats. In general, free-floating spores are likely to receive higher irradiances in the planktonic habitat than in the benthic habitat, especially when many of these propagules have been protected inside a fruiting body or underneath one or several layers of cells until release. It should be remembered that inhibition of photosynthesis at high light intensities is commonly encountered in nature (Darley, 1982). The inhibition appears to be due to photo-oxidation of both the photochemical and enzymatic reactions and becomes more pronounced with prolonged exposures to high intensities, at higher temperatures and under nutrient deficiency. This
214
BERNABÉ SANTELICES
explanation is consistent with the studies by Kain (1964) which showed that the viability of the spores of Laminaria hyperborea could be extended to several days under dark conditions. Extended spore survival under dark conditions was also reported by Ohno & Arasaki (1969) for a diversity of green, brown and red algae, but these authors did not specify whether or not the spores were freefloating. A third, alternative explanation arises from ultrastructural observations on the monospores of Smithora naiadum (McBride & Cole, 1971). The organelles are so crowded into small spaces between copious amounts of vesicular products, that little if any synthetic activity is likely prior to the attachment of the monospore and the ejection of the vesicular materials. Even though numerous floridean starch granules remain in the spore, they are normally isolated from the remaining bits of the cytoplasm. Perhaps the spore depletes its reserve materials while free-floating and the lack of free cytoplasm restricts the possibility of using the starch grains present in the cytoplasm. In this last explanation, the increased viability in darkness, might indicate that photorespiration or light respiration increase the speed of consumption of reserve materials in propagules. Photorespiration has been reported in adult individuals of green, brown and red seaweeds (see Kremer, 1981; Bidwell & McLachlan, 1985, for reviews) but so far it has not been found in seaweed propagules. However, Bidwell & McLachlan (1985) found that samples of Ulva lactuca and Laminaria digitata that were sporulating had high rates of light respiration. Attachment abilities The attachment abilities of benthic algae change with time and species. Some taxa such as the species of Monostroma or Endarachne lack adhesive capacities when recently released and are able to attach only after free-floating for 1–8 h (Suto, 1950a,b,c). Others, such as the species of Gloiopeltis, Undaria and Gelidium have the strongest capacity for attachment immediately after shedding. Still others, such as Enteromorpha, exhibit attachment abilities that remain unchanged for several hours after release. Furthermore, these capacities can change even after the spore settles. For example, the number of spores remaining attached while being subjected to a water flow (“water broom”) increases with time in Gracilariopsis and Agardhiella, while it decreases with time in Cryptopleura (Charters, Neushul & Coon, 1972). The causes of these differences in spore attachment capabilities are not well understood. Since slime secretion has been reported in almost all ultrastructural studies of newly settled spores, the basis for some of these differences has been ascribed to that phenomenon. Some differences do indeed exist. For example, the spores of Enteromorpha are able to settle again after enzymatic treatment of the glycoprotein secreted by the spore. This has been interpreted (Christie & Shaw, 1968; Christie, Evans & Shaw, 1970) as evidence of a continuous secretion for several hours after settlement. Such an interpretation is consistent with the early findings by Suto (1950b) that the attachment abilities of these spores remain unchanged over several hours. In contrast, the ability of developing germlings of Sargassum muticum to attach to the substratum rapidly and progressively declines with time (Deysher & Norton, 1982). Staining with
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
215
Alcin Blue revealed that the decline in attachment abilities was paralleled by a progressive reduction in the quantity of acidic mucopolysaccharides, the probable adhesive, in the tips of the rhizoids. The species that improve their fixing capacities after some hours may develop a different attachment system. For example, upon settlement the cells of Ulva mutabilis soon differentiated rhizoids. A continuous secretion of cementing materials takes place as the rhizoids grow (Bråten, 1975). The lack of electron dense particles in the cytoplasm of the rhizoid cells indicates a different origin for the adhesive material secreted by the rhizoidal cell compared with that of the zygote. Overall, the accumulated information, even though fragmentary and rather marginal, suggests the existence of alternative patterns of attachment abilities in these propagules. Spores of some species seem to be ready to attach as soon as they are released, while others seem to require some time before achieving readiness to attach. Some lose their fixing abilities with time while others seem to recover their fixing abilities after a time, perhaps secreting new slime. If these alternative patterns exist, they should have some importance for the dispersability of the propagules. However, it is still unknown how much of the observed variation might be due to variations in the degree of maturity of the experimental spores. These factors have not been taken into account in many studies because, among other reasons, it is often very difficult to distinguish mature from immature spores. Phototactic and chemotactic responses Propagules of green and brown algae are motile and able to react to physical and chemical stimuli. The chemotactic responses to pheromones by male, brown algal gametes has been discussed previously (p. 207). Interestingly, Amsler (1988) recently demonstrated acute sensitivity and strong chemotactic responses of the zoospore of Macrocystis to nitrogen concentration in the medium. This capacity might be especially important in ensuring the survival and growth of the future sporophyte in a nutrient-rich environment. Gametes of green algae and of some brown algae are often described as positively phototactic while spores and zygotes have often been recorded as negatively phototactic (Lobban, Harrison & Duncan, 1985). Negative phototaxis is thought to help the propagule reach the sea bed sooner while positive phototaxis may induce upward movements, lengthening the free-floating time and allowing for greater passive transport by currents. The swimming speeds of motile seaweed propagules are, however, extremely slow compared with water currents in the sea (Suto, 1950b; North, 1972) and these tactic responses seem important for localized movements only, such as gamete encounters or spore settlement. In addition, explanations do not always fit the expected patterns of response. For example, Reed, Laur & Ebeling (1988) invoked positive phototaxis, upward movements and improved transport by currents to explain dispersal patterns of a few kilometres in filamentous brown algae. Positive phototaxis, however, is supposed to be exhibited by gametes, not by spores, and gamete encounters a few kilometres away from the parent plants seem unexpected in view of dilution effects. In summary, experimental studies have shown that under laboratory conditions a diverse array of factors can modify the process of spore release. Little is known of the effects of these factors under field conditions, however,
216
BERNABÉ SANTELICES
and only preliminary explanations have been advanced regarding the adaptive values of most observed patterns and responses. The morphological and physiological changes occurring in the parental tissue during spore release have been explored infrequently. Most studies on spore physiology have been restricted to describing the extremely reduced viability of algal spores, but few have investigated the morphological or physiological basis for such reduced viability. Although there are some studies on the influence of specific gravity and spore diameter on sinking rates, changes that take place over time as a spore is suspended in water are largely ignored. Likewise, it is unexplained why the free-floating spore seemingly does not divide, while other planktonic, unicellular algae are able to do so. The ultrastructure of the released propagule, as well as the morphological changes occurring during spore differentiation, have been described for a number of species of green, brown and red algae but there is a paucity of data about the fine structure of the released, settled and germinating spore. Therefore, it is often very difficult to explain or even correlate functional responses with morphological changes in the spore. Overall, the accumulated evidence suggests that ultrastructure and ecophysiological responses of the free-floating propagules differ in several respects from the freeliving plankton to which they have been compared. Several biological systems, including the photosynthetic apparatus seem neither fully functional nor efficient in recently released spores.
DISPERSAL In seaweed biology, dispersal refers to the scattering of propagules in all directions from the parental thalli. Dispersal studies have often been associated with biogeographic patterns but they are also ecologically important. Individual species are doomed in their present habitats (Harper, 1977) and their continued survival depends on adaptations enabling the species to hold its place in the community as well as to establish elsewhere. Furthermore, any environment is subject to change and sessile organisms unable to adapt to change may become extinct. Because many changes are not synchronous over a large area (Levin, Cohen & Hasting, 1984) dispersal of propagules allows a fraction of them to reach a suitable habitat every generation. Thus, dispersal is conceived as a mechanism allowing the species to reach new habitats, to escape environmental unpredictability and to survive over large areas in spite of environmental change. Dispersal is an individual rather than a collective process which depends on the characteristics of the plants as well as on the environment. Dispersal patterns, frequency of new sites and the distance of the sites from the parent plants are important factors for successful dispersal in many organisms. In turn, dispersal patterns are the result of several variables. In the seaweeds these include, at least, the type and dispersability of the dispersal unit, their concentration at the source, the distance between the source and a new site and the nature and activity of the dispersing agent. In sharp contrast to dispersal mechanisms in land plants, most pertinent information on seaweed dispersal comes from laboratory experiments and is
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
217
fragmentary. Doubtless this reflects methodological problems involved in studying dispersal of microscopic propagules in the field. This section focuses first on dispersal agents, then on dispersal units, and ends with a discussion of the resulting dispersal patterns.
DISPERSAL AGENTS
Water masses, floating substrata and animals can all disperse benthic algae. Masses of moving water are the commonest transport agents of unicellular or multicellular propagules and of drifting plant fragments. Water may also transport floating substrata or animals that may be carrying algal species.
Water masses Field ecologists (e.g. Neushul, 1972a) have been able to distinguish several water movement regions in the water column. The current zone layer, which may include a large part of the water column, is characterised by unidirectional flows, net transport capacity and current velocities ranging from 1 to 30 m·s 1 . The surge zone is immediately below. It is characterised by oscillating motions of various velocities (1–10 m·s -1 ). Water velocity slows down around solid surfaces on the bottom. The layer immediately around a solid object is known as the boundary layer. It has an estimated thickness of 1 to 10 mm and velocities of about 0.1 m·s -1. The 10 to 150 µm space immediately around the solid surface is recognised as the laminar sublayer (Neushul, 1972a), with water velocities estimated to range from 0.01 to 0.001 m·s -1. Many objects in the water are not smooth and irregularities through the laminar sublayer generate eddying regions of their own with confused flow patterns. In these cases, however, the water will cease to move in the immediate vicinity of the surface of the object. The various characteristics of these regions of water movement imply different fates for the dispersal units that they contain. Permanence in the current zone is likely to result in net transport for some distance due to the unidirectional currents predominant in this layer. Owing to the oscillating water movement in the surge zone, net transport is probably reduced here, although the dispersal units are kept in motion. Both movement and transport are reduced at the boundary layer and are nil at the laminar sublayer. It is of interest that the estimated thickness of the laminar sublayer (about 150 µm) is in the range of the largest spore diameters (about 160 µm). Algal spores are small enough to occupy the slow-moving and non-moving layers of water in the boundary layers and the laminar sublayer, where they may attach to the substratum. The lack of movement of this sublayer seems to be a prerequisite for spore attachment, as even slight motions between the substratum and the overlying water strongly inhibit the ability of spores to settle (North, Mitchell & Jones, 1969; North, 1972). In fact, Neushul (1972a) has commented that the water movement in a kelp forest is so high that it is a wonder that the minute planktonic germ cells of benthic algae are able to reach the bottom at all.
218
BERNABÉ SANTELICES
Floating substrata Natural as well as man-made substrata can also act as dispersal agents of benthic algae. One of the best known examples of seaweed dispersal on manmade substrata is the introduction of Acanthophora spicifera to the Hawaiian Islands by a ship (Doty, 1961). Several examples have been added subsequently. Often the pattern of distribution of the species so dispersed is very different from that expected based solely on current systems or plate tectonics. Other man-made structures inadvertently facilitate dispersal. For example, Stegenga & Mol (1983) found that a diverse number of seaweed species could reach the shores of the Netherlands from Brittany, Normandy and S. England if growing attached to plastic or wood remains. The estimated distances of these drifts were 500 to 800 km (Hoek, 1987). Many seaweed species can be transported as epiphytes on drifting vegetation. Probably the best known example of such associations are the freeliving epipelagic Sargassum communities of the western Atlantic coast. Two major species, S. natans and S. fluitans, are assumed to be eupelagic forms which never carry attachment organs and reproduce only by vegetative propagation. The presence of a specific epifauna and epiflora is indicative of its phylogenetic age. They are presumed to have diverged from attached species becoming specialised for floating habitats (Austin, 1960). Both species are particularly effective carriers of other algae from one coast of the ocean to another (Hoek, 1987), including about 40 amphiatlantic tropical-to-warm temperate species. Other seaweed-dominated, drifting communities have been described from several latitudes. Most of them are free-floating rather than free-living species. For example, 23 of the 50 species of attached Sargassum reported in Japan (Yoshida, 1963) form free-floating drift. Cystoseira barbata, Chondria tenuissima, Gigartina acicularis, Cladophora sp., Valonia utricularis, Fucus mytilus and Furcellaria fastigiata also form free-floating communities in Danish waters (Austin, 1960). Thalli of Ascophyllum nodosum and Fucus vesiculosus transporting a diversity of Chlorophyta, Phaeophyta and Rhodophyta have been regularly recorded in the Sargasso Sea (Woelkerling, 1975) and healthy, freefloating, reproductive plants of Ascophyllum were found off the coast of W. Africa (John, 1974). According to Hoek (1987) these plants must have travelled at least 5500 km, which would take about 430 days at an average speed of 13 km·day -1 . Many of these examples of long range dispersal remain unexplained in the algae as they involve not only extended times floating at sea, but also a drift through very different oceanographic climates. Until recently, most studies on drifting vegetation have been essentially descriptive and taxonomic in nature. The introduction of experimental studies has suggested that drifting of seaweeds is a phenomenon more complex than a simple drift from one land mass to another. Both the drifting substratum as well as the epiphytic flora can be affected by factors other than the current system. For example, by suspending Tasmanian Macrocystis pyrifera holdfasts at sea, Edgar (1987) evaluated the potential of drifting kelps for epiplanktonic dispersal of associated plants and animals long distances around the southern seas. Most of the common animals and slightly over half of the plant species associated with the kelp in its original locality were still present after 191 days at sea. The grazers drifting in the holdfast may consume the epiphytic flora, however,
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
219
thereby reducing their diversity. Therefore, the dispersal patterns of epiphytic species should not be expected necessarily to reproduce the corresponding patterns of their hosts. In addition, insufficient nutrient concentrations or high temperature regimes can kill the stipes and blades of a drifting host such as Macrocystis, while dense aggregations of the boring isopod Phycolimnoria could disintegrate the holdfast while adrift. External surfaces of motile animals Seaweeds may grow on animals, sometimes even killing them by overgrowth and are frequently transported when growing on motile invertebrate species. In the field it is common to find seaweed covering the shell of a diversity of molluscs and some crustaceans. But the possibilities are by no means restricted only to these two types of invertebrates. For example, Tsuda (1965) and Tsuda, Larson & Lujan (1972) found that the green alga Pringsheimiella scutata grows on the face and belly of the Hawaiian monk seal, Monachus schauinslandi; some species of Polysiphonia form dark red tufts on the neck of the green turtle Chelonia mydas; several species of algae have been described on the ventral fins or the beak of parrot-fishes (Hartog, 1971; Tsuda, Larson & Lujan, 1972); and some species such as Fosliella farinosa even grow over the living spines of sea urchins (Lawrence & Dawes, 1969). Even small-sized invertebrates, such as amphipods have been found to transport seaweed propagules on their posterior legs (Buschmann & Santelices, 1987). Most of these relationships seem to have little specificity. For example, an essentially similar flora was found by Tsuda, Larson & Lujan (1972) on the beaks of each of seven species of parrot-fishes. It was concluded that the exposed dentition of the fishes merely provides yet another type of substratum on which algae grow. Some more specific relations are perhaps to be found in situations, such as the cases of amphipods, where the spore transport has a direct relationship with the specific feeding preferences of the invertebrate. In spite of the commonness of the transport of seaweeds by invertebrates, the phenomenon is often ignored not only by biogeographers and phycologists, but also by fishery specialists and aquaculturists. The recent introduction of two extremely invasive species of algae in different geographic areas illustrates this point. Codium fragile subsp. tomentosoides has rapidly spread along the Atlantic coast of the United States and Europe (Taylor, 1967; Ramus, 1971; Churchill & Moeller, 1972; Wassman & Ramus, 1973; Carlton & Scantlon, 1985), while Sargassum muticum has become distributed along the Pacific coast of the United States and Canada and the coast of Great Britain (Farnham, Fletcher & Irvine, 1973). Both species are suspected to have been introduced with the transplantation of oysters from Japan and other locations. These are but two of many potential cases of invasion via animal surfaces. Perhaps many other cases occur frequently, but the species have been introduced to poorly known floras where these changes remain undetected, or the introduced species are of undetectable sizes or have been unable to grow and propagate as efficiently as Codium fragile or Sargassum muticum. Faecal pellets
220
BERNABÉ SANTELICES
The biotic transport of seaweed propagules is by no means restricted to the external surface of motile animals. As already mentioned (p. 206), cultivation of faecal pellets from various marine invertebrates and fishes has revealed that the propagules of a large number of species of Chlorophyta, Phaeophyta and Rhodophyta pass through the animals and are capable of originating new individuals. As in the attachment to invertebrate surfaces, algal dispersal by faecal pellets show little specificity. It is true that propagule production by Chlorophyta and Bangiophycidae is stimulated by incomplete digestion. Also, it is clear that digestion survival among opportunistic forms is commoner than among late successionist algae. So far, however, no species has been found to depend entirely on this mechanism to disperse its propagules, or to have species of invertebrates or fishes as the exclusive dispersing agent.
DISPERSAL UNITS
There are three types of dispersal units in seaweeds: plant fragments, multi-cellular packages of propagules and unicellular sexual or asexual spores.
Drifting plant fragments As mentioned previously (p. 179), many frondose and filamentous seaweed species are able to fragment, float, drift for a period, re-attach to the substratum and regenerate new individuals. This is common in Ectocarpaceae (Russell, 1967), some filamentous Rhodophyta (Pearlmutter & Vadas, 1978), several frondose and cylindrical brown and red algae (Norton & Mathieson, 1983), and even in some frondose, normally attached species such as Solieria chordalis (Floc’h, Deslandes & Le Gall, 1987). Most free floating fragments or individuals are characterised by lack of ability to differentiate reproductive structures (Austin, 1960; Norton & Mathieson, 1983). This is not always the rule, however, because free-floating populations of Ectocarpus and drifting fragments of Sargassum muticum become fertile while suspended, resulting in an increased dispersal capacity (Russell, 1967; Norton, 1977a,b). While some seaweed species lack the capacity to produce spores while adrift, it is not uncommon for detached plant fragments to contain mature reproductive tissues. Several such species have developed reproductive traits that seem to combine seeding first the area around the parental plant, and then drifting, either the fertile tissues only or the whole plant. An example of this situation seems to have been described more than 33 years ago for the Spanish populations of Gelidium sesquipedale. The shore drift of this species increases towards the autumn and the per cent of fertile thalli in the cast weeds is higher than those in the populations that remains attached (Seoane-Camba, 1966). The difference was interpreted as a natural dispersal method of spores in this species (Seoane-Camba, 1969). A more recently studied example is provided by Postelsia palmaeformis sporophytes. In this species the sori are on the grooved blades. Sporulation occurs during low tides, when the plant is emersed and the blades hang adjacent
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
221
to the stipes. The spores literally flow down the stipe (Dayton, 1973) and settle in about 30 min, before the tides completely cover them (Lobban, Harrison & Duncan, 1985). This species lives in a high energy zone and eventually sporangial blades or the whole plant are dislodged by water movement. Fertile plants are able to float (Dayton, 1973), thus increasing the dispersal potential of Postelsia. Experimental demonstration of the seeding capacities of detached fertile fronds has been recently completed by Paine (1988). Although differing in mechanisms, the observations in Gelidium sesquipedale as well as those on Postelsia suggest adaptations for dispersing spores around the parent plants first and then drift-dispersal along longer distances. In both cases, however, as well as in many other species where similar responses seem to occur, we lack an understanding of the factors increasing the susceptibility of fertile fronds or plants to be removed by water drag. Increases in size or branching could be a factor (e.g. Chondrus) but more complex processes similar to the abscission of land plants may be involved.
Propagule packages Seaweeds can release multicellular packages of propagules. The ontogenic origin and the degree of cell compactness vary from one type to another. They have been regarded as adaptations for increasing sinking rates (Coon, Neushul & Charters, 1972; Neushul, 1972a). This has been especially well documented for brown algal species. The zoosporangial sori of Pelagophycus and Nereocystis are produced on fronds that float in the current zone, many metres away from the bottom (Neushul, 1972a). When the sori mature, the fertile segments in the blades are detached and sink to the bottom. The embryos of Sargassum muticum have also been described as examples of a fast sinking, multicellular propagule. In this species the eggs are released from the conceptacle and cluster outside the receptacle. There they are fertilised and develop into small germlings, usually without rhizoids, before they drop to the sea bed (Deysher & Norton, 1982). The relatively large propagules (about 160 µm) sink 5 to 10 times faster than propagules of other species. Species of Gracilaria, Champia, Rhodymenia, Palmaria, Gigartina and Chondrus, release aggregations of spores within mucilaginous streams (Oza, 1975; Boney, 1975, 1978). These spore aggregations have been reported as sinking to the bottom only when large strips of mucilage remain intact and carry a large number of spores. In contrast, small strips of mucilage containing spores normally drift away and exhibit decreased sinking rates. They are assumed to shed spores while being carried away by the currents. Propagule packages, therefore, do not always involve increased sinking velocities. As will be discussed with respect to individual propagules, several factors other than specific gravity are involved in the determination of suspension of planktonic forms. Sinking together also implies arriving together at a given site. In some species this might be beneficial. For example, in species such as Pelagophycus or Nereocystis that have heteromorphic alternation of generations and microscopic gametophytes, sinking together increases the probabilities of gametophytes developing in close proximity and of gamete encounters. In species such as Chondrus crispus or Gracilaria verrucosa, Sporelings can coalesce during early
222
BERNABÉ SANTELICES
growth (Jones, 1957; Tveter & Mathieson, 1976). The cells in the centre of the coalescent sporelings produce upright, multiaxial fronds that grow more rapidly than fronds of non-coalesced sporangia. In sharp contrast to the above the cases, there are many algal species where crowding can be a significant mortality factor (Chapman & Goudey, 1983) or where density-dependent mortality and strong interspecific interactions are ecologically very important. Given this diversity, it can be understood that the propagules of some species exhibit tendencies to sink together while others are shed in smaller numbers, even though they may be released from the cystocarp in common mucilage strips. Unicellular propagules Seaweed spores have no dormancy capabilities. Their viability and attachment capacities are limited. They lack protective outer covering and can be readily consumed by planktonic grazers and filter-feeders. Although spores of brown and green algae are motile, their swimming speeds are slow compared with water currents and they can be carried away by water masses from potential substrata or from the euphotic zone. Their survival, therefore, depends on landing on an adequate substratum while still possessing their capabilities for attachment. How does the minute, unicellular propagule sink through the water column and reach the bottom? Enormous distances relative to the spore size, and water movement are regarded as two very important factors. For example, under conditions of still water, a single carpospore of Cryptopleura violacea can remain in suspension for about 10 min if released from a 6 cm tall parent plant attached to the sea floor (Neushul, 1972a). On the other hand, it will take 3.5 days to fall from a parent plant living as an epiphyte on the floating blades of a giant kelp (Chapman, 1986a). In addition, water movements in the field are far from still. It is fairly evident, therefore that the problems faced by the propagules of benthic spores are, in general, the opposite of those faced by truly phytoplanktonic algae. In the latter organisms, sinking produces potential disadvantages by leading to their removal from the euphotic zone. While a relatively large body of work on sinking and floating of phytoplankton cells has been developed (see Smayda, 1970; Walsby & Reynolds, 1981; Sournia, 1981, for reviews), only some of those concepts have been applied to the unicellular propagules of the benthic algae. The following analysis reviews some of these and other concepts that might be applied to benthic algae propagules.
SINKING AND FLOATING OF UNICELLULAR PROPAGULES It is now understood that at least four sets of factors determine suspension of phytoplankton in the water column (Smayda, 1970; Walsby & Reynolds, 1981; Sournia, 1981; Darley, 1982). One set involves physiological and morphological adaptations at the cellular level. The second includes physicochemical conditions of the water. The third refers to the type of water movement prevalent in the mass of water where the cell is. The fourth group includes a heterogeneous assembly
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
223
of factors, biotic and abiotic, which results in accelerated sinking of phytoplankton. Morphological adaptations Terminal sinking velocity of inert bodies suspended in a viscous fluid (Stoke’s equation) is modified by spore radius and spore density (specific gravity). Therefore, terminal velocity will change from one species to another and between spores in a given species. Spore size (radius) is a most critical factor because terminal velocity is related to the square of the radius. Among seaweeds, spore size is a variable factor ranging from 5 µm to 160 µm (Coon, Neushul & Charters, 1972). In still water, large spores have been found to sink faster than small spores (Coon et al., 1972), but the correlation is not strict, as sinking velocity also depends on density. The fastest sinking spore (170 µm·s -1; Sarcodiotheca gaudichaudii) was about 50 µm in diameter and had a density of 1.181, while the largest spore tested (about 75 µm, Cryptopleura violacea) had a density of 1.085 and sank at about 100 µm·s -1 . From the above data it is evident that increased diameter does not necessarily mean increased density. In phytoplankton, cell wall components seem to be especially important in this respect, as they may contain very dense inclusions. When a cell with such a wall type increases in size, the volume of the wall relative to the total volume of the cell decreases (Walsby & Reynolds, 1981). Seaweed propagules generally lack a cell wall, but the principle could apply to other cellular components (e.g. high density reserve materials) that might have increased or decreased density. A second factor to be considered is whether increased diameter implies a proportionally larger increase in surface area or in volume. Cells with increased surface area to volume ratio have more frictional resistance and sink slowly. The shape of the propagule might also influence sinking velocities. For example, Walsby & Reynolds (1981) showed that the sinking velocity of a cylinder of constant diameter increases as its length increases, but the increase in velocity approaches a maximum when the length exceeds about 5 diameters. Long cylinders are considered more efficient at remaining in suspension. Interestingly, the propagules of three major groups of benthic algae have different shapes. Zoospores and gametes of Chlorophyta are ovoid, slightly elongated with two or four anterior flagella. In Phaeophyta all motile stages (spores and male gametes) are kidney-shaped with two laterally inserted flagella, while the propagules of red algae are spherical and lack flagella. It is completely unknown how the different shapes affect sinking patterns in these organisms. The only pertinent reference is the observation by Boney (1975) that the shape of the mucilage layers of red algae deform, increasing the form resistance. Mucilage layers are present in many propagules of benthic algae (Boney, 1975, 1981; Ngan & Price, 1983) and they have been regarded as a mechanism increasing significantly the spore buoyancy (Boney, 1975, 1981). As indicated previously (p. 212), the mucilage layer can be up to 80% of the combined spore plus mucilage volume, and is larger in immature spores. The mucilage is progressively lost after the spore is released, decreasing the effective diameter and the buoyancy of the spore and therefore increasing the probability of sinking.
224
BERNABÉ SANTELICES
Mucilages are gels form by cross-linked polysaccharides. The hydrophilic chains form a network which can immobilise a large volume of water. The density of the gel is close to that of the suspending water but it cannot be less than that of water. Therefore, the importance of mucilage is in potentially decreasing sedimentation rates rather than providing positive buoyancy. Furthermore, as Smayda (1970) and Walsby & Reynolds (1981) have noted, enclosing a cell in a mucilage sheath decreases its density but increases its effective radius. These two factors have opposite effects on sinking rates; under certain conditions a mucilage sheath might actually increase the sinking rate. Thus, the sinking rate of a cell with mucilage will be less than that of a cell without mucilage only when the density difference between the cell and the mucilage is at least twice the density difference between the mucilage and the suspending water. Under this relative density difference, there will be a range of thickness of the mucilage coat, from zero up to a critical maximum, which will provide a decreased sinking rate. Beyond that maximum the increase in size is no longer compensated for by the decrease in density (Walsby & Reynolds, 1981). None of these measurements seems to have been made on the spores of benthic algae. Most of the chemical components which make up the protoplasm of living cells are heavier than water. Carbohydrate has a density of about 1.5, protein 1.3, nucleic acids 1.7, and phosphates 2.5 g·cm-3. Only lipids have a density lower than that of water, down to 0.86 g·cm -3 . Therefore, fat accumulation was thought to be an adaptation increasing cell buoyancy of phytoplankton. It has been found, however, that the amount of lipids in most cells is not large enough to be an effective means of increasing cell buoyancy. A comparable investigation seemingly has never been undertaken with propagules of benthic algae. Physico-chemical changes in the water Changes in density and viscosity are common in surface waters. These changes cannot be viewed in isolation, as both are liable to bring about corresponding changes in the suspended propagules. The density of the suspending water can vary with the concentration of dissolved substances and with temperature. Viscosity of the water decreases with rising temperature and as a consequence, sinking rates increase. The viscosity of water is halved between 0°C and 25°C, resulting in a doubling of the sinking rate of equivalent cells. The above patterns may impose differences in sinking adaptations of propagules living, for example, in waters with different temperatures or in habitats subjected to predictable changes in dissolved organic matter. No data are available on this subject for benthic algae. Sinking in moving water Natural waters are rarely, if ever, still and the sinking and attachment of seaweed propagules is thought to be greatly modified by water movement. However, no experimental studies with sinking propagules have been done in the field or in large-scale facilities where different types of water movement could be simulated. Equivalent studies with phytoplanktonic cells suggest sinking is
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
225
possible both in convection cells in the water surface as well as in the turbulent waters close to the bottom. Mechanisms accelerating sinking At least three mechanisms that have been found to accelerate the sinking of phytoplanktonic cells (Smayda, 1970; Kessler, 1986) could favour the sinking of benthic algal propagules. One is the presence of density inversion currents. If the density of a micro-layer of water together with its contained organisms becomes greater than that of the underlying layer, a density inversion exists. A vertical density current will result which sinks with its particles to a depth of equivalent density. Such vertical density currents carry particles downward much more rapidly than settling calculated by Stokes’ Law. Wind-induced or salinity-induced downwelling water also accelerate sinking of surface water with its associated organisms. This could be an important factor in sinking of algal propagules in coastal waters, where the algae live, but the effects have not been studied with respect to distribution of seaweed propagules. Faecal pellets containing algal propagules sink significantly faster than the fastest sinking propagule of benthic algae. They might therefore, have an important role in the sinking of seaweed propagules. In phytoplankton, the size, shape and texture of the faecal pellets are dependent on the food source and are known to be factors influencing sinking rates.
DISPERSION PATTERNS
The dispersal patterns resulting from the interacting effects of dispersal units and dispersal agents are also poorly understood. Together with the methodological difficulties involved in measuring dispersal distances and settlement of microscopic propagules or of drifting plants, different methods have been used, yielding results that often cannot be compared. For example, dispersal distances have been inferred from juvenile recruitment in colonisation experiments. Recruitment is a function not only of the dispersal ranges of spores, but also of factors influencing settlement, recruitment and growth to sizes that are detectable in the field (Connell, 1985; Hoffmann, 1987). Many of these factors (e.g. grazing) may have little to do with the floating and sinking capabilities of a given propagule. Ecological studies with benthic algae have revealed two types of dispersal patterns, short- and long-distance dispersal. The mechanisms involved seem to be different and they will be reviewed separately. In a strict sense, though, only short distance dispersal seems to be achieved through release and settlement of unicellular or few-celled propagules. Short-distance dispersal Field experimental clearings followed by counting densities and measuring distances of juvenile recruits have always suggested short dispersal shadows for benthic algae. Perhaps the first such experiment was done by Sundene (1962) who
226
BERNABÉ SANTELICES
found that the dispersal distance of Alaria esculenta was about 10 m. Dispersal distances of Macrocystis pyrifera were about 5 m (Anderson & North, 1966); in Colpomenia peregrina the dispersal distance was 2 m (Vandermeulen & DeWreede, 1986) while the values for Postelsia palmaeformis range from 1.5 to 7 m (Dayton, 1973; Paine, 1979). In Sargassum muticum, appearance of new recruits was limited to 10 m from parent plants and they declined exponentially with distance (Chapman, 1986a). These limited dispersal distances can be increased if the number of source plants is increased, hence a dilution factor probably exists. For example, the maximum recruit distance of 5 m found in Macrocystis pyrifera could be increased to about 20 m if the source of propagules is increased from one to several plants and it increases to 40 m if the source is a dense plant stand (Anderson & North, 1966). The above results are consistent with the view that seaweed propagules are short-lived and have poor dispersal capacities, but they conflict with results of studies of the water column. Using glass slides set in the water, Amsler & Searles (1980) found seaweed propagules with attachment abilities at distances as far as 35 km away from the nearest parent population. Similar results have been reported by Zechman & Mathieson (1985). Enteromorpha was the species most commonly found in these samples. Several alternative hypotheses perhaps explain the discrepancy. The concentration of spores required to generate recruits of a size that can be discriminated by the human eye in the field may be several orders of magnitude higher than that required to be grown in the laboratory from impacted glass slides or water samples. Or perhaps both methods have preferentially sampled organisms with different dispersal shadows. Field removal experiments have worked mostly with kelps, while the most abundant organism in the slides in the water column was Enteromorpha. Spores of ephemeral, opportunistic species, such as Enteromorpha, are found throughout different water levels (Amsler & Searles, 1980) and have large dispersal shadows (Sousa, 1984). Those of more perennial, long lived species, such as kelp, occur near the bottom of the water column, suggesting small dispersal shadows. Although more recent data (Hoffmann & Ugarte, 1985) indicate that spores of late successionist forms are also found in the upper water layers, it is likely that propagules of different species travel at different heights along the water column. It would not be surprising to find that some species are able to achieve longer propagulemediated dispersal distances than other species. Distances of 25–30 km could be covered in 2–3 days by Enteromorpha propagules travelling at speeds of 13– 15 km·day -1 . The known viability of Enteromorpha propagules extends up to 8 days (Jones & Babb, 1968). Long distance dispersal There are numerous examples, some of which have been already mentioned in previous pages, of long distance seaweed dispersal that could not be achieved by propagules alone. Additional examples are the seaweed growing on oil drilling and pumping platforms in the North Sea (Chapman, 1986a) or in remote oceanic islands. Drifting of plants or parts of plants living on floating substrata, followed by propagule release are thought to be a likely explanation but it does not account
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
227
for all the observed examples. Crustose corallines are unlikely to float (Hoek, 1987) and many of such taxa are not regarded as early pioneer species, or as likely colonisers of floating substrata. In summary, the accumulated evidence suggests that there is a diversity of dispersal agents for benthic algae, but their ecological importance and roles are little understood. The evidence suggests, in addition, that seaweeds show an array of dispersal units, but it is as yet unknown if they represent adaptations for alternative dispersal styles. A comprehensive understanding of the biological changes experienced by the dispersal units while free-floating is also lacking. Depending on the dispersal units, such changes can range from subcellular modifications in unicellular propagules to community changes aboard floating substrata. These changes are particularly important for characterising alternative dispersal styles as well as for understanding the resulting dispersal patterns. Even though two such patterns, long- and short-distance, are distinguished in seaweeds, their mechanisms are not entirely understood. It would not be surprising if future studies describe additional patterns.
SETTLEMENT While studies on dispersal patterns stress intraspecific differences in dispersal units and dispersal agents, community studies of settlement focus on the effects of mixed populations of propagules arriving together in specific habitats. Both on land and in the sea a flux of propagules determines the potential vegetation of a given area (Harper, 1977; Fenner, 1985; Hoffmann, 1987). If the area is already colonised by seaweeds, these individuals may serve as a source of inoculum, providing propagules which can fall in their own area, or that can spread to other areas. Thus, most habitats seem to be continually invaded by propagule assemblages from organisms living in the area, as well as from organisms living elsewhere. These patchy propagule aggregations move in and out of potential habitats as water passes by. Either owing to local conditions or to morpho-functional adaptations of the propagules, a variable number of them may precipitate. Once in the boundary layer, propagules may settle. In sessile organisms, such as the seaweeds, settlement consists of the planktonic propagule cementing itself to the surface, taking up permanent residence on the substratum (Connell, 1985). Becoming fixed obviously means having no possibilities of habitat change under adverse conditions. Therefore, enormous propagule mortality often occurs after settlement and may determine to a large extent the observed pattern of species distribution in the field. The mortality factors may be biotic or abiotic in nature or an interaction of both. This section reviews the information available on arrival of propagules to the substrata, their attachment and germination. There is almost a complete absence of settlement studies in the field and much of the scarce information has originated from ultrastructural observation or from laboratory experiments. Several studies have addressed the problem of settlement but, in fact, have measured recruitment. Those studies will be reviewed in the next section.
228
BERNABÉ SANTELICES
THE SPORE CLOUD
Experimental evidence indicates that a flux of propagules suspended in the water is present for most of the time. For example, early studies on colonisation frequently reported that a seaweed cover always developed on any newly exposed rocky surface in the sea (Moore, 1939; Northcraft, 1948; Fahey & Doty, 1949; Varma, 1959). They also noted that often the algal cover that developed included species not necessarily represented in the neighbourhood of the experimental plots. More recent evidence, gathered by incubating coastal sea-water samples has revealed continuous presence of seaweed propagules in the water column (Zechman & Mathieson, 1985; Hoffman & Ugarte, 1985). By analogy with land plants, the flux of propagules in sea water has been named spore rain by Hoffmann (1987). Two processes are involved. One is the existence of propagules suspended in the water that McDermid (1988) has called spore clouds. The other is the rain of such propagules that reaches the substratum. Propagule clouds are here defined as patchy propagule aggregations suspended in the water column, which can be transported from their points of origin to other places. The composition of the cloud may change as propagules are lost by sinking or are gained, due to new spore releases. Several lines of research suggest that the propagule aggregations are patchy in space and time and, therefore, the rain falling from different clouds can result in completely different vegetation at different times or places. In fact, many repopulation experiments (Fahey & Doty, 1949; Kain 1975; Neushul el al., 1976; Emerson & Zedler, 1978; Hawkins, 1981; DeWreede, 1983; Reed & Foster, 1984) have resulted in different sequences of colonising species when the artificially cleared surfaces are exposed at different times of the year. Variability does not only involve different seasons; year to year fluctuations are also common. More recently, studies of propagule distribution in the water column have confirmed much variability in propagule composition (Hruby & Norton, 1979; Amsler & Searles, 1980; Hoffmann & Ugarte, 1985; Zechman & Mathieson, 1985). This variability includes temporal as well as spatial fluctuations both in the diversity and the abundance of propagules. The factors determining patchiness in the composition of propagule clouds have been reviewed in the previous sections. Patchiness is brought about by the periodicity of propagule formation and release; by the different numbers of propagules produced by different species; by the intermittent effects of the biotic and abiotic factors modifying the dispersability of the propagules; the variable distances and concentrations of propagules at the source of origin and by the biotic interactions that either increase (e.g. pheromoneor digestion-induced propagule release) or decrease (grazing, ingestion by filter-feeders, termination of viable period) the propagule densities in the cloud.
Temporal patchiness In a recent review, Hoffmann (1987) predicted that three types of temporal fluctuations in composition and abundance of propagules should be found in most habitats: seasonal, monthly and daily periodicities.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
229
Seasonal variations either in propagule quantities, propagule composition or both should be expected at all latitudes. In tropical regions it is likely that there will be propagules arriving at coastal regions throughout the year. The propagules of some species may be temporally patchy due to restricted fertility, while the propagules of other species could be expected to be present all year round. With increasing latitude, the proportion of species showing temporal patchiness should gradually increase. Seasonality in propagule production also seems to increase with latitude; seasonal fluctuations in quantities of propagules and composition of the clouds should, therefore, also increase. At the highest latitudes, fertility seems restricted to some part of the year only. Clouds are likely to be abundant and diverse only at those times and be very reduced at all other times. In addition to seasonal variations, monthly and daily periodicity of propagule production and release is likely to superimpose additional, small-scale patchiness. These types of rhythms seem to be species-specific. Therefore, the temporal patchiness induced by them is not related to latitude, as are the seasonal fluctuations. The relative importance of these phenomena will depend on the number of species in a given area where spore production or release will be triggered by factors such as the diurnal alternating periods of light and darkness or by changes in lunar phase. The temporal variability in abundance and composition of propagules in the spore clouds should have several important effects on community structure and organisation. Propagule availability determines the initial status of community development on substrata being exposed de novo to the sea, such as lava flows, or on areas opening seasonally or accidentally (Dayton, 1979; Keough, 1983; Underwood & Denley, 1984; Watanabe, 1984; Caffey, 1985). Temporal patchiness also imposes limitations on the consumers using the propagules as food. Gut content studies of invertebrate grazers, especially of molluscs (e.g. Steneck & Watling, 1982) and of filter-feeders (Santelices & Martinez, 1988) have often revealed the consumption of large quantities of seaweed propagules. None of these consumers seems, however, to rely on seaweed propagules only. Depending on their buccal apparatus, feeding habits and preferences, grazers generally consume microalgae or other seaweed parts as well. When seaweed propagules in the sea water have reduced representations, gut contents of filter-feeders show increased ingestion of other planktonic producers, such as diatoms and dinoflagellates (Santelices & Martinez, 1988). These temporal fluctuations in propagule abundance and composition have been used to explain the seeming lack of specialisation of grazers on either algal reproductive structures or algal propagules (Hoffmann, 1987). However, and as noted previously in this review (p. 206) a number of studies (Underwood, 1980; Underwood & Jernakoff, 1981; Jernakoff, 1983; Gaines, 1985; Gunnill, 1985; Watson & Norton, 1985; Buschmann & Santelices, 1987) have described grazers that either specialised on spore predation or are highly specific in their preference for algal reproductive tissues. Diurnal fluctuations of spore release have been interpreted by Ngan & Price (1983) as adaptations for reaching the higher shore. This might be true for species with propagules settling almost immediately after release. For most species, however, the amount of time spent by a given spore in the cloud is generally unknown, and few predictions can be made in this respect. Any delay between
230
BERNABÉ SANTELICES
release and sinking might result in settlement during low rather than high tide. In addition, many benthic grazers exhibit increased feeding activities during incoming tides and they would certainly increase the mortality rates of the algal propagules arriving at the shore at that time of the tidal cycle. Studies comparing the abundance and diversity of algal propagules during incoming and receding tides to clarify these problems would be especially rewarding. Spatial patchiness Location and fertility of the propagule source, intraspecific differences in the amounts of spores released and differences in the dispersability of the propagules are the principal factors determining spatial patchiness of the propagule clouds. As all these dissimilarities reflect species differences, spatial patchiness should depend on the local flora and not on latitude. Overall, the propagule composition of a cloud at any given site could be envisioned as including propagules with different dispersal capabities. At any given point these clouds should include at least propagules produced by local species with short dispersal shadows as well as propagules from local and distant species with long dispersal shadows. The local component is likely to vary from place to place, generating significant spatial differences among clouds. Spatial patchiness in propagule distribution is likely to have ecological consequences analogous to those already described for temporal patchiness. This patchiness has been found in colonisation studies, but there are no comparative studies that would allow evaluation of spatial patchiness as it affects other relevant ecological relationships, including, for example, spatial distribution of spore consumers. Both temporal and spatial patchiness should be expected as a result of the effects of oceanographic or climatic changes, which are so common in coastal area. For example, drastic changes in salinity or temperature regimes may affect massive numbers of propagules. One of the earliest of such reports (Burrows, 1961) refers to Fucus serratus. The low resistance of the zygote of this species to reduced salinities limits its distribution into habitats with freshwater influences. After fertilisation the zygote of this species requires 3 hours before the resistance to low salinity is developed. If the egg is immersed in low salinity conditions before this time, the fertilisation membrane bursts and the egg dies. Planktonic grazers are perhaps very important also because they can regulate abundance, species distribution, community composition and productivity of many phytoplanktonic assemblages. Their effect on algal propagules remains to be studied. Comparatively more attention has been given to the effects of filter-feeders on the consumption of seaweed propagules. Through experimental killing of barnacles, Jernakoff (1983, 1985b) demonstrated that these filter-feeders did not affect algal settlement and recruitment. In contrast, mussels seem to be very important because they filter particles well within the size range of seaweed propagules (Seiderer & Newell, 1985). Several authors suggested (Dayton, 1973; Foster, 1975) and recently demonstrated (Santelices & Martinez, 1988) that mussels ingest and digest large quantities of marine algal propagules in some seasons. Owing to the methodological problems involved in quantifying the
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
231
volumes of water and algal propagules simultaneously reaching a given area of rocky habitat during incoming tides, Santelices & Martinez (1988) could not conclude whether or not the trophic activity of these filter-feeders could severely limit the general availability of algal propagules in the water column. They suggested, however, it would not be unexpected if consumption by mussels were found to limit settlement and distribution of algal species that produce or release reduced numbers of propagules. Both the potential effect of planktonic grazers and the effects of filterfeeders might have important community consequences by reducing the numbers of propagules in the water or selectively removing the propagules of some species. Variations in settlement have been recognised by a number of authors (Dayton, 1979; Underwood & Denley, 1984; Watanabe, 1984; Connell, 1985; Gaines & Roughgarden, 1985; Gaines, Brown & Roughgarden, 1985) as affecting patterns of population abundance and distribution and community organisation. Consumers of algal propagules might have an effect analogous to those described by Gaines & Roughgarden (1987) for barnacle settlement in central California. The kelp forests in this area harbour juvenile rockfish that prey on the larvae of invertebrates from the rocky intertidal zone. This predation reduces recruitment of barnacle populations to 1/50 of the level in the absence of fish and changes significantly the probability and strength of several ecological interactions among benthic species.
THE SPORE RAIN
As mentioned previously (p. 228), due to local conditions or to morphofunctional properties of the propagules, a variable number of them will precipitate as the clouds pass over a given habitat. Thus, a rain of propagules is probably common in many coastal habitats. The concentration of propagules (as the thickness of any rain) is envisioned to be variable from place to place, depending on the characteristics of the propagules as well as on the local environmental conditions. Most of the available evidence describes patterns of spore sinking under relatively calm water conditions and has been reviewed already in the previous section (p. 222). The density of the spore and of the water, the viscosity of the water, the radius and shape of the spore and the acceleration due to gravity, are all important factors when sinking in calm waters. In contrast, it seems that no one has measured algal propagule rain in the field and, therefore, there is little understanding of the factors affecting propagule sinking and attachment under natural conditions. The factors most likely to affect the process are reviewed below.
Water movement Most field conditions imply moving waters. This is especially true for the coastal habitats where the seaweeds live and where productivity is directly related to enhancement of diffusion provided by water movement (Conover, 1964; Doty, 1971). The water velocities in the surf zone are typically in the order 1–10 m·s1 (Denny, 1988), vastly greater than the swimming velocity expected for the
232
BERNABÉ SANTELICES
moving propagules of brown and green seaweeds. Therefore, sinking and attachment under those conditions seem difficult. The density of sporeling settlement, however, is notorious for being a fickle phenomenon. In any given time or season, certain stretches of coastline are inundated with settling propagules while adjacent stretches are not. The density of settlement may vary widely from year to year, but given the proper conditions, settlement appears to be an effective process. The flow mechanism most likely to account for the apparent effectiveness of settlement under moving water is turbulent mixing (Denny, 1988). Under those conditions, a propagule is freely moved by the water in many directions. Whenever the propagule encounters the water surface it is reflected back and whenever it encounters the rock substratum it sticks and settles. Therefore, even though the spore can be seen to move around freely in many directions, it is only the movement towards and away from the rock surface that affects settlement. For moving invertebrates, Denny (1988) has calculated that the mean time to settlement for larvae in the surf zone is directly proportional to the depth of the water and inversely proportional to the mean transport velocity towards and away from the rock surface. From the above formulation it is clear that any momentary reduction in turbulence, allowing for increased sinking of the propagules or any momentary change in the water conditions allowing for the predominance of net movement towards rocky surfaces will significantly increase the probabilities of settlement by free-floating propagules. Depth of the water column The depth of the water is a factor that has rarely been incorporated in studies on dispersal of algal propagules. Perhaps more important than the depth of the water column is the distance between the tissues producing and releasing the propagules (gametangia or sporangia) and the bottom. External morphological characters in the benthic algae generally represent a compromise of responses to several selection factors (Neushul, 1972a; Littler & Littler, 1980). It should not be expected, therefore, that the position of the reproductive tissues along the axes will be related only to increased sinking possibilities and not to other factors, such as grazing. Nevertheless, it is still unknown if such relationships exist and if any morphological characteristics of the branches bearing reproductive tissues in the algae are directly related to propagule release and dispersal. It is difficult to understand why, for example, populations of Macrocystis pyrifera exhibit well differentiated sporophylls close to the ground in some geographic regions (e.g. California, southern Chile) while in other areas (e.g. Australia) sporophylls are lacking, the spores being released from undifferentiated fronds floating several metres from the bottom. Substratum On many rocky intertidal surfaces, turbulent deposition of propagules seems to be a common and important phenomenon (Norton & Fretter, 1981). Under those conditions, several physical and topographic characteristics of the substratum are
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
233
particularly important for algal settlement. One such factor is substratum slope. This substratum characteristic determines to a large extent the amount of wave action that the algae have to withstand. It can also determine, therefore, the difficulties of settlement of new stages, especially on smooth rocky surfaces with few cracks (Knight & Parke, 1950). Substratum texture is also an important factor involved in the turbulence associated with deposition of propagules and one that is amenable to experimental analysis. For example, sand grains, sorted to particular sizes were used by Norton & Fretter (1981) to create rough surfaces on artificial substrata. They found that the settlement of Sargassum propagules was best on a surface with a mean depression depth of 800 µm, irrespective of water speed (0.22 to 0.55 m·s -1 ). The largest size depressions, as well as the absence of sand grains, allowed spaces big enough to be swept clean by water flow, rather than creating depositional eddies. Previous vegetation Depositional eddies are also perhaps generated by the vegetation present in a given habitat. Certainly the vegetation on wave-beaten rocks disrupts the laminar flow and allows for the permanence in many places of thin lenses and films of water, which might contain propagules in suspension and whose settlement could be facilitated by the disruption of the water flow. Sediments Wherever water movement conditions are most suitable for algal spore settlement, they are also likely to be favourable for sediment settling. Several authors (e.g. Lilly et al., 1953; Moss, Mencer & Sheader, 1973; Neushul et al., 1976; De Vinny & Volse, 1978; Norton, 1978) have found that sediments inhibit algal colonisation. Spores that settle on sediment particles are apt to be moved away before long, especially as they grow into faster moving water layers. Indeed, De Vinny & Volse (1978) found that even small amounts of sediments introduced before, or along with, the spores greatly reduced the percentage of spores able to settle and grow on glass slides. When cultures were shaken, either from the time when spores and sediments were added, or starting 1 day later, survival was greatly reduced. More recently, however, Kennelly (1983) has reported a positive correlation between siltation and algal cover, suggesting that siltation may be beneficial to the algae, possibly by supplying more nutrients or protecting the algae from water movement and grazers. These results, however, relate to field experiments where the quantities of sediment and the growth conditions used are very different from those used by De Vinny & Volse (1978). In Kennelly’s experiments the amounts of sediment were comparatively lower and allowed the establishement of an algal population under field conditions of water movement. Mucus trails
234
BERNABÉ SANTELICES
Mucus trails are produced by many different organisms. Those secreted by certain species of intertidal limpets are made up of carbohydrates. In some cases (Connor, 1986) they serve as adhesive traps for the microalgae which are consumed by the limpets. Nevertheless, not all molluscs that produce mucus trails consume the mucus and many devote significant portion of their energy budget to podal mucus production. The density of these invertebrates can be as high as several hundred individuals per m 2 of rocky surface. Therefore, their contribution to trapping and settlement of spores could be significant. Faecal pellets Experimental studies indicate that the algal fragments egested alive inside faecal pellets have some ecological advantages over free propagules (Santelices & Paya, 1989). In intertidal habitats, the sticky nature of the pellet allows for attachment to the substratum while protecting the contained algae from desiccation. In sub tidal habitats, the pellets sink 8 to 22 times faster than the fastest sinking algal propagule. When continuously immersed, the pellet disintegrates within 2–3 days, liberating the algal propagules. Quantification of swarmers and protoplast released from fragments of Enteromorpha in the faecal pellets of one species of mollusc (Siphonaria lessoni) indicates densities of about 217 germlings·cm -2 and values of 300–1500 propagules per pellet. Extrapolation of these results to field conditions based on number of grazers and faecal pellets, suggests production figures varying from 0.5–3.5×10 5 to 1.3– 1.5×10 6 propagules·m 2 ·12 h -1. These values are within known density ranges of settling spores in the field (Hruby & Norton, 1979). Thus, the process seems to be ecologically important, especially at seasons when the density of grazers increases and the normal reproductive activity of the algae being consumed decreases. Sea foam The sea foam so frequently found in intertidal habitats also could play a role. Sea foam has traditionally been considered (Pérès, 1982) to originate from nonliving organic matter rising to the surface from the bottom and intermediate waters, together with terrigenic eolian organic materials. It is now known, however, that kelp mucilage and phytoplankton exudate also contribute significantly to the sea foam formation and to foam stability (Velimirov, 1980). The high content of organic matter in the foam supports a multiplicity of heterotrophic bacteria and fungi. However, foam also contains phytoplankton (cyanophytes, flagellates, coccolithophorids, dinoflagellates, diatoms) and ciliates. No one, apparently, has reported algal propagules, but there is no a priori reason not to expect them in the foam formed in intertidal regions as the waves break against the rocks. Part of this foam can be cast up on shore by wind, remaining stationary on the rock and allowing for the settlement of the organisms and propagules contained in the foam.
ATTACHMENT
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
235
The initial step in the attachment of the spore consists of the binding of the propagule to the substratum, a process aided by the high viscosity mucilage that surrounds the spore upon release. The mucilage acts as a thin layer of liquid that wets the two solid surfaces (spore and substratum). The pressure within the mucilage is less than the pressure surrounding it (Baier, 1970), resulting in an adhesive action. After this initial step, the newly settled propagule rapidly empties the Golgiderived adhesive vesicles and secretes the fibrillar adhesive materials formed in the propagules before release (Peyriere, 1970; McBride & Cole, 1971; Chamberlain & Evans, 1973; Forbes & Hallam, 1979). In Enteromorpha, as the first cell elongates, differentiates rhizoids and divides, it releases a continuous secretion of cementing material (Bråten, 1975) of a different origin from that of the zygote. This secretion, as well as the development of rhizoids, helps to attach the individual to the substratum. In the case of Hormosira zygotes, the rhizoids appear 14 to 16 h after fertilisation (Forbes & Hallam, 1979) and they attach both by mucopolysaccharides and by physical interaction with the microtopography of the substratum surface. It is not surprising, therefore, that attachment strength increases with time (Charters, Neushul & Coon, 1972, 1973). Thus, experiments designed to dislodge settled spores show that the number of spores that are washed away with a certain shear stress decreases the longer they have been allowed to settle. Similarly, the degree of shear stress that a settled spore can withstand increases with time. Once maximum attachment strength has been realised, increasing the shear stress one order of magnitude has little added effect on spore removal. Attached spores of Gracilariopsis lemaneiformis can resist a dislodging force 100 times their weight (Charters et al., 1972). Salinity and temperature have been found to affect the attachment process and the release of the fibrillar materials (Christie & Shaw, 1968). It is likely, however, that many other factors that severely stress cellular functioning or modify the chemical structure of the adhesive materials also interefere with the attachment process. Mortality of settlers As mentioned above (p. 227), settlement of seaweed propagules seemingly has never been measured in the field. Spores are too small to be counted by simple optical devices. Even though underwater microscopes have been designed and used in the field (Neushul, 1972b; Neushul, Coon & Charters, 1972; Kennelly & Underwood, 1984), it is often difficult to make the pertinent observations in habitats with moving water. In addition, propagules may settle in cryptic habitats, such as crevices or among settled animals or algae, where direct observation is simply impossible. Therefore, the mortality rates of early settlers and the mortality factors involved are largely unknown. A few general statements can be made, however, based on ecophysiological studies of germinating propagules under laboratory conditions. Spores, like any other living organisms, exhibit upper and lower tolerance limits to ecological factors such as temperature, light dosages, salinity and desiccation. Spores settling in habitats where the levels of these factors, or the interaction among these factors, fall above the upper or below the lower tolerance
236
BERNABÉ SANTELICES
limits for spore survival, obviously would suffer widespread mortality. Specific examples of these circumstances can be found in many reviews on seaweed ecology (e.g. Boney, 1966; Santelices, 1977; Dring, 1982; Lobban, Harrison & Duncan, 1985; Chapman, 1986a). In recent years, grazing of germlings has emerged as a most important factor regulating algal distribution patterns but most of these studies refer to recruits rather than early settlers and they will be reviewed in the next section. It should be recognised, however, that gut content analysis of different types of grazers such as sea urchins (e.g. Lawrence, 1975; Harrold & Pearse, 1987) and molluscs (Steneck & Watling, 1982: Hawkins & Hartnoll, 1983) often reveals the presence of large quantities of seaweed spores. In many cases it is unknown if the grazer actively searches for spores or if they are ingested together with other types of algae. However, a few examples of propagule “specialists” are known to have important consequences in the patterns of algal distribution. This is the case of Cellana tramoserica in the intertidal communities of New South Wales, southeast Australia. Cellana is an obligate microalgal grazer (Underwood, 1980; Underwood & Jernakoff, 1981; Jernakoff, 1983), able to consume all spores that settle at some middle and upper intertidal levels. Below this level, spores are able to settle and grow at a rate that exceeds the rate at which Cellana can consume them. Thus, as more sporelings reach a refuge in size, Cellana has less area in which to graze. Since it is a propagule specialist, the grazer eventually starves to death if surrounded only by established algae. Higher on the shore, the rate of consumption of algal spores by Cellana far exceeds the algal rate of growth to a safe size. As it is clear from the above example, grazing activities can keep extensive rocky areas (the upper and middle intertidal in this case) devoid of macroscopic vegetation. In addition, the mortality effects of grazing on early settlers can interact with the effects of other ecological factors, such as desiccation. Ectocrines and allelopathic substances released by germinating propagules, other seaweeds that are already established or by diatoms may also induce mortality of settled spores. The active liberation of polyphenols (tannins) from certain marine algae has been shown to have severe antibiotic effects on bacteria and algae (Conover & Sieburth, 1966; McLachlan & Craigie, 1964). Similarly, when grown with diatoms, the discoid sporelings of Gigartina stellata showed high mortalities, usually correlated with marked increases in the population sizes of the accompanying diatoms (Huang & Boney, 1983, 1984). Even the dried diatom mucilage containing dead cells released compounds that induced mortality and affected the growth of Gigartina sporelings. In contrast, sporelings of some other seaweed species may produce substances inhibiting diatom growth. For example, under laboratory conditions, contaminating benthic diatoms may show profuse growth on slides, except in the vicinity of Chondrus germlings, around each of which clear zones could be observed after 6 weeks of culture (Khfaji & Boney, 1979). All of the above mortality factors are likely to interact in the field, partially determining some of the patterns of distribution in space and time exhibited by seaweeds. Thus the presence or absence and the density of a population of recruits depends not only on the availability of spores but also on the frequency of habitat units that provide the precise conditions required by a particular spore. For land plants these habitat units have been named “safe sites” (Harper, 1977). Such a concept can be extended to seaweeds. For seaweeds such a “safe
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
237
site” is thought to be that zone in which a spore may find itself and which provides the substratum and water movement condition required for spore attachment; the energy (light intensity and temperature) and materials (organic and inorganic fertilizers, growth hormones, CO ) required for the germination 2 process; and where specific hazards, such as grazers, competitors, toxic elements and pathogens are absent. A population of a particular species may be absent from an area either because it offers no “safe sites” even though spores are abundantly present, or because spores are absent although “safe sites” are abundant. Different densities of sporelings may result from different spores deposited in a uniformly “safe” environment or a different frequency of “safe sites” when spores are abundant. In summary, the evidence on spore settlement suggests the existence of biologically important phenomena—such as the spore cloud or the spore rain— of very recent conceptualisation and whose importance for ecological processes may be very significant. So far, they have provided an alternative explanation for patchy patterns of distribution in various habitats. The evidence also suggests that a diversity of factors affecting sinking rate and attachment of seaweed spores has yet to be explored in order to evaluate their ecological importance. Mortality factors affecting early settlers seem to determine for seaweeds the equivalent of the “safe site” concept proposed for land plants.
RECRUITMENT In biology recruitment means the addition of individuals to a unit of population (Doherty & Williams, 1988). For marine organisms with planktonic larvae, recruitment refers to the recently settled juveniles that have survived for some time after settlement (Keough & Downes, 1982; Connell, 1985). Recruitment thus combines settlement with any early mortality that has occurred on the substratum up to the time of the first census. The distinction between settlement and recruitment was first formulated for sessile invertebrates (Keough & Downes, 1982) because it was not always obvious that settlement could be measured with sufficient accuracy by recruitment. The distinction between each process was considered useful for the study of population and community effects of differential settlement as well as for evaluating the possibilities of early mortality in different parts of an organism’s habitat. It should be realised, however, that following this operational approach, the period between settlement and recruitment does not correspond to a true lifehistory stage but reflects the limitations of the observer (Keough & Downes, 1982). Consequently, and depending on the observer’s interests and limitations, recruitment studies on algae have been made at variable post-settlement periods, including weeks (e.g. Hruby & Norton, 1979; Kennelly, 1987a,b; Reed, Laur & Ebeling, 1988), months (Kennelly & Larkum, 1983; Shannon, Crow & Mathieson, 1988), seasons or years (DeWreede, 1984; Foster, 1975) or in general when the new recruits have reached a size that was visible to the unaided eye (Chapman, 1984; Santelices & Ojeda, 1984a,b,c).
238
BERNABÉ SANTELICES
The variability of these methods is important for at least two reasons. The relative importance of various ecological factors (e.g. intraspecific competition, crowding, sensitivity to grazing) changes with thallus growth and age and with population development. Therefore, results on ecological determinants obtained with early recruits do not necessarily apply to more advanced stages of development or explain the observed patterns of distribution of adult organisms or of community structure. In addition, it is becoming increasingly clear that many seaweed species may suspend growth of their microscopic stages after germination. Seemingly, the early developmental stages are able to persist throughout periods that are stressful for the macrothalli. Thus, although these stages will be considered to be recruits by observers at the microscopic level, they will be generally ignored by those looking at macro-forms. The presence of these early developmental stages with suspended growth, together with the existence of microscopic forms that are alternate phases in the life history of previously identified macroscopic species, and of propagules in different degrees of development have led to an awareness of the common existence everywhere of a huge, unseen population of microscopic stages which are not usually identifiable. By analogy with the seed bank of land plants (Harper, 1977) this has been named the bank of microscopic stages of seaweeds (Chapman, 1986a). This section reviews the information related to post-settlement events in benthic algae. It starts with germination processes, followed by an analysis of the scattered information on the bank of microscopic forms and concludes with the factors that experimentally have been shown to affect recruitment in the field.
GERMINATION
Some time after attachment, the settling propagule germinates. Under laboratory conditions, (e.g. Kain, 1969; Perez, 1971; McLachlan, 1974; Lüning, 1980a,b, 1981a; Hoffmann & Santelices, 1982; Hoffmann, Avila & Santelices, 1984; Anderson & Bolton, 1985; Correa, Avila & Santelices, 1985) spores start to germinate within 24 h after settlement, but the germination process can extend for several days (5–7) after inoculation. The manner in which algal spores germinate has been especially well described because many authors have thought the pattern to be of diagnostic value in determining taxonomic and phylogenetic relationships (Oltmanns, 1904; Killian, 1914; Chemin, 1937; Inoh, 1947). Even though it is now understood that germination patterns within algal groups are too heterogeneous to be considered as a diagnostic character at any taxonomic level (Dixon, 1973; Gabrielson & Garbary, 1986), the variation is not unlimited. Furthermore, when the external morphology of some of these germinating spores is compared, some parallels can be found among green, brown and red algae. For example, in all three algal groups, spores can divide and develop directly into erect, uni- or multicellular tubes or filaments. Often, but not always, the first cross-wall divides the cell into an erect initial and rhizoidal initial. In another pattern, also represented in the three groups, the germinating spore develops a tube into which the protoplasm may or may not move and which may or may not be separated from the original spore by a cross wall. A filamentous or a discoid germling is formed later from one or both cells which subsequently
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
239
forms the erect and prostrate thalli. In still other cases, the germinating spores segment and produce regular or irregularly shaped crusts or a multicellular mass of cells resembling the morula stages of animals. With few exceptions, the adaptive values of these differences in spore germination are largely unknown. Experimental studies on plant-herbivore interactions (e.g. Lubchenco & Cubit, 1980; Slocum, 1980) suggest that crustose morphologies survive better under some grazing conditions. Similarly, the development of an erect filament without first producing a creeping stage would be understood as an adaptation allowing the filament to grow beyond the boundary layer in areas of higher diffusion gradients and nutrient exchanges. However, experimental data are lacking for the interpretation of the ecological meaning of the morphological patterns of spore germination in most seaweeds. In a few cases, explanations have been attempted, for example, Moorjani & Jones (1972) noted that most of the spores of Jania rubens attached to artificial substrata within 4.5 h after shedding, while those of Corallina officinalis did so only after 36–48 h. Upon germination, the upright axis of Jania developed from a basal disc of limited size within 7 to 8 days, while in Corallina, a widely expanded basal crust produced axes only after 12 to 13 weeks. The more rapid attachment of Jania spores, their limited basal development and early initiation of the axis were correlated with the epiphytic habit of the species and the tendency to grow on an inherently short-lived substratum. In brown algae, Pedersen (1981) suggested that stellate germination patterns could be regarded as adaptations to epiphytic habits. The same author recognised, however, that many species considered to be epiphytes do not have this type of germination. Furthermore, stellate germination seems genetically determined but, in some cases, it also seems to be triggered by contact with the substratum. Numerous investigations have been made on the effects of different environmental factors on the growth of sporelings of benthic algae and some also have described factors that affect spore germination. Rather than attempting a comprehensive review of all of those studies, the following account stresses certain common patterns emerging from some of these results. Even though the saturating light intensity for germination of spores varies from one to another species, it is well known that elevated irradiance or direct exposure to sunlight is generally damaging or lethal for them (Chemin, 1937; Jones, 1959; Burns & Mathieson, 1972). They may also be sensitive to extended long days or to a combination of both light effects (Boney & Corner, 1962). This extreme light sensitivity is perhaps related to shady habitats, either on the bottom at some depth from the surface, or underneath other algal canopies, where the propagules settle and germinate. Besides deleterious effects at the upper limits of light intensity, several studies have reported that germination of the propagules is unaffected by different levels of light (e.g. McLachlan, 1974; Correa, Avila & Santelices, 1985). Spore germination in many species is a seasonal phenomenon Thus, although the species might be fruiting all year round, only the spores released at a given time of the year are successful in generating new individuals. Several different ecological factors seem to be involved in this periodicity. For example, temperature was thought by Barilotti & Silverthorne (1972) to determine spore germination in the populations of Gelidium robustum from Baja California. In the case of Spyridia filamentosa, the tetraspores did not germinate under short day conditions although they remained alive in the culture medium for 1–2 months
240
BERNABÉ SANTELICES
(Provasoli, 1965). When brought into long day photo-regimes, however, they germinated. The nutrient concentration of the medium seems to have little effect on the germination process. For example, the meiospores of Lessonia nigrescens showed essentially similar germination percentages when incubated under different concentrations of nitrate and phosphate (Hoffmann, Avila & Santelices, 1984). In this species the germination process probably depends on the internal nutrient reserves of the meiospores, which is not modified by the concentrations of nutrients in the culture medium. As described in the next section, however, the development of the germlings is strongly influenced by nutrient concentrations. In a number of algae of the genera Antithamnion, Bonnemaisonia, Spyridia, Acrochaetium, Hypnea, Rhodochoton, Ceramium and Pachymeniopsis, the tetraspores in a sporangium occasionally germinate together and fuse within the sporangium jointly forming a single germling. This germination pattern was named syntagmatic spore germination (Tokida & Yamamoto, 1965) and it can cause important morphological modifications, because the resulting germlings may fuse and grow into lateral proliferations (Norton, Mathieson & Neushul, 1981). Some authors (Rao, 1969) have suggested that syntagmatic germination perhaps results from reduced water movement and hence insufficient dispersal of spores after release. The process is probably more complex, however, because germination in situ starts before spore release.
THE BANK OF MICROSCOPIC FORMS
Several lines of evidence have led to the idea that there is a bank of microscopic forms of seaweeds in many habitats. When the culture studies of Porphyra (Drew, 1949) showed that there was an alternate, filamentous, microscopic phase (Conchocelis) in the life history, that phase was expected to occur in the natural habitats of the leafy forms and perhaps deeper as well. In the subsequent 45 years, many life history studies of green, brown and red seaweeds (reviewed by Tanner, 1981; Pedersen, 1981, and West & Hommersand, 1981, respectively) have revealed the existence of alternate, microscopic phases for a diversity of macroscopic forms. As in Porphyra-Conchocelis, these microscopic phases are expected to occur around the habitat naturally occupied by the macroscopic forms and in many cases the microscopic phase has been found after adequate search. Additional evidence for the existence of a bank of microscopic forms has arisen from laboratory incubation of stones and peebles seemingly devoid of seaweeds. As early as 1958, Burrows obtained high densities of Laminaria and other species growing on field collected stones that had been incubated in enriched sea water. At the time of collection, the stones lacked any macroscopic vegetation. Similar results were obtained by Neushul & Dahl (1967), by incubating stones collected in a Macrocystis bed that were devoid of macrovegetation. In fact, Neushul (1972a) recognised that a diversity of filamentous forms, often microscopic, occur in the boundary layers of natural habitats. The filamentous morphology could be a manifestation of competition for nutrients in the slow moving waters of the boundary layer.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
241
The possibility of persisting as a microscopic form with suspended growth is generally recognised as an adaptation of the algae to survive through conditions stressful for the macroscopic thallus. This has been particularly well explored with young and microscopic stages of Laminariales. In the field, the kelps frequently shade their own recruits. Early measurements of light intensities in Macrocystis (Clendenning, 1961) and Laminaria forests (Kain, 1966; Smith, 1967) suggested intensity values far below the optimum required for active growth of young sporophytes. In fact, from 222 light determinations measured over 2 years in open waters at depths typically inhabited by Macrocystis, Anderson & North (1969) concluded that bottom light intensities could be limiting for growth about 50% of the time, but without preventing kelp establishment. These low light conditions allow these microscopic stages to persist until the limiting conditions change and growth is resumed. An additional example has been reported from Port Erin Bay, U.K. Here, the reproductive sporophytes of Desmarestia aculeata gave rise to microscopic gametophytes during winter. The further development of these microscopic stages is suspended until spring (Chapman & Burrows, 1970) when the light irradiance increases. The winter levels of illumination in the field (40 g cal·cm 2 ) induced a suspended state of development when tested in laboratory experiments. Similar suspensions of growth or development have been found in many species of brown and red algae (Burrows, 1971; Sheader & Moss, 1975; Schonbeck & Norton, 1980; Novaczek, 1984a,b). In some cases the limiting factor could be light, in others (e.g. Ecklonia radiata) it could be temperature, in still others, as discussed earlier, it could be photoperiod or nutrients. The time of suspended growth can vary from a few days to several months. For example, Schonbeck & Norton (1980) have reported finding viable microscopic Pelvetia germlings beneath adult stands of the same species 8 months after the end of the fertile season. Although comparatively fewer data have been produced, evidence indicates that the same condition also applies in tropical latitudes and coral reefs. While studying the phenology of six species of Gracilaria in Caribbean waters, Hay & Norris (1984) found that for most species there was a 4- to 5-month delay between the reproductive peak in December-January and the increase in plant density in late April or early May. The most probable explanation suggested for this lag was the persistence of early development stages in a state of suspended growth. Grazing can also contribute to the existence of a bank of microscopic forms by cropping the macroscopic thalli as soon as they are produced. One such example has been described by Lewis, Norris & Searles (1987) for Padina jamaicensis in Belize. The grazing activities of parrot fishes maintain these populations with a highly branched turf morphology. When protected from grazing, the plants develop an erect, foliose morphology. However, this process is conceptually different from that of suspended growth. Microforms caused by grazing are the result of consumption rather than suspension of growth and they probably do not result from growth or metabolic adjustments. A bank of microscopic forms of macroalgae exhibits some similarities with the general characteristics of the seed bank of land plants. As in the case of these latter organisms (Harper, 1977), the number of individuals present as microscopic forms with suspended growth vastly exceeds the numbers present as growing individuals. Since propagules are continually added by the propagule rain, the bank represents
242
BERNABÉ SANTELICES
a record of past as well as present vegetation growing in the area. As in land plants, perhaps this bank of microscopic forms can be regarded as a “deposit account” a source from which new vegetation may quickly arise if the existing stand is destroyed. Other comparisons, however, are difficult to make owing to the lack of studies of the general ecological characteristics of the microscopic stages of seaweeds. For example, in land plants, the seeds are lost from the seed bank due to predation, pathogen attacks, decay, germination or old age. With the microscopic forms of seaweeds it could perhaps be expected that pathogen attacks, decay and growth also could be important, but how age or grazing could affect their survival is largely ignored. Similarly, it could be anticipated that allelopathic effects and competitive interactions could be comparatively more important among the microforms of the seaweeds than among dormant seeds of land plants in a seed bank. The bank of microscopic forms seems to exhibit conspicuous differences from the concept of a seed bank of land plants with respect to some community characteristics. The buried seed population of mature or climax land communities generally contains a living, although dormant and heavily biased, record of the past vegetation history of the succession (Harper, 1977). In general, the species of early successional phases contribute more to the buried population than do the dominant species of the more mature phase. The pioneer species of succession commonly lie dormant, ready, as it were, to initiate the next succession after some disaster has destroyed the mature system. Species which have pioneered the succession are strongly persistent in the soil and so appear as pioneer species in the next succession of the area. This seems not to be the case in seaweeds, where the pioneer species seem to be poorly represented in the bank of microscopic forms. Their characteristics as pioneer species seem more related to their dispersal mechanisms and to their reproduction and growth capabilities (Sousa, 1984). However, as mentioned before (p. 240), the species dynamics in the bank of microscopic forms have not been the subject of detailed ecological studies, and most of the above conclusions should be regarded as tentative. The recognition of a bank of microscopic forms of benthic algae in many habitats poses some serious questions with respect to those studies that have followed seaweed recruitment on artificial substrata (glass slides, ceramics, bricks). Such studies disregard the ecological roles of the bank of microscopic forms in the establishment of the local vegetation.
EXPERIMENTAL STUDIES ON RECRUITMENT
In recent years an increasing number of studies have been able to isolate and experimentally evaluate the effects of one or a few ecological factors on the recruitment of benthic algae. Owing to logistic problems, it has not always been possible to evaluate all the interactive effects among these factors, but the accumulated information often points to such interactions. The role of abiotic factors
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
243
The limiting effects of abiotic factors on algal recruitment have been especially well studied in some stressful habitats, such as upper intertidal rocky surfaces or in the bottom of Macrocystis beds. The idea that only certain species have the ability to withstand the environmental stress characteristic of the intertidal zone has been implicit in the literature since Doty’s (1946) formulation of the critical tidal factor hypothesis. While attempting to test this hypothesis, several authors (Townsend & Lawson, 1972; Edwards, 1977; Hruby & Norton, 1979) have experimented with seaweed propagules attached to glass substrata. The slides with propagules have been lowered into and out of tanks of enriched sea water in a way that simulates submergence and emergence on intertidal shores. The results of these experiments have been somewhat variable because, as Chapman (1986a) has noted, authors have used atmospheres with different levels of water saturation in their experiments. Perhaps the most realistic and accurate approximation has been that of Hruby & Norton (1979) who simultaneously studied the propagule abundance in the water, the species distribution in the field, the recruitment of thalli on experimental slides placed at different vertical levels of the shore and the survival and distribution of recruits in a tide-simulating machine. They concluded that regardless of inoculum availability, only those species normally found in the littoral fringe or at the top of the eulittoral zone colonised the slides placed at these intertidal levels. Species of Spongomorpha, Ceramium, Gelidium and Sphacelaria were never seen in the field above the 2.40-m level, and although their propagules were frequently found in the water samples, they never colonised slides placed at the 2.49- or the 2.89-m level. The authors concluded that even though they settled, the abiotic stress eliminated the susceptible species within a few days. These results were later confirmed through experiments in a tidal simulator. The three upper intertidal species, Ulothrix pseudoflacca, Blidingia minima and Prasiola stripitata all survived at higher levels than did the middle intertidal Enteromorpha linza. Furthermore, Ulothrix pseudoflacca survived at higher levels than Blidingia minima, while Prasiola stripitata survived highest of all. This distribution pattern was correlated with the field distribution of these species. In their experiments, Hruby & Norton (1979) also found that if the sporelings of Blidingia minima were incubated completely submerged for 2 weeks and then placed in the simulated tidal regime, they could survive higher on the plates than those put on the simulator immediately after settlement. These results suggested that the earliest stages are the most vulnerable to environmental stress. Similarly, sporelings survived higher on plates with high recruit densities than on those with lower densities. This density-dependent effect was observed when spores densities differed by a factor ranging from two to ten. Such variability in survival would reinforce the patchiness in species distributions introduced by other means, and may help to explain the prevalence of patchiness in many rocky shore communities. Abiotically induced mortality of the uppermost individuals in each of these intertidal populations might occur weeks or even months after settlement. For example, the intertidal-shallow subtidal kelp Lessonia nigrescens in central Chile is able to recruit in a vertical range wider than the one occupied by adult individuals (Santelices & Ojeda, 1984a). Within 1 month after the recruits have
244
BERNABÉ SANTELICES
reached a size visible to the unaided eye (late winter), the recruit densities of the uppermost levels were between 1/4 and 1/2 the values found in the middle and the low levels of the Lessonia zone. The survival and mortality curves for both populations were similar during spring months, but the day-time low tides coupled with the increased solar radiation and increased temperatures occurring during late spring and early summer decimated most of the uppermost intertidal individuals. A few plants can occasionally survive, generally as dwarf, infertile individuals, in small pools that retain some water during low tides. Similar recruit limitations due to intertidal abiotic extremes have been described also by Dayton (1971), Schonbeck & Norton (1978) and Lubchenco (1980). In deeper waters, where light and nutrients can be limiting, the combination of factor levels required for successful recruitment, the so-called “recruitment windows” (Deysher & Dean, 1986) occur infrequently. The concept was developed while working with artificial substrata inoculated in the laboratory with zoospores of Macrocystis pyrifera and planted out at field stations with various levels of temperature, irradiance and vertical seston flux. Recruitment of sporophytes at densities representing sporophyte production at approximately 0.1% of the planted out female gametophytes, occurred at temperatures below 16.3°C and irradiation levels above 0.4 E·m -2·day -1. These limits constitute the recruitment windows for this species. Based on laboratory results which previously had shown sporophyte recruitment between 11 and 19°C, high densities of sporophytes were expected at field temperatures of 17°C. However, low fertility values were observed at that temperature, suggesting that some factor correlated with temperature was inhibiting recruitment at higher temperatures. Nutrients were supposed to be the factor and experiments with nutrient enrichment were developed. Enrichment of nitrogen and phosphorus in the vicinity of the gametophyte population increased sporophyte recruitment, albeit at low densities, up to temperatures of 18°C. Even though Deysher & Dean (1986) could define the recruitment window based on the direct effects of light and temperature and the modifying effects of nutrients, they suggested that other factors might play a role as shown by a lack of recruitment on artificial substrata during some apparent window periods. Wave surge was thought to be a potential candidate as high surge would increase the abrasion of seston particles, especially on the bottom, and thereby increase the mortality rate of gametophytes and recruited sporophytes. Various biological factors, such as grazing and the settlement of other organisms, could also adversely affect recruitment. The effects of substratum Among the abiotic factors influencing seaweed recruitment, substratum deserves special mention because it has been studied in greater detail. Similar experiments often have yielded variable results, seemingly because substratum topography can interact with other factors in determining algal recruitment. Surface roughness has been one of the substratum properties under analysis. In 1953, Ogata reported that the settlement of coralline algal spores on glass substrata in shallow water was enhanced by surface roughness of the order of 0.5 to 0.75 mm. When Foster (1975) placed experimental plates in a Macrocystis forest in California, however, he found that variations in the order of millimetres
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
245
had little effect on algal colonisation. Topographic variations in the order of centimetres, on the other hand resulted in increased numbers of Macrocystis pyrifera sporophytes and higher algal diversity and sessile animal biomass on his experimental plates. The lack of effect of surface roughness of the order of millimetres was explained by a reduction in light (Foster, 1975). These plates were placed at deeper levels than those used by Ogata (1953) and inside a kelp bed. Therefore, the light reductions in crevices and grooves probably more than compensated for any increase in spore settlement. Alternative explanations were later offered by Harlin & Lindberg (1977) to explain some of their experimental findings. They used three grades of discrete monolayers of sand particles differing only in diameter (0.1–0.5 mm; 0.5–1.0 mm; 1.0–2.0 mm) which were cemented to the surface of three quadrats on acrylic discs. One smooth control was also used. They found that the initial settlement did not differ significantly among the experimental surfaces, but with time the patterns in the distribution of these populations correlated with the type of surface beneath them. Dominant species in the area, Chondrus crispus and Ulva lactuca mostly appeared on the two surfaces with the largest particles. Populations were considerably smaller on the smallest grained discs, and on the smooth quadrats only a few individuals of these two species appeared. Several alternative explanations were offered for these results. Larger particle size might provide larger areas on which to settle, the interstitial space may be critical in providing resistance to desiccation at low tide, or the particles may cause small eddies that facilitate spore settlement. The interstitial space could also serve as a trap for detritus. Organic matter could be caught more easily among the larger particles than the smaller ones and any electrical charge from the adsorbed organic constituents would be greater on the surface with the greater relief. If algal settlement is influenced by electrical charge, this difference could offer an additional explanation for the greater affinity of algae for these sizes. In agreement with the early results by Ogata (1953), Harlin & Lindberg (1977) found that Corallina officinalis showed optimal development on the smallest particle size. It is possible that the optimum particle size for recruitment also changes with the species being considered. The effect of edges (called the edge or border effect) on algal settlement is the second aspect of substratum topography that has been studied. Working with experimental blocks, Foster (1975) described a distinct difference between the algal abundance near the upper, horizontal edges and on the flat areas of blocks. The number of sporophytes was significantly higher within 1 cm of the edges than on areas further away. These changes in species composition and abundance were explained on the basis of changes in water-flow patterns (Foster, 1975). Turbulent eddies result from flow separation associated with water movement over edges. Water speed in these eddies is lower than in the laminar flow region over the central, flat portion of the blocks. This reduction in speed may enhance spore and larval settlement. Water speed is also reduced in areas where the flow meets vertical or sloping obstructions, and this could contribute to additional settlement near the edges. In addition, the eddies entrap and concentrate particles and this may enhance settlement. This type of experiment was later repeated by Kennelly (1983) with larger plates (0.12 m 2 ), some of which were protected from fish grazing by cages. The pattern of establishment of algae was such that no edge effects were detected
246
BERNABÉ SANTELICES
within the first 4 weeks. Thereafter, more algae were growing on the edges than in the middle portions of uncaged plates, but no edge effect was found in the grazer-protected plates. One alternative explanation advanced was that these differences were caused, as predicted by Foster (1975) by differences in water movement between the plates’ edges and the middle parts, leading to an increased availability of nutrients in the micro-eddies formed on the edges. The absence of this response in the caged plates could be explained by disruption of the micro-eddies on the edges of the plates as a long term artifact of caging. Kennelly (1983) suggested, however, that an alternative explanation for his and Foster’s results is grazing. In his experiments, herbivorous fishes could have preferentially grazed the plates in the middle, after the algae had reached a certain size. Such a circumstance could explain both the lack of an edge effect on all sorts of plates during the first weeks of experiments and the later appearance of an edge effect on the unprotected plates only. Clearly the subject requires additional experimental work. Substratum texture could affect algal recruitment in still another way. In intertidal habitats, crevices may provide refuges from desiccation and/or grazing of algal spores. Experimental manipulation of crevices by filling up middle and upper intertidal crevices with fibreglass resin (Jernakoff, 1983) showed that crevices may be important during spring and autumn as refuges from desiccation, but only if grazers were absent. Grazing The limiting effects of grazing on algal recruitment have been anticipated in the section on settlement. Almost every major type of grazer (e.g. echinoids, molluscs, amphipods and fishes) have been shown to be able to limit seaweed recruitment in different habitats. The effects of grazing by echinoids in kelp forests and by molluscs in intertidal habitats have been studied in greater detail than other species and will be discussed briefly in the following paragraphs. Echinoids on rocky bottom habitats throughout the world can greatly reduce the standing stocks of marine plants by means of their grazing activities (see Lawrence, 1975 and Harrold & Pearse, 1987 for reviews). Often this intense grazing leads to the complete removal of benthic macroalgae from rocky substrata. What remains is apparently bare rock with encrusting coralline algae, an alternate state (sensu Sutherland, 1974) often named “barren grounds” (Pearse et al., 1970), “isoyake” (Noro, Masaki & Akioka, 1983) or “coralline flat” (Ayling, 1981). Persistence of echinoid populations in these overgrazed areas may be due to a number of physiological and behavioural traits, including the ability of echinoids to reduce somatic and gonadal tissue development (Lang & Mann, 1976) or even reabsorb their own tissues (Johnson & Mann, 1982). More important for seaweed survival, some species have the ability to graze on microalgae (Breen & Mann, 1976; Chapman, 1981). In so doing, they are able seriously to affect seaweed recruitment by consumption of microscopic stages. If echinoid populations persist in the barren areas and continue their grazing activities, these barren areas may persist for years. But if grazing pressure is relaxed, either due to declining echinoid population or behavioural changes, seaweeds may recruit and an algal-dominated assemblage may develop.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
247
In many of the cases studied, the grazing activities of sea urchins remove almost all the benthic macroalgae in the area (see Harrold & Pearse, 1987 for examples). In other cases, however, the effects of grazing are more complex, and factors such as echinoid food preferences and temporal and spatial escapes from grazing may influence the persistence of some vegetation. For example, in Torch Bay, Alaska, Duggins (1980) described patches of vegetation dominated by annual kelps which were able to persist because they rapidly recruit into areas temporarily free from echinoids. In a few cases, kelp recruits into overgrazed areas without a corresponding decline in echinoid population. In Torch Bay, Alaska, two species of echinoids ceased active grazing of the substrata and fed on salps and filamentous diatoms when these alternate food items become available (Duggins, 1981). Several species of brown algae could then recruit, with no corresponding decline in grazer abundance. In California, Harrold & Reed (1985) described how echinoids moved from open to protected crevice microhabitats. Unusually intense algal recruitment overwhelmed the capacity of echinoids to consume all macroalgae, which further enhanced algal recruitment and allowed full development of a kelp forest. In intertidal habitats of temperate latitudes, molluscs are the most important grazers (Hawkins & Hartnoll, 1983) and their limiting effects on seaweed recruitment have been repeatedly described for such latitudes (e.g. Zaneveld, 1969; Dayton, 1971; Underwood & Jernakoff, 1981). In common with barren grounds, almost 100% mortality for several seaweed species subjected to molluscan grazing has been documented. The limiting effects of grazers on the upper and middle intertidal vegetation on the rocky habitats of southeastern Australia (Underwood & Jernakoff, 1981; Jernakoff, 1983, 1985a; Underwood & Jernakoff, 1984) which were discussed previously are a good example of such mortalities. Other examples are the experiments reported by Vadas (1986) with Ascophyllum nodosum. Survival of artificially recruited zygotes on natural or pottery chip surfaces was virtually non-existent, except when protected from intertidal snails. As suggested previously, crevices may provide refuges from grazing for algal spores. For example, as early as 1950, Burrows & Lodge suggested that the movements of the limpet Patella vulgata could be physically restricted by the presence of barnacles such as Balanus. Therefore, crevices among barnacles could be important refuges for algal propagules from the grazing limpets. Similar suggestions were made by Choat (1977). Schonbeck & Norton (1980) and Lubchenco (1980, 1983) experimentally tested this idea, finding that the few survivors of molluscan grazing were the individuals that had settled in rocky crevices. Escape was achieved not only by settling in cracks but also by elongating rapidly to sizes that escape grazing. The protective effects of crevices on seaweed recruitment depend, however, on the size of the grazer relative to the size of the crevice. For example, Cubit (1975) found that Littorina littorea could use crevices for shelter, browsing on and reducing the green algal cover found in nearby barnacle-dominated levels. Similarly, the exclusion of Patella from middle and upper intertidal levels by Hawkins (1981) did not result in increased algal cover because high densities (over 4000 ind·m-2) of the small-sized Littorina neglecta remained in the rocks using crevices as shelter. A similar condition exists in the intertidal areas of southeastern Australia (Jernakoff, 1983). On this coast Littorina unifasciata and Patelloidea latistrigata
248
BERNABÉ SANTELICES
are highly efficient at finding and consuming propagules (Underwood, 1981; Jernakoff, 1983, 1985a). Rough topography or crevices amongst barnacles provide germlings with little shelter from being grazed. Even the largest limpets are able to maintain a home scar on the side of barnacles, and crevices appear to be entirely accessible to these grazers (Creese, 1982). In many of these areas, therefore, the patchy distribution of algae is thought to reflect areas where the spores have “escaped” being grazed. Many of these specialised spore consumers are unable to graze upon grown thalli. Therefore, any propagule that initially escapes being grazed has a possibility of surviving subsequent encounters with the grazers.
Intraspecific interactions Field experimental studies have revealed both negative and positive intraspecific interactions among seaweed populations which seem to be important to the recruitment process. One form of negative interaction is crowding and overshading among conspecific individuals growing in close proximity in a given habitat. Seaweed recruitment is often fickle, with large numbers of recruits appearing in a given area. Their density gradually decreases with time, as their sizes increase, suggesting a densitydependent survival. This factor seems to be most important in ecological situations with reduced grazing or reduced disturbances. Such an effect has been experimentally tested for Egregia laevigata (Black, 1974), Leathesia difformis (Chapman & Goudey, 1983) and Lessonia nigrescens (Santelices & Ojeda, 1984c). Experimental thinning of individuals in Egregia laevigata resulted in significantly greater growth rates when compared with the control populations. In the case of Leathesia difformis, experimental thinning reduced mortality. In control plots the rate of mortality of this last species increased as crowding increased and the plants detached one another. Experimental thinning of the uppermost intertidal individuals in the Lessonia nigrescens band increased survival and allowed for a downward extension of the lower limit of the belt. In control plots the lowermost individuals exhibited decreased growth rates and increased mortality due to holdfast overgrowth by fast growing individuals and dislodgement by wave impact of dwarf, slowgrowing plants. The negative effects of algal canopy on juvenile recruitment have been shown in a number of brown algae, including species of Macrocystis (Rosenthal, Clarke & Dayton, 1974; Pearse & Hines, 1979; Dayton et al., 1984; Reed & Foster, 1984; Santelices & Ojeda, 1984b,c), Egregia (Black, 1974), Durvillaea (Hay & South, 1979; Santelices, Castilla, Cancino & Schmiede, 1980), Laminaria (Velimirov & Griffiths, 1979), Ecklonia (Kirkman, 1982; Kennelly, 1987a,b,c) and Lessonia (Santelices & Ojeda, 1984a). The mature canopy can influence recruitment of conspecifics in at least two ways. Species with dense, floating canopies, such as Macrocystis, reduce irradiance reaching the bottom to levels below those required for the recruitment and growth of sporophytes. Species with hanging canopies such as Laminaria and Lessonia can, in addition, affect recruitment, by the sweeping action of their fronds. Even though these negative effects of an established canopy on juvenile recruitment have been reported almost exclusively in large Phaeophyta, not all of
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
249
them exhibit such a response. No negative relationship between density of adults and recruits were found either by Chapman (1984) or Smith (1986) in Laminaria digitata or in L. longicruris. This example is interesting, in addition, because in L. longicuris there was a close linear correlation between the number of spores produced (over different time periods in the year) and the number of microscopic benthic recruits. Therefore, and contrary to all other known cases of brown algae, cutting of mature plants in this species would result in a proportionate reduction in juvenile recruits. Intraspecific interactions affecting recruitment, however, do not only involve negative responses. The already mentioned observation by Hruby & Norton (1979) that sporelings of Blidingia minima could survive higher on plates with high recruit density points to positive intraspecific interactions. Along the same line of thinking, Schiel & Choat (1980) found that for Ecklonia radiata and Sargassum sinclairii, plant size was positively correlated with density on a shallow subtidal reef. Based on these results they concluded that density affects marine and terrestrial plants differently and suggested that these differences were due to protection from wave shock and the differences in plant-arthropod associations. Opposite results were, however, found by Cousens & Hutchings (1983) working with monospecific stands of several other seaweed species. They found that mortality increased with density. Two years later, however, Schiel (1985b) reported on his monitoring of naturallyoccurring monospecific stands of Sargassum sinclairii and Carpophyllum maschalocarpum, finding that the individuals of both species grew faster and attained a larger size in the highdensity stands. The reasons for the improved growth at higher density were not clear, but Schiel (1985b) suggested that perhaps competition for light was reduced, nutrients were not differentially limiting or perhaps some protection was afforded from severe water movement. Even though his results clearly pointed to intraspecific positive interactions, Schiel (1985b) anticipated that the assessment of plant performance with respect to density in marine environments would probably be modified as more experiments were done. Even if there appeared to be few detrimental effects and several advantages to being in dense aggregations, he anticipated that there was obviously a limit to how many individuals may be packed into an area without negative consequences. In contrast to land plants, however, the answer to how many individuals may be packed into an area without negative consequences is by no means obvious in seaweeds. While much of the controversy so far has involved mainly brown algal species, many red algal taxa, including species of Chondrus, Gigartina and Gracilaria show sporeling coalescence during early growth (Jones, 1956; Tveter & Mathieson, 1976; Huang & Boney, 1984). In many of these cases the central erect axes (individuals?) show more vigorous growth than the peripheral ones. Similarly, experimental cultivation of some economically important species of Gracilaria have shown that growth rates increase with decreasing inter-thallus distances up to the minimum experimentally tested (5 cm) (Santelices & Fonck, 1979). Compared with the peripheral thalli the central thalli, in these experimental quadrats also exhibited increased growth in a way similar to coalesced sporelings. In this last case the protection of the central axes by the peripheral thalli was suggested to be related to sediment deposition, grazing and/or high nutrient concentrations. Thinking along the same lines, Smith, Nichols & McLachlan (1984) found that by interposing at very short inter-thallus distances the long and
250
BERNABÉ SANTELICES
flexible thalli of Gracilaria domingensis between the more rigid, but economically useful G. debilis, they could successfully cultivate the latter species protected from the otherwise deleterious sediment. Depending on the species and habitat, therefore, intraspecific positive interactions can be expected in seaweeds. Up to now the controversy on the subject (e.g. Schiel & Choat, 1980, 1981; Brawley & Adey, 1981; Cousens & Hutchings, 1983; Schiel, 1985b) has been heavily influenced by the —3/2 thinning law described for land plants (Harper, 1977). Perhaps a more productive approach would be to study density-dependent interactions in seaweeds with contrasting morphologies (sensu Littler & Littler, 1980), different life styles and occurrence in different habitats. Interspecific interactions As many as six different kinds of interspecific interactions can affect seaweed recruitment. At least four of them (overgrowth and crowding, shading, sweeping effect and positive interactions) are somewhat similar to the examples already described for intraspecific interactions. Two others (pre-emption and allelopathy) have been primarily described from interspecific contests. Overgrowth, shading and sweeping effects have been especially well documented for kelps (Rosenthal, Clarke & Dayton, 1974; Dayton, 1975b; Foster, 1975; Pearse & Hines, 1979; Cowen, Agegian & Foster, 1982; Dayton et al., 1984; Reed & Foster, 1984; Santelices & Ojed, 1984a,b; Foster & Schiel, 1985). Many of these kelps are able to exert a negative effect on their potential competitors through three different parts of their thallus structure. Spreading holdfasts are able to overgrow other established plants and animals, gradually covering them completely, their dense canopies can shade the juveniles of potential competitors, and the sweeping action of their fronds mediated by water movement can reduce the number of settling propagules. The above types of interactions are by no means restricted to kelps only. Overgrowth of other algal recruits are achieved by species of very different morphologies that are able to grow fast and escape grazing. For example, in the subtidal Macrocystis forest of California, Foster (1975) reported that Rhodymenia californica rhizomes could overgrow species such as Pterosiphonia dendroidea and Herposiphonia plumula, while in the middle intertidal rocky habitats of central Chile, the fast growing crustose chlorophyte Codium dimorphum is one of the species able to overgrow other middle intertidal forms (Santelices, Montalva & Oliger, 1981). Pre-emption is understood as the monopolisation of the space resource by one species, preventing the settlement of a potential competitor. The effect seems especially well represented by turf species. Perhaps Seshappa (1956) was the first to notice this interaction in the field when he suggested that a dense turf of Blidingia minima could prevent the settlement of Fucus spiralis zygotes. In the last 10 years, the idea has been experimentally tested in several communities. In southern California, Hruby & Norton (1979) found that the presence of a turf of any one of at least eight species of algae could totally inhibit colonisation by Sargassum muticum by interposing a physical barrier between the settling germlings and the substratum. The barrier was effectively re-established on denuded surfaces within 1–3 months. In southwestern Nova
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
251
Scotia, Canada, Chapman (1984) found that the recruitment of visible sporophytes of Laminaria longicruris was enhanced 10-fold by removal of a red algal turf. In central Chile, Ojeda & Santelices (1984) found that the recruitment of Lessonia nigrescens was inhibited by a dense carpet of Gelidium chilense. While the above results have suggested that turfing species inhibit kelp recruitment, either by physical occupation of space and reducing the area available for settlement of algal spores, or outcompeting the juvenile kelps for light, a different type of effect has been suggsted by Kennelly (1987a,b,c). In the subtidal kelp forests of New South Wales, dictyotalean turfing algae dominate the substratum in areas where kelp canopies have been removed by storms. Areas of turfing algae were experimentally cleared at a time of kelp settlement but such a clearing did not result in increased kelp recruitment. Kennelly (1987a,b,c) suggested that some lingering influence of turf seemingly affected the substratum in clearings, such that the kelp could not recruit to such areas. Perhaps a chemical influence by these turfing algae may be acting on the encrusting organisms living on the substratum in the kelp forest. Kennelly noted that the phenolic contents of dictyotalean algae similar to those at the study site were known to be quite high and that it was conceivable that these substances could stay in the substratum or around encrusting organisms and may kill or otherwise inhibit gametophytes or young sporophytes of kelp. Allelopathic effects on recruitment are known not only for brown algae with high phenolic compounds but also for coralline crusts. For example, Masaki, Fujita & Akioka (1981) described the coralline alga Lithophyllum yesoense as inhibiting the development and survival of Laminaria japonica germlings. Similarly, Breitburg (1984) reported that Padilla (1981) found that in the intertidal zone of the coast of Oregon several genera of coralline algae inhibited barnacles and filamentous diatoms from recruitment to rocks. After sea urchins were removed from tide pools dominated by crustose coralline algae, recruitment of both brown and red algae was relatively slow and sparse. Kitting & Morse (in Breitburg, 1984) also found that recruitment of filamentous green algae is lower on Lithophyllum and Lithothamnion than on bare rocky substrata. The inhibitory effects of coralline crusts also affect invertebrates, as the crusts significantly decrease recruitment by sessile epibenthic species from several taxa. Positive interactions, facilitating seaweed recruitment also have been described, although they are less understood than negative interactions. Some of them refer to protection from desiccation provided by established vegetation over recruiting propagules. For example, as early as 1932, Hatton reported that a turf of Enteromorpha intestinalis could raise the level on the shore at which Fucus vesiculosus survived. Using a tidal simulator, Hruby & Norton (1979) experimentally demonstrated this effect as dense turfs of Enteromorpha intestinalis raised the level at which newly-settled spores of Ulothrix pseudoflacca survived. More recently, Santelices & Norambuena (1987) have shown that the recruits of Iridaea laminarioides could grow faster if coexisting with opportunistic species of Ulva and Enteromorpha. Seemingly, these opportunistic blades reduced desiccation of the Iridaea recruits. Facilitation mechanisms have been suggested for the recruitment of some species. For example, Ang (1985) found that the pre-conditioning of artificial substrata (coralline rocks) appeared to be a prerequisite for settling of Sargassum germlings. A period of at least 3 months was necessary before these rocks could be colonised. This length of time was associated with the appearance of a thin
252
BERNABÉ SANTELICES
mucilaginous layer on the rock surface, perhaps of bacterial origin. A time lag of 9–10 months needed for the colonisation of Sargassum plagiophyllum on fresh substratum had been previously reported by Raju & Venugopal (1971). Ang (1985) therefore suggested that facilitation may be the mode of primary succession that is taking place in the recruitment of these species of Sargassum. Experimental testing of the interaction, however, as Turner (1983) showed for surfgrass recruitment, is still lacking. Experimental evidence of positive interactions stimulating growth of seaweed recruits by benthic diatoms has been described by Huang & Boney (1984). These authors noted that diatoms usually dominate the surface of submerged substrata before or after bacterial attachment. Many diatom species found in the littoral zone produce large amounts of mucilaginous substances that could affect spore germination and growth of some species. They studied the interactions between juvenile plants of green, brown and red seaweeds and 31 diatom clones isolated from a variety of marine eulittoral habitats. The interactions seemed to be of an individual nature for both juvenile plants and diatoms. Among them, the growth of Ulva lactuca germlings showed enhanced growth, often with significant increase in population sizes of the accompanying diatoms. Positive effects have also been described in plant-plant and animal-plant defense associations (Hay, 1986; Littler, Littler & Taylor, 1987b). In these cases, palatable seaweed species can gain significant protection from herbivores by associating with abundant competitors that are less susceptible to consumption. Some of the palatable species escaping herbivory are epiphytes that grow on unpalatable species. Their ability to germinate and grow as a cryptic epiphyte during seasonal periods of intense herbivory may allow some of these species to remain predictable components of communities for a long time. Interaction of factors The number of factors and interactions that affect seaweed recruitment seems to be so diverse and their study has been so recent that there has been little opportunity to analyse experimentally their field interactions. By integrating observations and some experimental results gathered with various species of kelps, however, a few patterns can be outlined. As discussed previously, interference by adult plants and the grazing effects of herbivores can completely inhibit recruitment of juveniles in several species of kelps. Nevertheless interference by adult plants and grazing are often mutually exclusive in the field. Movement of fronds resulting from water movement deter populations of herbivores, expecially of sea urchins, away from kelps. Therefore, recruitment of juveniles could be expected in areas where these two factors counteract each other. In the case of Lessonia nigrescens in central Chile, this situation corresponds to vegetation openings small enough to show reduced grazing pressure, yet large enough to have reduced disturbance by adult plants (Santelices & Ojeda, 1984c). Field measurements in search of such optimal-sized spaces indicate that vegetational discontinuities of 1.0 to 2.0 m of interholdfast distance exhibited increased juvenile recruitment. That an optimal inter-plant distance is required for successful recruitment of juveniles also has been described by Dayton et al., (1984) for several California kelps.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
253
In the Laminaria beds of South Africa, the relationship is slightly different. There, the patches of Laminaria are consistently formed of a dense, central part with adult plants and progressively smaller individuals towards the margins. A distinct belt of bare rock separates these kelp patches from patches of herbivorous animals. This barren interphase is the result of sweeping action by the most peripheral plants as they are bent by incoming swells. Juveniles can recruit inside the kelp patch, underneath the canopy and be protected from herbivory by the sweeping action of the larger plants. As these juveniles grow, they start exerting their own sweeping action and allowing for the recruitment of new juveniles peripheral to them. In this way the existing kelp patches expand over time. It is interesting that the requirement for a suitable opening for recruitment provides an ecological meaning to several other biological responses of these kelps. In the case of Lessonia nigrescens, the size of such a discontinuity is within the size likely to be produced by the detachment of one or a few old, eroded plants. These plants are weakened by boring invertebrates and removed by storms (Santelices et al., 1980). Storms strong enough to remove these plants are much more common in winter, when L. nigrescens has maximum fertility and the prevailing abiotic conditions, including temperature, light intensity, photoperiod and nutrients, are adequate (Hoffmann, Avila & Santelices, 1984) for gametophyte growth, and reproduction and sporophyte development. Thus, the most probable outcome of the recolonisation following these disturbances should be the establishment of juveniles of L. nigrescens (Ojeda & Santelices, 1984). Their fast growth and large sizes allow them to overgrow and overshade potential competitors for light or space, reestablishing the kelp population. It is unknown if a similar integration of events takes place in populations of other kelp species, but Markham (1973), Dayton (1975a) and Smith (1986) have all recognised that the seasonal reproductive pattern of species of Laminaria and Hedophyllum represent adaptive responses to seasonally predictable patches of substratum produced by storms. Very likely these seasons also have an abundance of recruitment windows (sensu Deysher & Dean, 1986). Approached from this perspective, the recruitment responses, at least of these kelps, appear as rather complex phenomena which integrate and explain several often seemingly unrelated biological responses in seaweeds. Pertinent data so far have been produced only for kelp but equally integrated sets of responses may occur in other types of seaweeds as well. In summary, field experimental studies have been successful in uncovering the interacting effects of a diversity of environmental factors on seaweed recruitment. Studies revealing functional relationships between species and between environmental factors, and those exploring recruitment success as a function of inter-plant distances or plant sizes are leading to a more integrated and perhaps more realistic understanding of recruitment patterns in natural populations. This last type of study, however, has been mainly restricted to kelps and it remains to be seen if the conclusions reached apply also to other types of seaweeds. The evidence has revealed, in addition, the natural occurrence of a bank of microscopic forms, whose ecological roles and relative importance as potential vegetation show functional similarities to and differences from the seed bank of land plants. This bank of microscopic seaweeds provides fertile grounds for further exploration.
254
BERNABÉ SANTELICES
CONCLUSIONS The present state of knowledge of patterns of reproduction, dispersal and recruitment of benthic algae appears heterogeneous and fragmentary. There are large numbers of questions that remain unanswered and of hypotheses that remain untested. The problems can be grouped in four categories, which require different types of studies. The first category refers to processes that have gone unnoted or unstudied, but which seem to be especially important for the biological understanding of seaweeds. They include, for example, the nature and dynamics of the spore clouds; the persistence, turn-over and ecological roles of the bank of microscopic forms; the importance of foam, and of the mucilage produced by invertebrates in algal spore settlement; and the adaptive significance of germination patterns in seaweeds. The second category refers to problems that, although previously studied, remain poorly understood. This includes, for example, the effects of ecological factors on parental tissues and propagules before and during spore release; the morphological and physiological basis for the reduced viability of algal spores; the role of grazers on spore production, release and dispersal; the mechanisms of long-range dispersal; and the frequency and ecological importance for recruitment of positive intraspecific and interspecific interactions. The third type of problem arises from the methods and approaches used to study reproductive processes in benthic algae. The experimental evidence has often been obtained under controlled laboratory conditions, with little concern for the interaction of factors, expected modifications of such factors under field conditions or for the adaptive value of such responses maximising the probabilities of survival of the species offspring. Furthermore, the results obtained with one stage infrequently have been related to other stages in the process. For example, it is largely unknown how in the field the factors determining spore production and release relate to those determining dispersal, settlement or germination; and how the abiotically defined recruitment windows can be modified by biotic interactions; how natural selection operates independently on each phase of a seaweed life history. The fourth category of problems relates to the application to seaweeds of ecological methods and principles that have been developed with other organisms, but with little allowance for their morphological, physiological and life history characteristics. For example, several of the present problems involved in evaluating reproduction-associated costs arise from the application to the algae of methods developed with the morphologically more complex land plants. The frequent exceptions found among the seaweeds to the general belief that diploid organisms are ecologically more resilient than haploid forms, or that isomorphic forms are adapted to stable environments while heteromorphic forms have evolved in response to seasonally fluctuating environments, or the difficulties encountered when trying to apply the r- and k-selection concepts to species with ecologically dissimilar phases point to the need for consideration of the biology of these organisms before applying those generalisations to them. The different biology of seaweeds should allow a good test of the hypotheses, extending and modifying them as dictated by the evidence. This last type of problem is not restricted to the visible life stages. The ecophysiological responses of seaweed propagules while free-floating have been assumed to be similar to these of planktonic producers, an assumption that
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
255
remains largely untested and that, under the evidence gathered for this review, seems to be inappropriate. While free-floating, the seaweed propagules neither exhibit net production nor are they able to divide. They have a limited longevity and their survival (and settlement and growth) depends on adaptations that increase sinking rather than floating. It seems that a much better understanding of the reproduction, dispersal and recruitment processes of the benthic algae will result if the above four categories of problems are recognised, critically analysed and approached according to their different natures. It is likely that to solve some of them a plurality of disciplines will be required. At the same time, a better understanding of these seaweed patterns and processes will contribute to the understanding of fields other than seaweed biology. For example, without a comprehensive knowledge of alternative colonisation styles by different seaweed species or without knowing the roles and dynamics of the bank of microscopic forms it is likely that little advance will be gained on the question of the importance of settlement and recruitment on community structure. In a similar way, the understanding of the adaptive values of isomorphic and heteromorphic cycles, or of haploidy versus diploidy dominance will probably lead to a better understanding of evolutionary processes in plants in general.
ACKNOWLEDGEMENTS My gratitude to I.A.Abbott, E.Glenn and J.McLachlan for reviewing, correcting and criticising the manuscript and to M.S.Doty for providing working conditions and exchanging ideas on various subjects here discussed. This review was done while the author was a Guggenheim Fellow and a Visiting Professor at the Department of Botany of the University of Hawaii. International Foundation for Sciences and Fundación Andes contributed additional funds and Pontificia Universidad Católica de Chile granted sabbatical and study leave. My gratitude to all these Institutions for their support.
REFERENCES Allsopp, A., 1966. Developmental stages and life histories in the lower green plants. In, Trends in Morphogenesis, edited by E.E.Cutter, Longmans, Green & Co., London, pp. 64–87. Amsler, C.D., 1988. Kelp spore chemotaxis and chemoperception. Book of Abstracts, Third International Phycological Congress. Monash University, Australia, p. 2 only. Amsler, C.D. & Searles, R.B., 1980. Vertical distribution of seaweed spores in a water column offshore of North Carolina. J. Phycol., 16, 617–619. Anderson, E.K. & North, W.J., 1966. In situ studies of spore production and dispersal in the giant kelp Macrocystis. Proc. Int. Seaweed Symp., 5, 73– 86.
256
BERNABÉ SANTELICES
Anderson, E.K. & North, W.J., 1969. Light requirements of juvenile and microscopic stages of the giant kelp, Macrocystis. Proc. Int. Seaweed Symp., 6, 3–15. Anderson, R.J. & Bolton, J.J., 1985. Suitability of the agarophyte Suhria vittata (L.) J. Ag. (Rhodophyta: Gelidiaceae) for mariculture: geographical distribution, reproductive phenology and growth of sporelings in culture in relation to light and temperature. S. Afr. J. Mar. Sci., 3, 169–178. Ang, P.O., 1985. Studies on the recruitment of Sargassum spp. (Fucales: Phaeophyta) in Balibago, Calatagan, Philippines. J. Exp. Mar. Biol. Ecol., 91, 293–301. Austin, A.P., 1960. Observations on Furcellaria fastigiata (L.) Lam. forma aegagropila Reinke in Danish waters together with a note on other unattached algal forms. Hydrobiologia, 14, 255–279. Ayling, A.M., 1981. The role of biological disturbance in temperate subtidal encrusting communities. Ecology, 62, 830–847. Baier, R.E., 1970. Surface properties influencing biological adhesion. In, Adhesion in Biological Systems, edited by R.S.Manly, Academic Press, New York, pp. 15– 48. Baker, J. & Evans, L.V., 1973a. The ship fouling alga Ectocarpus. I. Ultrastructure and cytochemistry of plurilocular reproductive stages. Protoplasma, 77, 1–13. Baker, J. & Evans, L.V., 1973b. The ship fouling alga Ectocarpus. II. Ultrastructure of the unilocular reproductive stages. Protoplasma, 77, 181–189. Barilotti, D.C., 1971. Ecological implications of haploidy and diploidy for the isomorphic brown alga Zonaria farlowii Setch. et Gardn. J. Phycol., 7(suppl.), 4only. Barilotti, D.C. & Silverthorne, W., 1972. A resource management study of Gelidium robustum. Proc. Int. Seaweed Symp., 7, 255–261. Bazzaz, F.A. & Reekie, E.G., 1985. The meaning and measurement of reproductive effort in plants. In, Studies on Plant Demography. A Festschrift for John L. Harper, edited by J.White, Academic Press, London, pp. 373–387. Bhattacharya, D., 1985. The demography of fronds of Chondrus crispus Stackhouse. J. Exp. Mar. Biol. Ecol., 91, 217–231. Bidwell, R.G.S. & McLachlan, J., 1985. Carbon nutrition of seaweeds: photosynthesis, photorespiration and respiration. J. Exp. Mar. Biol. Ecol., 86, 15–46. Black, R., 1974. Some biological interactions affecting intertidal populations of the kelp Egregia. Mar. Biol., 28, 189–198. Bold, H.C. & Wynne, M.J., 1985. Introduction to the Algae. Structure and Reproduction. Second edition, Prentice-Hall Inc., New Jersey, 662 pp. Boney, A.D., 1966. A Biology of Marine Algae. Hutchinson Educational Ltd., London, 216 pp. Boney, A.D., 1975. Mucilage sheaths of spores of red algae. J. Mar. Biol. Assoc. U.K., 55, 511–518. Boney, A.D., 1978. The liberation and dispersal of carpospores of the red alga Rhodymenia pertusa (Postels et Rupr.) J. Ag. J. Exp. Mar. Biol. Ecol., 32, 1–6. Boney, A.D., 1981. Mucilage: the ubiquitous algal attribute. Br. Phycol. J., 16, 115– 132. Boney, A.D. & Corner, E.D.S., 1962. The effect of light on the growth of sporelings of the intertidal red alga Plumaria elegans (Bonnem.) Schm. J. Mar. Biol. Assoc. U.K., 42, 65–92. Borowitzka, M., 1978. Plastid development and floridean starch grain formation during carposporogenesis in the coralline red alga Lithothrix aspergillum Gray. Protoplasma, 95, 217–228. Bråten, T., 1971. The ultrastructure of fertilization and zygote formation in the green alga Ulva mutabilis Foyn. J. Cell Sci., 9, 612–635.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
257
Bråten, T., 1975. Observations on mechanisms of attachment in the green alga Ulva mutabilis Foyn. An ultrastructral and light microscopical study of zygotes and rhizoids. Protoplasma, 84, 161–173. Brawley, S.H. & Adey, W.H., 1981. Micrograzers may affect macroalgal density. Nature, (London), 292, 177 only. Breeman, A.M., Bos, S., van Essen, S. & van Mulekom, L.L., 1984. Light-dark regimes in the intertidal zone and tetrasporangial periodicity in the red alga Rhodochorton purpureum. Helgol. Meeresunters., 38, 365–387. Breeman, A.M. & Hoeksema, B.W., 1987. Vegetative propagation of the red alga Rhodochorton purpureum by means of fragments that escape digestion by herbivores. Mar. Ecol. Prog. Ser., 35, 197–201. Breen, P.A. & Mann, K.H., 1976. Changing lobster abundance and the destruction of kelp beds by sea urchins. Mar. Biol. 34, 137–142. Breitburg, D.L., 1984. Residual effects of grazing: inhibition of competitor recruitment by encrusting coralline algae. Ecology, 65, 1136–1143 Buggeln, R.G., 1981. Morphogenesis and growth regulators. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, University of California Press, Berkeley and Los Angeles, pp. 627–660. Bünning, E. & Müller, D., 1961. Wie messen Organismen lunare Zyklen? Z. Naturforsch., 166, 391–395. Burns, R.L. & Mathieson, A.C., 1972. Ecological studies of economic red algae. III: growth and reproduction of natural and harvested populations of Gigartina stellata (Stackhouse) Batters in New Hampshire. J. Exp. Mar. Biol. Ecol., 9, 77–95. Burrows, E.M., 1958. Sublittoral algal population in Port Erin Bay, Isle of Man. J. Mar. Biol. Assoc. U.K., 37, 687–703. Burrows, E.M., 1961. Ecological experiments with species of Fucus. Proc. Int. Seaweed Symp., 4, 166–170. Burrows, E.M., 1971. Assessment of pollution effects by the use of algae. Proc. R. Soc. London, Ser B, 177, 295–306. Burrows, E.M. & Lodge, S.M., 1950. Note on the inter-relationships of Patella, Balanus and Fucus on a semi-exposed coast. Rep. Mar. Biol. St., Port Erin, 62, 30–34. Buschmann, A. & Santelices, B., 1987. Micrograzers and spore release in Iridaea laminarioides Bory (Rhodophyta: Gigartinales). J. Exp. Mar. Biol. Ecol., 108, 171–179. Caffey, H.M., 1985. Spatial or temporal variation in settlement and recruitment of intertidal barnacles. Ecol. Monogr., 55, 313–332. Callow, M.E. & Evans, L.V., 1974. Studies on the ship-fouling alga Enteromorpha. III. Cytochemistry and autoradiography of adhesive production. Protoplasma, 80, 15–27. Carlton, J.F. & Scantlon, J.A., 1985. Progression and dispersal of an introduced alga: Codium fragile spp. tomentosoides (Chlorophyta) on the Atlantic Coast of North America. Bot. Mar., 28, 155–165. Carter, A.R., 1985. Reproductive morphology and phenology, and culture studies of Gelidium pristoides (Rhodophyta) from Port Alfred in South Africa . Bot. Mar., 38, 303–311. Chamberlain, A.H.L. & Evans, L.V., 1973. Aspects of spore production in the red alga Ceramium. Protoplasma, 76, 139–159. Chapman, A.R.O., 1981. Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret’s Bay, eastern Canada. Mar. Biol., 62, 307–311. Chapman, A.R.O., 1984. Reproduction, recruitment and mortality in two species of Laminaria in southwest Nova Scotia. J. Exp. Mar. Biol. Ecol., 78, 99–109.
258
BERNABÉ SANTELICES
Chapman, A.R.O., 1986a. Population and community ecology of seaweeds. Adv. Mar. Biol., 23, pp. 1–161. Chapman, A.R.O., 1986b. Age versus stage: an analysis of age- and size-specific mortality and reproduction in a population of Laminaria longicruris Pyl. J. Exp. Mar. Biol. Ecol., 97, 113–122. Chapman, A.R.O. & Burrows, E.M., 1970. Experimental investigations into the controlling effects of light conditions on the development and growth of Dermarestia aculeata (L.) Lamour. Phycologia, 9, 103–108. Chapman, A.R.O. & Goudey, C.L., 1983. Demographic study of the macrothallus of Leathesia difformis (Phaeophyta) in Nova Scotia. Can. J. Bot. 61, 319–323. Charters, A.C., Neushul, M. & Coon, D.A., 1972. Effects of water motion on algal spore attachment. Proc. Int. Seaweed Symp., 7, 243–247. Charters, A.C., Neushul, M. & Coon, D.A., 1973. The effect of water motion on algal spore adhesion. Limnol. Oceanogr., 18, 884–896. Chemin, M.E., 1937. Le developpement des spores chez les Rhodophycees. Rev. Gen. Bot., 49, 205–236; 300–327; 353–374; 424–448; 478–536. Chen, L.C.-M., Edelstein, T. & McLachlan, J., 1974. The life history of Gigartina stellata (Stackh.) Batt. (Rhodophyceae, Gigartinales) in culture. Phycologia, 13, 287–294. Chen, L.C.-M. & Taylor, A.R.A., 1976. Scanning electron microscopy of early sporeling ontogeny of Chondrus crispus. Can. J. Bot., 54, 672–678. Chi, E.Y. & Neushul, M., 1972. Electron microscopic studies of sporogenesis in Macrocystis. Proc. Int. Seaweed Symp., 7, 181–187. Choat, J.H., 1977. The influence of sessile organisms on the population biology of three species of acmaeid limpets. J. Exp. Mar. Biol. Ecol., 26, 1–26. Christie, A.O. & Evans, L.V., 1962. Periodicity in the liberation of gametes and zoospores of Enteromorpha intestinalis Link. Nature, (London), 193, 193– 194. Christie, A.O., Evans, L.V. & Shaw, M., 1970. Studies on the ship-fouling alga Enteromorpha. II. The effect of certain enzymes on the adhesion of zoospores. Ann. Bot. (London), 34, 467–482. Christie, A.O. & Shaw, M., 1968. Settlement experiments with zoospores of Enteromorpha intestinalis (L.) Link. Br. Phycol. Bull., 3, 529–534. Churchill, A.C. & Moeller, H.W., 1972. Seasonal patterns of reproduction in New York populations of Codium fragile (Sur.) Harriot subsp. tomentosoides (Van Goor) Silva. J. Phycol., 8, 147–152. Clayton, M.N., 1978. Morphological variation and life history in cylindrical forms of Scytosiphon lomentaria (Scytosiphonaceae: Phaeophyta) from southern Australia. Mar. Biol., 47, 349–357. Clayton, M.N., 1981. Correlated studies on seasonal changes in the sexuality, growth rate and longevity of complanate Scytosiphon (Scytosiphonaceae: Phaeophyta) from southern Australia growing in situ. J. Exp. Mar. Biol. Ecol., 51, 87–96. Clayton, M.N., 1988. Evolution and life histories of brown algae. Bot. Mar., 31, 379–387. Clendenning, K.A., 1961. Photosynthesis and growth in Macrocystis pyrifera. Proc. Int. Seaweed Symp., 4, 56–65. Cody, M.L., 1966. A general theory of clutch size. Evolution, 20, 174–184. Connell, J.H., 1975. Some mechanisms producing structure in natural communities: A model and evidence from field experiments. In, Ecology and Evolution of Communities, edited by M.L.Cody & J.M.Diamond, Harvard University Press, Cambridge, pp. 480–490. Connell, J.H., 1985. The consequences of variation in initial settlement vs. post settlement mortality in rocky intertidal communities. J. Exp. Mar. Biol. Ecol., 93, 11–45.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
259
Connor, V.M., 1986. The use of mucous trails by intertidal limpets to enhance food resources. Biol. Bull. (Woods Hole, Mass.), 171, 548–564. Conover, J.T., 1964. The ecology, seasonal periodicity and distribution of benthic plants in some Texas lagoons. Bot. Mar., 7, 4–41. Conover, J.T. & Sieburth, J.McN., 1966. Effect of tannins excreted from Phaeophyta on planktonic animals survival in tide pools. Proc. Int. Seaweed symp., 5, 99– 100. Coon, D., Neushul, M. & Charters, A.C., 1972. The settling behavior of marine algal spores. Proc. Int. Seaweed Symp., 7, 237–242. Cormaci, M., Duro, A. & Furnari, G., 1984. On reproductive phenology of Ceramiales (Rhodophyta) of East Sicily. Bot. Mar., 27, 95–104. Correa, J., Avila, M. & Santelices, B., 1985. Effects of some environmental factors on growth of sporelings in two species of Gelidium (Rhodophyta). Aquaculture, 44, 221–227. Correa, J., Novaczek, I. & McLachlan, J., 1986. Effect of temperature and daylength on morphogenesis of Scytosiphon lomentaria (Scytosiphonales, Rhodophyta) from eastern Canada. Phycologia, 25, 469–475. Cousens, R., 1986. Quantitative reproduction and reproductive effort by stands of the brown alga Ascophyllum nodosum (L.) Le Jolis in south-eastern Canada. Estuarine Coastal Shelf Sci., 22, 495–507. Cousens, R. & Hutchings, M.J., 1983. The relationship between density and mean frond weight in monospecific seaweed stands. Nature (London), 302, 240–241. Cowen, R., Agegian, C.R. & Foster, M.S., 1982. The maintenance of community structure in a central California giant kelp forest. J. Exp. Mar. Biol. Ecol. 64, 189– 201. Craigie, J.S. & Pringle, J.D., 1978. Spatial distribution of tetrasporophytes and gametophytes in four maritime populations of Chondrus crispus. Can. J. Bot., 56, 2910–2914. Creese, R.G., 1982. The distribution and abundance of the limpet Patelloidea latistrigata, and its interaction with barnacles. Oecologia (Berlin), 52, 85–96. Cubit, J.D., 1975. Interactions of seasonally changing physical factors and grazing affecting high intertidal communities on a rocky shore . Ph.D. thesis, University of Oregon, Eugene, Oregon, U.S.A., 177 pp. D’Antonio, C., 1986. Growth and reproduction of the red alga Rhodomela larix. Can. J. Bot., 64, 1499–1506. Darley, W.M., 1982. Algal Biology: A Physiological Approach. Blackwell Scientific Publication, London, 168 pp. Dayton, P.K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., 41, 351–389. Dayton, P.K., 1973. Dispersion, dispersal and persistence of the annual intertidal alga Postelsia palmaeformis Ruprecht. Ecology, 54, 433–438. Dayton, P.K., 1975a. Experimental evaluation of ecological dominance in a rocky intertidal algal community. Ecol. Monogr., 45, 137–159. Dayton, P.K., 1975b. Experimental studies of algal canopy interactions in a sea-otter dominated kelp community at Amchitka Island, Alaska. Fish. Bull., 73, 230–237. Dayton, P.K., 1979. Ecology: science or religion? In, Ecological Processes in Coastal and Estuarine Systems, edited by R.Livingston, Plenum Press, New York, pp. 3–17. Dayton, P.K., 1984. Processes structuring some marine communities: are they general? In, Ecological Communities: Conceptual Issues and the Evidence, edited by D.R.Strong et al., Princeton University Press, Princeton, pp. 181–197. Dayton, P.K., Currie, V., Gerrodette, T., Keller, B.D., Rosenthal, R. & Ventresca, D., 1984. Patch dynamics and stability of some California kelp communities. Ecol Monogr., 54, 253–289.
260
BERNABÉ SANTELICES
De Boer, J.A., 1981. Nutrients. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley and Los Angeles, 17, 356–392. Denny, M., 1988. Biology and the Mechanics of the Wave-swept Environment. Princeton University Press, Princeton, 330 pp. De Ruyter van Steveninck, E.D. & Breeman, A.M., 1987. Population dynamics of a tropical intertidal and deep-water population of Sargassum polyceratium (Phaeophyceae). Aquat. Bot., 29, 139–156. Dethier, M., 1981. Heteromorphic algal life histories: the seasonal pattern and response to herbivory of the brown crust, Ralfsia californica. Oecologia (Berlin), 49, 333–339. De Vinny, J.S. & Volse, L.A., 1978. Effects of sediments on the development of Macrocystis pyrifera gametophytes. Mar. Biol., 48, 343–348. DeWreede, R., 1976. The phenology of three species of Sargassum (Sargassaceae, Phaeophyta) in Hawaii. Phycologia, 15, 175–184. DeWreede, R., 1978. Phenology of Sargassum muticum (Phaeophyta) in the Strait of Georgia, British Columbia. Syesis, 11, 1–9. DeWreede, R., 1983. Sargassum muticum (Fucales, Phaeophyta): regrowth and interaction with Rhodomela larix (Ceramiales, Rhodophyta). Phycologia, 22, 153–160. DeWreede, R., 1984. Growth and age class distribution of Pterygophora californica (Phaeophyta). Mar. Ecol. Prog. Ser., 19, 93–100. DeWreede, R., & Klinger, T., 1988. Reproductive strategies in algae. In, Plant Reproductive Ecology. Patterns and Strategies, edited by J.Lovett-Doust & L.LovettDoust, Oxford University Press, Oxford, pp. 267–284. Deysher, L. & Dean, T.A., 1986. In situ recruitment of the giant kelp, Macrocystis pyrifera: effects of physical factors. J. Exp. Mar. Biol. Ecol., 103, 41–63. Deysher, L. & Norton, T.A., 1982. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J. Exp. Mar. Biol. Ecol., 56, 179–195. Dixon, P.S., 1965. Perennation, vegetative propagation and algal life histories, with special reference to Asparagopsis and other Rhodophyta. Bot. Gothoburg., 3, 67–74. Dixon, P.S., 1973. Biology of the Rhodophyta. Hafner, New York, 258 pp. Doherty, P. & Williams, D. McB., 1988. The replenishment of coral reef fish populations. Oceanogr. Mar. Biol. Annu. Rev., 26, 487–551. Doty, M.S., 1946. Critical tide factors that are correlated with the vertical distribution of marine algae and other organisms along the Pacific coast. Ecology, 27, 315– 328. Doty, M.S., 1961. Acanthophora, a possible invader of the marine flora of Hawaii. Pac. Sci., 15, 547–552. Doty, M.S., 1971. Antecedent event influence on benthic marine algal standing crops in Hawaii. J. Exp. Mar. Biol. Ecol., 6, 161–166. Drew, K.M., 1949. Conchocelis-phase in the life history of Porphyra umbilicalis (L.) Kuetz. Nature (London), 164, 748–749. Drew. K.M., 1955. Life histories in the algae with special reference to the Chlorophyta, Phaeophyta and Rhodophyta. Biol. Rev., 30, 343–390. Dring, M.J., 1974. Reproduction. In, Algal Physiology and Biochemistry, edited by W.D.P.Stewart, Botanical Monographs, University of California Press, Berkeley and Los Angeles, 10, 814–837. Dring, M.J., 1982. The Biology of Marine Plants. Arnold, London, 199 pp. Dring, M.J., 1984. Photoperiodism and phycology. Prog. Phycol. Res., 3, 159– 192. Dring, M.J. & West, J.A., 1983. Photoperiodic control of tetrasporangium formation in the red alga Rhodochorton purpureum. Planta, 159, 143–150.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
261
Druehl, L.D., 1981. Geographical distribution. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, University of California Press, Berkeley and Los Angeles, pp. 306–325. Duggins, D.O., 1980. Kelp beds and sea-otters: an experimental approach. Ecology, 61, 447–453. Duggins, D.O., 1981. Sea urchins and kelp: the effects of short term changes in urchin diet. Limnol. Oceanogr., 26, 391–394. Dyck, L., DeWreede, R. & Garbary, D., 1985. Life history phases in Iridaea cordata (Gigartinaceae): relative abundance and distribution from British Columbia to California. Jap. J. Phycol., 33, 225–232. Edgar, G.J., 1987. Dispersal of faunal and floral propagules associated with drifting Macrocystis pyrifera plants. Mar. Biol., 95, 599–610. Edwards, P., 1969. Field and cultural studies on the seasonal periodicity of growth and reproduction of selected Texas benthic marine algae. Univ. Tex. Contrib. Mar. Sci., 14, 59–114. Edwards, P., 1971. Effects of light intensity, day length and temperature on growth and reproduction of Callithamnion bissoides. In, Contributions to Phycology, edited by B.C.Parker & R.M.Brown, Allen Press Inc., Lawrence, U.S.A., pp. 163–174. Edwards, P., 1977. An investigation of the vertical distribution of selected marine algae with a tide-simulating machine. J. Phycol., 13, 62–68. Edyvean, R.G. J. & Ford, H., 1984a. Population biology of the crustose red alga Lithophyllum incrustans Phil. 2. A comparison of populations from three areas of Britain. Biol. J. Linn. Soc., 23, 353–363. Edyvean, R.G.J. & Ford, H., 1984b. Population biology of the crustose red alga Lithophyllum incrustans Phil. 3. The effects of local environmental variables. Biol J. Linn. Soc., 23, 365–374. Emerson, S.E. & Zedler, J.B., 1978. Recolonization of intertidal algae: an experimental study. Mar. Biol., 44, 315–324. Evans, L.V. & Christie, A.O., 1970. Studies on the ship-fouling alga Enteromorpha. I. Aspects of the fine-structure and biochemistry of swimming and newly settled zoospores. Ann. Bot., 34, 451–466. Fahey, E.M. & Doty, M.S., 1949. Pioneer colonization on intertidal transects. Biol. Bull. (Woods Hole, Mass.), 97, 238–239. Farnham, W.F., Fletcher, R.L. & Irvine, L.M., 1973. Attached Sargassum in Britain. Nature (London), 243, 231–232. Feldmann, J., 1952. Les cycles de reproduction des algues et leurs rapports avec la phylogénie. Rev. Cytol Biol Veg., 13, 1–49. Fenner, M., 1985. Seed Ecology. Chapman & Hall, London, England, 151 pp. Fetter, R., 1977. Red algae reproduction via spermatia containing slime strands. J. Phycol., 13 (Suppl.), 466 only. Fletcher, R.L. & Fletcher, S.M., 1975. Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt. I. Ecology and reproduction. Bot. Mar., 18, 149–156. Floc’h, J.Y., Deslandes, E. & Le Gall, Y., 1987. Evidence for vegetative propagation of the carrageenophyte Solieria chordalis (Solieriaceae, Rhodophyceae) on the coast of Brittany (France) and in culture. Bot. Mar., 30, 315–321. Forbes, M.A. & Hallam, N.D., 1979. Embryogenesis and substratum adhesion in the brown alga Hormosira banksii (Turner) Decaisne. Br. Phycol. J., 14, 69–81. Ford, H., Hardy, F.G. & Edyvean, R.G.J., 1983. Population biology of the crustose red alga Lithophyllum incrustans Phil. Three populations on the east coast of Britain. Biol. J. Linn. Soc., 19, 211–220.
262
BERNABÉ SANTELICES
Foster, M.S., 1975. Regulation of algal community development in a Macrocystis pyrifera forest. Mar. Biol., 12, 331–342. Foster, M.S. & Schiel, D.R., 1985. The ecology of giant kelp forests in California: a community profile. Fish Wildl. Serv. (U.S.) Biol. Rep., 85, 1– 152. Friedlander, M. & Dawes, C.J., 1984a. Studies on spore release and sporeling growth from carpospores of Gracilaria foliifera (Forsskal) Borgesen var. angustissima (Harvey) Taylor. I. Growth responses. Aquat. Bot., 19, 221–232. Friedlander, M. & Dawes, C.J., 1984b. Studies on spore release and sporeling growth from carpospores of Gracilaria foliifera (Forsskal) Borgesen var. angustissima (Harvey) Taylor. II. Photosynthetic and respiratory responses. Aquat. Bot., 19, 233–241. Gabrielson, P.W. & Garbary, D., 1986. Systematics of red algae (Rhodophyta). Crit. Rev. Plant Sci., 3, 325–366. Gaines, S., Brown, S. & Roughgarden, J., 1985. Spatial variation in larval concentrations as a cause of spatial variation in settlement for the barnacle, Balanus glandula. Oecologia (Berlin), 67, 267–272. Gaines, S. & Roughgarden, J., 1985. Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone. Proc. Nat. Acad. Sci. U.S.A., 82, 3707–3711. Gaines, S.D., 1985. Herbivory and between-habitat diversity: the differential effectiveness of defenses in a marine plant. Ecology, 66, 473–485. Gaines, S.D. & Roughgarden, J., 1987. Fish in offshore kelp forests affect recruitment to intertidal barnacle populations. Science, 235, 397–512. Garbary, D., Grund, D.W. & McLachlan, J., 1980. Branching patterns and life history stages in Ceramium rubrum (Huds.) C. Ag. Nova Hedwigia, 33, 249– 260. Guiry, M.D., 1984. Photoperiodic and temperature responses in the growth and tetrasporogenesis of Gigartina acicularis (Rhodophyta) from Ireland. Helgol Meeresunters., 38, 335–347. Guiry, M.D. & Cunningham, E.M., 1984. Photoperiodic and temperature responses in the reproduction of north eastern Atlantic Gigartina acicularis (Rhodophyta: Gigartinales). Phycologia, 23, 357–367. Gunnill, F.C., 1985. Growth, morphology and microherbivore faunas of Pelvetia fastigiata (Phaeophyta, Fucaceae) at La Jolla, California, USA. Bot. Mar., 28, 187–199. Guzmán del Pró, S.A., De la Campa, S. & Pineda-Barrera, J., 1972. Shedding rhythm and germination of spores in Gelidium robustum. Proc. Int. Seaweed Symp., 7, 221–228. Hannach, G. & Santelices, B., 1985. Ecological differences between the isomorphic reproductive phases of two species of Iridaea (Rhodophyta: Gigartinales). Mar. Ecol. Prog. Ser., 22, 291–303. Hannach, G. & Waaland, J.R., 1986. Environment, distribution and production of Iridaea. Aquat. Bot., 26, 51–78. Hansen, J.E., 1977. Ecology and natural history of Iridaea cordata (Gigartinales, Rhodophyta) growth. J. Phycol., 13, 395–402. Hansen, J.E. & Doyle, W.T., 1976. Ecology and natural history of Iridaea cordata (Rhodophyta, Gigartinaceae): population structure. J. Phycol., 12, 273–278. Harlin, M.M. & Lindberg, J.M., 1977. Selection of substrata by seaweeds: optimal surface relief. Mar. Biol., 40, 33–40. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London, 892 pp. Harrold, C. & Pearse, J., 1987. The ecological role of echinoderms in kelp forests. In, Echinoderm Studies, Vol. 2. , edited by M.Jangoux & J.M.Lawrence, Balkema, Rotterdam, pp. 137–233.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
263
Harrold, C. & Reed, D.C., 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology, 66, 1160–1169. Hartog, C.Den, 1971. Substratum. Plants. In, Marine Ecology, A comprehensive, integrated treatise of life in oceans and coastal waters, Vol. 1, edited by O.Kinne, Wiley Interscience, New York, pp. 1277–1289. Hasegawa, Y., 1962. An ecological study of Laminaria angustata Kjellman on the coast of Hidaka Prov., Hokkaido. Bull. Hokkaido Reg. Fish. Lab., 24, 116–138. Hatton, H., 1932. Quelques observations sur le repeuplement en Fucus vesiculosus des surfaces rocheuses denudees. Bull. Lab. de St. Servan, 9, 1–6. Hawkes, M.W., 1980. Ultrastructure characteristics of monospore formation in Porphyra gardneri (Rhodophyta). J. Phycol., 16, 192–196. Hawkins, S.J., 1981. The influence of season and barnacles on algal colonization of Patella vulgata exclusion areas. J. Mar. Biol. Assoc. U.K., 47, 81–95. Hawkins, S.J. & Hartnoll, R.G., 1983. Grazing of intertidal algae by marine invertebrates. Oceanogr. Mar. Biol. Annu. Rev., 21, 195–282. Hay, C.H. & South E.R., 1979. Experimental ecology with particular reference to proposed commercial harvesting of Durvillea (Phaeophyta, Durvilleales) in New Zealand. Bot. Mar., 22, 431–436. Hay, M., 1986. Associational plant defenses and the maintenance of species diversity: turning competitors into accomplices. Am. Nat., 128, 617–641. Hay, M.E. & Norris, J.N., 1984. Seasonal reproduction and abundance of six sympatric species of Gracilaria Grev.(Gracilariaceae; Rhodophyta) on a Caribbean subtidal sand plain. Hydrobiologia, 116/117, 63–94. Hellebust, J.A., 1970. Light-plants. In, Marine Ecology, edited by O.Kinne, Wiley-Interscience, London, pp. 125–158. Hoek, C.van den, 1982. The distribution of benthic marine algae in relation to the temperature regulation of their life histories. Biol. J. Linn. Soc., 18, 81–114. Hoek, C.van den, 1987. The possible significance of long-range dispersal for the biogeography of seaweeds. Helgol. Meeresunters., 41, 261–272. Hoffmann, A.J., 1987. The arrival of seaweed propagules at the shore: a review. Bot. Mar., 30, 151–165. Hoffmann, A.J., 1988. Daylength and light responses in growth and fertility of Glossophora kunthii (Phaeophyta, Dictyotales) from Pacific South America. J. Phycol., 24, 203–208. Hoffmann, A.J., Avila, M. & Santelices, B., 1984. Interactions of nitrate and phosphate on the development of microscopic stages of Lessonia nigrescens Bory (Phaeophyta). J. Exp. Mar. Biol. Ecol., 78, 177–186. Hoffmann, A.J. & Santelices, B., 1982. Effects of light intensity and nutrients on game to genesis of Lessonia nigrescens Bory (Phaeophyta). J. Exp. Mar. Biol. Ecol., 78, 177–186. Hoffmann, , A.J. & Ugarte, R., 1985. The arrival of propagules of marine macroalgae in the intertidal zone. J. Exp. Mar. Biol. Ecol., 92, 83–95. Hommersand, M.H. & Fredericq, S., 1988. An investigation of cystocarp development in Gelidium pteridifolium with a revised description of the Gelidiales (Rhodophyta). Phycologia, 27, 254–272. Hori, T. & Enomoto, S., 1978a. Developmental cytology of Dictyosphaeria cavernosa. I. Light and electron microscope observations on cytoplasmic cleavage in zooid formation. Bot. Mar., 21, 401–408. Hori, T. & Enomoto, S., 1978b. Developmental cytology of Dictyosphaeria cavernosa. II. Nuclear division during zooid formation. Bot. Mar., 21, 477– 481. Hoyle, M.D., 1978. Reproductive phenology and growth rates in two species of Gracilaria from Hawaii. J. Exp. Mar. Biol. Ecol., 35, 273–283. Hoyt, W.D., 1907. Periodicity in the reproduction of the sexual cells of Dictyota dichotoma. Bot. Mar., 43, 383–392.
264
BERNABÉ SANTELICES
Hoyt, W.D., 1927. The periodic fruiting of Dictyota and its relation to the environment. Am. J. Bot., 14, 592–618. Hruby, T. & Norton, T.A., 1979. Algal colonization on rocky shores in the Firth of Clyde. J. Ecol., 67, 65–77. Hsiao, S.I.C., 1969. Life history and iodine nutrition of the marine brown alga Petalonia fascia (O.F.Mull.) Kuntze. Can. J. Bot., 47, 1611–1616. Hsiao, S.I.C. & Druehl, L.D., 1973. Environmental control of gametogenesis in Laminaria saccharina. IV. In situ development of gametophytes and young sporophytes. J. Phycol., 9, 160–164. Huang, R. & Boney, A.D., 1983. Effects of diatom mucilage on the growth and morphology of marine algae. J. Exp. Mar. Biol. Ecol., 67, 79–81. Huang, R. & Boney, A.D., 1984. Growth interactions between littoral diatoms and juvenile marine algae. J. Exp. Mar. Biol. Ecol., 81, 21–45. Inoh, S., 1947. Kaiso no hassei (Development of Marine Algae, in Japanese). Tokyo, 255 pp. Istock, C.A., 1966. The evolution of complex life cycle phenomena: an ecological perspective. Evolution., 21, 592–605. Jernakoff, P., 1983. Factors affecting the recruitment of algae in a midshore region dominated by barnacles. J. Exp. Mar. Biol. Ecol., 67, 17–31. Jernakoff, P., 1985a. Interactions between the limpet Patelloida latistrigata and algae on an intertidal rock platform. Mar. Ecol. Prog. Ser., 23, 71– 78. Jernakoff, P., 1985b. An experimental evaluation of the influence of barnacles, crevices and seasonal patterns of grazing on algal diversity and cover in an intertidal barnacle zone. J. Exp. Mar. Biol. Ecol., 88, 287–302. John, D.M., 1974. New records of Ascophyllum nodosum (L.) Le Jol. from the warmer parts of the Atlantic Ocean. J. Phycol., 10, 243–244. Johnson, C.R. & Mann, K.H., 1982. Adaptations of Strongylocentrotus droebachiensis for survival on barren grounds in Nova Scotia. In, Echinoderms: Proceedings of the International Conference, Tampa Bay, edited by J.M. Lawrence, Balkema, Rotterdam, pp. 277–283. Johnstone, G.R. & Feeney, F.L., 1944. Periodicity of Gelidium cartilagineum, a perennial red alga. Am. J. Bot., 31, 25–29. Jones, W.E., 1956. Effect of spore coalescence in the early development of Gracilaria verrucosa (Huds.) Papenfuss. Nature (London), 178, 426–427. Jones, W.E., 1957. The autoecology of Gracilaria verrucosa (Huds.) Papenf. J. Mar. Biol. Assoc. U.K., 38, 47–56. Jones, W.E., 1959. Experiments on some effects of certain environmental factors on Gracilaria verrucosa (Hudson) Papenfuss. J. Mar. Biol. Assoc. U.K., 38, 153–167. Jones, W.E. & Babb, M.S., 1968. The motile period of swarmers of Enteromorpha intestinalis (L.) Link. Br. Phycol. Bull., 3, 525–528. Kain, J.M., 1964. Aspects of the biology of Laminaria hyperborea. III. Survival and growth of gametophytes. J. Mar. Biol. Assoc. U.K., 44, 415– 433. Kain, J.M., 1966. The role of light in the ecology of Laminaria hyperborea. Br. Ecol. Soc. Symp., 6, 319–334. Kain, J.M., 1969. The biology of Laminaria hyperborea. V. Comparison with early stages of competitors. J. Mar. Biol. Assoc. U.K., 49, 455–473. Kain, J.M., 1975. Algal recolonization of some cleared subtidal areas. J. Ecol., 63, 739–765. Kain, J.M., 1982. The reproductive phenology of nine species of Rhodophyta in the subtidal region of the Isle of Man. Br. Phycol. J. 17, 321–331. Kain, J.M., 1987. Photoperiod and temperature as triggers in the seasonality of Delesseria sanguinea. Helgol. Meeresunters., 41, 355–370.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
265
Kaliaperumal, N. & Umamaheswara Rao, M., 1982. Seasonal growth and reproduction of Gelidiopsis variabilis (Greville) Schmitz. J. Exp. Mar. Biol. Ecol., 61, 265–270. Kapraun, D.F., 1978. Field and cultural studies on selected North Carolina Polysiphonia species. Bot. Mar., 21, 143–153. Katada, M., 1955. Fundamental studies on the propagation of gelidiaceous algae with special reference to shedding and adhesion of the spores, germination, growth and vegetative reproduction. J. Shimonoseki Coll. Fish., 5, 1–87. Kawashima, S., 1983. Sporangial sorus formation of Laminaria angustata Kjellman. Jap. J. Phycol., 31, 208–216. Keddy, P.A., 1981. Why gametophytes and sporophytes are different: form and function in a terrestrial environment. Am. Nat., 118, 452–454. Kennelly, S.J., 1983. An experimental approach to the study of factors affecting algal colonization in a sublittoral kelp forest. J. Exp. Mar. Biol. Ecol., 68, 257– 276. Kennelly, S.J., 1987a. Physical disturbances in an Australian kelp community. II. Effects on understorey species due to differences in kelp cover. Mar. Ecol. Prog. Ser., 40, 155–165. Kennelly, S.J., 1987b. Physical disturbances in an Australian kelp community. I. Temporal effects. Mar. Ecol. Prog. Ser., 40, 145–153. Kennelly, S.J., 1987c. Inhibition of kelp recruitment by turfing algae and consequences for an Australian kelp community. J. Exp. Mar. Biol. Ecol., 112, 49– 60. Kennelly, S.J. & Larkum, A.W. D., 1983. A preliminary study of temporal variation in the colonization of subtidal algae in an Ecklonia radiata community. Aquat. Bot., 17, 275–282. Kennelly, S.J. & Underwood, A.J., 1984. Underwater microscopic sampling of a sublittoral kelp community. J. Exp. Mar. Biol. Ecol., 76, 67–78. Keough, M.J., 1983. Patterns of recruitment of sessile invertebrates in two subtidal habitats. J. Exp. Mar. Biol. Ecol., 66, 213–245. Keough, M.J. & Downes, B.J., 1982. Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia (Berlin), 54, 348–352. Kessler, J.O., 1986. The external dynamics of swimming micro-organisms. Prog. Phycol. Res., 4, 257–301. Khfaji, A.K. & Boney, A.D., 1979. Antibiotic effects of crustose germlings of the red alga Chondrus crispus Stackh. on benthic diatoms. Ann. Bot., 43, 231–232. Killian, C, 1914. Ueber die Entwicklung einiger Floridean. Z. Bot., 6, 219–278. Kim, D.H., 1970. Economically important seaweeds in Chile. I. Gracilaria. Bot. Mar., 13, 140–162. Kirkman, H., 1982. The first year in the life history and the survival of the juvenile marine macrophyte, Ecklonia radiata (Turn.) J. Agardh. J. Exp. Mar. Biol. Ecol., 55, 243–254. Knaggs, F.W., 1966. Rhodochorton purpureum (Lightf.) Rosenvinge. Observations on the relationship between morphology and environment. II. Nova Hedwigia, 11, 337–349. Knaggs, F.W., 1967. Rhodochorton floridulum (Dillwn.) Hag. Observations on the relationship between reproduction and environment. Nova Hedwigia, 14, 31–38. Knight, M. & Parke, M., 1950. A biological study of Fucus vesiculosus L. and F. seratus L. J. Mar. Biol. Assoc. U.K., 29, 439–514. Kremer, B.P., 1981. Carbon metabolism. In, The Biology of Seaweeds, Edited by C. S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley and Los Angeles, 17, 493–558. Krishnamurthy, V., 1965a. Marine algal cultivation—necessity, principles and problems. In, Proc. Sem. on Sea, Salt and Plants, edited by V.Krishnamurthy, Bhavnagar, India, pp. 327–333.
266
BERNABÉ SANTELICES
Krishnamurthy, V., 1965b. The output, liberation and germination of carpospores and tetraspores in Polysiphonia platycarpa Boerg. together with some remarks on the adult plants. In, Proc. Sem. on Sea, Salt and Plants. , edited by V.Krishnamurthy, Bhavnagar, India, pp. 202–208. Kristiansen, A. & Pedersen, P.M., 1979. Studies on life history and seasonal variation of Scytosiphon lomentaria (Phaeophyceae, Scytosiphonales) in Denmark. Bot. Tidsskr., 74, 31–56. Kugrens, P. & Delivopoulos, S.G., 1986. Ultrastructure of the carposporophyte and carposporogenesis in the parasitic red alga Plocamiocolax pulvinata Setch. (Gigartinales, Plocamiaceae). J. Phycol., 22, 8–21. Kugrens, P. & West, J.A., 1972. Ultrastructure of tetrasporogenesis in the parasitic red alga Levringiella gardneri (Setchell) Kylin. J. Phycol., 8, 370– 383. Kugrens, P. & West, J.A., 1973. The ultrastructure of carpospore differentiation in the parasitic red alga Levringiella gardneri (Setchell) Kylin. Phycologia, 12, 163–173. Kugrens, P. & West, J.A., 1974. The ultrastructure of carposporogenesis in the marine hemiparasitic red alga Erythrocystis saccata. J. Phycol., 10, 139– 147. Lang, C. & Mann, K.H., 1976. Changes in sea urchin populations after destruction of kelp beds. Mar. Biol., 36, 321–326. Lawrence, J.M., 1975. On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol. Annu. Rev., 13, 213–286. Lawrence, J.M. & Dawes, C.J., 1969. Algal growth over the epidermis of sea urchin spines. J. Phycol., 5, 269. Levin, S.A., Cohen, D. & Hasting, A., 1984. Dispersal strategies in patchy environments. Theor. Popul. Biol, 26, 165–191. Lewis, I.F., 1910. Periodicity of Dyctiota at Naples. Bot. Gaz., 50, 59–64. Lewis, S.M., Norris, J.N. & Searles, R.B., 1987. The regulation of morphological plasticity in tropical reef algae by herbivory. Ecology, 68, 636–641. Liddle, L.B., 1968. Reproduction in Zonaria farlowii. I. Gametogenesis, sporogenesis, and embryology. J. Phycol., 4, 298–305. Lilly, J.S., Sloane, J.F., Bassindale, R., Ebling, F.J. & Kitching, J.A., 1953. The ecology of the Lough Ine rapids with special reference to water currents. J. Anim. Ecol., 22, 87–122. Littler, M.M. & Littler, D.S., 1980. The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat., 116, 25–44. Littler, M.M. & Littler, D.S., 1983. Heteromorphic life-history strategies in the brown alga Scytosiphon lomentaria (Lyngb.) Link., J. Phycol., 19, 425–31. Littler, M.M., Littler, D.S. & Taylor, P.R., 1987a. Functional similarity among isomorphic life-history phases of Polycavernosa debilis (Rhodophyta, Gracilariaceae). J. Phycol., 23, 501–505. Littler, M.M., Littler, D.S. & Taylor, P.R., 1987b. Animal-plant defense associations: effects on the distribution and abundance of tropical reef macrophytes. J. Exp. Mar. Biol. Ecol., 105, 107–121. Littler, M.M. & Murray, S.N., 1975. Impact of sewage on the distribution, abundance and community structure of rocky intertidal macro-organisms. Mar. Biol., 30, 277–291. Liu, X.-W., & Gordon, M.E., 1986. Tissue and cell cultures of New Zealand Pterocladia and Porphyra species. Proc. Int. Seaweed Symp., 12, 95 (Abstract). Lobban, C.S., Harrison, P.J. & Duncan, M.J., 1985. The Physiological Ecology of Seaweeds. Cambridge University Press, Cambridge, 242 pp.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
267
Lofthouse, P.F. & Capon, B., 1975. Ultrastructural changes accompanying mitosporogenesis in Ectocarpus (Phaeophyta, Ectocarpales). Phycologia, 16, 235–243. Lubchenco, J., 1980. Algal zonation in a New England rocky intertidal community: An experimental analysis. Ecology, 61, 333–344. Lubchenco, J., 1983. Littorina and Fucus: effects of herbivores, substratum heterogeneity and plant escapes during succession. Ecology, 64, 1116–1123. Lubchenco, J. & Cubit, J., 1980. Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology, 61, 676–687. Lüning, K., 1980a. Critical levels of light and temperature regulating the gametogenesis of three Laminaria spp. (Phaeophyceae). J. Phycol., 16, 1–15. Lüning, K., 1980b. Control of algal life history by daylength and temperature. In, The Shore Environment: Methods and Ecosystems, edited by J.H.Price et al., Academic Press, New York, pp. 915–945. Lüning, K., 1981a. Light. In, The Biology of Seaweeds, edited by C.S.Lobban & M. J.Wynne, Botanical Monographs, University of California Press, Berkeley and Los Angeles, 17, 326–355. Lüning, K., 198 1b. Egg release in gametophytes of Laminaria: induction by darkness and inhibition by blue light and U.V. Br. Phycol J., 16, 379–393. Lüning, K., 1988. Photoperiodic control of sorus formation in the brown alga Laminaria saccharina. Mar. Ecol. Prog. Ser., 45, 137–144. Lüning, K. & Dring, M., 1975. Reproduction, growth and photosynthesis of gametophytes of Laminaria saccharina grown in blue and red light. Mar. Biol., 29, 195–200. Luxoro, C. & Santelices, B., 1989. Additional evidence for ecological differences among isomorphic reproductive phases of Iridaea laminarioides (Rhodophyta: Gigartinales). J. Phycol., 25, 206–212. Markey, D.R. & Wilce, R.T., 1976. The ultrastructure of reproduction in the brown alga Pylaiella littoralis. I. Mitosis and cytokinesis in the plurilocular gametangia. Protoplasma, 85, 219–241. Markham, J.W., 1973. Observations on the ecology of Laminaria sinclairii (Harvey) Farlow, Anderson et Eaton. Syesis, 1, 125–131. Masaki, T., Fujita, D. & Akioka, H., 1981. Observations on the spore germination of Laminaria japonica on Lithophyllum yessoense(Rhodophyta, Corallinaceae) in culture. Bull. Fac. Fish. Hokkaido Univ., 32, 349–356. Mathieson, A.C. & Burns, R.L., 1975. Ecological studies of economic red algae. V. Growth and reproduction of natural and harvested populations of Chondrus crispus Stackhouse in New Hampshire. J. Exp. Mar. Biol. Ecol., 17, 137–156. Mathieson, A.C., Shipman, J.W., O’Shea, J.R. & Hasevlat, R.C., 1976. Seasonal growth and reproduction of estuarine fucoid algae in New England. J. Exp. Mar. Biol. Ecol., 25, 273–284. May, G., 1986. Life history variations in a predominantly gametophytic population of Iridaea cordata (Gigartinaceae, Rhodophyta). J. Phycol., 22, 448–55. McBride, D.L. & Cole, K., 1971. Electron microscopic observations on the differentiation and release of monospores in the marine red alga Smithora naiadum. Phycologia, 10, 49–61. McBride, D.L. & Cole, K., 1972. Ultrastructural observations on germinating monospores in Smithora naiadum (Rhodophyceae, Bangiophycidae). Phycologia, 11, 181–191. McCandless, E.L. & Craigie, J.S., 1975. Carrageenans of gametangial and tetrasporangial stages of Iridaea cordata (Gigartinaceae). Can J. Bot., 53, 2315– 2318. McCourt, R.M., 1984. Seasonal patterns of abundance, distributions and phenology in relation to growth strategies of three Sargassum species. J. Exp. Mar. Biol. Ecol., 74, 141–156.
268
BERNABÉ SANTELICES
McDermid, K.J., 1988. Community ecology of some intertidal subtropical algae, and the biology and taxonomy of Laurencia (Rhodophyta) on Hawaii. Ph.D. dissertation, University of Hawaii, Honolulu, Hawaii, USA, 332 pp. McLachlan, J., 1974. Effects of temperature and light on growth and development of embryos of Fucus edentatus and F. distichus spp. distichus. Can. J. Bot., 52, 943–951. McLachlan, J. & Bidwell, R.G.S., 1978. Photosynthesis of eggs, sperms, zygotes and embryos of Fucus serratus. Can. J. Bot., 56, 371–373. McLachlan, J., Chen, L.C.-M. & Edelstein, T., 1971. The culture of four species of Fucus under laboratory conditions. Can. J. Bot., 49, 1463–1469. McLachlan, J. & Craigie, J.S., 1964. Algal inhibition by yellow ultraviolet absorbing substances from Fucus vesiculosus. Can. J. Bot., 42, 287–292. Mohsen, A.F., Khaleafa, A.F., Hashem, M.A. & Metwalli, A., 1974. Effect of different nitrogen sources on growth, reproduction, amino acid, fat and sugar contents in Ulva fasciata Delile. Bot. Mar., 17, 218–222. Mooney, P.A. & van Staden, J., 1984. Seasonal changes in the levels of endogenous cytokinins in Sargassum heterophyllum (Phaeophyceae). Bot. Mar., 27, 437–442. Mooney, P.A. & van Staden, J., 1987. Tentative identification of cytokinins in Sargassum heterophyllum. Bot. Mar., 30, 323–325. Moore, H.B., 1939. The colonization of a new rocky shore at Plymouth. J. Anim. Ecol., 8, 29–38. Moore, P.G., 1977. Organization in simple communities: observations of the natural history of Hyale nilsonii (Amphipoda) in high littoral seaweeds. In, Biology of Benthic Organisms, edited by B.F.Keegan et al., Pergamon Press, Oxford, Proc. 11th Eur. Mar. Biol. Symp., pp. 443–51. Moore, P.G., 1986. Seaweed-associated animal communities in the Firth of Clyde, with special reference to the population biology of the amphipod Hyale nilssoni (Rathke). Proc. R. Soc. Edinburgh, Ser. B, 90, 271–286. Moorjani, S. & Jones, W.E., 1972. Spore attachment and development in some coralline algae. Br. Phycol. J., 7, 282. Moss, B., Mencer, S. & Sheader, A., 1973. Factors affecting the distribution of Himanthalia elongata (L.) S.F.Gray on the north-east coast of England. Estuarine Coastal Mar. Sci., 1, 233–234. Mshigeni, K., 1974. An extended review on the literature on Hypnea, a red algal genus. U.S. Sea Grant Program. University of Hawaii. Technical Report, 2, 1–22. Mshigeni, K., 1976. Studies on the reproduction of selected species of Hypnea (Rhodophyta, Gigartinales) from Hawaii. Bot. Mar., 19, 341–346. Müller, D.G., 1981. Sexuality and sex attraction. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley, 17, 661–674. Müller, D.G., 1986. The role of pheromones in sexual reproduction of kelps. Monografias biologicas, 4, 245–254. Müller, S. & Clauss, H., 1976. Aspects of photomorphogenesis in the brown alga Dictyota dichotoma. Z. Pflanzenphysiol., 78, 461–465. Nakahara, H. & Masuda, M., 1971. Type of life cycle and geographical distribution of marine green and brown algae in Japan. Mar. Sci. Mon., 3(III), 24–26. (Japanese, with English summary). Nakamura, Y., 1954. The structure and reproduction of the genera Ceramium and Compylaephora in Japan with special reference to criteria of classification. Sci. Pap. Inst. Algol. Res. Fac. Sci. Hokkaido Univ., 4, 15– 62. Nasr, A.H. & Bekheet, I.A., 1970. Effect of certain trace elements and soil extract on some marine algae. Hydrobiologia, 36, 53–60.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
269
Neushul, M., 1972a. Functional interpretation of benthic marine algal morphology. In, Contributions to the Systematics of Benthic Marine Algae of the Northern Pacific, edited by I.A.Abbott & M.Kurogi, Japanese Society of Phycologists, Kobe, Japan, pp. 47–74. Neushul, M., 1972b. Underwater microscopy with an encased incident-light dippingcone microscope. J. Microsc. (Oxford), 95, 421–424. Neushul, M., Coon, D.A. & Charters, A.C., 1972. Direct observation of algal spores under natural conditions. Proc. Int. Seaweed Symp., 7, 231–236. Neushul, M. & Dahl, A.L., 1967. Composition and growth of subtidal parvosilvosa from Californian kelp forests. Helgol. Wiss. Meeresunters., 15, 480–488. Neushul, M., Foster, M.S., Coon, D.A., Woessner, J.W. & Harger, B.W., 1976. An in situ study of recruitment, growth and survival of subtidal marine algae: techniques and preliminary results. J. Phycol., 12, 397–408. Ngan, Y. & Price, I.R., 1979. Systematic significance of spore size in the Florideophyceae (Rhodophyta). Br. Phycol. J., 14, 285–303. Ngan, Y. & Price, I.R., 1980. Seasonal growth and reproduction of intertidal algae in the Townsville region (Queensland, Australia). Aquat. Bot., 9, 117–134. Ngan, Y. & Price, I.R., 1983. Periodicity of spore discharge in tropical Florideophyceae (Rhodophyta). Br. Phycol. J., 18, 83–95. Niemeck, R.A. & Mathieson, A.C., 1976. An ecological study of Fucus spiralis L. J. Exp. Mar. Biol. Ecol., 24, 33–48. Niesembaum, R.A., 1988. The ecology of sporulation by the macroalga Ulva lactuca L. (Chlorophyceae). Aquat. Bot., 32, 155–166. Nilsen, G. & Nordby, O., 1975. A sporulation-inhibiting substance from vegetative thalli of the green alga Ulva mutabilis Foyn. Planta, 125, 127–140. Norall, T.T., Mathieson, A.C. & Kilar, J.A., 1981. Reproductive ecology of four subtidal red algae. J. Exp. Mar. Biol. Ecol., 54, 119–136. Noro, T., Masaki, T. & Akioka, H., 1983. Sublittoral distribution and reproductive periodicity of crustose coralline algae (Rhodophyta, Cryptonemiales) in southern Hokkaido, Japan. Bull. Fac. Fish. Hokkaido Univ., 34, 1–10. North, W.J., 1971a. Introduction and background. In, The Biology of Giant Kelp Beds (Macrocystis) in California, edited by W.J.North, Nova Hedw. Beih., 32, 1–97. North, W.J., 1971b. Culturing and dispersing Macrocystis embryos. In, Kelp Habitat Improvement Project. Annual report, W.M.Keck Laboratory of Environmental Health Engineering, California Institute of Technology, pp. 42– 54. North, W.J., 1972. Mass cultured Macrocystis as a means of increasing kelp stands in nature. Proc. Int. Seaweed Symp., 7, 394–399. North, W.J., Mitchell, C.T. & Jones, L.G., 1969. Mass culture of Macrocystis. In, Kelp Habitat Improvement Project. Annual report, W.M.Keck Laboratory of Environmental Health Engineering, California Institute of Technology, pp. 48– 69. Northcraft, R.D., 1948. Marine algal colonization on the Monterey Peninsula, California. Am. J. Bot., 35, 396–404. Norton, T.A., 1977a. The growth and development of Sargassum muticum (Yendo) Fensholt. J. Exp. Mar. Biol. Ecol., 26, 41–53. Norton, T.A., 1977b. Ecological experiments with Sargassum muticum. J. Mar. Biol. Assoc. U.K., 57, 33–43. Norton, T.A., 1978. The factors influencing the distribution of Saccorhiza polyschides in the region of Lough Ine. J. Mar. Biol. Assoc. U.K., 58, 527–536. Norton, T.A., 1981. Gamete expulsion and release in Sargassum muticum. Bot. Mar., 24, 465–470. Norton, T.A. & Fretter, R., 1981. The settlement of Sargassum muticum propagules in stationary and flowing water. J. Mar. Biol. Assoc. U.K., 61, 929–940.
270
BERNABÉ SANTELICES
Norton, T.A. & Mathieson, A.C., 1983. The biology of unattached seaweeds. In, Progress in Phycological Research, Vol. 2, edited by F.E.Round & D.J. Chapman, Elsevier, Amsterdam, pp. 333–386. Norton, T.A., Mathieson, A.C. & Neushul, M., 1981. Morphology and environment. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley, 17, pp. 421–455. Novaczek, I., 1984a. Development and phenology of Ecklonia radiata at two depths in Goat Island Bay, New Zealand. Mar. Biol., 81, 189–197. Novaczek, I., 1984b. Response of Ecklonia radiata (Laminariales) to light at 15°C with reference to the field light budget at Goat Island Bay, New Zealand. Mar. Biol., 80, 263–272. Ogata, E., 1953. Some experiments on the settling of spores of red algae. Bull Soc. Pl. Ecol. Tokyo, 3, 128–134. Ohno, M., 1972. The periodicity of gamete liberation in Monostroma. Proc. Inst. Seaweed Symp., 7, 405–409. Ohno, M. & Arasaki, S., 1967. Pigments in spores and thallus of Ulva pertusa. Inf. Bull. Planktology Japan, 187–190. Ohno, M. Arasaki, S., 1969. Examination of the dark treatment at spore stage of seaweeds. Bull. Jap. Soc. Phycol., 27, 37–42. Ojeda, P. & Santelices, B., 1984. Ecological dominance of Lessonia nigrescens (Phaeophyta) in central Chile. Mar. Ecol. Prog. Ser., 19, 83– 91. Okuda, T. & Neushul, M., 1981. Sedimentation studies on red algal spores. J. Phycol., 17, 113–118. Oltmanns, F., 1904. Morphologie und Biologie der Algen, Vol. I. Fisher, Jena, 733 pp. Oza, R.M., 1975. Studies on Indian Gracilaria. I. Carpospores and tetraspore germination and early stages of development in Gracilaria corticata J. Ag. Bot. Mar., 18, 199–201. Oza, R.M., 1977. Culture studies on induction of tetraspores and their subsequent development in the red alga Falkenbergia rufolanosa (Harvey) Schmitz. Bot. Mar., 20, 29–32. Oza, R.M. & Krishnamurthy, V., 1968. Studies on carposporic rhythm of Gracilaria verrucosa (Huds.) Papenf. Bot. Mar., 11, 118–121. Padilla, D., 1981. Selective factors influencing the morphology of coralline algae. M.Sc. thesis, Oregon State University, Corvallis, Oregon, USA, 112 pp. Paine, R.T., 1979. Disaster, catastrophe and local persistence of the sea palm, Postelsia palmaeformis. Science, 205, 685–687. Paine, R.T., 1988. Habitat suitability and local population persistence of sea palm Postelsia palmaeformis. Ecology, 69, 1787–1794. Paine, R.T., Slocum, C.J. & Duggins, D.O., 1979. Growth and longevity in the crustose red alga Petrocelis middendorfii. Mar. Biol., 51, 185–192. Paya, I. & Santelices, B., 1989. Macroalgae survive digestion by fishes. J. Phycol., 25, 186–188. Pearlmutter, N.L. & Vadas, R.L., 1978. Regeneration of thallus fragments of Rhodochorton purpureum (Rhodophyceae, Nemalionales). Phycologia, 17, 186–190. Pearse, J.S., Clark, M.E., Leighton, D.L., Mitchell, C.T. & North, W.J., 1970. Marine waste dispersal and sea urchin ecology. In, Kelp Habitat Improvement Project. Ann. Rep. California Institute of Technology, Pasadena, California, pp. 1–87. Pearse, J.S. & Hines, A.H., 1979. Expansion of a central California kelp forest following the mass mortality of sea urchins. Mar. Biol. 51, 83–91.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
271
Pedersen, P.M., 1981. Phaeophyta: Life histories. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, University of California Press, Berkeley, pp. 194–217. Pérès, J.M., 1982. Specific pelagic assemblages. In, Marine Ecology. A Comprehensive, Integrated Treatise on Life in Oceans and Coastal Waters, Vol. 5, edited by O. Kinne, John Wiley & Sons, New York, pp. 313–372. Perez, R., 1971. Influence de quelques facteurs physiques sur le developpement de Laminaria digitata (L.) Lamour. Bull. Soc. Phycol. Fr., 16, 89–105. Peyriere, M., 1970. Evolution de 1’appareil Golgi de la tetrasporogenese de Griffithsia flosculosa (Rhodophycea, Ceramiacee). C.R. Acad. Sci., 270, 2072– 2074. Pianka, E.R., 1970. On r- and k-selection. Am. Nat., 104, 592–597. Pickmere, E.S., Parsons, M., & Bailey, R.W., 1973. Composition of Gigartina carrageenan in relation to sporophyte and gametophyte stages of the life cycle. Phytochemistry, 12, 2441–2444. Polanshek, A.R. & West, J.A., 1977. Culture and hybridization studies on Gigartina papillata (Rhodophyta). J. Phycol., 13, 141–149. Polne-Fuller, M. & Gibor, A., 1984. Developmental studies in Porphyra. Blade differentiation in Porphyra perforata as expressed by morphology, enzymatic digestion, and protoplast regeneration. J. Phycol., 20, 609–616. Pringle, J.D., 1986. Swarmer release and distribution of life-cycle phases of Enteromorpha intestinalis (L.) (Chlorophyta) in relation to environmental factors. J. Exp. Mar. Biol. Ecol., 100, 97–111. Provasoli, L., 1965. Growing marine seaweeds. Proc. Int. Seaweed Symp., 4, 9– 17. Pueschel, C.M. & Cole, K.M., 1985. Ultrastructure of germinating carpospores of Porphyra variegata (Kjellm.) Hus. (Bangiales, Rhodophyta). J. Phycol., 21, 146–154. Raju, P.V. & Venugopal, R., 1971. Appearance and growth of Sargassum plagiophyllum (Mert.) C.Agardh on a fresh substrate. Bot. Mar., 14, 36–38. Ramus, J., 1969. The developmental sequence of the marine red alga Pseudogloiephloea in culture. Univ. Calif., Berkeley Publ. Bot., 52, 1–28. Ramus, J., 1971. Codium: the invader. Discovery, 6, 59–68. Rao, C.S.P., 1969. In situ germination of tetraspores of Gymnothamnion elegans (Sch.) J.Agardh. Phykos, 8, 52–55. Rao, P.S., 1971. Studies on Gelidiella acerosa (Forsskal) Feldmann et Hamel. IV. Spore studies. Bull. Jap. Soc. Phycol., 19, 9–14. Reed, D.C., 1987. Factors affecting the production of sporophylls in the giant kelp Macrocystis pyrifera (L.) C.Agardh. J. Exp. Mar. Biol. Ecol., 113, 61–69. Reed, D.C. & Foster, M.S., 1984. The effects of canopy shading on algal recruitment and growth in a giant kelp forest. Ecology, 65, 937–948. Reed, D.C., Laur, D.R. & Ebeling, A.W., 1988. Variation in algal dispersal and recruitment: the importance of episodic events. Ecol. Monogr., 58, 321–335. Reekie, E.G. & Bazzaz, F.A., 1987a. Reproductive effort in plants. 1. Carbonallocation to reproduction. Am. Nat., 129, 876–896. Reekie, E.G. & Bazzaz, F.A., 1987b. Reproductive effort in plants. 2. Does carbon reflect the allocation of other resources? Am. Nat., 129, 897–906. Reekie, E.G. & Bazzaz, F.A., 1987c. Reproductive effort in plants. 3. Effect of reproduction on vegetative activity. Am. Nat., 129, 907–919. Rietema, H., 1982. Effects of photoperiod and temperature on macrothallus initiation in Dumontia contorta (Rhodophyta). Mar. Ecol. Prog. Ser., 8, 187– 196. Rietema, H. & Breeman, A.M., 1982. The regulation of the life history of Dumontia contorta in comparison to that of several other Dumontiaceae (Rhodophyta). Bot. Mar., 25, 569–576.
272
BERNABÉ SANTELICES
Rosenthal, R.J., Clarke, W.D. & Dayton, P.K., 1974. Ecology and natural history of a stand of giant kelp, Macrocystis pyrifera, off Del Mar, California. Fish. Bull., 72, 670–684. Russell, G., 1967. The ecology of some free-living Ectocarpaceae. Helgol. Wiss. Meeresunters., 15, 155–162. Sanbonsuga, Y. & Hasegawa, Y., 1969. Studies on Laminariales in culture. II. Effects of culture conditions on the zoosporangium formation in Costaria costata (Turn.) Saunders. Bull. Hokkaido Reg. Fish. Lab., 35, 198–202. Santelices, B., 1977. Ecologia de Algas Marinas Bentonicas. Efecto de Factores Ambientales. Editiones Vicerrectoría Académica, Universidad Catolica de Chile, 488 pp. Santelices, B., Castilla, J.C., Cancino, J. & Schmiede, P., 1980. Comparative ecology of Lessonia nigrescens and Durvillaea antarctica (Phaeophyta) in central Chile. Mar. Biol., 59, 119–132. Santelices, B. & Correa, J., 1985. Differential survival of macroalgae to digestion by intertidal herbivore molluscs. J. Exp. Mar. Biol. Ecol., 88, 183–191. Santelices, B., Correa, J. & Avila, M., 1983. Benthic algal spores surviving digestion by sea urchins. J. Exp. Mar. Biol. Ecol., 70, 263–269. Santelices, B., & Doty, M.S., 1989. A review of Gracilaria farming. Aquaculture, 78, 95–133. Santelices, B. & Fonck, E., 1979. Ecologia y cultivo de Gracilaria lamamaeformis en Chile central. In, Actas I Symp. Alg. Mar. Chilenas. Subsecretaria de Pesca, Ministerio de Econmomia, Fomento y Reconstruccion, Santiago, Chile, pp. 165– 200. Santelices, B. & Martinez, E., 1988. Effects of filter-feeders and grazers on algal settlement and growth in mussel beds. J. Exp. Mar. Biol. Ecol., 118, 281–306. Santelices, B., Montalva, S. & Oliger, P., 1981. Competitive algal community organization in exposed intertidal habitats from central Chile. Mar. Ecol. Prog. Ser., 6, 267–276. Santelices, B. & Norambuena, R., 1987. A harvesting strategy for Iridaea laminarioides in central Chile. Hydrobiologia, 151/152, 329–333. Santelices, B. & Ojeda, P., 1984a. Effects of canopy removal on the understory algal community structure of coastal forests of Macrocystis pyrifera from southern South America. Mar. Ecol. Prog. Ser., 14, 165–173. Santelices, B. & Ojeda, P., 1984b. Population dynamics of coastal forests of Macrocystis pyrifera in Puerto Toro, Isla Navarino, southern Chile. Mar. Ecol. Prog. Ser., 14, 175–183. Santelices, B. & Ojeda, P., 1984c. Recruitment, growth and survival of Lessonia nigrescens (Phaeophyta) at various tidal levels in exposed habitats of central Chile. Mar. Ecol. Prog. Ser., 19, 73–82. Santelices, B. & Paya, I., 1989. Digestion survival of algae: some ecological comparisons between free spores and propagules in fecal pellets. J. Phycol., 25, 693–699. Santelices, B. & Ugarte, R., 1987. Algal life-history strategies and resistance to digestion. Mar. Ecol. Prog. Ser., 35, 267–275. Santelices, B. & Vera, M.E., 1984. Variacion estacional de la flora marina de Caleta Horcon, Chile central. Phycol. Lat. Am., 2, 83–101. Sawada, T., 1978. Periodic fruiting of Ulva pertusa at three localities in Japan. Proc. Int. Seaweed Symp., 7, 229–230. Schiel, D.R., 1985a. A short-term demographic study of Cystoseira osmundacea (Fucales: Cystoseiraceae) in central California. J. Phycol., 21, 99–106. Schiel, D.R., 1985b. Growth, survival and reproduction of two species of marine algae at different densities in natural stands. J. Ecol., 73, 199–217. Schiel, D.R. & Choat, J.H., 1980. Effects of density on monospecific stands of marine algae. Nature (London), 285, 324–326.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
273
Schiel, D.R. & Choat, J.H., 1981. Micrograzers may affect macroalgal density: a reply. Nature (London), 292, 177 only. Schonbeck, M.W. & Norton, T.A., 1978. Factors controlling the upper limits of fucoid algae on the shore. J. Exp. Mar. Biol. Ecol., 31, 303–313. Schonbeck, M.W. & Norton, T.A., 1980. Factors controlling the lower limits of fucoid algae on the shore. J. Exp. Mar. Biol. Ecol., 43, 131–150. Searles, R.B., 1980. The strategy of the red algal life history. Am. Nat., 115, 113– 120. Seiderer, L.J. & Newell, R.C., 1985. Relative significance of phytoplankton, bacteria and plant detritus as carbon and nitrogen resources for the kelp bed filter-feeders Choromytilus meridionalis. Mar. Ecol. Prog. Ser., 22, 121–139. Seoane-Camba, J., 1966. Algunos datos de interes en la recoleccion de Gelidium sesquipedale. Junta de Estudios de Pesca. Publicaciones Tecnicas. Madrid., 5, 437–455. Seoane-Camba, J., 1969. Crecimiento, produccion y desprendimiento de biomasa en Gelidium sesquipedale (Chem.) Thuret. Proc. Int. Seaweed Symp., 6, 365–374. Seshappa, G., 1956. Observations on the recolonization of denuded intertidal rocks. J. Univ. Bombay, 24, 12–27. Shannon, R.K., Crow, G.E & Mathieson, A.C, 1988. Recruitment patterns of Petalonia fascia (O.F.Muller) Kuntze and Scytosiphon lomentaria (Lyngbye) Link var. lomentaria in New Hampshire, USA. Bot. Mar., 31, 207–214. Sheader, A. & Moss, B., 1975. Effect of light and temperature on germination and growth of Ascophyllum nodosum (L.) Le Jol. Estuarine Coastal Mar. Sci., 3, 125–132. Sideman, E.J. & Mathieson, A.C., 1983. The growth, reproductive phenology, and longevity of non-tide-pool Fucus distichus (L.) Powell in New England. J. Exp. Mar. Biol. Ecol., 68, 111–127. Slocum, C.J., 1980. Differential susceptibility to grazers in two phases of an intertidal alga: advantages of heteromorphic generations. J. Exp. Mar. Biol. Ecol., 46, 99–110. Smayda, T.J., 1970. The suspension and sinking of phytoplankton in the sea. Oceanogr. Mar. Biol. Annu. Rev., 8, 353–14. Smith, A.H., Nichols, K. & McLachlan, J., 1984. Cultivation of seamoss Gracilaria in St. Lucia, West Indies. Hydrobiologia, 116/117, 249–251. Smith, B.D., 1986. Implications of populations dynamics and interspecific competition for harvest and management of the seaweed Laminaria. Mar. Ecol. Prog. Ser., 33, 7–18. Smith, G.M., 1947. On reproduction of some Pacific coast species of Ulva. Am. J. Bot., 34, 80–87. Smith, R., 1967. Sublittoral ecology of marine algae on the North Wales coast. Helgol. Wiss. Meeresunters., 15, 467–469. Sournia, A., 1981. Morphological bases of competition and succession. In, Physiological Bases of Phytoplankton Ecology, edited by T.Platt, Can. Bull. Fish. Aquat. Sci., 210, pp. 339–346. Sousa, W.P., 1984. Intertidal mosaics: patch size, propagule availability, and spatially variable patterns of succession. Ecology, 65, 1918–1935. Sreenivasa Rao, P., 1974. Studies on Gelidiella acerosa (Forsskal) Feldmann et Hamel. II. Growth and phenological events in the annual life of an alga. Phykos, 13, 7–15. Stebbins, G.L. & Hill, G.J.C., 1980. Did multicellular plants invade the land? Am. Nat., 115, 342–353. Stegenga, H. & Mol, L, 1983. Flora van de Nederlandse Zeewieren. Koninkl. Ned. Natuurhist. Ver., Hoodwoud, Netherlands, 263 pp. Steneck, R.S., 1982. A limpet-coralline algal association: adaptations and defenses between a selective herbivore and its prey. Ecology, 63, 507–522.
274
BERNABÉ SANTELICES
Steneck, R.S. & Watling, L., 1982. Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar. Biol., 68, 299–319. Sundene, O., 1962. The implications of transplant and culture experiments on the growth and distribution of Alaria esculenta. Nytt Mag. Bot., 9, 155–174. Suto, S., 1950a. Shedding, floating and fixing of the spores of Gelidium. Bull. Jap. Soc. Sci. Fish., 15, 671–673. Suto, S., 1950b. Studies on a counting method of spores of seaweeds in the sea. Bull. Jap. Soc. Sci. Fish., 15, 674–677. Suto, S., 1950c. Shedding, floating and fixing of spores of seaweeds. Bull. Jap. Soc. Sci. Fish., 16, 1–9. Svedelius, N., 1929. An evaluation of the structural evidences for genetic relationships in plants: Algae. Proc. Int. Congr. Plant Sci., Ithaca, 1, 457– 71. Sweeney, B.M., 1983. Circadian time-keeping in eukaryotic cells, models and hypothesis. In, Progress in Phycological Research, Vol. 2, edited by F.E.Round & D. J.Chapman, Elsevier, Amsterdam, pp. 189–226. Tanner, C.E., 1981. Chlorophyta: Life Histories. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley, 17, 218–247. Taylor, J.E., 1967. Codium reported from a New Jersey estuary. Bull. Torrey Bot. Club., 94, 57–59. Tokida, J. & Yamamoto, H., 1965. Syntagmatic germination of tetraspores in Pachymeniopsis yendoi. Phycologia, 5, 15–20. Toth, R., 1974. Sporangial structure and zoosporogenesis in Chorda tomentosa (Laminariales). J. Phycol., 10, 170–185. Toth, R., 1976. The release, settlement and germination of zoospores in Chorda tomentosa (Laminariales). J. Phycol., 12, 222–233. Townsend, C. & Lawson, G., 1972. Preliminary results on factors causing zonation in Enteromorpha using a tide simulating apparatus. J. Exp. Mar. Biol. Ecol., 8, 265–276. Tripodi, G., 1974. Ultrastructural changes during carpospore formation in the red alga Polysiphonia. J. Submicrosc. Cytol., 6, 275–286. Tsuda, R.T., 1965. Marine algae from Laysan Island with additional notes on the vernacular flora. Atoll Res. Bull, 110, 1–31. Tsuda, R.T., Larson, H.K. & Lujan, R.J., 1972. Algal growth on beaks of live parrot fishes. Pac. Sci., 26, 20–23. Turner, T., 1983. Facilitation as a successional mechanisms in a rocky intertidal community. Am. Nat., 121, 729–738. Tveter, E. & Mathieson, A.C., 1976. Sporeling coalescence in Chrondrus crispus (Rhodophyceae). J. Phycol., 12, 110–118. Umamaheswara Rao, M., 1974. Observations on fruiting cycle, spore output and germination of tetraspores of Gelidiella acerosa in the gulf of Mannar. Bot. Mar., 17, 204–207. Umamaheswara Rao, M. & Kaliaperumal, N., 1983. Effects of environmental factors on the liberation of spores from some red algae of Visakhapatnam coast. J. Exp. Mar. Biol. Ecol., 70, 45–53. Umamaheswara Rao, M. & Subbarangaiah, G., 1981. Effects of environmental factors on the diurnal periodicity of tetraspores of some Gigartinales (Rhodophyta). Proc. Int. Seaweed Symp., 10, 209–214. Underwood, A.J., 1980. The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia (Berlin), 46, 201–213. Underwood, A.J., 1981. Structure of a rocky intertidal community in New South Wales: patterns of vertical distribution and seasonal changes. J. Exp. Mar. Biol. Ecol., 51, 57–85.
REPRODUCTION, DISPERSAL AND RECRUITMENT IN SEAWEEDS
275
Underwood, A.J. & Denley, E.J., 1984. Paradigms, explanations and generalizations in models for the structure of intertidal communities on rocky shores. In, Ecological Communities: Conceptual Issues and the Evidence, edited by D.Strong et al., Princeton University Press, Princeton, New Jersey, pp. 151–180. Underwood, A.J. & Jernakoff, P., 1981. Effects of interactions between algae and grazing gastropods on the structure of a low-shore intertidal algal community. Oecologia (Berlin), 48, 221–233. Underwood, A.J. & Jernakoff, P., 1984. Effects of tidal height, wave-exposure, seasonality and rockpools on grazing and the distribution of intertidal macroalgae in New South Wales. J. Exp. Mar. Biol. Ecol., 75, 71–96. Vadas, R.L., 1977. Preferential feeding: An optimization strategy in sea urchins. Ecol Monogr., 47, 337–371. Vadas, R.L., 1979. Seaweeds: an overview; ecological and economical importance. Experientia, 35, 435–37. Vadas, R.L., 1986. Recruitment, growth and management of Ascophyllum nodosum. In, Actas II Congr. Alg. Mar. Chilenas, edited by R.Westermeier, Universidad Austral de Chile, Valdivia, Chile, pp. 101–113. Van der Meer, J.P., 1977. Genetics of Gracilaria sp. (Rhodophyceae, Gigartinales). II. The life history and genetic implications of cytogenetic failure during tetraspore formation. Phycologia, 16, 367–371. Vandermeulen, H. & DeWreede, R.E., 1986. The phenology, mortality, dispersal and canopy species interaction of Colpomenia peregrina (Sauv.) Hamel in British Columbia. J. Exp. Mar. Biol. Ecol., 99, 31–47. Varma, R.P., 1959. Studies on the succession of marine algae on a fresh substratum in Palk Bay. Proc. Indian Acad. Sci., 49, 245–263. Velimirov, B., 1980. Formation and potential trophic significance of marine foam near kelp beds in the Benguela upwelling system. Mar. Biol., 58, 311–318. Velimirov, B. & Griffiths, C.L., 1979. Wave-induced kelp movement and its importance for community structure. Bot. Mar., 22. 169–172. Vermaat, J.E. & Sand-Jensen, K., 1987. Survival, metabolism and growth of Ulva lactuca under winter conditions: a laboratory study of bottlenecks in the life cycle. Mar. Biol., 95, 55–61. Vernet, P. & Harper, J.L., 1980. The cost of sex in seaweeds. Biol. J. Linn. Soc., 13, 129–138. Vidaver, W., 1972. Pressure. Plants. In, Marine Ecology. A comprehensive treatise on life in oceans and coastal waters, Vol. 1, edited by O.Kinne, WileyInterscience, New York, pp. 1389–1405. Vielhaben, V., 1963. Zur Deutung des semilunaren Fortflanzungs-zykls von Dictyota dichotoma. Z. Bot., 51, 156–173. Waaland, J.R., 1975. Differences in carrageenan in gametophytes and tetrasporophytes of red algae. Phytochemistry, 14, 1359–1362. Walsby, A.E. & Reynolds, C.S., 1981. Sinking and floating. In, Physiological Ecology of Phytoplankton, edited by I.Morris, Blackwell Scientific Publications, Oxford, pp. 371–412. Wassman, R., & Ramus, J., 1973. Seaweed invasion. Nat. Hist., 82, 24–36. Watanabe, J.M., 1984. The influence of recruitment, competition and benthic predation on spatial distribution of three species of kelp forest gastropods (Trochidae: Tegula). Ecology., 65, 920–936. Watson, D.S. & Norton, T., 1985. Dietary preference of the common periwinkle, Littorina littorea (L.). J. Exp. Mar. Biol. Ecol., 88, 193–211. West, J.A., 1968. Morphology and reproduction of the red alga Acrochaetium pectinatum in culture. J. Phycol., 4, 89–99. West, J.A. & Crump, E., 1975. Carpospore discharge periodicity in excised cystocarpic papillae of Gigartina-Petrocelis (Rhodophyta). J. Phycol., 11 (Suppl.), 17 only.
276
BERNABÉ SANTELICES
West, J.A. & Hommersand, M.H., 1981. Rhodophyta. In, The Biology of Seaweeds, edited by C.S.Lobban & M.J.Wynne, Botanical Monographs, University of California Press, Berkeley, 17, 133–193. West, J.A. & Polanshek, A., 1972. A Gigartina species with a crustose tetrasporophyte. J. Phycol., 8 (suppl.), 11–12. Wetherbee, R., 1978a. Differentiation and continuity of the Golgi apparatus during carposporogenesis in Polysiphonia (Rhodophyta). Protoplasma., 94, 341–345. Wetherbee, R., 1978b. The presence of tubular plasmalemmal structure during carposporogenesis in the red alga Polysiphonia. Protoplasma, 94, 341–345. Wetherbee, R. & West, J.A., 1977. Golgi apparatus of unique morphology during early carposporogenesis in a red alga. J. Ultrastruct. Res., 58, 119–133. Williams, J.L., 1898. Reproduction in Dictyota dichotoma. Ann. Bot. (London), 12, 559–560. Williams, J.L., 1905. Studies in the Dictyotaceae. III: The periodicity of the sexual cells in Dictyota dichotoma. Ann. Bot. ( London), 19, 531–559. Woelkerling, W.J., 1975. On the epibiotic and pelagic Chlorophyceae, Phyaeophyceae and Rhodophyceae of the Western Sargasso Sea. Rhodora, 77, 1–40. Woolery, M.L. & Lewin, R.A., 1973. Influence of iodine on growth and development of the brown alga Ectocarpus siliculosus in axenic cultures. Phycologia, 12, 131–138. Yamada, N., 1976. Current status and future prespects for harvesting and resource management of the agarophyte in Japan. J. Fish. Res. Board Can., 33, 1024– 1030. Yoshida, T., 1963. Studies on the distribution and drift of the floating seaweeds. Bull. Tohoku Reg. Fish. Res. Lab., 23, 141–186. Zaneveld, J.S., 1969. Factors controlling the delimitation of littoral benthic marine algal zonation. Am. Zool., 9, 367–391. Zaneveld, J.S. & Barnes, W.D., 1965. Reproductive periodicities of some benthic algae in lower Chesapeake Bay. Chesapeake Sci., 6, 17–32. Zechman, F.W. & Mathieson, A.C., 1985. The distribution of seaweed propagules in estuarine coastal and offshore waters of New Hampshire, U.S.A. Bot. Mar., 28, 283–294.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 277–352 Margaret Barnes, Ed. Aberdeen University Press
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA IN THE MARINE ENVIRONMENT D.PRIEUR, G.MÉVEL CNRS, LP 4601 and Université P. et M.Curie, Station Biologique, BP 74, 29682 Roscoff, France
J.-L. NICOLAS IFREMER, Centre de Brest, DRV, BP 70, 29280 Plouzané, France
A.PLUSQUELLEC Université de Bretagne Occidentale, IUT, 29000 Quimper, France and
M.VIGNEULLE CNEVA-LPAA, BP 70, 29280 Plouzané, France
ABSTRACT The different kinds of interactions between bivalves (edible and nonedible species) and bacteria in the marine environment are reviewed. Bacteria are used as food by adults and larvae, but may also be accumulated within the digestive tract, in a living state. The particular cases of spirochaetes and cellulolytic bacteria are also considered. In coastal areas exposed to urban pollution, accumulation concerns potentially pathogenic bacteria. The accumulation factors, the risks of human diseases, and the standards of control are reviewed. Recent studies concerning symbiotic bacteria found in the gills of deep-sea hydro thermal vent and cold-seep bivalves are described. Similar associations found in bivalves living in coastal sulphide-enriched environments are also presented. Finally, interactions between bivalves and their environment are considered. All these examples clearly indicate that bivalves represent a fascinating model of invertebratebacteria interactions, and suggest that bacterial flora associated with marine organisms should be more studied in the future.
INTRODUCTION Bivalve molluscs are appreciated as seafood in many countries of the five continents. Oysters, mussels, scallops, and clams are caught from natural beds or, for some particularly valuable species, are cultivated in protected areas. Most of the
278
D.PRIEUR ET AL.
bivalve beds of edible species are located in estuaries, lagoons, and coastal areas and are more or less exposed to polluted waters from continental origin. Since the beginning of the 20th century, several observations suggested that bivalves could contain or accumulate enteric bacteria introduced into the marine environment by sewage discharges and could be responsible for human diseases. For these reasons, bivalves have been intensively analysed by microbiology laboratories to control their quality before being delivered to seafood markets. For a better understanding of the routine data, experiments were carried out to establish rates of accumulation and release of enteric bacteria as a function of environmental conditions. In the years 1950–1960, several workers considered bivalves living in nonpolluted waters from a bacteriological point of view, and published data on the natural microflora of commercial and non-commercial bivalve species. More recently, the role of bacteria in the marine food web has also been investigated, and several experiments have demonstrated that bivalves are able to ingest and digest bacteria. These results, that could appear to be contradictory to previous results, led to consideration of feeding and accumulation as an unusual alimentary process, influenced by environmental conditions and by the bivalve’s physiology. The development of bivalve cultures in the open sea or the production of spat in hatcheries, was accompanied by diseases, some of them produced by bacterial agents. In several cases, the financial cost of the diseases was rather high. The lack of acquired immunity for the bivalves increased the difficulty of controlling the diseases. Consequently, prevention and hygiene are the more efficient tools against bacterial pathology. Because of high densities in some bivalve cultivation areas or natural beds, environmental interactions must not be ignored, and the bivalve’s excretion may influence the immediate environment and subsequently the bivalves themselves. For the above reasons, edible species of bivalves have been the more studied. Interesting data have, however, been published about non-edible species, particularly in the last ten years. The discovery of deep-sea hydrothermal vents and their associated fauna, led to the investigation of symbiotic interactions between bacteria and bivalves from vent sites, and also from coastal zones. The aim of this review is to gather data dealing with all these different aspects of interactions between bivalves and bacteria in the marine environment.
BACTERIA AS FOOD FOR BIVALVES After ZoBell & Feltham showed in 1937 that the mussel, Mytilus californianus could grow with bacteria as one source of food, many experiments and observations have been carried out in order to prove the role played by bacteria in the nutrition of bivalves. We have tried to synthesise the data although the species and ecosystems studied are very scattered. BACTERIAL YIELD IN THE NATURAL ENVIRONMENT
Bacterioplankton occurs in all ecosystems of the ocean and especially in coastal and estuarine sea water. In the sea-water column, Sorokin (1978) estimated that
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
279
the bacterial yield was equivalent to the phytoplankton yield. All authors agree, however, that the main production of bacteria is achieved by the phytoplankton excretion or dying microalgae (Nienhuis, 1981). The growth of bacterioplankton occurs just after the maximal production of phytoplankton (McManus & Peterson, 1988) and consequently, the heterotrophic bacterial yield is always lower in rank than the phytoplankton yield. According to Ferguson & Rublee (1976), the amount of bacterial carbon in coastal water may range between 4% and 25% of total biomass of carbon. Meyer-Reil (1977) found a bacterial biomass production in Kiel Fjord and Bight (Baltic) between 15% and 29% of the primary production. McManus & Peterson (1988) found that bacterial production reached up to 50% of primary production in upwelling systems. Finally, Cole, Stuart & Michael (1988) concluded in a recent review that bacterial production may range from 0.4 up to 150 µg C·l -1·day -1 and reach an average of 20% of the planktonic primary production. Recently, several authors (Johnson & Sieburth, 1979, 1982; Joint & Pomroy, 1983; Murphy & Haugen, 1985; Booth, 1988; Fenchel, 1988) assumed that phytoplankton as small as <1 µm including cyanobacteria and eucaryotic algae are widespread in the sea. In the Atlantic and Pacific tropical oceans, Gieskes & Kraay (1986) and Li et al. (1983) found between 20 and 80% of the production in the <1 µm-size fraction. In the subarctic Pacific Ocean, the primary production of picoplankton was essentially due to cyanobacteria, Synechococcus spp, and contributed between 16 and 40% to plant carbon. Cyanobacteria may have been under-estimated when the counts were performed by epifluorescence (Schubert, Shiewer & Tschirner, 1989). The bacterial part of primary production must also be considered as a potential food resource for bivalves. The conversion efficiency of the bacterioplankton depends on the C/N ratio of phytoplankton debris (Stuart, Newell & Lucas, 1982). The conversion efficiency is approximately 10% for carbon, whereas it is 80% for nitrogen. Because the conversion efficiency of carbon only ranges from 10 to 15%, Stuart et al. (1982) suggested that bacteria could not provide a substantial amount of carbon for animals in coastal waters. Nevertheless, because they exhibit a C/N lower than that of phytoplankton (3.5 compared with 6.6) (Seiderer & Newell, 1985) they could better meet the nitrogen needs of bivalves. In sediments, the heterotrophic bacterial production is significantly correlated to sediment organic carbon content (Cole, Stuart & Michael, 1988) and sustained by biodeposits of animals (faeces and pseudofaeces) and organic particles from phytoplankton and macrovegetation (Nienhuis, 1981). In most situations, the major part of detritus originates from pelagic algal cells (Blackburn, 1988). In experiments, bacteria first colonise fresh detritus and faecal material. Then, they are progressively replaced by flagellates and ciliates (Newell, Lucas & Linley, 1981; Stuart et al., 1982; Biddanda & Pomeroy, 1988). Experimentally, the conversation efficiency in terms of carbon for decomposition of phytoplankton was about 5% (Newell, Lucas & Linley, 1981). In the natural environment, bacteria of organic sediments are associated with fungi, and microalgae (Tenore, 1988) to transform organic detritus. The net production values of bacteria vary largely according to the location, temperature and sediment characteristics. Blackburn (1988) reported rates of cell production ranging from 1 to 747 mg N·m 2 ·day -1, assuming a C/N molar ratio of 6.25. SIZE OF MARINE BACTERIA Bacteria are dominated by free-living cells but 20–30% of them exist within aggregates exceeding 5 µm in size (Sorokin, 1981; Wangersky, 1977). Jacq &
280
D.PRIEUR ET AL.
Prieur (1986) observed a rate of bound bacteria ranging between 1 and 50% off the west coast of Brittany and in the Bay of Brest. The amount of bacteria in aggregates seems to correlate with dead phytoplankton, detritus and silt (Cammen & Walker, 1982). The size of free-living bacteria varies with available nutrients. Most marine bacteria survive in the form of small cells or even ultramicrocells (Morita, 1985) and more than 80% of bacteria are smaller than 1 µm (Wright et al., 1982; Joint & Pomroy, 1983).
RETENTION EFFICIENCY OF BACTERIA BY BIVALVES
Adult bivalves According to Morton (1983), most lamellibranch bivalves can retain 1 to 2-µm particles, whereas protobranch bivalves are less efficient. The retention seems to depend on the presence of eulaterofrontal cirri (Owen & McCrae, 1976; Wright et al., 1982; Morton, 1983; McHenery & Birkbeck, 1985). Bivalves with large laterofrontal cirri retain small particles more efficiently than bivalves which have small or no laterofrontal cirri. The distance between adjacent laterofrontal cirri is, however, generally 2.0–3.5 µm (Owen, 1978) and cannot explain the retention of 1 to 2-µm particles. Jørgensen (1983) and Riisgård (1988) suggested that the laterofrontal cirri do not act as sieves, but as modulators in a fluid mechanical process of particle retention. All things considered, this point remains very controversial (Wright et al., 1982). In any case, the retention efficiency of most bivalves decreases below 4 to 5-µm particles. For certain bivalves such as Cardium echinatum, Modiolus modiolus, and Arctica islandica, the retention of 1-µm particles (Møhlenberg & Riisgard, 1978) is still substantial but probably not below. As most marine bacteria are smaller than 1 µm, the retention efficiency may not exceed 20–30%. Nevertheless, some particular bivalves, such as Geukensia demissa can retain 0.2 to 0.4-µm and 0.4 to 0.6-µm bacteria with, respectively, 30% and 86% efficiency (Wright et al., 1982). The lack of experiments with bacterioplankton or particles smaller than 1 µm makes it difficult to assess the quantity of bacteria retained by bivalves. Nevertheless, a simple calculation, assuming 20% retention efficiency and a heterotrophic bacterial production estimated around 20% of the phytoplankton production, indicates that free-living bacteria may meet only 4% of bivalve needs. Bacteria could, however, provide more nitrogen for bivalves than carbon, because they contain twice as much nitrogen as phytoplankton (Seiderer & Newell, 1985). In addition, if all bacteria bound to particles are retained, about the same quantity of carbon and nitrogen as that provided by free-living bacteria could be furnished to bivalves. Finally, the total bacterial contributions to bivalve nutrition could reach an average of 8% in terms of carbon. On the west coast of the Cape Peninsula, South Africa, Newell & Field (1983) estimated that bacteria could constitute 9% of the carbon requirement of the benthic community of which the principal species were Aulacomya ater (mussel), Thetya sp (sponges), and Pyura stolonifera (ascidian). Stuart & Klumpp (1984) recorded, for <1-µm particles 20% retention efficiency with Aulacomya ater and 30% with Choromytilus meridionalis. Free bacteria and <1-µm particles could meet
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
281
between 1 and 4% of the carbon requirements of the filter-feeders. Bivalves require much less nitrogen than carbon. Therefore, total bacterial nitrogen could meet 73% of the needs of bivalves according to Newell & Field (1983). This percentage is certainly over-estimated, because the authors did not take into account the retention efficiency. Finally, Seiderer & Newell (1985) denied that free-living bacteria provided the bivalve C. meridionalis with substantial amounts of nutrient, because it retained less than 20% of bacterioplankton (Stuart & Klumpp, 1984); they suggested, however, that bacterial aggregates would be utilised by this mussel. According to Tenore (1988), a part of detrital organic matter such as seagrassderived detritus is directly available for deposit-feeders without undergoing alteration by microbes. Thus, bacteria compete with bivalves for this detritus type. Other detritus, containing refractory material, especially that derived from vascular plants, is assimilated only after slow microbial decomposition. During this long period of “aging”, fresh faecal pellets containing vascular plant detritus are degraded by microbes which transform the refractory material into substrates, especially nitrogen, available for macro-consumers (Tenore, 1988). Finally, the uptake of bacteria by filter-feeding bivalves may vary with the abundance of bacteria, bacteria bound to particles, the species of bivalve, season, and so on. Bacteria are more efficiently ingested by deposit-feeding bivalves. In both cases, bacteria do not seem to constitute the main part of food of bivalves. Bivalve larvae Hardly anything is known about the efficiency of retention by bivalve larvae. The larva of Ostrea edulis does not have the same pattern of retention efficiency as that of adult (Wilson, 1980). Its optimum size of retention is lower than that of adults. For Mytilus edulis veliger, the clearance rate decreases dramatically below 2-µm particles as is the case for adults. Possibly, according to the species, different behaviours are exhibited by larva and adult. No bivalve larvae, however, efficiently retain particles smaller than 1 µm (Bayne, 1983).
VARIATION OF RETENTION EFFICIENCY AND PUMPING RATE
Particle selection was recorded by Shumway et al. (1985) for different algae of the same size and by Kiørboe, Møhlenberg & Nøhr (1980) for algae and silt. No information is available on retention selectivity concerning bacteria themselves and bacteria and algae, except by size. On the other hand, the presence of microalgae increased the clearance rate of free-living bacteria by the mussel, M. edulis (McHenery & Birkbeck, 1985), although bacteria remained free. Production of mucus did not seem to be stimulated by the presence of algae. McHenery & Birkbeck thought that the pumping rate could only be increased with the presence of algae. Therefore, the retention efficiency of bacteria by bivalves could be under-estimated, when determined without algae. MacDonald (1988) observed that the filtration rate of Patinopecten yessoensis veligers was reduced from 40 µl·h -1 to 5 µl·h -1 when the density of larvae increased from 0.5 larva·ml -1 to 2 larvae·ml -1 . Similar results were recently
282
D.PRIEUR ET AL.
obtained with Crassostrea gigas veligers (B. Besse, pers. comm.). Therefore, the pumping rate and the quantity of bacteria retained by veligers in experiments or in a hatchery may be far from that observed at a low density, in the natural environment.
DIGESTION OF BACTERIA BY BIVALVES
Experimental uptake of bacteria by bivalves In experiments, cultured bacteria are rapidly removed by Mytilus edulis, Venus verrucosa, etc from sea water (Prieur, 1981; McHenery & Birkbeck, 1985; Amouroux, 1986a), although as has been previously indicated, the clearance of bacteria requires generally more time than that needed for algae (McHenery & Birkbeck, 1985). Bacteria supplied to Mytilus edulis rapidly filled the whole digestive tract (Prieur, 1981a, b). They were coated by mucus in the stomach where an extracellular lysis occurred as early as 15 min after the addition of bacteria. Labelling experiments demonstrated that cell-wall components passed through the digestive gland for further degradation, while the dissolved material was directly digested and assimilated (McHenery & Birkbeck, 1985). Soluble bacterial components were found in mantle and gill tissues only 1 h after exposure to bacteria. The assimilation efficiency of heterotrophic bacteria appears to be equivalent to that of algae. McHenery & Birkbeck (1985) reported a slightly better assimilation by M. edulis. Amouroux (1986a, b) observed that only 40 to 50% of labelled Lactobacillus were incorporated in the soft tissues of the clam, Venus verrucosa, compared with 60% for algae. Like algae, a part of the assimilated components of bacteria was metabolised within 24 h as a source of energy. The other part was incorporated into soft tissues: gill, muscles, foot, visceral mass. Unfortunately, no information is available on the digest-ability of cyanobacteria. Digestive enzymes A correlation between lysozyme-sensitive bacteria and assimilation by bivalves was reported by Birkbeck & McHenery (1982). Lysozyme-resistant bacteria are rejected by bivalves without degradation. Bacteria are resistant because lysozyme can be inactivated by acidic polymers in the outer layers of the bacteria cell or physically prevented from access to the underlying peptidoglycan, which may also be resistant to lysozyme activity. Significant lysozyme-like activity was found in the style of 30 bivalve species (McHenery & Birkbeck, 1986a). Seiderer et al. (1984), on the basis of bacterial susceptibility to lysozyme, stated that only 57% of bacteria from the sea-water column could be digested by the bivalve, Choromytilus meridionalis. Prieur (1981a, b) did not, however, find lysozymeresistant bacteria among six tested marine bacteria. Finally, it is likely that not all bacteria in the natural environment can be degraded by bivalves. Obviously, this phenomenon reduces the available quantity of bacteria as a source of food for bivalves. In addition, not all the products of bacteria are digested. According to Harvey & Luoma (1984) the deposit-feeding bivalve, Macoma balthica, does
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
283
not efficiently utilise the exopolymer produced in large quantities by bacteria in sediments. Lysozyme from the crystalline style of Mytilus edulis was purified by McHenery & Birkbeck (1979). It was a true lysozyme in accordance to the criteria proposed by Salton (1957) and Jollès (1969). Two optimal pH values (7.1 and 4.6) for lysozyme activity were observed by McHenery & Birkbeck (1982). The tolerance to cations at pH 4.6 suggested that the lysozyme acts in an acidic environment in the stomach. Lysozyme from other bivalves (Ruditapes philippinarum, Pecten maximus) shows, however, some discrepancy with previous results in the effect of cations and optimal pH (Maginot et al., in press). After lysis of bacteria, the enzymes such as proteases (exopeptidase, endopeptidase), carbohydrases, lipases, esterases, and phosphatases act in the digestive tract and in the digestive gland to produce degradation (Reid, 1966; Wojtowicz, 1972). Bacteria are not degraded close to the style and some bacteria can be enclosed intact within the style (Prieur, 1981a, b). The lysozyme and the other enzymes released by the style are likely to act in the stomach where the pH is optimal and co-enzymes are present. Crystalline style extracts from Mytilus edulis can detach bacteria and algae from sediment particles (Lopez, 1980), although bacteria adhere quite firmly to particles (Meyer-Reil et al., 1978). Lopez (1980) did not, however, report whether, in vivo, the detachment occurred in the stomach or close to the crystalline style. Commonly, the role of the crystalline style is to triturate particles against the gastric shield (Morton, 1983) and to provide enzymes in the process of digestion.
DISSOLVED ORGANIC MATTER
The relationship between bacteria, dissolved organic matter (DOM) and bivalves is certainly complex, because the bivalves, like bacteria, release and assimilate DOM (Berland et al., 1976; Rice, Wullis & Stephens, 1980; Manahan & Crisp, 1982; Fergusson, 1982). In a comprehensive review on the direct absorption of DOM, Steward (1979) concluded that free amino acids, carbohydrates, and fatty acids were directly absorbed by various marine invertebrates including bivalves. Bacteria could provide bivalves with DOM as well as competing with them for DOM. Manahan & Richardson (1983) studied the competition between larval mussels and bacteria for dissolved glycine and glucose. Animals can effectively compete with surrounding bacteria for the available DOM in sea water. As observed by Amouroux (1986a), using labelled food, bacteria can recycle an important part of the organic and mineral matter released by the bivalve, Venus verrucosa, if the sea water in the vessel containing the bivalve is not renewed. In previous experiments, Amouroux (1984) emphasised that the exudates of bacteria in sea water were better assimilated by the bivalve, Venus verrucosa than those of the alga, Pavlova lutheri. It is possible that uptake of growth factors such as vitamins, and peptidic hormones could also be performed by bivalves but no data are available on these subjects. Marine bacteria excrete various substances, including amino acids, carbohydrates, and vitamins of group B etc (Kurata, 1986). Therefore, DOM from bacteria could represent a substantial resource of food and eventually growth factors for bivalves. Further investigations are required on this topic.
284
D.PRIEUR ET AL.
GROWTH OF LARVAE WITHOUT BACTERIA
Many authors thought that experiments with axenic bivalve larvae were necessary to assess the uptake of DOM or the influence of bacteria in culture (Rice et al., 1980; Manahan & Crisp, 1982; Stephens, 1982). Hidu & Tubiash (1963) obtained bacteria-free fertilised eggs of Mercenaria mercenaria by repeatedly washing them in sterile sea water and by using antibiotics but in the absence of added algal food, they grew little. Millar & Scott (1967) maintained axenic flat oyster (Ostrea edulis) larvae, previously decontaminated by strong antibiotics solution, over 22 days. Larvae fed on axenic algae, Monochrysis lutheri, grew well, although the conditions of rearing were far from conventional. Langdon (1983) obtained successful axenic larval rearing of oysters (Crassostrea gigas) by aseptic removal of gametes from gonads and in vitro fertilisation. Growth and survival of these axenic larvae fed on axenic algae were close to those of controls, but the conditions of rearing were again different to routine contaminated cultures. Regarding these experiments, it could by concluded that bacteria other than pathogenic bacteria do not influence larval culture. Recent experiments (B. Besse, pers. comm.) in axenic conditions close to conventional conditions did not, however, agree with the previous attempts. Conventional starved larvae of C. gigas increased by 60% in size after 7 days of experiment, whereas starved axenic larvae did not grow. In addition, axenic larvae fed on Pavlova lutheri ingested considerable amounts of algae to reach a growth which was in all cases below that of conventional controls. If this experiment is confirmed, the role of bacteria in larvae culture could be essential.
BACTERIA ASSOCIATED WITH LARVAL CULTURE
Many studies have emphasised the detrimental effect of unchecked bacterial development on larval life (Loosanoff, 1954; Walne, 1956; Guillard, 1959; Elston, 1979). Bacteria isolated during periods of mortality were often true pathogens (see p. 321 ) but many bacteria could produce toxins which slowed down growth (Loosanoff & Davis, 1963). The main control of bacterial development consists of renewing sea water and preventing the introduction of pathogenic bacteria by decontamination of water (Loosanoff & Davis, 1963). For certain species, preventive use of antibiotics seems, however, necessary. The positive effect of streptomycin reported by Hidu & Tubiash (1963) consisted not only in repressing pathogenic strains but also in favouring beneficial bacteria. Antibiotics added without algae into a vessel containing larval Crassostrea virginica encouraged growth, whereas without antibiotics the size of larvae did not increase. Martin & Mengus (1979) emphasised that selected and cultured bacteria offered with algae improved the rate of larval growth of Mytilus provincialis. Particles of a size between 0.22 and 1 µm, in the sea water improved the growth of scallop larvae (Pecten maximus) by up to 20%. Possibly, this may be a bacterium (Samain et al., 1987). There may be as many as 105 or 10 6 cell·ml -1 of bacteria in larval culture vessels but the biomass may be negligible compared with the algae offered (Jeanthon, Prieur & Cochard, 1988). Consequently, bacteria could not provide larvae with substantial amounts of macronutrient but they could produce growth factors
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
285
including vitamins or peptides. Although 10 6 bacterial cells·ml -1 may be maximal level in larval culture, bacteria may be intensively grazed by bivalve larvae and replaced continuously by multiplication. This turnover could explain why bacteria provide starved larvae with sufficient nutrients to induce their growth during the early stages of development. With the exception of ZoBell & Feltham (1937), no authors have suggested that bacteria alone could sustain growth of adult bivalves. Moreover, the growth rate of Mytilus californianus observed by ZoBell & Feltham was very low. Certainly, bacteria cannot support substantial growth because they lack longchain polyunsaturated fatty acids and sterols and they are deficient in essential amino acids (Tenore, 1988). The heterotrophic bacterial yield only represents about 20% of the primary yield in sea-water columns, all bacteria cannot be digested and bivalves retain much less bacterioplankton than phytoplankton. For many bivalves, bacterioplankton may have a minor role in supplying macronutrients. For some bivalves including the filter-feeding Geukensia demissa and the detritus-feeding, Macoma balthica, bacteria could make a greater contribution. From the point of view of an ecologist, the question, however, remains: what is the mean contribution of bacteria to the nutrition of bivalves? In terms of macronutrients they could provide 5 to 10% of the carbon and 20% of the nitrogen requirements. To all appearances, the role of bacteria consists both in supplementing other foods resources and providing the bivalves with growth factors (dissolved or included in bacteria). Further investigations on the role of vitamins, hormones, and co-enzymes in development and growth of bivalves may answer this question. The main grazers of bacteria are certainly the heterotrophic flagellates which occur at densities of 10 3 to 104 cells·ml-1 in nearshore water (Sieburth, Smetacek & Jürgen, 1978; Sherr, Sherr & Newell, 1984; Fenchel, 1988). They only decrease to 5×102 cells·ml -1 in euphotic offshore water. They clear 20– 50% of the freeliving bacteria of the water in 24 h (Fenchel, 1988). In addition, Fuhrman, Ammerman & Azam (1980) found that bacteria were influenced more by phytoplankton biomass than by primary production and suggested the organic source was dissolved organic carbon released by grazing zoo-plankton including ciliates. Consequently, the heterotrophic nanoplankton must be considered in the context of trophic relationships between bivalves and bacteria.
ASSOCIATED MARINE MICROFLORA HETEROTROPHIC BACTERIA ASSOCIATED WITH BIVALVE TISSUES
Digestive tract microflora Bivalve molluscs are appreciated as seafood in many countries, but since the end of the 19th century (Foote, 1895) they have been frequently suspected of being a possible source for bacterial human diseases. Indeed, the records of potential pathogenic bacteria cultivated from bivalve tissues are innumerable, and this point will be considered on pp. 308–310 of this review. Such observations imply that
286
D.PRIEUR ET AL.
bivalves harbour living and culturable bacteria, a point that could, however, be at odds with the bacterial food reported in the previous section. When they published their work on the bacterial flora of marine invertebrates, Colwell & Liston (1962) pointed out that, at that time, “the literature available on the natural flora of marine invertebrates was extremely limited”. Most of the data previously published had dealt with potential pathogens occurring in bivalves collected from sewage-polluted areas, although several non-enteric bacteria (Alcaligenes, Pseudomonas, Vibrio, etc) had also been noticed in some cases (Berry, 1916; Geiger, Ward & Jacobson, 1926; Eliot, 1926). Some works reported by Colwell & Liston (1960) concerning spoilage of edible molluscs had, however, already indicated that some “indigenous marine organisms” (Achromobacter, Pseudomonas, Flavobacterium or Micrococcus) were involved in the spoilage process (Symons, 1921; Hunter & Linden, 1923; Rice, 1929; Tanikawa, 1937; Lartigue, Novak & Fieger, 1960; Novak, Fieger & Stolzle, 1960). Colwell & Liston (1959, 1960) carried out an extensive study on the natural flora of the Pacific oyster, Crassostrea gigas. They found that the predominant genera were Achromobacter, Flavobacterium, Pseudomonas, and Vibrio, the last two genera being reported together. Ambient sea water was not analysed in the same way. Brisou et al. (1962) described 44 strains isolated from Mytilus galloprovincialis collected in the Mediterranean Sea, that they assigned to the genus Vibrio. The proportion of this particular genus within the total microflora was not indicated nor the methods used for processing the bivalve (grinding, dissection) for analysis. Chakroun (1964) studied the microflora associated with the digestive tract of M. galloprovincialis, and made viable counts and phenotypic characterisation of isolates from the gills, mantle, and digestive tract. The digestive tract contained the highest numbers of bacteria. Achromobacter and Vibrio were the most represented genera, and proteolytic bacteria were the most abundant in the digestive tract. This qualitative study involved, however, only 29 isolates. Lovelace, Tubiash & Colwell (1968) analysed the microflora associated with Crassostrea virginica from two sites in Chesapeake Bay (USA), including the surrounding sea water and sediment. For the oysters, they analysed the gills and the water of the mantle cavity. Different results were obtained according to the collection site but in most cases, the genus Vibrio was the most abundant, particularly for one site, where it represented as much as 50% of the isolates. Murchelano & Brown (1968) also studied the microflora associated with C. virginica, but not the surrounding sea water. They noted the importance of the genus Pseudomonas (31.2%), then the genera Flavobacterium/Cytophaga (26%) and Vibrio (25%), for a set of 96 isolates. They also noted a high percentage of proteolytic strains (87.4%). Murchelano & Bishop (1969) isolated bacteria associated with the juveniles of Crassostrea virginica, reared in a hatchery. The molluscs and surrounding sea water were analysed in the same way, but it seems that the procedure of pure strain isolation was not suitable for comparing the structures of the bacterial communities studied. Cundell & Young (1975) studied the role of the microflora occurring in the hind gut of Mya arenaria, in the degradation of hydrocarbons contained in polluted sediments. Using a culture medium supplemented with hydrocarbons, they isolated only 7 strains, belonging to the genera Achromobacter, Vibrio, Corynebacterium, Arthrobacter, Flavobacterium, and Pseudomonas. Martin
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
287
(1976) published the results of a single analysis of the sea water collected over a mussel bed, and of the gut of mussels from the same area. He showed the abundance of the bacterial communities living in the gut. The gut isolates were mainly assigned to the Vibrionaceae, while these bacteria were rare in the sea water. He estimated the number of gut bacteria as 2.5×10 6 CFU (colony forming units) per gram of intestine. Rajagopalan & Sivalingam (1978) studied the bacterial flora of a cultured green mussel, Mytilus viridis, and of a naturally occurring rock oyster, Crassostrea cuculata. The stomach and the adjacent tissues, and the rest of the flesh, were separately processed and analysed. Gram negative bacteria (Pseudomonas, Vibrio, Achromobacter, Escherichia, and Neisseria) and also Gram positive genera (Corynebacterium, Streptococcus, and Micrococcus) were found in both kinds of samples. Bacterial counts were found to be higher in the digestive tissues of both species, than in the rest of the flesh. Bianchi et al. (1979) analysed the bacteria associated with the digestive tracts of deep-sea invertebrates, including one bivalve species, probably starved, which had only few associated bacteria. Prieur (1981b), published data on the microflora of adults of Venerupis semidecussata and Mytilus edulis, on larvae of Crassostrea gigas and Venerupis semidecussata, and on different larval and post-larval stages of Mytilus edulis reared in an experimental hatchery. For all the samples analysed, he noted a higher proportion of Gram negative fermentative bacteria in the ground whole flesh than in the surrounding sea water. These bacteria were assigned to the genera Photobacterium and Vibrio. For each pair of samples (sea water + mollusc, adult or larvae), the numerical taxonomy data showed that the fermentative bacteria from both origins were almost identical with one another, indicating a relationship between the microflora associated with the mollusc and that of the surrounding sea water. The bacteria isolated from the molluscs were also characterised by an important proportion of proteolytic and lipolytic strains. Complementary bacteriological analysis and SEM observations of male and female gametes, revealed practically no bacteria associated with the spermatozoa and oocytes, indicating that these gametes were probably not responsible for a transmission of the microflora from the adult to the larvae. These results led Prieur (1981b) to suggest and test several hypotheses explaining the occurrence and location of this particular microflora within the molluscs, which will be reported and discussed later. Sugita et al. (1981) studied the bacterial flora of six species of bivalves, Tapes philippinarum, Mactra veneriformis, Mytilus coruscus, Crassostrea gigas, Phacosoma japonicum, and Scapharca broughtonii, and surrounding water and sediments from Tokyo Bay. Aerobic bacteria (or facultative anaerobic) were dominant with the genera Vibrio, Aeromonas, Pseudomonas, Moraxella, Micrococcus, and Enterobacteriae. Strict anaerobic bacteria (Bacteroides and Clostridium) were minor components. Although frequently in lower numbers, the bacterial components of sediment and sea water were similar to those of bivalves, suggesting again that the bacterial flora of bivalves was influenced by the environmental microflora. Comparisons between the bacterial flora of the sea water, sediments, and bivalves using pure strain isolation, phenotypic characterisation, and sometimes numerical taxonomy represents a hard task, and is time-consuming when the isolates are more than one or two hundred. Prieur (1981b) checked that TCBS, a selective medium for Vibrio (Kobayashi et al., 1963) provided reliable viable
288
D.PRIEUR ET AL.
counts of Vibrionaceae from marine samples. Using for the same samples both TCBS and 2216E medium, designed for heterotrophic bacteria by Oppenheimer & ZoBell (1952), it was possible to assess the relative abundance of Vibrionaceae in a sample of mollusc, sea water or sediment. This method was used for analysing 18 species of marine bivalves living on or within the sediment, collected at low tide or by dredging from different areas of the Bay of Brest (France). The results obtained confirmed clearly that Vibrio-like bacteria were always more abundant in the bivalve studied than in sea water, and frequently more than in the sediment. The data obtained led to the conclusion that such bacteria were a regular component of the bivalve microflora and that the molluscs certainly represented an important ecological niche for these bacteria. Kueh & Chan (1985) compared the microflora of Crassostrea gigas, Perna viridis, and Scapharca cornea with that of the surrounding sea water and found differences in both numbers and generic composition. The three bivalve species contained higher numbers of heterotrophic bacteria than the sea water. Mainly Pseudomonas, but also Vibrio, Acinetobacter, and Aeromonas dominated the mollusc flora while the sea water flora was mainly composed of coliform and coryneform bacteria. Most of the mollusc bacteria were found in the digestive tract, coliforms being mainly found in the stomach, while the non-enteric heterotrophs were located both in the stomach and the intestine. The location of the bivalve flora was previously studied by Prieur (1981a), who showed that the composition of bivalve microflora was not due to selective ingestion or digestion but to accumulation in the hind gut, because of a slow intestinal transit. This slow accumulation (up to 3 days) allowed adapted bacteria to survive and probably to grow in the hind gut. Minet et al. (1987) studied, during an annual survey, the marine and contamination microflora in several organs of Mytilus edulis (mantle, gills, water of the mantle cavity, digestive mass, and isolated hind gut). They showed that the hind gut was really the place where bacteria of marine or terrestrial origin were accumulated within the bivalves. When the total microflora, estimated by the plate count method on ZoBell agar was around 10 2 CFU·ml -1 in sea water, bacterial concentrations in intervalvar water, whole meat, and hind gut, were, respectively, 10 3 to 10 5, 10 5 to 10 7 , and 10 7 to 10 9 CFU·g -1 humid weight. In this study, the high proportion of Vibrio-like bacteria previously found in bivalves, was not, however, noted in all the samples. Barbosa’s (1987) results revealed that the important factor acting on the selection of bacteria during the accumulation process was more their ability to degrade the organic matter than facultative anaerobic metabolism, as was previously suggested by Prieur (1981b). Although bacteria can be found within the alimentary groove of the gills or in the stomach before the digestion of some of them, the hind gut is the site of the highest accumulation. This statement received confirmation from the work of Garland, Nash & McMeekin (1982) who examined with electron microscopy the internal surfaces of Crassostrea gigas tissues, and noted that the epithelial surfaces of the organs of the mantle cavity were not colonised by bacteria. Because of the complexity of the anterior loops of the hind gut which go through the digestive gland, the digestive mass (stomach+gut+digestive gland) is certainly the richest (in bacterial density) part of the mollusc flesh. Because the microflora of molluscs is retained for some days before being rejected as faeces, and because its density can reach 10 9 CFU·g -1 the question of the role of this microflora within the digestive tract can be raised. The
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
289
qualitative study of strains isolated from adults and larvae of Mytilus edulis (Prieur, 1981b) revealed that most of the components of this microflora had extracellular enzymes and especially proteases. These enzymes have only been recorded a few times in bivalves, particularly in the Mytilidae (Reid, 1978). The hypothesis of a proteolytic microflora using the material not used by the bivalves, as suggested by Prieur (1981b) has yet to be verified but, in any case, it is clear that live heterotrophic bacteria do exist in great numbers within the digestive tract of marine bivalves. Some weak enzymatic activities found in the digestive tissues of bivalves could be due to the occurrence of bacteria. On this point, Blaschko & Hope (1956) wrote “the digestive gland of Mytilus edulis is so intimately connected with the lumen of the digestive tract, that the possibility that the oxydase detected is a bacterial enzyme cannot be completely eliminated”. Bivalve associated spirochaetes The microflora that were described in the previous section must be considered as transit microflora, as they may vary according to the environmental conditions of the molluscs’s habitat. More stable bacterial associations within the digestive tract have, however, been described, all of them involving spirochaetes. These bacteria are usually described as mollusc-associated prokaryotes, and particularly involve the genus Cristispira. Mollusc-associated spirochaetes have been known since 1882, when Certes reported his first observations in Ostrea edulis. The genus Cristispira was erected by Gross (1910), and records of similar bacteria have been published for various species of bivalves by Bernard (1970) who found Cristispira in 12 out of the 62 species he examined from eastern Canadian waters. Bernard (1973) noted that all individuals of a same species are not obligately infested by Cristispira, and that they were found more abundantly in species or specimens from intertidal areas. He also found that sites of infection may be variable. Cristispira were earlier described as inhabitants of the crystalline style. According to the species, Bernard (1970) found the spirochaetes within the style sac and adhering to the style, in the stomach or in the intestine. He reported that the location and abundance could vary with the season, being more abundant in summer with, for example, in the genus Trevus, concentrations of 8×10 6 ·ml-1 of stomach content. Several Cristispira-free populations of Crassostrea gigas and Venus japonica were found in low salinity areas, while populations of the same species living in more saline areas were 100% infested, suggesting that salinity could be an important factor for the distribution of Cristispira. The exact role of Cristispira is not well defined, because these bacteria cannot be regularly obtained in culture, however, Kubomura (Baranton, pers. comm.) designed a fructose-containing medium allowing Cristispira enrichment and growth, but only for a few days. Mayasich & Smucker (1987) compared chitinase and chitobiase activities of Crassostrea virginica crystalline style with counts of Cristispira and chitinoclastic bacteria. They found one correlation between chitobiase activity and Cristispira counts, but found also enzyme activity when Cristispira was not present. They concluded that the enzymes studied were endogenously produced by the oyster, and that the spirochaetes did not significantly contribute to the pool of style chitinase and chitobiase.
290
D.PRIEUR ET AL.
Moreover, as previously reported by Bernard (1970), because molluscs containing and not containing Cristispira appear identically healthy, a pathogenic role for the spirochaetes cannot be suspected. Microbial flora associated with teredinid bivalves The Teredinidae are wood-boring bivalves that bore into immersed wooden objects and live in the galleries so-formed. These animals were particularly feared at the time of wooden ship construction. One of the main issues concerning these animals, is their ability to use as food a part of the wood debris resulting from their boring activity. Indeed, small wood fragments have been observed within their digestive tract. To verify this hypothesis, the detection of cellulase was necessary. Morton (1978) published a complete review on this subject. Some authors suggested that the detected cellulases could be endogenous, while others put forward the view that the enzymes might be produced by fungi or bacteria. Several authors, and particularly Hidaka & Saito (1956), Cutter & Rosenberg (1971), and Rosenberg & Cutter (1973), isolated cellulolytic bacterial strains. Martinez & Trique (1986) carried out laboratory experiments and studied the degradation of carboxymethylcellulase into reducing sugar, by isolated guts of Teredo navalis. They reported that the cellulose degradation was inhibited by sodium azide, suggesting participation of a microbial population in this enzymatic activity. These authors also isolated cellulolytic bacteria from the digestive tract and water gallery of T. navalis, that had the ability to degrade mannose and galactose. In an earlier paper, Martinez (1984) reported that the gut flora of T. navalis was more adapted to carbohydrate degradation than microflora isolated from the gallery and surrounding sea water, however, no data demonstrating definitely that the decomposed cellulose (or wood) is used by the teredinids are at present available. Nevertheless, if the diet of these molluscs is mainly composed of carbohydrates, they cannot fulfil their nitrogen requirements (Dean, 1978). This function could be effected by some associated bacteria, and Carpenter & Culliney (1975) isolated from the gut of Teredora malleolus one bacterial strain capable of cellulolytic activity and nitrogen fixation under anaerobic conditions. Deshayes (1845, vide Waterbury, Turner & Calloway, 1983) described a “brown, irregular mass of tissue lining the afferent branchial vein and penetrating the gill lamellae”. Subsequently, this structure was named and described by Sigerfoos (1908) as the Gland of Deshayes. Deshayes (1948, vide Nair & Saraswathy, 1971) suggested that this particular structure could have a nutritional function. Morton (1978) showed a cellulolytic activity in this gland, and Trytek & Allen (1980) reported amino-acid production. The first new observation was published by Popham & Dickson (1973) who examined the Gland of Deshayes in Bankia australis by transmission electron microscopy (TEM) and found that this structure was an association of bacteria. Similar data were obtained for Teredo navalis, Lyrodus pedicellatus, and L. medilobata. Waterbury et al. (1983) dissected the glands of individuals belonging to six species of teredinids (Lyrodus pedicellatus, Bankia gouldi, Teredo navalis, T. furcifera, T. bartschi, and Psiloteredo healdi) and made enrichment bacterial cultures, in a medium containing cellulose as the source of
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
291
carbon and energy. The isolates obtained from the six species appeared similar, representing probably a single species of bacterium. The isolate was a Gram negative motile rod (0, 4–0, 6 µm wide, 3–6 µm long), aerobic and chemoheterotrophic. It was able to fix molecular nitrogen when grown under microaerophilic conditions. These bacteria were considered by Waterbury et al. (1983) as symbionts, and represent the single record of an animal having a nitrogen fixer, in pure culture, in a particular organ. These authors also noted that cellulose degradation and the ability to fix nitrogen in a single bacterium could make it a suitable candidate for biotechnological purposes.
AUTOTROPHIC GILL SYMBIONTS
The discovery of deep-sea hydrothermal vents and their associated rich macrofauna may be considered as the most important event of recent years in biological oceanography. While the deep-sea benthic fauna is usually scarce (Sanders & Hessler, 1969), vent communities are extraordinary luxuriant. Several works clearly demonstrated that the primary consumers of vent communities (vestimentiferans and bivalves) obtain their trophic resources through highly efficient symbiotic associations. Further exploration of deepsea areas indicated that, in addition to hydrothermal vent areas, seeping zones resulting from different tectonic events, were inhabited by vent-like intertebrates, showing similar nutritional adaptations. The investigations on deep-sea bivalves led to new research on coastal molluscs, that revealed comparable features here too. Deep-sea hydrothermal vents Calyptogena magnifica belongs to the family of Vesicomyidae, and is well represented at Galapagos and 21°N sites (East Pacific Rise) (Grassle, 1985). This large species (30 cm in length) was first considered as a classical filterfeeder ingesting particulate matter and bacteria (Lonsdale, 1977). A study of its functional anatomy indicated, however, that the labial palps, organs usually involved in the transport of food particles were small. Moreover, the digestive tract appeared to be reduced, mostly empty and contained no recognisable material (Boss & Turner, 1980). More recently, Fiala-Médioni & Métivier (1986) showed that the gill of this species was only slightly adapted to the transport of particulate matter. Analysis of the stable isotopes of carbon and nitrogen in the tissues of C. magnifica indicated that the carbon sources were probably local (Rau, 1981a,b). The enzymes involved in the autotrophic fixation of carbon dioxide via the Calvin-Benson cycle (ribulose-1,5-biphosphate carboxylase, ribulose-5phosphate kinase) were found in the gill tissues (Felbeck, Childress & Somero, 1981), while prokaryotic cells were observed in this organ by TEM (Cavanaugh, 1983). These cells showed the typical structure of Gram negative bacteria, and appeared as cocci or short rods, with a diameter of 0.64 µm. The bacteria were located within the cells (bacteriocytes) of the gill lamella, and clustered in bacteria “pockets” (Fiala-Médioni, 1984). Numerous cells were in a dividing stage, and no lysing stages of bacteria were observed. Further observations
292
D.PRIEUR ET AL.
revealed that the bacteriocytes showed different stages, and Fiala-Médioni & Métivier (1986) suggested the occurrence of a cyclic process: bacterial growth, re-absorption and lysis of bacteria, transfer of organic molecules through the circulatory system of the mollusc, and infestation of gill cells which become bacteriocytes. Arp, Childress & Fisher (1984) suggested that the blood of C. magnifica had properties close to Riftia blood (vestimentiferan tube worm from hydrothermal vents) and could effect the transport of hydrogen sulphide, carbon dioxide, and oxygen which are required for the metabolism of the symbiotic bacteria. Bathymodiolus thermophilus was found to be abundant at the Galapagos and sites 13°N (Grassle, 1985). The animal is 15–16 cm in length (Kenk & Wilson, 1985) and analysis of the stable isotopes of carbon by Rau & Hedges (1979) indicated that local bacteria constituted their trophic source. The nutritional process appeared, however, to be different from that of Calyptogena magnifica. There are well developed labial palps. Although it is more simple than the digestive tract of coastal mytilid species, the digestive tract of Bathymodiolus thermophilus is functional and the categories of digestive cells described previously in coastal bivalves were found within the digestive gland (Hily, Le Pennec & Henry, 1986). The stomach is bulky and contains particles clearly identified as bacteria of different shapes, benthic foraminiferans, and also fragments of diatom frustules (Le Pennec & Prieur, 1984). These results clearly indicate that Bathymodiolus feed on suspended particles, some of them stemming from the euphotic zone. As a complement to this usual nutrition, the gill filaments of Bathymodiolus also showed associated microorganisms. Some external filamentous forms could correspond to Actinomycetes (Le Pennec & Prieur, 1984). In addition, particular cells of gill filaments contain Gram negative bacteria, with a diameter of 0.5 µm, clustered in small vacuoles, located at the apical part of the bacteriocytes, and containing ten bacterial cells (Le Pennec & Hily, 1984). Some crater-like cavities were observed at the top of some gill cells (Le Pennec & Prieur, 1984) and Le Pennec (1987) suggested that the gill cells could take up bacteria through a process of endocytosis, such as that described by De Burgh & Singla (1984) for a gastropod found at Juan de Fuca hydro thermal vents. Some bacterial cells seemed to be in a degenerating stage and no division figure was observed. Belkin, Nelson & Jannasch (1986) showed that the gill tissues of B. thermophilus, and particularly the associated bacteria, were capable of CO fixation. Fiala-Médioni, Alayse & Cahet (1986) also 2 showed that gill cells which contained more bacteria incorporated more labelled CO . These results indicated that the symbiotic bacteria have an 2 autotrophic metabolism. Enzyme analysis by Felbeck et al. (1981), however, indicated low levels of Calvin-Benson cycle enzymes, and no sulphide oxidation enzyme activity. Taking into account these observations, and those concerning the digestive tract, it is probable that B. thermophilus is a mixotrophic species (Le Pennec, Prieur & Lucas, 1985). This species would be less dependent on hydrothermal activity than Calyptogena, and that could explain why these invertebrates have been observed also on the fringe of active hydrothermal areas. The bacteria associated with the gills of B. thermophilus have not yet been cultivated, but some heterotrophic bacteria, probably from the alimentary groove, have been isolated and described (Prieur, 1987; Prieur & Jeanthon, 1987).
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
293
Bivalves from cold seeps and subduction zones A few years after the discovery of deep-sea hydrothermal vents, invertebrate communities resembling those of deep-sea vents were discovered in several cold seepage areas. Paull et al. (1984) reported dense biological communities, including mussels and vesicomyid bivalves, along the Florida escarpment, in the Gulf of Mexico. Kennicut et al. (1985) discovered on the Louisiana slope (Gulf of Mexico) vent-type taxa, including different species of bivalves (Lucinidae and Vesicomyidae). Kulm et al. (1986) also found vent-type animals in the Oregon subduction zone, and bivalves of the genera Calyptogena and Solemya. In the western Pacific, in the Japan subduction zone, Laubier, Ohta & Sibuet (1986) and Juniper & Sibuet (1987) reported beds of Calyptogena at depths between 3850 and 6000 m. Clear similarities between those newly discovered communities and East Pacific Rise hydrothermal-vent communities, in the chemical composition of seeping fluids, and the stable isotope composition of the invertebrates suggested that the trophic resources of these bivalves were probably chemosynthetic. Childress et al. (1986) studied undescribed mussels living in the vicinity of hydrocarbon seeps in the Gulf of Mexico (Louisiana slope). Mussels were collected at depths of 600 to 700 m and used for O and CH consumption 2 4 experiments. The data indicated that methane was consumed by gill tissues, exclusively, and was associated with an increase of oxygen consumption and carbon dioxide production. TEM observation of the gill filaments showed bacteriocytes containing symbiotic bacteria with stacked internal membranes, typical of type I methanotrophs. Mussels from the Florida escarpment were studied by Cavanaugh et al. (1987). These mussels have large thick gills that contain Gram negative bacteria of two morphological types. The larger (1.6 µm in diameter) are coccoid and contain internal membranes. The smaller (0.4 µm in diameter) are coccoid or rod-shaped, without internal membranes. No explanation on the role of the smaller bacteria was found, the internal membranes, however, of the large coccoid bacteria and the detection of hexulose phosphate synthetase (a key enzyme of one of the carbon assimilatory pathways of methane-oxidisers) suggested that the larger mussel symbionts are methylotrophs. Brooks et al. (1987) examined different bivalve species from the Louisiana slope area. Enzyme assays, sulphur analysis and CO fixation experiments indicated that the 2 clams Pseudomiltha sp (Lucinidae) and probably Calyptogena ponderosa and Vesicomya cordata contained autotrophic sulphur-oxidising bacteria. Analysis of carbon stable isotopes confirmed that the mussel symbionts were methanotrophs. Analysis of stable isotopes of nitrogen could be in favour of a fixation of nitrogen by bacteria. Fisher et al. (1987) compared the symbiotic associations of Bathymodiolus thermophilus with those of similar mussels from the Louisiana slope. The seep mussel symbionts differ in their larger size, the occurrence of internal membranes, and also the small number of symbionts (three or less) within each vacuole. These authors confirmed the occurrence of methanotrophy for the seep mussel only. In addition, they looked for ribulose-biphosphate-carboxylase activity, and found low activity levels for the seep mussel and Bathymodiolus. The absence of ATP sulphurylase and ATP reductase within the seep mussel gill tissues indicated that sulphur oxidation was not a major energy source for this animal. The low level
294
D.PRIEUR ET AL.
of RuBP carboxylase could, however, be due to a contaminant or a minor gill associated bacterium. In the case of Bathymodiolus, these results could indicate that the major symbiont was a thiosulphate-oxidising bacterium (perhaps mixotrophic), but not an autotrophic sulphur bacterium. Two new species of the genus Calyptogena were collected and described from the Japan subduction zone. C. laubieri (Okutani & Métivier, 1986) was found between 3800 and 4020 m, and C. phaseoliformis between 5130 and 5960 m. Both species have large and thick gills in which bacteriocytes are abundant (Fiala-Médioni & Le Pennec, 1988). TEM observations were carried out on C. phaseoliformis only. The bacterial cells within the bacteriocytes were 0.6 to 1 µm in diameter, and showed the typical cell wall of Gram negative bacteria. Some dividing stages were observed. The bacteriocytes also contained lipidic inclusions and lysozomes which were involved in bacteria reabsorption. The metabolic type of these endocellular bacteria has not yet been determined. These bivalves are living in sulphide-enriched sediments, but the emitted fluids contain also methane. Boulègue et al. (1986), on the basis of geochemical analysis, suggested that the endosymbionts would be methanotrophs. These endocellular bacteria did not, however, show any internal membranes, which were always present in methanotrophs (Whittenburry & Dalton, 1981), and the question of their energy source remains open. Sulphide-enriched coastal areas The discovery of deep-sea hydrothermal vents and associated symbiotic associations initiated a new series of work on invertebrates living in coastal, sulphide-enriched habitats, and particularly on bivalves (Felbeck et al., 1981; Cavanaugh, 1983; Felbeck, 1983). Felbeck et al. (1981) found enzymes associated with autotrophic CO fixation, and sulphide oxidation in tissues of the bivalves 2 Solemya panamensis and Lucinoma annulata collected, respectively, from sewage outfall areas and in the Santa Barbara Basin, where the sulphide concentration is high. Solemya panamensis have a reduced digestive tract, sometimes lacking in some specimens (Felbeck et al., 1981). The lack of a digestive system is a constant feature of another protobranch mollusc, S. reidi, living exclusively in habitats rich in hydrogen sulphide. Felbeck (1983) found high densities of bacteria, intracellularly located in gill tissues. The outer layer of the gill filaments contains two types of cells. One type does not have bacteria but many mitochondria. The second type, the bacteriocyte, contains numerous bacteria (1 µm in diameter) with Gram negative envelopes and enclosed individually or in groups by a membrane probably animalderived. Fixation of 14CO by the gill tissues was demonstrated. 2 The experimental data suggested that CO was initially fixed into four-carbon 2 compounds (aspartate and malate), and then decarboxylated to furnish CO to the 2 Calvin-Benson cycle. S. reidi is, however, also capable of absorbing dissolved organic molecules from the surrounding sea water. Further experiments on this species by Fisher & Childress (1986) demonstrated that the symbiotic bacteria fixed carbon at a high rate, and that more than 45% of the fixed carbon was translocated to the host. Seagrass beds stand as very productive marine areas, and the degradation of the associated organic matter is partly carried out by anaerobic bacteria, including sulphate-reducers which produce high concentrations of hydrogen
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
295
sulphide. Lucina floridana is a eulamellibranch living within the sediment, in the vicinity of the roots of the seagrass, at the interface between the aerobic niche induced by the root metabolism, and the anaerobic zone resulting from hydrogen sulphide production (Fisher & Hand, 1984). These authors reported that L. floridana contained gill endosymbiotic bacteria, located within special large cells (up to 60 µm), bacteriocytes, that are rich in bacteria-containing vacuoles. Enzymatic analyses indicated that autotrophic CO fixation occurs 2 within the gill tissues, and that the associated bacteria were sulphur-oxidising organisms (ribulose 1,5-biphosphate carboxylase, APS reductase and ATP sulphurylase were detected). Giere (1985) extended the study to four species of Lucinidae from Bermuda (Anodontia philippiana, Lucina multilineata, L. radians, and L. costata) and also found bacterial symbionts within the gills of those bivalves. Bacteria were included within bacteriocytes (smaller than those of L. floridana) and differed in size, according to the bivalve species. Particularly, Anodontia philippiana and Lucina multilineata had elongated rodshaped microorganisms (up to 8.9 µm) among smaller oval forms which were predominant. Schweimanns & Felbeck (1985) demonstrated that the symbionts of Anodontia philippiana were able to fix CO autotrophically, and extended their 2 analysis to four other bivalve species living in the same area: Codakia orbiculata, C. costata, Lucina radians, and Parvilucina multilineata that also belong to the family Lucinidae. Vetter (1985) examined the fine structure and sulphur contents of the tissues of the three bivalve species, Lucinoma annulata and Calyptogena elongata from the Santa Barbara Basin and Lucina floridana from Florida seagrass beds. He reported that gill tissues contained from 2.5 to 5.6% (dry weight) of elemental sulphur, and that sulphur globules were only found within bacteria and not in the animal cell cytoplasm. On the basis of these data, he suggested that the sulphur deposits probably represented reserves of energy, allowing the symbionts to work, even during a temporary absence of environmental sulphide. While the bivalve species previously considered lived in rather sulphide-rich sediments, other species from low sulphide-level habitats also seemed to host gill symbionts. Dando, Southward & Southward (1986) demonstrated the presence of chemoautotrophic symbionts within the gills of Lucinoma borealis, a species widely distributed in the northeastern Atlantic. Gill tissues of this species showed CO fixation and sulphide oxidation enzymatic activity, and contained elemental 2 sulphur. The authors noted that, despite the low level of dissolved sulphide in the sediments, this species was able to obtain half its carbon requirements from the associated autotrophic bacteria. Dando et al. (1985) studied another species of lucinacean Myrtea spinifera, collected from the sediment of a Norwegian fjord where it cohabited with Lucinoma borealis and Thyasira flexuosa. Myrtea spinifera, again, carried many Gram negative bacteria containing elemental sulphur within the gill epithelial cells. Carbon dioxide fixation was demonstrated by enzyme analysis and the enzymes involved in sulphide oxidation were detected in gill tissues. The presence of elemental sulphur within the gill tissues was interpreted as a proof of active sulphur metabolism and as a form of storage of a source of energy. Another species of Lucinidae, Lucinella divaricata was also found to host symbiotic auto trophic bacteria within the gill tissues (Le Pennec et al., 1987).
296
D.PRIEUR ET AL.
The Thyasiridae and Lucinidae are members of the superfamily Lucinacea. The Thyasiridae also have a simplified (particularly stomach) digestive tract. Analysis of stable isotopes of carbon indicated that two species, Thyasira flexuosa and T. sarsi were depleted in 13 C (Spiro et al., 1986) suggesting they get most of their carbon from autotrophic bacteria. The two species have thick gill filaments which contain numerous prokaryotic cells between the cuticle and the cell membrane (Southward, 1986). Enzymes involved in CO fixation and 2 sulphide oxidation were also detected (Dando & Southward, 1986), some of them being also found by Herry & Le Pennec (1987). Compared with the previously reported bivalve symbionts, those of Thyasira were not found intracellularly, but in a subcuticular space in the gill filaments, where they are phagocytosed by epidermal cells (Southward, 1986). In addition to those bivalves living in enriched sulphide habitats, some other species were found to have associated bacteria. Bouvy et al. (1986) and Soyer et al. (1987) reported bacteria associated with the gill of a coastal species of Mactridae, Spisula subtruncata, that lives in fine well-sorted sands of the infralittoral zone. Two types of bacteriocytes were distinguished on the basis of their size and shape, and on their bacterial contents. Bacteriocytes of type 1 had a flattened spherical shape with a size up to 30 µm and contained numerous (more than 200 in one histological section) comma-shaped Gram negative organisms (0.9 to 1×2,5 to 3 µm). Bacteria were often observed in a dividing stage. The bacteriocytes of type 2 were spherical (20 µm in diameter). The bacteria were also abundant but their shape was ovoid (0.8×1 µm). Enzyme assays indicated that the gills of S. subtruncata possessed autotrophic activity and were able to use sulphur compounds as a source of energy. The values obtained for these activities were rather low, compared with other symbiontassociated bivalves, indicating that the contribution of this autotrophic association to the bivalve’s nutrition was probably rather low. Henry, Vicente & Cornet (1981) reported that the cockle, Cerastoderma glaucum, had some gill cells that contained bacteria. This time, however, the bacteria were located within the host cell nucleus and several types of the bivalve’s cells contain bacteria. Some of these cells might be necrosed, the bacteria being then expelled out of the gill filament. In other cases, the contaminated but normal cells were extruded out of the filaments, and then the bacteria were expelled. No enzyme analyses were carried out and the function of these microorganisms, symbionts or pathogens, has not yet been elucidated. Reid & Brand (1986) raised the question of the transmission of symbionts with regard to the case of Parvilucina tenuiscalpa, another symbiont hosting Lucinidae, previously studied from an enzymatical point of view by Felbeck et al. (1981). The question remains open for all the species found associated with bacteria, except for Solemya reidi. Reid & Brand (1986) reported work by Gustafson who assumed that the transmission of symbionts of S. reidi took place through the eggs. Soyer et al. (1987) had three hypotheses concerning the transmission of symbionts: (1) acquisition during the ontogenic development of the clam; (2) acquisition of a mixed population of bacteria from the ambient environment followed by selection of only certain species of strains; (3) ancestral acquisition before the evolution of bivalves into the present-day Classes and Orders. Concerning this last point, in the case of lucinacean evolution, Reid & Brand (1986) proposed a scheme, starting from an ancestral lucinacean, similar to the actual Ungulinidae and having sulphide-oxidising
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
297
symbionts. The ancestral branch would give rise to the actual Ungulinidae, by loss of symbiosis, and to the Lucinidae and Thyasiridae by reduction of the gut and increase in a part of the gill tissues. One of the remaining questions concerning symbionts is the similarity, or not, between symbionts of different bivalve species. The classical microbiological methods (i.e., culture techniques) have not been very successful in this case. Prieur & Jeanthon (1987) isolated several heterotrophic bacterial strains from Bathymodiolus thermophilus which might have stemmed from the alimentary groove. Wood & Kelly (1989) reported the isolation of strains from several lucinid species (Lucinoma borealis, Thyasira flexuosa, T. sarsi, T. obsoleta, and Myrtea spinifera) that are facultative methylotrophs, may oxide thiosulphate to tetrathionate, and also showed a heterotrophic metabolism. No data concerning the similarity between the supposed symbionts from the different bivalves analysed were, however, given. More reliable information has been gathered using molecular biology techniques. Stahl et al. (1984), establishing the rRNA sequences of several invertebrate symbionts, concluded that the symbionts of Calyptogena magnifica, Solemya velum and the vestimentiferan, Riftia pachyptila, were at least 90% homologous (Soyer et al., 1987). These data supported Reid & Brand (1986) who wrote that only a small number of free-living sulphur-oxidising bacteria would have had the possibility to become symbionts, a hypothesis also suggested by Wilkinson (1984) in the case of sponge symbionts. More extensive studies with molecular biological techniques of the symbiotic associations presently reported would highlight this issue.
INDUCTION OF METAMORPHOSIS
The interactions between bivalves and bacteria, so far reported in this section, occur within the bivalve tissues (digestive tract or gills). Some external interactions that happen during metamorphosis have, however, been recently demonstrated. Many marine invertebrates, including bivalves, undergo a pelagic larval stage. At the end of the pelagic life, the larvae need to settle on a convenient substratum before metamorphosing, these two phenomena being irreversible (Chia & Rice, 1978). Among the environmental factors that induce or influence settlement and metamorphosis, the occurrence and the nature of the bacterial film covering the substratum used for settlement have been investigated by several authors (Crisp & Ryland, 1960; Scheltema, 1974; Brancato & Woollacott, 1982; Kirchman et al, 1982). When immersed in sea water, substrata are rapidly colonised by bacteria, that precede diatoms, protozoa, and invertebrate larvae (Corpe, 1970). The bacterial film may influence invertebrate settlement in different ways. ZoBell (1935) and Mitchell & Young (1972) write that the adhesive properties of the bacterial film could help the fixation. ZoBell (1935) suggested that the bacteria constituting the film, and the organic particles trapped within the film, could also be used as food by the larvae ready to metamorphose. Mitchell & Young (1972) suggested that the biofilm might produce locally particular pH conditions, more favourable for the occurrence of calcium carbonate, this compound being necessary for shell-building in the post-larvae. Alternatively, bacteria living in the biofilm could synthesise certain compounds, diffusible into the environment,
298
D.PRIEUR ET AL.
which could induce metamorphosis. Those compounds might be produced only by certain specific bacteria. Two mechanisms have been demonstrated. Kirchman & Mitchell (1981) and Kirchman et al. (1982) studied the metamorphosis of the polychaete Janua brasiliensis, and proposed the “lectin” model. According to these authors, larvae of Janua produce a lectin and the bacterial film produces carbohydrates able to bind specifically to this protein. The receiving site seemed to be a glucose polymer. Weiner & Colwell (1982) and Weiner, Segall & Colwell (1985) suggested another hypothesis, in the case of bivalves. Weiner & Colwell (1982) isolated a bacterial strain, named at first LST, from tanks used for rearing Crassostrea virginica. This particular bacterium, then named Alteromonas colwelliensis (Weiner, pers. comm.) was considered to be responsible for the attraction of Crassostrea virginica pediveligers to the substratum. In the environment, LST stick to surfaces by a polysaccharidic compound. This bacterium also produces L. DOPA, and other precursors of melanine, and melanine itself, these compounds attracting the pediveligers towards the substratum. Laboratory experiments by Weiner et al. (1985) demonstrated that collectors pre-fouled with LST were more attractive to C. virginica pediveligers than sterile collectors or those pre-fouled with another bacterium. Coon, Bonar & Weiner (1985) demonstrated that L. Dopa really induced C. gigas settlement, at a concentration of 10 -4 to 10 -5 M·l -1. Tritar (1987) carried out hatchery experiments with LST-D, a mutant of the previous strain, that was also efficient for C. virginica settlement. He tried to induce metamorphosis of C. gigas, Ostrea edulis, and Pecten maximus. Half of the experiments gave comparable results to those of Weiner & Colwell (1982); in the cases of the oyster species, however, the responses of P. maximus larvae to LST-D was always negative. These results could suggest that LST-D is specific to oysters. The optimum temperature for this bacterium is, however, 30°C, and the settlement of oysters was carried out at 26°C, a temperature commonly used in oyster hatcheries. P. maximus larvae, however, need lower temperatures (12 to 15°C) to be reared and metamorphose, these being temperatures at which LST does not grow. Another explanation would be the occurrence of LST-like bacteria on the collectors used for the experiments. The enrichment of melanin-producing bacteria in various samples collected in hatcheries and the coastal environment (Tritar, 1987) revealed that this type of bacteria was rather common, but showed phenotypic features different from those of LST. This subject certainly needs further investigation but the potential of LST-like bacteria could probably be used in hatcheries in the future.
MICROBIAL CONTAMINATION OF COMMERCIAL BIVALVES
KINETICS OF ACCUMULATION AND ENRICHMENT FACTORS
Kinetics of accumulation
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
299
Most of the data concerning accumulation of bacteria in bivalves have been obtained under experimental conditions. Cabelli & Heffernan (1970a, 1971) performed in vitro studies to establish the kinetics of accumulation of Escherichia coli by Mercenaria mercenaria and the influence of some environmental factors on the rate of accumulation. After 24 h of contamination by Escherichia coli, the clams could be differentiated into two groups. The first group comprised animals homogeneously contaminated, at a maximum concentration level. The second group consisted of animals contaminated at different levels. The authors considered that the maximum level observed for the first group corresponded to a steady state and that the clams of the second group had not yet reached this equilibrium. Cabelli & Heffernan (1970a, 1971) observed also that clams exposed to contamination during periods from 6 to 48 h, reached the equilibrium previously established, but the number of animals reaching this level increased with the time of exposure to contaminated water. The value of this steady state is directly correlated to the bacterial load in sea water. The correlation found between steady state level in the animal (Y) and E. coli concentration in the water (X) was Y=0.96X+0.97. Paoletti (1968) studied the uptake of bacteria by Mytilus edulis using tracing bacteria (Mycobacterium tuberculosis) followed by fluorescence techniques and 32P radiolabelled Salmonella. He reported that the uptake of bacteria occurred rapidly, and that equilibrium was reached within 2 h. Plusquellec et al. (in press) carried out experiments on the accumulation of enteric bacteria by Mytilus edulis. They observed that contamination was very fast and that the maximum level could be reached within 30 min. This equilibrium state was directly dependent on the bacterial concentration in sea water in the range of 4×101 to 3×107 cells·ml-1. In natural conditions, Trollope & Al Salihi (1984) found that an immersion period of 2 h was sufficient to reach the steady state level, while 15 or 40 h of immersion might provide unreliable results. They showed that a continuous immersion of 48 h produced mussels containing more marine bacteria than mussels exposed to 6 h of immersion, and that could affect the subsequent uptake of sewage-derived bacteria. After 48 h of immersion, however, mussels reached a level of contamination similar to indigenous mussels, independently of their initial concentration. When comparing the ability of bivalves to concentrate bacteria from sea water, some differences have been pointed out, according to the bivalve species. Mercenaria mercenaria and Mya arenaria differ in their rates of accumulation and enrichment factors (Cabelli & Heffernan, 1970b). Trollope (1984) observed that coliforms were accumulated in greater numbers in Scrobicularia plana than in mussels. Results presented by Sugita et al. (1981) indicated enrichment from one to three magnitude in Mactra veneriformis, Tapes phillipinarum, and Crassostrea gigas, while low or no concentration was observed in Phacosoma japonicum, Mytilus coruscus, and Scapharca broughtonii. It is often concluded, however, that concentrating effects are of the same order in several shellfish: e.g., Scrobicularia plana, Mya arenaria, Cerastoderma edule, Mytilus edulis (Al Jebouri & Trollope, 1984); mussels and cockles (Delattre & Delesmont, 1981). Enrichment factors The bacterial enrichment obtained in shellfish meat in comparison with the bacterial level in the overlaying water is of great significance for hygienists and especially
300
D.PRIEUR ET AL.
modelists. Their aim is to forecast the contamination of bivalves, given the sea-water contamination. Nevertheless, a general value cannot be expected according to the conditions influencing the accumulation process. Cabelli & Heffernan (1970a) defined the accumulation factor as A=Ba/Bw, where A is the accumulation factor, Ba the bacterial level per gram of shellfish tissue and Bw the bacterial level per ml of sea water. Thus, log A is the difference between the log value counts in bivalve meat and sea water. Review of the data concerning enrichment in bivalves allows the main factors influencing the value of the accumulation factor to be discussed (Table I). Comparative studies suggest that the A value differs between bacterial groups. Most of the data available concern indicator groups or Salmonella, and it appears that the values reported for enterobacteria and faecal streptococci are very different. The enrichment factor is about 10 for faecal coliforms and Salmonella, and over 100 for streptococci (Delattre & Delesmont, 1981; Plusquellec, Beucher & Le Gall, 1983; Plusquellec et al., in press). No clear difference appears from comparison between Salmonella and the faecal coliform group (Timoney & Abston, 1984; Plusquellec et al., in press); some differences exist, however, within the coliform group. The results presented by Cooke (1976) and Perkins et al. (1980) show that accumulation factors are lower when calculated from counts of faecal coliforms than from counts of total coliforms. Equally, in Pacific oysters and Tapes japonica, Escherichia coli appears to be less concentrated than other coliforms (Vasconcelos & Lee, 1972). In addition, bivalves may differ in their ability to concentrate bacteria, for instance, the accumulation factor achieved by the soft shell clam, Mya arenaria, was higher than the factor observed with the northern quahaug, Mercenaria mercenaria, under the same conditions (Cabelli & Heffernan, 1970b). The experimental conditions used in evaluating the accumulation factor also influence the result; Plusquellec et al. (in press) estimated that the enrichment observed in situ is higher than that obtained under laboratory conditions. The accumulation may also be affected by the duration of the contamination period (Timoney & Abston, 1984) although Cabelli & Heffernan (1970a) demonstrated that enrichment is independent of accumulation for intervals between 6 and 48 h. These authors proposed a model allowing the prediction of an accumulation factor taking into account the physiological characteristics of the bivalve and the bacteria, pumping rate, transport time in the bivalve, filtration efficiency, survival ratio of the bacteria during transport time, liquid volume in the bivalve, and the wet weight of the animal (Cabelli & Heffernan, 1970a). Essential data concerning enrichment by bivalves, summarised in Table I, appear to be rather homogeneous, ranging from 3 to 50 for the coliform group and Salmonella.
LOCATION OF ACCUMULATED BACTERIA
Knowledge of the location of accumulated bacteria within contaminated bivalves is interesting in order to improve the methods of bacteriological analysis. Boury & Borde (1964a) showed that the bacterial level in bivalve flesh was generally higher than in water of the mantle cavity, especially in cases of heavy pollution. More precise location studies indicated generally a digestive accumulation. Cabelli & Heffernan (1970a, 1971) found that the bacteria accumulated by
Essential data concerning enrichment by bivalves
TABLE I
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA 301
302
D.PRIEUR ET AL.
Mercenaria mercenaria were mainly located in the digestive gland, and in the siphon tissues. Leung et al. (1973) also found that bacteria of faecal origins were mainly present in the digestive diverticula of Crassostrea gigas. Al Jebouri & Trollope (1981) reported that 75 to 95% of the bacterial contents in the mussel were located in the digestive tract and in the stomach, while the foot, labial palps, gills, mantle, and residual tissues which constituted 80% of the total mussel flesh (by volume) contained low bacterial numbers. Perkins et al. (1980) found that coliforms were accumulated in the visceral mass and siphons of clams, as other tissues showed bacterial levels similar to those of sea water. Ledo et al. (1983) examined separately mantle, gills, digestive gland, and total flesh of oysters, mussels, and clams for their Escherichia coli contents. They found the highest concentrations in the digestive gland, even in the case of low contaminations. Kueh & Chan (1985) estimated that in the oyster Crassostrea gigas, 93% of the coliforms and 90% of the heterotrophic flora were present in the digestive tract, distributed between the stomach and the lower intestine. Coliforms were mainly found in the stomach (85%) and hardly any were to be found in the digestive diverticula and lower intestine (3.4%), while heterotrophs were present in the stomach (47%) and lower intestine (42%). These results suggested that bacteria in the digestive tract stemmed from the ambient sea water, and that a process of degradation and growth gradually replaced the exogenous flora by a more autochtonous one which was dominant in the lower intestine. The results of Minet et al. (1987) indicated clearly that the process of bacteria accumulation by Mytilus edulis occurred in the digestive tract, and particularly in the hind gut. With one or several loops (according to the bivalve species) passing through the digestive mass (digestive gland, stomach, and gut) this fraction of the bivalve soft tissues certainly represents the most bacteriaenriched part of the animal.
RELEASE OF CONTAMINATING BACTERIA AND SHELLFISH DEPURATION
The first important experimental data concerning the release of contaminating bacteria by contaminated shellfishes were published by Cabelli & Heffernan (1970a, 1971). From study of Mercenaria mercenaria, they pointed out that bivalve depuration corresponded to a particular case of the feeding mechanism, and so was controlled by the pumping rate and the filtration efficiency, two parameters themselves influenced by environmental conditions such as temperature or salinity. During these experiments, the level of Escherichia coli in individual clams (Mercenaria mercenaria) was monitored during depuration. The results obtained showed that the distribution depended on the initial concentration within the animals: for an initial level of 10 2 to 10 3 E. coli·100 g 1 , depuration was achieved within 24 h for the whole clam population. In contrast, for an initial contamination of 10 5, only 40% of the clams could be considered as depurated within 48 h. This study indicated that the variability in the response of individual clams was a problem for depuration: about 12% of the clams could not be expected to reduce their level of coliforms. Heffernan & Cabelli (1971) estimated that this difficulty could be avoided by restricting depuration to
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
303
moderately polluted animals, and by stimulating the cleaning activities by chemical or physical agents. In addition to M. mercenaria, the release of contaminating bacteria has been studied for Crassostrea virginica (Janssen, 1973; Metcalf, Slanetz & Bartley, 1973), C. gigas (Vasconcelos & Lee, 1972), C. commercialis (Rowse & Fleet, 1984), Mytilus edulis (Ledo et al., 1983; Trollope & Al Salihi, 1984; Plusquellec et al., in press), etc. Most of the data obtained by these authors indicated that depuration to a rather low level usually occurred within 24 to 48 h, and was more important during the first hours. As previously noted by Cabelli & Heffernan (1970a), several authors reported that the duration and efficiency of depuration were affected by environmental conditions such as temperature and salinity, that first influenced the feeding behaviour of the molluscs. Some differences were noted according to the type of bacteria studied during the depuration process. In most cases, contaminating bacteria were eliminated while marine bacteria remained at their initial level. According to the experiments, pathogenic bacteria like Salmonella were eliminated simultaneously with the bacterial indicators, faecal coliforms (Rowse & Fleet, 1984; Plusquellec et al., in press), either more quickly (Metcalf et al., 1973) or more slowly (Timoney & Abston, 1984). This slow elimination was particularly evident for marine pathogenic bacteria (Vibrio parahaemolyticus, V. harveyi) that would be able to grow within the digestive tract (Greenberg, Duboise & Palhof, 1982). Janssen (1973) found new differences between the bacterial species he tested, but unlike the other authors, he noted retention times as long as 49 days for Salmonella within the tissues of Crassostrea virginica. Further controls have also been carried out on molluscs stored under different conditions between harvest and consumption. In these cases, storage temperature played the primary role. At room temperature (20°C), Boury & Borde (1964b) noted low fluctuations in bacterial densities within oysters, mussels, and clams stored during 2 to 3 days. For longer periods (up to 14 or 16 days) N’Guyen Thi Son & Fleet (1980) reported, however, a small increase of the marine microflora, an 11-fold decrease of Salmonella, and an increase of Vibrio parahaemolyticus during the first 4 days. At low temperatures, the contaminating bacteria decreased slowly, but they could remain viable for up to 140 days, even stored at -20°C (Nishio et al., 1981).
ENVIRONMENTAL CONDITIONS RELEVANT TO ACCUMULATION AND ELIMINATION OF BACTERIA
Cabelli & Heffernan (1970a) had emphasised that accumulation and elimination were dependent on physiological functions of the bivalves which are themselves under influence of environmental conditions such as turbidity, temperature, and salinity of the sea water. The values of the steady state described by Cabelli & Heffernan (1970a) were correlated to the ratio of Escherichia coli to the total ingested particles, leading to a decrease of the accumulation factor when the particle density in sea water (bentonite suspension) was increased. Similar results were obtained with mussels by Plusquellec et al. (1987) using sterilised sewage as particles. Similarly, Paoletti (1968) observed that bacterial accumulation in Mytilus edulis was dependent on water turbidity, increasing in
304
D.PRIEUR ET AL.
non-turbid waters. Wood (1957) estimated also that the filtration rate and bacterial accumulation were affected by suspended particles. In contrast, the elimination process was not affected by particle density: addition of bentonite to sea water to a level of 25 JTU (Jackson Turbidity Units) led to a more effective elimination of Escherichia coli by Mercenaria mercenaria (Heffernan & Cabelli, 1970). The temperature of sea water significantly influences the physiological activity of bivalves. Cabelli & Heffernan (1971) observed that few coliforms were recovered from M. mercenaria when the water temperature fell below 10°C, even in heavily polluted waters. These authors and Perkins et al. (1980) considered that below 10°C accumulation is more strongly inhibited than elimination, resulting in a steady state level lower than contamination level. Elimination is, however, affected by low temperatures: according to Haven et al. (1977), depuration of faecal coliforms in oysters is inhibited below 10– 12°C. Purification of Crassostrea commercialis contaminated by Salmonella charity was incomplete and inconsistent below 17°C and rapid and uniform at 18 to 22°C (Rowse & Fleet, 1984). Concerning the effects of temperature, mussels differ clearly from clams and oysters, because it is considered that Mytilus edulis may be active down to 0°C (Wood, 1957; Ayres, 1975). In Mya arenaria, elimination rates are similar at 10 and 20°C, but markedly reduced at 2°C (Perkins et al., 1980). The consequence of this temperature effect is the observation of marked seasonal changes in contamination and depuration of bivalves (Trollope, 1984). Generally, indicator contents in bivalves are higher in summer than in winter (Wood, 1957; Cabelli & Heffernan, 1971; Leung et al., 1973). In Chesapeake Bay, coliform counts in oysters were found to increase significantly in OctoberNovember, in the absence of any increase in the water column (Hussong, Colwell & Weiner, 1981). Elimination of bacteria from contaminated bivalves is less effective in winter (Fuks & Filic, 1977). Animals collected during late winter or early spring do not eliminate bacteria as readily as animals collected in other seasons (Cabelli & Heffernan, 1971). Salinity has been regarded as a factor likely to influence bacterial contamination of bivalves and more especially elimination of bacteria. At high salinities (43 to 47‰) elimination was similar to that observed at normal salinities (32 to 36‰) (Perkins et al., 1980; Rowse & Fleet, 1984). In contrast, low salinities reduced the depuration rate of oysters (Perkins et al., 1980). Heffernan & Cabelli (1970) estimated that below a salinity of 22‰, a low depuration was observed in Mercenaria mercenaria due to closure of the bivalves. After adaptation, normal activity was recovered. Rowse & Fleet (1984) reported a minimum salinity of 20.5‰ for an effective purification of Crassostrea gigas and C. angulata, whereas C. virginica may be purified at lower salinities. This is consistent with the results of Hussong et al. (1981) attesting that Chesapeake Bay oysters were not affected by salinity levels ranging from 24 to 14‰.
TENTATIVE SCHEME OF BACTERIAL TRANSIT
Some of the data reported previously may be considered contradictory. Evidence of digestion of bacteria by bivalves, but also accumulation of living bacteria have been
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
305
clearly established. Taking into account these results and new data concerning exchanges of bacteria between the different compartments of the bivalves, Barbosa (1987) suggested the following scheme. At a particular moment, ambient sea water contains a complex microflora made of cells of different origins (marine or continental), physiological states (viable, starved, stressed) or sizes (free-living or particle bound). In the case of a mussel, immersed in sea water, all this material enters the mantle cavity, as a function of filtration activity of the animal, which may be influenced by environmental conditions such as temperature, salinity, and concentration of organic and particulate matter. A fraction of this material is retained by the gills and transported towards the labial palps. The remaining part is rejected outside. Then, the labial palps, according to the particle sizes and the amount of food previously ingested, reject a fraction of the particulate material, in the mantle cavity, and then outside, as pseudofaeces. The particles that enter the digestive tract may be exposed to different treatments at the stomach level. Usually, particles are attacked in the stomach by extracellular enzymes. These enzymes are mainly concentrated within the crystalline style, which also mixes the ingested food. Small particles, including bacteria, may enter the ducts of the digestive gland, then the tubules and the digestive cells themselves, where they are digested intracellularly. The sensitivity of bacteria to these enzymatic actions, may vary as a function of the type of bacterium, of its physiological state or of its inclusion or not in organic material that can have a protective role. Products resulting from digested and non-digested material are evacuated in the mid gut, and then in the hind gut. According to the food content of the digestive gland, particles that enter the stomach may stay a more or less long time in the stomach and mid gut, before entering the hind gut. From this digestive process, it is possible to consider the nature and state of bacteria associated to the animal tissues. The gills transport food particles and contain a microflora, not identical, but very close to that of sea water. The duration of food transportation along the gill groove is not well known, and some minutes are enough to make this transported microflora different from that of sea water. The water of the mantle cavity is a complex compartment, which really exists only for the emersed animals (it is the case in all animals collected for analysis). Even a short time between sampling and analysis is enough to modify the microflora of the mantle cavity, which comprises bacteria from the ambient sea water or the digestive tract. The digestive mass is a more complex compartment, made of the different organs of the digestive tract, that are impossible to separate by techniques allowing further bacteriological analysis. More than half of the hind gut is enclosed in the digestive mass. So, the digestive mass (stomach, style sac, mid gut, digestive gland, hind gut) contains new ingested material and material in digestion or more or less refractory to digestive enzymes. The stability of this microflora depends on the sensitivity of bacteria to enzymes, and the digestive rhythm of the animal, affected in some cases by tide, food supply, etc. The hind gut is the place where the highest bacterial concentrations were found, as a result of the slow intestinal transit, which allows accumulation of material during periods as long as three days. Viable bacteria found at this level are resistant to digestion or passed rapidly through the stomach. So, in the hind gut are concentrated bacteria, but also organic material, digested or not, that
306
D.PRIEUR ET AL.
constitutes available substrates. All these conditions are responsible for the establishment of a temporary microflora during intestinal transit, which is clearly different, but not independent from that of sea water, and dependent also on the nature of organic material present in the hind gut.
SANITARY ASPECTS OF BIVALVE CONSUMPTION POTENTIAL RISKS AND DISEASES
Potential human health risks Edible bivalves have been reported for a long time to be responsible for a wide variety of human diseases. Health hazards related to shellfish consumption are well documented (Earampamoorthy & Koff, 1975; Portnoy, 1975; Wood, 1975; Brown & Dorn, 1977; Bryan, 1980). The diseases mentioned range from serious infectious bacterial diseases such as typhoid, paratyphoid, cholera, and dysentry to miscellaneous cases of more or less serious gastroenteritis (Fleet, 1978). Any bivalve may be involved in disease outbreaks but the most commonly quoted are oysters, mussels, and clams. The risks resulting from consumption of these seafoods are related to some specific aspects of their physiology, their production, and their consumption (Fleet, 1978). Most of the bivalves are active filter-feeders and this concentrate particulates, bacteria and viruses from sea water. Cultured bivalves are generally reared in protected areas, such as estuaries or bays, which are frequently densely populated and sensitive to heavy pollution from human activities. The handling of shellfish and the marketing process may be the cause of the contamination input or the multiplication of existing contamination to unsafe levels. A large number of shellfish is consumed raw or after a light cooking that is ineffective in eliminating pathogenic bacteria and viruses. Incidence of bacterial shellfish-borne poisoning The available data especially concern the USA. There, seafoods accounted for approximately 11% of the food-borne disease outbreaks reported from 1970 to 1978, and molluscs represented only 2% (Bryan, 1980). For 1967 to 1969, the outbreak frequency imputed to shellfish was 4% (Bryan, 1973). Grimes et al. (1986) estimated that in both the USA and Canada 12000 cases of shellfish-borne diseases had been reported since 1900. This number is in agreement with data by Guzewich & Morse (1986) for the USA from 1900 to 1983: of 198 incidents or outbreaks involving 8659 cases, 94 were typhoidic outbreaks, but relative to a period from 1900 to 1954 only. Gastroenteritis, diarrheic poisoning represented 65 outbreaks, and 29 outbreaks were of viral origin (Hepatitis, Norwalk agent). Among the 58 outbreaks reported by Bryan (1980) for 1970 to 1978, 33 were of unknown etiology, 14 were cases of paralytic shellfish poisoning due to dinoflagellates and 3 were of viral origin. Among bacterial outbreaks Vibrio parahaemolyticus was the main agent. Other cases were due to V. cholera,
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
307
Escherichia coli, Shigella, and Staphylococcus aureus. Clams were the most frequent vehicle in those outbreaks. These data and the census of hepatitis outbreaks (Baron, 1985) emphasise the fact that diseases of viral etiology or due to toxic dinoflagellates (diarrheic shellfish poisoning—DSP or paralytic shellfish poisoning—PSP) are actually much more important than bacterial shellfish-borne diseases. Pathogens potentially associated with shellfish-borne diseases Every pathogen present in sea water may be trapped and concentrated in bivalve tissue, and so represents a potential hazard. Nevertheless, the pathogens transmitted by the human digestive course are the most commonly involved and the discharge of sewage polluted by human and animal pathogens into the sea represents the main source of bacterial pollution. The most serious bacterial diseases likely to be transmitted by shellfish are infectious diseases. Typhoid fever caused by Salmonella typhi and paratyphoid fever (S. paratyphi) in association with shellfish are well known (Buttiaux, 1961; Brown & Dorn, 1977). Brisou (1968) estimated that typho-paratyphoid fevers resulting from shellfish consumption are always more serious than those stemming from other sources. The diarrheal disease cholera is due to the ingestion by susceptible human hosts of enterotoxigenic Vibrio cholerae serotype O1 (Levine, Black & Clement, 1984). Shellfish are often involved in cholera outbreaks which can be explosive and lead to dehydration and death. In addition, non-O1 V. cholerae is associated with food-borne outbreaks expressed in sporadic gastroenteritis (Joseph et al., 1984). Dysentry caused by Shigella is more rare, probably because this bacterium does not survive for long in a marine environment (Moore, 1970). In addition to those serious infections, every disease transmissible by a feeding source has to be considered in health risks associated with shellfish. These include more or less severe miscellaneous gastroenteritis caused by Salmonella spp, enterotoxic strains of Escherichia coli, Yersinia enterocolitica, Plesiomonas shigelloides, Campylobacter jejuni, Clostridium perfringens, Bacillus cereus (Fleet, 1978; N’Guyen Thi Son & Fleet, 1980; Grimes et al., 1986). Staphylococcus aureus can contaminate more particularly processed seafoods (Bryan, 1980). Vibrio parahaemolyticus is responsible for gastroenteritis with symptoms which are quite similar to those of salmonellosis but unlike previous bacteria considered, V. parahaemolyticus is a halophilic bacterium widely distributed in the marine environment. Diseases different from gastroenteritis may be carried by bivalves such as botulism caused by the spore-forming bacterium Clostridium botulinum although Earampamoorthy & Koff (1975) estimated that there is no risk of botulism when molluscs are eaten fresh. A recent interest has pointed out the importance of foods in the transmission of listeriosis caused by Listeria monocytogenes and bivalves are assumed to be a possible vehicle (Huchon, 1980). In addition, Brisou (1968) considered that even in the absence of any pathogenic bacteria, shellfish may be responsible for gastroenteritis when a large quantity of bacteria is ingested. Another sanitary aspect of the sewage pollution of bivalves is the presence of a wide proportion of antibiotic resistant bacterial strains in shellfish tissue: 73% of the faecal coliforms isolated from shellfish by Cooke (1976) were resistant to at
308
D.PRIEUR ET AL.
least one antibiotic and 45% of them were able to transfer their resistance. In addition to hazards relevant to shellfish ingestion, some diseases may result from handling of shellfish by inoculation through breaks in the skin. Handlers may develop erysipeloid from Erysipelothrix rhusiopathiae or infection and septis due to halophilic vibrios including Vibrio parahaemolyticus (Earampamoorthy & Koff, 1975).
PATHOGENS ASSOCIATED WITH BIVALVES
Most of the previously mentioned pathogens have been isolated from the bivalves. For some their presence was directly associated with reported epidemic cases but, on the other hand, pathogens are often isolated without reference to observed pathology. Furthermore, pathogenic bacteria only rarely involved in shellfish transmitted diseases can be isolated from shellfish. Salmonella Salmonella are widely distributed in the marine environment and the isolation of these bacteria from shellfish has been frequently reported (Andrews et al., 1975; N’Guyen Thi Son & Fleet, 1980; Hernandez, Oger & Delattre, 1984; Plusquellec, Beucher & Le Gal, 1986). This group can be finely serotyped and this has produced useful epidemiological data: thus Salmonella isolated by Thomas & Jones (1971) can be related to the incidence of salmonellosis in the population. The same remark was reported by Chugh (1985) who also observed that a quarter of Salmonella isolated from clams were antibiotic resistant. Fraiser & Koburger (1983) investigated the presence of Salmonella in various seafoods (crabs, mullets, clams, and oysters); Salmonella were recovered from each product except mullets. The highest incidence was found in clams (43% positive). The concentration encountered in oysters is unlikely to be related to gastroenteritis. These authors estimated that the consistency of recovery and the variety of serotypes isolated, suggest that Salmonella represents a portion of the free-living flora in the marine environment. Vibrio cholerae The isolation of Vibrio cholerae from bivalves has often been reported from various geographic areas, although Bryan (1980) estimated that this bacterium survives in water only for a short time. Kaper et al. (1979) isolated V. cholerae from a wide range of samples in Chesapeake Bay from different salinities but without seasonal incidence. Most of the isolates were toxic (82%). It was concluded that V. cholerae was an autochtonous resident in this area. In the same way, Hood, Ness & Rodrick (1981) isolated in Florida V. cholerae serotype O1 from oysters with low faecal coliform counts. Most of the strains isolated by Twedt et al. (1981) were non-O1 V. cholerae and none were enterotoxic. Vibrio parahaemolyticus
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
309
V. parahaemolyticus contaminates molluscs in the marine habitat, particularly in warm waters. When eaten uncooked, these products can be responsible for gastroenteritis (Bryan, 1980). In Japan V. parahaemolyticus is the case of more than 70% of the cases of food poisoning resulting generally from ingestion of uncooked sea products (Liston, 1973). The isolation of these organisms from the marine environment has recently received widespread attention in various geographic areas. Their occurrence in North American coastal areas has been established for nearly 20 years, especially on oysters (Baross & Liston, 1970) and from miscellaneous shellfish of the Canadian Atlantic coast (Thompson & Trenholm, 1971). Ayres & Barrow (1978) found low concentrations of V. parahaemolyticus in British shellfish, unlikely to present significant health hazards. N’Guyen Thi Son & Fleet (1980) considered that, generally speaking, contamination levels around 100 V. parahaemolyticus per gram of shellfish are commonly reported. The range reported for Brazilian oysters (Gelli, Tachibana & Sakuma, 1979) was in accordance with this statement. For various countries, relatively high frequencies of positive shellfish samples are reported: from 3.8 to 25% in Dutch mussels (Van Den Broek, Mossel & Eggenkan, 1979), 19% in Brazil (Franca et al., 1980). The presence of V. parahaemolyticus in shellfish is closely related to their occurrence in sea water, which depends upon the water temperature. They are isolated with a higher frequency in summer (Weagant & Kaysner, 1982). All these data emphasise the wide distribution of V. parahaemolyticus in bivalves and N’Guyen Thi Son & Fleet (1980) consider that health risks associated with low numbers of these organisms are due to their ability to develop during shellfish handling operations. Liston (1973) confirms that V. parahaemolyticus can be isolated with high frequency and in significant numbers from shucked oysters.
Escherichia coli Enterotoxic E. coli may be involved in shellfish-borne outbreaks as pointed out by Cross et al. (1979). Some investigations demonstrate the effective presence of enterotoxic E. coli in bivalves. Kokubo et al. (1978) estimated that 3% of E. coli isolated from Tokyo marketed oysters were enterotoxin producers and in Wales (UK) Al Jebouri & Trollope (1984) encountered 6% of enteropathogenic strains among E. coli isolated from edible mussels.
Pathogenic spore forming bacteria Clostridium botulinum type E is present and relatively abundant in some marine areas such as the Baltic sea (Brisou, 1968) and can contaminate shellfish. Thus Presnell, Miescier & Hill (1975) isolated C. botulinum type E from oysters but with a low frequency (2.7%). Similarly C. perfringens and their spores can reach bivalves in their habitat. N’Guyen Thi Son & Fleet (1980) investigated their incidence in oysters. C. perfringens were present in all the samples but at a level unlikely to pose any direct threat. The same authors recovered another spore-
310
D.PRIEUR ET AL.
forming enterotoxic bacterium, Bacillus cereus, but also in concentrations far from the generally admitted infective dose. In dealing with these spore-forming bacteria particular attention should be paid to cooked contaminated products where spores can survive and then germinate and develop to hazardous levels. Other pathogens A systematic search for pathogens in bivalve flora may result in different kinds of isolations. Thus, Trollope (1984) isolated from marine shellfish such bacteria as Salmonella hadar, Shigella dysenteriae, Campylobacter jejuni, Clostridium perfringens, Vibrio parahaemolyticus, Staphylococcus spp., and Yersinia enterocolitica. Other researchers have investigated the presence of a particular pathogen in bivalves and have been generally successful. Yersinia enterocolitica was found to be present in oysters (Peixotto et al.; Weagant & Kaysner, 1982) and mussels (Hernandez et al., 1984) in relatively high numbers throughout the year. Denis (1975) found Pseudomonas aeruginosa and its specific bacteriophage in oysters and mussels. This bacterium was present in 48% of oysters samples and 74% of mussel samples. It was concluded that an exposure to shellfish could be a mechanism involved in the transmission of P. aeruginosa. Concerning the pathogenic yeasts, Buck, Bubucis & Combs (1977) clearly demonstrated their presence in shellfish but considered that there is still no clear evidence of association of human mycoses with shellfish consumption. This list of the pathogens isolated from shellfish is certainly not exhaustive, but isolation of pathogens from bivalves must not be regarded as evidence of pathogenicity.
RECORDS OF HUMAN DISEASES AND EPIDEMIOLOGY
Reality of human health risks (reported outbreaks) The real incidence of the previously listed isolations appears through the report of outbreaks connected with these pathogens. Thus, it can be stated that typhoid fever is actually unlikely to spread in the USA and reported outbreaks are remote (Bryan, 1980). Similarly, in France Pinot, Riou & Chaperon (1988) consider that the last epidemic outbreaks due to Salmonella happened 20 years ago. In contrast, Fraiser & Koburger (1983) estimate that in the USA the incidence of salmonellosis has been increasing over these years. Cholera is a contemporary problem as is shown by the review of cholera associated with seafoods presented by Bryan (1980). Cholera outbreaks occurred in Malaysia in 1971, in Italy in 1973 (mussels were involved) and in the Gilbert Islands in 1979 (raw clams and fish). The most severe cholera epidemic related to shellfish occurred in Portugal in 1974 with 2467 bacteriologically confirmed cases and 48 deaths, due to the consumption of raw or poorly cooked cockles (Blake et al., 1977). More recently, Vibrio cholerae non-O1 were indicated as the chief causative agents of gastroenteritis outbreaks linked particularly to consumption of raw oysters (Wilson et al., 1981; Bradford, 1984).
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
311
Raw oysters are often involved in V. parahaemolyticus outbreaks (Spite, Brown & Twedt, 1978). Nolan et al. (1984) reported six cases of gastroenteritis outbreaks due to V. parahaemolyticus along the Pacific coast (USA). Similarly, the consumption of oysters was the source of an outbreak in Australia in which enterotoxic Escherichia coli were identified (Cross et al., 1979). In 1980 an outbreak of gastrointestinal illness occurred in New Jersey. It was associated with the ingestion of raw clams contaminated by Campylobacter jejuni (Griffin et al., 1983). Several food poisoning cases due to spore-forming bacteria in shellfish could also be listed: five outbreaks of botulism were reported in the USA from 1900 to 1978 (Bryan, 1980). Clostridium botulinum type E was involved in all the cases relating to clams or clam juice. N’Guyen Thi Son & Fleet (1980) reported Bacillus cereus as responsible for food poisoning involving oysters. Pinot et al. (1988) point out a lethal enteritis due to Clostridium perfringens after ingestion of oysters. Epidemiology Reports of collective diseases related to shellfish consumption do not reflect the real incidence of shellfish poisoning. An epidemiologic knowledge of this problem requires an evaluation of the frequency of the pathologic manifestations connected with ingestion of bivalves (Pinot et al., 1988). Such an investigation needs improved shellfish-borne disease surveillance. Centres for epidemiologic survey exist in the USA (CDC), in Great Britain (CDSC), and in France. Mackowiack, Caraway & Portnoy (1976), estimated that in cases of outbreak of assumed shellfish origin, it is necessary: (1) to known if diseases are really related to shellfish; (2) to identify clearly the origin of the shellfish; (3) to determine if shellfish were harvested from approved growing areas; and (4) to specify if the contamination occurred before or after harvesting. Baron (1985) considered that particular attention should be paid to shellfish conforming with bacteriological standards but presenting a low viral contamination. Most epidemiologic studies have been retrospectively carried out. In France, a clear demonstration of the association of typhoid fever with contaminated oysters was shown (Martin-Bouyer, 1978). It was established that typhoidic mortality was associated with coastal areas and that an endemic situation existed around oysterproducing areas. A general methodology to assess the sanitary hazards resulting from bivalve consumption is proposed by Pinot et al. (1988) with a view to answering two important questions: what risks are shellfish consumers exposed to and what is the relationship between pathology due to the consumption of bivalves and contamination of these bivalves?
PREVENTION OF SHELLFISH-BORNE DISEASES
Although epidemiological evidence is lacking, the pollution by domestic sewage of areas used in the growing of shellfish and the subsequent ingestion of contaminated shellfish appears to be the main source of viral and bacterial shellfish-borne diseases. Public health protection needs a permanent survey of
312
D.PRIEUR ET AL.
shellfish quality which requires National Shellfish Sanitation Programmes. Guzewich & Morse (1986) defined the main points of such a programme. (1) Improvement of shellfish-borne disease surveillance and reporting. (2) Development of microbiological standards for shellfish and growing waters to insure bacterial and viral safety. (3) Classification of shellfish harvesting waters and adoption of a tagging system. (4) Requirement for depuration of all shellfish sold. (5) Campaigns of advice against the consumption of raw or partially cooked shellfish. In addition to these Bryan (1980) advocates the setting up of a sanitary policy in processing plants and markets. He estimates that the treatment of sewage is essential for reducing shellfish-borne diseases. The efficiency of sanitation programmes is clearly demonstrated by the decrease of infectious diseases. In the countries that have developed surveys and standards, typhoid and cholera related to shellfish have almost disappeared.
EVALUATION OF BIVALVE QUALITY
A permanent survey of shellfish quality, as described above, with classification according to standards cannot be achieved directly for many reasons. The presence of pathogenic bacteria in shellfish is erratic. Techniques for their investigation are elaborate and expensive and the detection of pathogens is generally semiquantitative and inadequate for classification. The necessity for a quantitative evaluation through indicators appeared very early. In 1910 Johnstone estimated that “quantitative results are essential…it is desirable that some generally recognized series of tests should be uniformly adopted by bacteriologists”. Consequently, indicator groups defined for water examination have been adopted for shellfish monitoring: the coliform group or, more closely, faecal coliform or Escherichia coli and faecal streptococci are the most commonly adopted. Their value will be discussed later. In addition, more particular indicators have been proposed in the context of shellfish evaluation. According to Madden, Buller & McDonell (1986) Clostridium perfringens can indicate faecal pollution in mussels and oysters when Escherichia coli shows none and thus can be used as an indication of good depuration. Ayres (1975) estimated that Clostridium perfringens and faecal streptococci utilisation might be useful in shellfish survey as a complement rather than a substitute for using Escherichia coli. The use of phages and especially coliphages as indicators of the viral contamination of shellfish has been contemplated (Vaughn & Metcalf, 1975) but it was shown that the simultaneous presence of coliphages and enteric viruses in oysters was not related; oysters can, however, retain and eliminate phages and viruses in the same way.
STANDARDS OF ANALYSIS
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
313
Microbiological standards relating to shellfish safety may concern shellfish growing waters or shellfish themselves. Shellfish standards were reviewed by Pinot et al. (1988); they are essentially based on bacterial indicator levels. Standards for shellfish growing waters Large differences exist between international prescriptions, ranging from the absence of standards to precise directives. In the USA, standards concerning the quality of shellfish growing waters are essentially indicatives (Shear & Gottlieb, 1980). Shellfish growing areas are classified into categories according to their quality. (1) 1st and 2nd class: approved areas conforming to less than 70 total coliforms per 100 ml and 14 faecal coliforms per 100 ml (with 10% tolerance of, respectively, 230–100 ml and 43–100 ml). (2) 3rd class: areas subjected to restriction presenting from 70 to 700 total coliforms per 100 ml of water. (3) 4th and 5th class: prohibited areas with coliform levels over 700 per 100 ml. Shellfish from these areas may be marketed only after relaying or depuration. In Australia oysters are subjected to depuration and growing waters have to present less than 70 coliforms per 100 ml. In Europe a directive from the European Economic Community (30/10/1979) refers to the quality of shellfish growing waters. This quality is monitored through the shellfish and a guideline value of 300 faecal coliforms per 100 ml of shellfish content (meat and shellfish water) is recommended. Standards for shellfish In the USA directives for marketed shellfish microbiological quality are elaborated by the “National Shellfish Sanitation Programme (NSSP)” and consumer protection is ensured by a guideline of 230 faecal coliforms per 100 grams of shellfish meat (Cole et al., 1986). In Australia the standards for shellfish at consumption level are the following (Fleet, 1978): 2.3 Escherichia coli per g of bivalve content (with a 20% tolerance under 70 E. coli per g) and 105 total viable cells count per g (with a 20% tolerance under 5×10 5 per g). In the UK systematic depuration is carried out and although formal standards do not exist, shellfish treated by depuration system are expected to contain less than 2 E. coli per gram of tissue (Trollope, 1982). In Spain, the use of a depuration process is obligatory for seven shellfish species (Pinot et al., 1988). Standards applied to depurated shellfish are the following (for 100 ml of bivalve content): total bacterial count (20°C), 10 7; E. coli, 50; faecal streptococci, 104 with absence of Salmonella in 25 ml (orden del 31/05/1985). In France, market shellfish standards establish a three class survey based on the following values: faecal coliforms 300 per 100 ml, faecal streptococci 2500 per 100 ml, Salmonella should be absent in 25 g (arrêté du 21/12/1979).
314
D.PRIEUR ET AL.
TECHNIQUES
The quantitative microbiological analysis of shellfish needs a preliminary preparation of tissue suspension. A representative number of shellfish, depending on the size of the bivalve, is washed, dried, and aseptically opened. Either the whole content or the meat alone (according to the recommendations) is collected in a sterile cylinder and diluted by sterile diluent (Trollope, 1982). A single dilaceration is not sufficient for the removal of the bacteria which needs the use of a blender (Boury & Borde, 1964a). The Colworth stomacher is very appropriate to this use (Trollope, 1984). The MPN method (More Probable Number) using a 5 tubes or a 3 tubes technique is generally recommended for indicator enumeration (American Public Health Association—APHA; Standards Association of Australia— SAA; Association Française de Normalisation—AFNOR). This general recommendation is due to the low bacterial levels to be detected (about 2 or 3 cells per gram of tissue). Concerning the coliform group, or more especially faecal coliforms or Escherichia coli, a large number of techniques have been proposed. The APHA (1970) recommended the use of MacConkey Broth incubated at 37°C for 48 h as the presumptive medium. Tubes showing positive fermentation are subcultured into Brilliant Green Bile lactose Broth (BGB) and incubated at 37°C for 48 h to confirm the presence of coliform bacteria. Another subculture in BGB incubated at 44.5°C permits to confirm the presence of faecal coliforms. A tryptone water may be added to test indole production at 44.5°C. A positive result in both BGB (growth and gas) and tryptone water is considered as positive for E. coli (Cooke, 1976). The Australian recommendations are very similar. In France, the shellfish suspension is directly inoculated in BGB Broth incubated at 37°C (Norme AFNOR NFV45110, Anonymous, 1981). Several modifications of the APHA procedure have been suggested in order to obtain a result more quickly. Hunt & Springer (1978) proposed a modification of the Al medium developed by Andrews & Presnell (1972), giving results for E. coli within 24 h, but according to Yoovidhya & Fleet (1981) the counts obtained are lower than those with the method recommended by the APHA. Rapid methods presented by Quadri, Buckle & Edwards (1974) also offer a one-day response. The more recent use of methyl 4 umbelliferyl glucuronide (MUG) permits a direct confirmation of E. coli in BGB Broth (Koburger & Miller, 1986). Nevertheless, these MPN procedures, in all cases, lack accuracy and methods using agar media may be preferred. The roll-tubes method of Clegg & Sherwood (1947) has been largely used in England. Al Jebouri & Trollope (1981) recommended a pour plate method: inclusion of shellfish suspension into MacConkey agar. Lastly, the Anderson & Baird-Parker (1975) permitting a direct enumeration of E. coli by a membrane overlay plate technique was found to be sensitive and accurate in the range of 2–5 E. coli per gram (Yoovidhya & Fleet, 1981). Modifications of those agar enumeration techniques, permitting an increased sensitivity would offer new possibilities in shellfish microbiological control.
RELATION BETWEEN PATHOGENS AND INDICATORS
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
315
The question of the value of the evaluation of shellfish quality by bacterial indicators is of great importance for hygienists and has been the subject of many investigations, carried out to answer two precise questions. What is the most reliable indicator group as an indication of the presence of pathogens and what level of indicator will insure satisfactory shellfish? First, it must be admitted that the significance of the usual indicators is limited to an indication of pathogens transmitted by the faecal route. Consequently, marine indigenous pathogens will not be related with enteric pathogens or faecal indicators. This has been confirmed many times with Vibrio parahaemolyticus. Thus, Greenberg et al. (1982) established that these bacteria were not more abundant in clams harvested in polluted areas. V. parahaemolyticus presents no particular association with faecal pollution (Sobsey et al., 1980) and its frequency of isolation shows little connection with faecal coliform levels (Metcalf et al., 1973; Rodrick et al., 1984). Occurrence of V. parahaemolyticus in oysters is only dependent on occurrence of these organisms in the overlying water and on water temperature (Cole et al., 1986). Similar conclusions were obtained by Kaper et al. (1979) and Hood et al. (1981) with isolation of V. cholerae and faecal coliform counts. It is concluded that V. cholerae may be an autochtonous resident of the marine environment. Clostridium botulinum type E, a non-faecal bacterium, also has a distribution independent of sewage pollution (Bryan, 1973). With regard to faecal transmitted pathogens, many data concern the relative validity of indicator groups. Faecal coliforms and Escherichia coli are the most commonly used and many authors have demonstrated the greater validity of the faecal coliform group compared with the total coliform group in indicating the presence of Salmonella. (Geldreich, 1965; Andrews et al., 1975, 1976). E. coli levels correlate very strongly with faecal coliform levels in oysters and clams, so that there is no advantage in replacing faecal coliforms by E. coli as an indicator (Hood, Ness & Blake, 1983). Faecal streptococci (FS) are generally found in all samples containing faceal coliforms (FC). The ratio FC/FS averaged about 2 (Slanetz et al., 1968). In addition, faceal coliform counts are significantly correlated with standard plate count in oysters (Cole et al., 1986) although an opposite conclusion was given by Comar, Kane & Jeffreys (1979). Data concerning the relation between indicator levels and pathogens are generally obtained with Salmonella and are in some ways inconsistent. Marjori, Campello & Crevatin (1977) established a clear correlation between Salmonella isolation and indicator counts while this relation did not exist in water or between Salmonella detection and faecal streptococci pollution. Consequently, Salmonella are only recovered in samples with coliform levels above shellfish tissue standards (Hood et al., 1983), although this relation is not as clear in stored bivalves. For Andrews et al. (1975), the recovery of Salmonella from oysters increased with total and faecal coliform levels in shellfish meat, likewise faecal coliform counts increased in the water but did not follow increase of total coliforms in the water. This relationship between Salmonella and faecal coliforms was also found by Hernandez et al. (1984) who demonstrated the same good correlation between Escherichia coli counts in mussel meat and detection of another enteric pathogen bacterium Yersinia enterocolitica.
316
D.PRIEUR ET AL.
On the other hand, many results lead to the conclusion of a defective or limited relation between indicator levels and pathogen isolation. Thus, the isolation of Salmonella from oysters by Slanetz et al. (1968) generally arose from sea water presenting indicator levels below the recommended standards. The author estimated that current criteria do not insure that the oysters are free from pathogens. In the same way, Metcalf et al. (1973) showed that Salmonella occurrence in shellfish did not parallel the occurrence of Salmonella in the overlying water or of Escherichia coli MPN in shellfish. Consequently, Salmonella can be isolated from shellfish growing in water consistent with bacteriological standards. Metcalf et al. (1973) estimated that in shellfish a better correlation existed between enteroviruses and Salmonella than between these two pathogen groups and faecal coliform levels. According to Fraiser & Koburger (1983) this low coincidence between pathogen incidence and indicator levels may be due to “the ability of many pathogens to establish a niche for themselves far removed from a host”. This hypothesis may also be valuable for viruses because the numerous data concerning isolation of viruses related to bacterial indicators, generally lead to the failure of indicators to reflect occurrence of enteroviruses. Gerba et al. (1980) demonstrated that no relationship exists between viruses in oysters and viruses in water, or between viruses in oysters and bacterial indicators in oysters. The authors estimated that the usual standards did not reflect viral contamination. Cole et al. (1986) obtained similar results. Virus levels in the oysters appeared to be only correlated with total coliforms counts in water and total plate counts in the oysters. This question was recently reviewed by Baron (1985) who concluded that in the absence of epidemic outbreaks, the incidence of viruses in bivalves was not related with their presence in sea water and sediment. If there is a weak relationship between incidence of viruses in water and indicator levels in water, shellfish or sediment the occurrence of viruses in shellfish is not, however, related with the usual bacteriological criteria in those shellfish either in water or in sediment. It is, therefore, clear that bacterial indicators are unable to indicate viruses in the marine environment. The review of viral epidemic outbreaks (Baron, 1985), however, shows that most resulted from consumption of shellfish heavily contaminated in terms of bacterial indicators or harvested in areas known to be polluted. On the other hand Portnoy (1975) and Mackowiack et al. (1976) recorded a hepatitis outbreak resulting from oysters meeting bacteriological standards, but harvested in an area which had previously exhibited contamination. This observation suggests that elimination of viruses by the shellfish does not follow the same course as elimination of the indicators. Bostock (1979) reported a hepatitis outbreak caused by mussels subjected to depuration which emphasises this hypothesis. Therefore, if pathogens can frequently be isolated from bivalves presenting satisfactory indicator levels, the sanitary significance of these isolations has to be established. Epidemiological data relating health risks to bacterial pollution are lacking but the survey of shellfish by bacterial indicators remains a useful tool for public health protection as suggested by the decrease in pathology observed in countries carrying out a shellfish sanitation programme.
BIVALVES AS INDICATORS OF POLLUTION
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
317
The monitoring of sewage pollution of marine waters using mussels has been known for a long time (Dodgson, 1928 vide Trollope, 1984). The survey of chemical pollutants in the marine environment by means of mussels has been developed (Goldberg, 1975). Similarly, potentialities of bivalves in microbiological surveys have been frequently contemplated and are presented by Ayres et al. (1978): “As molluscan shellfish have the ability to concentrate bacteria, they are useful tools in surveying areas for evidence of faecal pollution and represent an extra dimension in sampling which often cannot be achieved by bacteriological sampling of water alone”. Metcalf (1974) proposed the extension of the use of molluscs to the detection of viruses. Mussels appear to be the most reliable material in this application (Wood, 1957). The variability observed in volume and contamination of internal shellfish liquid leads to the recommendation that this fraction be eliminated (Boury & Borde, 1964; Plusquellec et al., in press). This elimination leads, moreover, to an increased sensitivity. Furthermore, if the digestive tract alone is used as inoculum, it becomes possible to detect lower bacterial concentrations (Al Jebouri & Trollope, 1981; Barbosa, 1987). Survey of bacterial pollution by means of shellfish has been applied in pathogen detection, especially of Salmonella. Slanetz et al. (1968) reported that Salmonella were present from all samples in a station although no isolation was obtained from water. This efficiency in Salmonella detection was also stated by Plusquellec et al. (1986); the frequency of isolation was 41% in mussels compared with 11% in paired sea-water samples. Marjori et al. (1977) compared mussels, sea-water filtration and pad concentration in Salmonella detection and obtained, respectively, 41%, 27%, and 30% of positive results. A laboratory study done by Hernandez et al. (1984) demonstrated the sensitivity of mussels to detect pathogens: Salmonella and Yersinia were isolated from mussels set into sea water artificially contaminated by 5 to 20 cells·l -1 of these pathogens. More generally, the bacterial enrichment performed by the shellfish will be applied to an indirect evaluation of the sea-water contamination through the measurement of the bivalve faecal bacteria level. Experimental studies of Cabelli & Heffernan (1970a, b, 1971) attested that the coliform concentration in the bivalve was a reflection of the water contamination during the preceding hours. Thus, Trollope & Al Salihi (1984) attempted to use molluscs in order to monitor bacteria in the water. It was demonstrated that the immersion of captive mussels for 2 h or more was sufficient to reflect bacterial changes in the water column (Trollope, 1984). Delattre & Delesmont (1981) tested the value of shellfish for bacteriological survey of sea water used in bathing. Mussels and cockles were used as sampling material and compared with water contamination. An effective enrichment of indicator bacteria was noted in the bivalves but the authors considered the contamination in the shellfish to be as variable as the contamination in the water. A report from CETE (Anonymous, 1982) reached a similar conclusion. It was estimated that the survey by mussels did not reflect spatial or temporal variations better than the water survey. Nevertheless, Plusquellec et al. (1983) pointed out that a decrease in variability was obtained with indigenous mussel tissue as compared with sea-water counts, in the case of a daily survey. This reduction was more marked for faecal streptococci than for faecal coliforms. Moreover, the same observation was obtained with short
318
D.PRIEUR ET AL.
temporal variations during a tidal cycle: while faecal coliform levels in mussels paralleled water variations, faecal streptococci counts in mussels presented few variations. The authors concluded that an estimation of the faecal pollution of an area by means of faecal streptococci in mussels, constitutes a sensitive method which offers a decrease in variability and so provides a mean evaluation of water contamination. It remains essential to complete these inconsistent data and particularly to establish to what extent mussels are able to ‘integrate’ short term variations in water contamination.
MICROBIAL DISEASES IN BIVALVE MOLLUSCS Numerous diseases with different etiology have been described for bivalve molluscs. Disease is defined as a demonstrable negative deviation from the normal state (health) of a living organism. It is measurable, for example, in terms of rates of survival, growth, reproduction or competitive capacity. It may be due to a single cause or to several causes acting in concert. The balance between a potential pathogenic agent and the ability of the animal to interact with it depends on environmental and nutritional conditions, and on the physiological state of the mollusc. Normal bivalve bacterial populations may turn into a “lethal disease agent” as soon as the biological state of the mollusc becomes impaired due to multiple factors (environmental deterioration, nutritional deficiency, competition or senility). Therefore, the bacterial origin of the observed diseases is not always well defined, as bacteria from normal microflora are mostly potential pathogens. Bacterial pathology in bivalve molluscs will be discussed in both adults and larvae.
ADULT PATHOLOGY
The described and analysed bacterial diseases are sporadic. Epidemic constants are not defined for multiple reasons. One is the high density of bacteria which is tolerated by adult molluscs. Another is the presence in the organism of cellular and humoral means of defence against foreign agents such as bacteria.
Agents: Rickettsiae, Chlamydiae, mycoplasma The members of these 3 groups are similar to bacteria (but different from viruses) with respect to their ability for independent protein synthesis, their mode of reproduction by binary fission, and their susceptibility to antibiotics. Rickettsia-like organisms have been described in numerous molluscs such as clams, scallops, mussels, oysters. They are obligate intracellular organisms. The main infected organs are: gills (Gulka & Chang, 1984a; Mialhe et al., 1987; Le Gall et al., 1988a; Le Gall, Miahle & Grizel, 1988b), gut (absorptive epithelium) (Comps, 1983; Elston & Peacock, 1984), and kidney (Morrison & Shum, 1983). The organisms appear as basophilic inclusions. Ultrastructurally
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
319
the inclusions are round membrane-bound vacuoles containing procaryote forms (Elston & Peacock, 1984). The prevalence is variable with species, populations and geographic sites, ranging from about 30% according to most authors, to occasionally 100% (Le Gall, Miahle & Grizel, 1988b). Rickettsia infections occur only in juveniles and adults. Larvae would appear not to be susceptible (Elston & Peacock, 1984; Le Gall et al., 1988a). Rickettsia cannot be grown in artificial acellular medium, because they have a strict intracellular multiplication, and mollusc cell cultures are not yet available. Therefore, only histological description of the infestation is done. The infested animal’s response to infection consists only in rounding the Rickettsia and detachment of the infected cells (Elston & Peacock, 1984; Gulka & Chang, 1984b). Rickettsia themselves do not cause mortality but are often associated with mass mortality in bivalve populations. Nevertheless, the elimination of numerous infected cells could affect the mobility of the molluscs (e.g., by reduction of swimming), and therefore their avoidance of predators, especially in scallops (Gulka & Chang, 1984a), and could enhance disease susceptibility by debilitating action. Chlamydiae display a characteristic infectious cycle. The cellular multiplication results in the production of dense bodies which, because of the rupture of the host cell, are released and repeat the cycle. Chlamydiae have been described in particular in clams (Meyers, 1981) and scallops (Morrison & Shum, 1981; Page & Cutlip, 1982). Cytopathology of the digestive diverticula could produce disturbance of the digestive function. Mycoplasmas, the smallest free-living organisms without cell wall, have been observed in oysters (Meyers, 1981). It seems possible that mycoplasma(s) do not produce disease symptoms in their bivalve mollusc hosts.
Agents: Bacteria Among the bacteria Pseudomonas enalia was isolated from diseased oysters in greater number than from healthy oysters, and its pathogenicity was demonstrated after experimental inoculation (Colwell & Sparks, 1967). All other pathogenic bacteria, except this Pseudomonas belong to the Vibrio family. A cardiac oedema is described in oysters with a low incidence in the population (0.04%). The isolated Vibrio is not experimentally pathogenic, and the molluscs have no other lesions (Tubiash, Otto & Hugh, 1973). Among the Vibrio group, V. alginolyticus is considered as a potential pathogen, and V. anguillarum is more pathogenic (Tubiash, 1974). Nevertheless, some particular conditions are required: high temperature (maximum mortality at 21°C), poor physiological condition of the mollusc and large rate of bacterial contamination. Under such conditions, however, the mortality is relatively low (30%) (Lipovsky & Chew, 1972; Grischkowsky & Liston, 1974; Tubiash, 1974; Kaneko, Colwell & Hamons, 1975). As far as adult molluscs are concerned, it seems that the isolated Vibrio are to be considered as bacteria of secondary infection, rather than strict primary pathogens. In the natural environment, the estimation of characteristic “disease animals” and, consequently, sampling, make it difficult to distinguish between primary and secondary infection.
320
D.PRIEUR ET AL.
LARVAL PATHOLOGY
For larvae, infectious processes of bacterial etiology have been frequently observed in hatcheries and in laboratories. Host range and geographic distribution Most of the susceptible mollusc species are oysters (Tubiash, Chanley & Leifson, 1965; Tubiash, 1972; Brown & Losee, 1978; Elston & Leibovitz, 1980a; Bolinches et al., 1986) or clams (Guillard, 1959; Tubiash et al., 1965; Brown, 1974; Elston, Elliot & Colwell, 1982; Nicolas & Cochard, 1987). The geographical distribution of the bacterial pathology of larvae includes the USA, and at least three European countries (the UK, Spain, and France). Course of the disease—clinical signs As far back as 1959, a connection was shown between larval mortality and the presence of bacteria, more especially as the disease was transmitted to healthy larvae with strains isolated from diseased animals. This disease was named “Bacillary necrosis” (Guillard, 1959). Since then similar infectious processes have been repeatedly described. Each observation depends on the species, the age of larvae, and the proper environmental conditions. The general characteristics, however, are two-fold. (1) A rapid (settlement in some hours) and inexorable phenomenon (a considerable mortality ranging from 90 to 100% is observed in 24 h) (Elston et al., 1981). The older the larvae are, the less sensitive they are (Nottage & Birkbeck, 1986). (2) An immobility of larvae as a mean clinical expression: they stop swimming and lie on the bottom. More than 1% of non-mobile larvae would be characteristic of a “disease tank” (Jeffries, 1982). The velum and the foot are distended. The larvae stop feeding and are surrounded by a bacterial swarm, then granular necrosis appear. The bacteria attach to the shell and invade the velum, the internal shell, and the visceral cavity, causing death. This clinical and lesional state occurs in all larval stages. Two other clinical manifestations are experimentally described by Elston & Leibovitz (1980b). (1) The early veligers remain active but display a variety of velar damage, mainly the loss of the ciliated cells, which produces a decrease in mobility, and consequently a decrease in food intake. The larvae, being unable to renew their reserves, die of starvation. The velar lesions could be due to the action of a bacterial toxin which involves a modification of the intercellular adhesion. (2) The late veligers become sedentary and exhibit progressive and extensive visceral atrophy. Cells of the digestive gland are shed first. A secondary invasion of bacteria involves focal lesions in organs of the
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
321
digestive tract. The destruction of the nutrient assimilative capacity, as the consequence of a primary toxic cause, produces general shrinkage of the tissues into unrecognisable masses. Some authors also account for shell fragility as the consequence of under calcification of the peripheral shell and excessive chalky deposits, up to 50%. Juveniles showed eroded ligaments, malformations and a decrease of growth (Elston et al., 1982).
Bacteria and pathogenicity The involved bacteria belong to the genus Pseudomonas and especially to the genus Vibrio (Brown, 1973). Among Pseudomonas, a red pigmented strain produces mortality with concentrations above 103 bacteria·ml -1, whereas a non-pigmented mutant is inactive (Brown, 1981a). The main pathogenic bacteria are Vibrio (Tubiash, Colwell & Sakazaki, 1970). From the numerous isolated strains, a new genus has been proposed: V. tubiashi, pathogenic for larvae of clams and oysters, the distinctive biochemical characteristics of which are xanthin degradation and tyrosin hydrolysis (Hada et al., 1984). V. aestuarinus (lactose +, acetoïn—), V. anguillarum, V. fisheri have also been often isolated (Brown, 1981b; Jeffries, 1982; Garland et al., 1983; Tison & Seidler, 1983; Lodeiros et al., 1987; Nicolas & Cochard, 1987). Recently, Brown & Tettelbach (1988) characterised a pathogenic non-motile Vibrio. The multiple action mechanism of these bacteria on larvae has not yet been explained. Bacteria act by their numbers. Mortality after experimental vibriosis of oyster larvae increases from 40 to 100% if the initial contamination rate increases from 10 3 bacteria·ml -1 to 107 bacteria·ml” 1 (Elston & Leibovitz, 1980b). In mussels, infestation rates of less than 100 bacteria·ml -1 cause little larval mortality due to vibrosis, whereas a rate of 10 5 bacteria·ml -1 produces death in 48 h. These results are not constant. As Brown (1981b) reported that vibriosis (V. anguillarum) could be initiated in the laboratory with 2 bacteria·ml -l after each change of larval culture water, in 10-day old oyster larvae. Bacteria also act by releasing substances. An early filtrate from a Vibrio culture is described as a swimming inhibitor, as a necrosis producer, and as having a teratogenic effect (Brown & Losee, 1978; DiSalvo, Blecka & Zebal, 1978). In the same way the pigments of the red pigmented Pseudomonas, are responsible for the observed delay in embryonic development. Generally the toxin acts in proportion to its concentration, that is similar to the total bacterial culture. Its maximum action is observed after 48 to 72 h bacterial culture. The toxin could be either a secondary metabolite, or a bacterial constituent released after the death of the bacteria (Brown & Roland, 1984; Nottage & Birkbeck, 1986). Fractionation of a Vibrio culture supernatant displays several components (Nottage & Birkbeck, 1987a,b,c): one component is a proteinase, and a second is a hemolysin. They produce experimental disaggregation of adult mussel gill tissue in 72 h. These two factors are heat labile. A third component, active in weak concentration, shows ciliostatic activity. This activity would be more intensive with more pathogenic bacteria.
322
D.PRIEUR ET AL.
Radiolabelled Escherichia coli degradation is inhibited for mussels previously exposed to Vibrio anguillarum, especially, and also to V. fisheri, while degradation is normal for mussels previously exposed to Pseudomonas (McHenery & Birkbeck, 1986b); Vibrio anguillarum inhibits the mussel’s nitration. Only 20% of Vibrio are excluded from the water by mussels, whereas 90% of Pseudomonas are excluded after the same exposure time. Inhibition of nitration probably relies on the release of low molecular weight ciliostatic thermostable factors from the bacteria (Nottage & Birkbeck, 1986; McHenery & Birkbeck, 1986b; Birkbeck, McHenery & Nottage, 1987). Vibrio present in sufficiently high concentrations would probably inhibit growth of juvenile and adult bivalves and lead to debility in the larvae, rendering them more susceptible to infection by pathogenic agents. Prevention and treatment Pathogenic agents can enter hatcheries by several routes: sea water, brood stock, algae, husbandry system. Bolinches et al. (1986) point to hatchery conditioning of wild adult oysters during summer as one route of contamination, as gonads of nonconditioned brood stock are free of Vibrio, Larvae would be contaminated through the paleal cavity of conditioned oyster brood stock. Presence of bacteria is related to closed husbandry techniques. Vibrio was isolated three days after a first inoculum, although the water in the culture was changed daily (Brown, 1981b). Treatment of such an infectious process is hazardous, because it often takes place too late. Elston et al. (1982) recommend, however, a larval treatment consisting of a 1-min bath in a 10 ppm sodium hypochlorite solution, if the valves are intact enough to close. Preventive action aimed at the reduction of pathogenic bacteria in the husbandry system would be expected to involve the following. (1) Maintenance of pathogen-free incoming sea water by UV treatment (Brown & Russo, 1979; Brown, 1981b; Brown & Tettelbach, 1988) and algal stocks and expanded cultures. (2) Maintenance of a low level of bacteria in the system. (3) Disinfection systematically of the equipment, and strict adherence to the hygiene rules in the hatchery. Also less frequent changes of sea water in static larval cultures (48 h rather than 24 h) reduce losses due to bacterial diseases (Leibovitz & Elston, 1980). The preventive use of antibiotic is still contested (Le Pennec & Prieur, 1972, 1977; Martin & Vicente, 1975). The utility of antibiotics has never been substantiated in production scale culture, and antibiotics are not widely used in such applications (Elston, 1984). Nevertheless, in French commercial hatcheries, antibiotics are occasionally used to control bacterial populations in some life stages (Buestel et al., 1982). The possibility that resistant strains of bacteria will be created by this sytematic use, has been demonstrated (Jeanthon et al., 1988). The therapeutic use of antibiotics to stop bacterial infection must be carried out in conjunction with appropriate antibiotic sensitivity screening. Some antibiotics have been recommended (Brown, 1974; Grischkowsky & Listen, 1974; Brown & Losee, 1978; Brown & Tettelbach, 1988; DiSalvo et al., 1978) but their
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
323
use could be toxic for larval development (e.g., the furans). In production it is usually more effective in control of the disease, to discard infected larval cultures and to sterilise the system components rather than to attempt to carry out a treatment with antibiotics. Bacterial pathology of bivalve molluscs is mainly a larval pathology, widely spread in most species, with large economical loss, the mechanisms of which are only partially explicit. On the other hand, in the case of adults, proper pathology could be excluded. In addition to their role in the field of human health, molluscs could, however, harbour bacteria pathogenic for other aquatic animals, especially fishes.
IMMUNOLOGY OF BIVALVE MOLLUSCS All metazoan animals are protected against invading foreign substances or organisms by an internal defence system. This system includes various cells, free or connected in tissues and organs, and humoral factors. The vertebrate means of defence are divided in two groups: natural immunity and acquired immunity. Natural immunity allows the organism to contend with foreign materials without any previous contacts with them. Acquired immunity is closely specific and follows a first contact with an antigen. After a second contact with the same antigen, the higher and faster secondary immune response is the result of memory formation. This response is characterised by the production of antibodies. Because of their phylogenic position, bivalve molluscs possess only the first part of this immune system; they do not produce antibodies.
CELLULAR EFFECTORS
The cells are the principal component of the immune response of bivalve molluscs. Haemocytes or amoebocytes are present in the haemolymph in numbers varying between individuals and over time (Narain, 1973). In Mytilus edulis circulating counts vary from 0.4×10 6 ·ml -1 up to 20×106·ml -1 (Renwrantz & Stahmer, 1983). Pericardial haemolymph contains 1.5×106·ml -1 in Mercenaria (Friedl & Alvarez, 1988) and 7 to 8×107ml -1 in Crassostrea gigas (Bachere, Chagot & Grizel, 1988). With regard to their morphology the haemocytes fall into two groups: the granulocytes, large granular cells with intra-cytoplasmic vesicules; and the hyalinocytes, small agranular cells (Moore & Lowe, 1977; Ruddel et al., 1978; Cheng et al., 1980; Rasmussen, Hage & Karlog, 1985). Among the haemocytes 70% in C. virginica (Renwrantz et al., 1979), and 84% in Mytilus edulis (Renwrantz & Stahmer, 1983) are granulocytes. Rasmussen et al. (1985) suggested, however, that agranular and granular haemocytes could be two different stages of the same cell line. Haemocytes are heterogenous in each group. Subpopulations have been described with regard to their cytochemistry (Moore & Lowe, 1977), their ultrastructure (Rasmussen et al., 1985; Auffret, 1986), their density (Cheng et al., 1980; Bachere et al., 1988), the biochemical composition of their granules
324
D.PRIEUR ET AL.
(Cheng & Downs, 1988) or their surface binding sites (Cheng et al., 1980). Nevertheless, no common scheme of haemocyte classification has yet been evolved.
HUMORAL EFFECTORS
The haemolymph contains a variety of biologically active molecules. Most of them take part in foreign material destruction. Haemocytes of M. edulis (Wittke & Renwrantz, 1984; Leippe & Renwrantz, 1988), of Crassostrea gigas (Leippe & Renwrantz, 1985), of Corbicula fluminea (Yoshino & Tuan, 1985), and of Mercenaria mercenaria (Anderson, 1981) are able to secrete cy to toxic molecules, as shown by the occurrence of a ring of lysed mammalian erythrocytes in agar. The release of haemolysin(s) is independent of contact with target erythrocytes and haemocyte dose but is temperature-dependent. The haemolysin is a heat labile protein, the chemical nature of which is still under investigation (Yoshino & Tuan, 1985; Leippe & Renwrantz, 1988). The lectins, proteins or glycoproteins, are able to interact specifically with carbohydrates of foreign organisms inducing cell agglutination (erythrocytes) or precipitation of molecules (polysaccharides). Widespread throughout the biological world, agglutinins have also been isolated from bivalves: Mytilus (Renwrantz & Stahmer, 1983; Leippe & Renwrantz, 1988), oysters (Acton et al., 1969; Cheng et al., 1980), clams (Johnson, 1964; Arimoto & Tripp, 1977; Baldo et al., 1978). Lectins are heterogenous molecules, with some specificity for the chemical composition and spatial structure of the oligosaccharides belonging to the lectin receptor. The haemolymph of Mercenaria mercenaria was found to agglutinate only four of the 30 bacteria tested, and none after bacterial absorption (Arimoto & Tripp, 1977). Calcium and magnesium were required for the activity of the agglutinin and contributed to the heat stability of the molecule (Arimoto & Tripp, 1977; Renwrantz & Stahmer, 1983). Most microorganisms, and several subpopulations of haemocytes possess lectin surface receptors (Cheng et al., 1980; Vasta, Cheng & Marchalonis, 1984; Renwrantz, Daniels & Hansen, 1985). The lectins are probably involved in the elimination of bacteria, promoting their immobilisation, their binding, and their destruction by phagocytic cells. The agglutinins may function as opsonins (Leippe & Renwrantz, 1988) but apparently have no relationship to vertebrate immunoglobulins. Several enzymes are present in the haemocytes of molluscs (Cheng et al., 1975; Moore & Lowe, 1977). Some lysosomal hydrolases, such as acid phosphatase and lysozyme, could be released by degranulation from haemolymph cells into the serum, where they exert microbiocidal effects on bacterial membranes (Cheng et al., 1975; Cheng, 1976; Cooper-Willis, 1979; Mohandas & Cheng, 1985). Haemocytes are able to produce in vitro hydrogen peroxide; this capacity is stimulated by the presence of bacteria (Nakamura et al., 1985).
DEFENCE MECHANISM
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
325
In bivalve molluscs, immunity is a natural phagocytic immunity, involving all or part of the haermocytes (especially granulocytes). Phagocytosis can be divided into at least four distinct stages: attraction, adherence, endocytosis, and destruction.
Attraction By chemotaxis, the effector cell is attracted to the target through a rising gradient of concentration. Haemocytes of Crassostrea virginica are attracted to Gram positive or Gram negative live bacteria but not to heat-killed bacteria. Furthermore, Vibrio parahaemolyticus, live or heat-killed, is not attractive to oyster haemocytes. This would explain its pathogenicity (Cheng & Rowland, 1979). Rowland & Cheng (1982) isolated from the cytoplasm and the membrane of Escherichia coli and Bacillus megaterium, chemo-attractive glycoproteins and lipoproteins for the haemocytes of Crassostrea virginica. The spatial structure of the haemocyte wall plays an important role in the process of attraction. An intact cytoskeletal system, external microtubules, and microfilaments, are necessary for movements (Cheng & Rowland, 1982). An in vitro reduction in chemotaxis of haemocytes is observed 2 h after the first contact with Bacillus megaterium, and involves therefore a diminution of disease resistance in pre-exposed molluscs (Cheng et al., 1981).
Adhesion After non-self recognition, adhesion between haemocytes and foreign materials takes place, promoted by physical forces such as hydrophobicity and charge interaction, and especially by surface receptors. The lectin membrane of the Crassostrea virginica haemocyte is a surface receptor and allows the recognition of foreign material (Vasta, 1982). Lectin(s) from haemolymph are involved in the attachment of yeast cells to Mytilus edulis haemocytes by an opsonising activity (Renwrantz & Stahmer, 1983).
Endocytosis and destruction Haemocyte cell membrane invagination at the site of foreign particle adhesion results in the internalisation (or endocytosis) of the particle in a single membrane vesicle. This vesicle called a “primary phagosome”, in the cytoplasm, comes into contact and fuses with granules which have a complex wall in order to constitute a “secondary phagosome”. In the secondary phagosomes, various enzymes, according to species, break up foreign particles without rupture of the plasma membrane. This phenomenon occurring after contact with bacteria or inert materials (beads, carbon particles, erythrocytes), has been described in Mercenaria mercenaria (Foley & Cheng, 1977; Mohandas & Cheng, 1985), M. campechiensis (Rodrick & Ulrich, 1984; Alvarez & Friedl, 1988; Hinsch & Hunte, 1988), Mytilus edulis (Moore & Lowe, 1977), and M. californianus (Bayne et al, 1979).
326
D.PRIEUR ET AL.
In vitro phagocytosis increases with temperature (Rodrick & Ulrich, 1984). Inhibition occurs at low (0–5°C) and high (37–50°C) temperatures with a normal level of phagocytosis over a large range of temperature (10–37°C), even in anaerobiosis (Alvarez & Friedl, 1978). Bacteria and haemolymph enhance phagocytosis (Tripp, 1966; Cheng et al., 1975; Arimoto & Tripp, 1977; Renwrantz & Stahmer, 1983; Rodrick & Ulrich, 1984; Mohandas & Cheng, 1985; Mori, Nakamura & Nomura, 1988). After bacterial destruction, glycogen granules are made in the haemocytes and glycogen levels increase in the haemolymph. Haemocytes thus play a part, not only in defence, but also in the nutrition of bivalves (Rodrick & Ulrich, 1984). In the haemolymph, enzyme concentration increases. The enzymes released from lysozomes are able to kill microorganisms which have not yet been phagocytosed and to destroy bacterial membranes, thus stimulating and amplifying phagocytosis (Cheng et al., 1975; Rodrick & Ulrich, 1984). In bivalve molluscs, the defence mechanisms belong to natural immunity, and comprise primarily phagocytosis. Subtle interactions take place between phagocytes and humoral factors in the haemolymph. Most of these substances, lectins in particular, are not yet well known. Without lymphocytes and antibodies, the immune response after a contact with an antigen is non-specific and takes place without any immune memory sensu stricto. It appears that acquired immunity is absent in bivalve molluscs.
ENVIRONMENTAL INTERACTIONS PHYSICO-CHEMICAL CHARACTERISTICS OF A BIVALVE ECOSYSTEM
Water column It is widely assumed that bivalve molluscs modify the environment in which they live. Dense assemblages can greatly influence the overlying water masses (Galtsoff, 1964; Dame, Zingmark & Nelson, 1979). Filter-feeding can remove significant amounts of suspended particles (Verwey, 1954), often depleting phytoplankton in the overlying water (Wright et al., 1982; Carlson et al., 1984; Cohen et al., 1984; Nichols, 1985). Excretion products of bivalve molluscs, predominantly ammonia with relatively small quantities of amino acids (Srna & Baggaley, 1976; Bayne & Scullard, 1977) must also have an impact on the overlying water. Stevens (1983) observed an increase in ammonia concentration near oyster reefs, and Dame, Zingmark & Haskin (1984), the first to measure the fluxes in situ using a feasible method with a plastic tunnel, observed that oyster reefs released 1680–7250 µg at N-NH ·m -2·h -1. The release rate of ammonia from oyster 4 reefs is very similar to the rate reported by Nixon et al. (1976) on a mussel bed in Rhode Island but it is higher than estuarine and coastal rates reported in the literature. According to Nixon et al. (1976), Jordan & Valiela (1982), and Dame et al. (1984), however, the ammonia excreted by bivalve molluscs is an important source of nitrogen and is probably recycled by bacteria and phytoplankton within coastal ecosystems.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
327
Superficial sediment A large part of ingested participate material is voided as faeces and pseudofaeces. This production of faecal material by bivalves molluscs, has been widely studied and is remarkably high in some dense communities (Haven & Morales-Alamo, 1966; Tenore & Dunstan, 1973a, b; Bernard, 1974; Foster-Smith, 1975; Kraeuter, 1976; Kusuki, 1978; Tsuchiya, 1980, 1981). This biodeposit production increases the rates of sedimentation. Indeed, Dahlbäck & Gunnarsson (1981) reported that sedimentation is increased three-fold under mussel culture rafts compared with control sites in Sweden. The biodeposits reach the sediment as particulate organic matter and change the characteristics of the superficial sediment. Thus, the sediment under mussel cultures had a finer structure, lower bulk density, a higher water content and a lower pH (Dahlbäck & Gunnarsson, 1981; Kaspar et al., 1985).
IMPACT ON BENTHIC BACTERIA
Bacterial enrichment In a community of bivalves, the production of aggregated faecal material and the associated permeability changes in the surface layers of sediments, are likely to increase the available surface for bacterial colonisation (Rhoads, 1973, 1974; Johnson, 1974, 1977; Driscoll, 1975) while the faecal material is processed as a source of bacterial production. This is due to their large surface area compared with the fine particles composing the sediment and their high organic content which favours bacterial colonisation (Fenchel, 1970).
Rapidity of the colonisation According to laboratory experiments, bacterial colonisation of faecal material is very rapid (Newell, 1965; Newell, Field & Griffiths, 1982; Stuart et al., 1982). The dry biomass of initial bacterial colonisers on the faecal material reached a maximum value of 1.8 mg·l-1 as early as Day 2 (Stuart et al., 1982). The speed of this process may be because the sedimenting faeces are already enriched by bacteria (especially Vibrio) which survive and can multiply when passing through the digestive tract of the mussel (Prieur, 1981). Studies of C/N ratios also prove that the faecal material is exposed to a microbial colonisation during its sedimentation (Dahlbäck & Gunnarsson, 1981). The sedimenting faeces undergo very rapid microbial changes (Stuart et al., 1982). The faecal material is first colonised by bacteria, which are subsequently replaced by flagellates and ciliates; a relatively large part of the deposited material is, however, processed by bacteria. Thus, bacterial enrichment allows the mineralisation of the organic matter within the faeces and is a potential trophic resource for consumers.
BACTERIAL MINERALISATION OF BIODEPOSITS
328
D.PRIEUR ET AL.
Aerobic and anaerobic metabolism After colonisation, bacterial mineralisation is very rapid; the processed faecal material is mineralised within 33 days at 10°C (Stuart et al., 1982), allowing rapid cycling of carbon, nitrogen, phosphorus, and sulphur. The organic enrichment results, however, in an increase in the consumption of oxygen by heterotrophic bacteria within the sediments. Heterotrophic bacteria use oxygen for oxidising carbohydrates. Bacterial mineralisation of proteins (ammonification and nitrification) to produce nitrate, also uses dissolved oxygen. Organic sulphur compounds are oxidised into sulphate and this oxidation, with or without bacteria, is a major sink for oxygen (Berner, 1971). This increase in the oxygen consumption is followed by anoxia of the sediment which favours the denitrification process (Kaspar et al., 1985) and a speeded sulphate reduction. Probably, this does not occur, either in most natural bivalve communities or in the culture ropes where mussels are suspended in a minimum of 15 m of water. A high depth of water (culture ropes) and a rapid tidal current flow favour the dispersal of biodeposits (Rodhouse et al., 1985) and allow enough water exchange to prevent the sediments from being deprived of oxygen. Impact on nitrogen, carbon and phosphorus percentages Despite higher rates of denitrification and nitrogen mineralisation in mussel farm sediments (Kaspar et al., 1985), the percentage of nitrogen mainly increases because the percentage of carbon in faecal material generally decreases with age during decay as a result of respiratory losses of CO , (review 2 in Valiela, 1984). This is shown by lower C/N ratios in the sediment under mussels and oysters. The lower organic phosphorus in faecal material compared with natural sedimentation may be due to a leaching from cells that are ruptured and fragmented during their passage through the gut (Kautsky & Evans, 1987) and much of the phosphorus excreted by bivalve molluscs is used by bacteria or absorbed to sediment particles (Doering et al., 1987). Higher organic N/P ratios observed by Kautsky & Evans (1987) in the ecosystem of mussels indicate, despite nitrogen losses through denitrification and nitrogen mineralisation (Kaspar et al., 1985), an accumulation of organic nitrogen relative to organic phosphorus (Kautsky & Evans, 1987). Rapidity of mineralisation Laboratory experiments (Newell, 1965; Newell et al., 1982; Stuart et al., 1982) and studies of C/N ratios (Dahlbäck & Gunnarsson, 1981) showed that the bacterial mineralisation of the faecal material is very rapid. Dahlbäck & Gunnarsson (1981) found that the C/N ratios of the sedimenting particles under bivalve cultures (fresh faecal material) were always higher (12 to 14) than those in the top layer of the deposited sediment under the cultures (6 to 9). They interpreted the higher C/N values for sedimenting particles as a result of a faster degradation and recycling of nitrogen compared with carbon.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
329
This high nitrogen mineralisation was also shown by Henriksen, Rasmussen & Jensen (1982) who measured high potential nitrification rates in faeces of Macoma balthica. Thus, these authors proved that the faecal material was exposed to microbial degradation during its sedimentation and that the nitrogen was mineralised first.
FAECAL BACTERIA: A POTENTIAL TROPHIC RESOURCE
Nutritional value The faecal material delivered by bivalves may be a source of food for depositfeeders (Kuenzler, 1961; Haven & Morales-Alamo, 1966; Kraeuter, 1976). Faeces and pseudofaeces are, however, initially low in nitrogen (C/N ratios 12 to 14) and the nitrogen content is regarded as an important factor of nutritional value (RussellHunter, 1970; Boyd & Goodyear, 1971). Bacteria have a C/N ratio of approximately 5.5 (Fenchel & Blackburn, 1979). The biodeposits are colonised by bacteria which use the faeces as a surface and a carbon substrate and fix inorganic nitrogen from the environment. This results in organic nitrogen enrichment indicated by lower C/N ratios (e.g., Newell, 1965; Frankenberg & Smith, 1967; Fenchel, 1972; Mann, 1972; Hargrave, 1976; Levinton & Lopez, 1977). Thus, it is widely assumed that the colonisation by benthic bacteria and fungi increases the nutritional value within a few days due to a “protein enrichment” of faecal material. After ingestion by deposit-feeders, the bacteria are stripped from the inert detrital particles which, subsequently, shift back to the environment for further microbial recolonisation and possible re-ingestion. Bacterial colonisation leads to an increase of organic nitrogen content in biodeposits. Microbial nitrogen is not, however, the only item accounting for all of the nitrogen recovered in aged faecal material (Odum, Kirk & Zieman, 1979; Cammen, 1980a,b). Significant amounts result from probably microbial accumulation of the extracellular protein and the nitrogen containing exudates (Glenn, 1976; Hobbie & Lee, 1980). Moreover, microbial activity is required not only to increase organic nitrogen levels (the intra- and extra-cellular protein enrichment concept) but also, perhaps more important initially, to degrade the decay-resistant faecal material (mineralisation: see above). Indeed, much faecal material is composed of highly complex structural materials which most macrobenthic deposit-feeders cannot assimilate. Energetic value In degrading biodeposits, bacteria convert the faecal material into suitable food for the macrofauna. The efficiency of faecal carbon conversion by bacteria is very low (6 to 14%) and the carbon losses incurred imply a small energetic value even although their protein, and consequently their nutritional value is high. In conclusion, this review shows that bivalves, with their high faecal production, sustain the development of benthic bacteria. After its settlement, the faecal material is rapidly colonised by bacteria which increase its nutritional value. Thus, it may be a potential food resource for deposit-feeders. Moreover, since they
330
D.PRIEUR ET AL.
have low density and a high water content, biodeposits are easily resuspended by even low turbulence (Rhoads & Young, 1970; Stuart et al., 1982). This faecal resuspension leads to a high bioseston production (Theede, 1981) and it is obvious that such a processed material is potentially available as a food resource for suspension-feeding bivalves. The dissolved nutrients stemming from bacterial mineralisation of biodeposits, and from bivalve excretion, are partly consumed by microbenthic algae living on mussel beds (Dame & Dankers, 1988) but are of most potential importance to phytoplankton in the water column. Thus, benthic filter-feeders may affect populations living in the water column (bacteria and phyto-plankton), not only through the removal of suspended particles, but also through an enhanced return of nutrients. This feedback is ultimately controlled by the supply of an organic matter to the benthos (Kemp & Boynton, 1981; Kelly & Nixon, 1984) and by bacterial activity. Thus, the bivalvebacteria association allows a reciprocal coupling of benthic and pelagic biogeochemical cycles; in addition, the ecosystem is in steady state. In an intense bivalve culturing area, however, where the water exchange is limited, the case may be quite different. Increased benthic microbial activity will often result in oxygen depletion and a low macrofauna diversity as shown by Tenore et al. (1982), Mattsson & Lindén (1983), and Kaspar et al. (1985). There is a general trend towards eutrophication with anaerobic decomposition taking over with H S and CH as end-products. The hydrogen sulphide is toxic and 2 4 consequently, there is a risk of a harmful feedback affecting bivalve communities.
CONCLUSIONS Because of their economic importance in many countries, marine bivalves have probably been studied more than other invertebrates. Among those studies, bacteriological surveys have been carried out to explain the accumulation of pathogenic bacteria and to understand bivalve bacterial diseases. Non-edible or non-commercially important bivalves have revealed, in addition to the above topics, interesting and sometimes unusual interactions with marine bacteria. For all the topics reviewed in this paper, several questions remain that need further investigation but, considering the data already available, marine bivalves could be considered as a fascinating model of interactions between bacteria and aquatic invertebrates. Bacteriological investigations in the marine environment have dealt mainly with microorganisms living in the water column or in the sediments. Taking into account the example of bivalves, it is clear that the interaction of the bacterial flora with marine animals and plants, should be more considered in future work, as it represents an important component of the microbial ecosystem and will probably lead to the discovery of new types of interactions.
ACKNOWLEDGEMENTS
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
331
The authors thank Drs J.Chaperon, J.-C.Martinez, J.Moullec, M.Pinot, F.Riou, and J.-F. Samain who provided useful information, Mr R.Conq for his help with English translation, and Mrs N.Thepaut for typing the manuscript.
REFERENCES Acton, R.T., Bennett, C, Evans, E.E. & Schrohenloher, R.A., 1969. Physical and chemical characterization of an oyster hemagglutinin. J. Biol. Chem., 244, 4128– 4145. Al Jebouri, M.M. & Trollope, D.R., 1981. The Escherichia coli content of Mytilus edulis from analysis of whole tissue and digestive tract. J. Appl. Bateriol., 51, 135–142. Al Jebouri, M.M. & Trollope, D.R., 1984. Indicator bacteria in freshwater and marine molluscs. Hydrobiologia, 11, 93–102. Alvarez, M.R. & Friedl, F.E., 1988. Factors affecting in vitro phagocytosis in hemocytes of the American oyster. 3rd Int. Colloq. Pathol. Mar. Aquacult., p. 109 only. Amouroux, J.M., 1984. Preliminary study on the consumption of dissolved organic matter (exudates) of bacteria and phytoplankton by the marine bivalve Venus verrucosa. Mar. Biol., 82, 109–112. Amouroux, J.M., 1986a. Comparative study of the carbon cycle in Venus verrucosa fed on bacteria and phytoplankton. I Consumption of bacteria (Lactobacillus sp.). Mar. Biol., 90, 237–241. Amouroux, J.M., 1986b. Comparative study of the carbon cycle on Venus verrucosa fed on bacteria and phytoplankton. II Consumption of phytoplankton (Pavlova lutheri) Mar. Biol., 92, 349–354. Anderson, J.M. & Baird-Parker, A.C., 1975. A rapid and direct plate method for enumerating E. coli bioti in food. J. Appl. Bacteriol., 39, 111–117. Anderson, R.S., 1981. Inducible hemolytic activity in Mercenaria mercenaria hemolymph. Dev. Comp. Immunol., 5, 575–585. Andrews, W.H., Diggs, C.D., Miescier, J.J., Wilson, C.R., Adams, W.N., Furfari, S.A. & Musselman, J.F., 1976. Validity of members of the total coliform and fecal coliform groups for indicating the presence of Salmonella in the quahaug Mercenaria mercenaria. J. Milk Food Technol., 39, 5, 322–324. Andrews, W.H., Diggs, C.D., Presnell, M.W., Miescier, J.J., Wilson, C.R., Goodwin, C.P., Adams, W.N., Furfari, S.A. & Musselman, J.F., 1975. Comparative validity of the total coliform and fecal coliform groups for indicating the presence of Salmonella in the eastern oyster Crassostrea virginica. J. Milk Food Technol., 38, 453–56. Andrews, W.H. & Presnell, M.W., 1972. Rapid recovery of E. coli from estuarine water. Appl. Microbiol., 23, 521–523. Anonymous, 1970. (Apha., American Public Health Association), Recommended procedures for the examination of sea water and shellfish 4th Ed. APHA, New York. Anonymous, 1981. (AFNOR, Association française de normalisation): Norme NF V 45110. Coliformes fécaux dans les eaux conchylicoles et les coquillages marins. Anonymous, 1982. (CETE, Centre des études techniques de l’équipement), Suivi de la salubrité des eaux de baignade a l’aide de coquillages. Ministère de l’environnement (DPP). Arimoto, R. & Tripp, M.R., 1977. Characterization of a bacterial agglutinin in the hemolymph of the hard clam, Mercenaria mercenaria. J. Invertebr. Pathol., 30, 406–413.
332
D.PRIEUR ET AL.
Arp, A.J., Childress, J.J. & Fisher, C.R., 1984. Metabolic and blood gas transport characteristics of the hydrothermal vent bivalve Calyptogena magnifica. Physiol. Zool., 57, 648–662. Auffret, M., 1986. Internal defence in bivalve molluscs: ultrastructural observations on the fate of experimentally injected bacteria in Ostrea edulis granular hemocytes. In, Pathology in Marine Aquaculture, edited by C.P. Vivarès et al., European Aquaculture Society, Spec. Publ. No. 9, 351–356. Ayres, P.A., 1975. Recovery of E. coli and coliform from macerated shellfish. J. Appl. Bacteriol., 39, 353–356. Ayres, P.A. & Barrow, G.C., 1978. The distribution of V. parahaemolyticus in British coastal waters. J. Hyg., 80, 281–294. Ayres, P.A., Burton, H.W. & Cullum, M.L., 1978. Sewage pollution and shellfish. In, “Techniques for the Study of Mixed Populations,” edited by L. Davies, Academic Press, New York, pp. 51–62. Bachère, E., Chagot, D. & Grizel, H., 1988. Separation of Crassostrea gigas hemocytes by density gradient centrifugation and counterflow centrifugal elutriation. Dev. Comp. Immunol, 12, 549–559. Baldo, B.A., Sawyer, W.H., Stick, R.V. & Uhlenbruck, G., 1978. Purification and characterization of a galactose-reactive agglutinine from the Tridacna maxima (Roding) and a study of its combining site. Biochem. J., 175, 467–477. Barbosa, T. C, 1987. Le processus d’accumulation des bactéries chez les mollusques bivalves. Etude expérimental chez Mytilus edulis. Thèse Doct. Océanogr. Biol. Brest, 134pp. Baron, D., 1985. Recherche de virus hydriques humains dans 1’environnement marin (eau-sédiments, mollusques) et épidémologie des viroses transmises par les coquillages. These Doctorat d’Etat en Pharmacie, Université de Paris V. Baross, J. & Liston, J., 1970. Occurrence of V. parahaemolyticus and related hemolytic vibrios in marine environments of Washington state. Appl. Microbiol., 20, 179–186. Bayne, B.L., 1983. Physiological ecology of marine mulluscan larvae. In, Wilbur, K. M. (ed), The Mollusca, Vol. 3. Development, edited by K.M. Wilbur, Academic Press, New York, pp. 299–343. Bayne, B.L. & Scullard, C., 1977. Rates of nitrogen excretion by species of Mytilus (Bivalvia: Mollusca). J. Mar. Biol. Assoc. U.K., 57, 355–369. Bayne, C.J., Moore, M.N., Carefoot, T.H. & Thompson, R.J., 1979. Hemolymph functions in Mytilus californianus: the cytochemistry of hemocytes and their responses to foreign implants and hemolymph factors in phagocytosis. J. Invertebr. Pathol., 34, 1–20. Belkin, S., Nelson, D.C. & Jannasch, H.W., 1986. Symbiotic assimilation of CO2 in two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tube worm Riftia pachyptila. Biol. Bull. (Woods Hole, Mass.), 170, 110–121. Berland, B.R., Bonin, D.J., Fiala, M. & Maestrini, S.Y., 1976. Importance des vitamines en eau de mer. Consommation et production par les algues et les bactéries. In, Actualité de Biochim. Mar., pp. 121–146. Bernard, F.R., 1970. Occurrence of the spirochaete genus Cristispira in western Canadian marine bivalves. Veliger, 13, 33–36. Bernard, F.R., 1973. Crystalline style formation and function in the oyster Crassostrea gigas (Thunberg 1975). Ophelia, 12, 159–170. Bernard, F.R., 1974. Annual biodeposition and gross energy budget of mature Pacific oysters, Crassostrea gigas. J. Fish. Res. Board Can., 31, 185–190. Berner, R., 1971. Principles of chemical sedimentology. McGraw-Hill, New York, 240 pp. Berry, F., 1916. The bacterial content of market oysters. J. Bacteriol., 1, 107–108. Bianchi, A.J., Bianchi, M., Scoditti, P.M. & Bensoussan, M.G., 1979. Distribution des populations bactériennes hétérotrophes dans les sédiments et les tractus digestifs d’animaux benthiques recueillis dans la faille Vema et les plaines abyssales du Demerara et de Gambie. Vie Marine, 1, 7–12.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
333
Biddanda, B.A. & Pomeroy, L.R., 1988. Microbial aggregation and degradation of phytoplankton-derived detritus in sea water. I. Microbial succession. Mar. Ecol. Prog. Ser., 42, 79–88. Birkbeck, T.H. & McHenery, J.G., 1982. Degradation of bacteria by Mytilus edulis. Mar. Biol., 72, 7–15. Birkbeck, T.H., McHenery, J.G. & Nottage, A.S., 1987. Inhibition of filtration in bivalves by marine vibrios. Aquaculture, 67, 247–248. Blackburn, T.H., 1988. Benthic mineralization and bacterial production. In, Nitrogen Cycling in Coastal Marine Environments, edited by T.H.Blackburn & J. Sorensen, John Wiley & Sons, Chichester, pp. 175–190. Blake, P., Rosenberg, M.L., Bandeira Costa, J., Soares Ferreira, P., Levy Guimaraes, C. & Gangarosa, E.J., 1977. Cholera in Portugal, 1974. Am. J. Epidemiol, 105, 337–343. Blaschko, H. & Hope, D.B., 1956. The oxidation of L. amino acids by Mytilus edulis. Biochem. J., 62, 335–339. Bolinches, J., Toranzo, A.E., Silva, A. & Barja, J.L., 1986. Vibrosis as the main causative factor of heavy mortalities in the oyster culture industry in Northwestern Spain. Bull. Eur. Assoc. Fish. Pathol., 6, 1–4. Booth, B.C., 1988. Size classes and major and major taxonomic groups of phytoplankton at two locations in the subarctic Pacific Ocean in May and August, 1984. Mar. Biol, 97, 275–286. Boss, K.J. & Turner, R.D., 1980. The giant white clam from the Galapagos rift, Calyptogena magnified, sp. nov. Malacologia, 20, 161–194. Bostock, A.D., 1979. Hepatitis A infection associated with the consumption of mussel. J. Infect. Dis., 1, 171–177. Boulègue, J., Benedetti, E.L., Dron, D., Mariotti, A. & Letolle, R., 1987. Geochemical and biogeochemical observations on the biological communities with fluid venting in Nankai Trough and Japon Trench subduction zones. Earth Planet. Sci. Lett., 83, 343–355. Boury, M. & Borde, J., 1964a. La contamination bactérienne des coquillages. In, Pollut. Mar. Micro. Prod. Petrol. Symp. Monaco, CIESM, pp. 277–284. Boury, M. & Borde, J., 1964b. L’évolution de la flore bactérienne dans les coquillages conservés hors de l’cau. In, Pollut. Mar. Micro. Prod. Petrol. Symp. Monaco, CIESM, pp. 285–292. Bouvy, M., Cahet, G., De Billy, F., Soyer, L., Soyer-Gobillard, M.O. & ThiriotQuiévreux, C., 1986. Sur la présence de bactéries dans la branchie d’un mollusque bivalve littoral Spisula subtruncata (Da Costa) (Mactridae). C.R. Acad. Sci. Paris Ser. III, 303, 257–262. Boyd, C.E. & Goodyear, C.P., 1971. Nutritive quality of food in ecological systems. Arch. Hydrobiol., 69, 256–270. Bradford, H.B., 1984. An epidemiological study of V. Cholera in Louisiana. In, Vibrios in the Environment, edited by R.R. Colwell, Wiley Interscience Publ., New York, 59–72. Brancato, M.S. & Woollacott, R.M., 1982. Effect of microbial films on settlement of Bryozoan larvae (Bugula simplex, Bugula stolonifera and Bugula turrita). Mar. Biol, 71, 51–56. Brisou, J., 1968. La pollution microbienne virale et parasitaire des eaux littorales et ses consequences pour la santé publique. Bull. W.H. O., 38, 79–118. Brisou, J., Tysset, C., Mailloux, M. & Espinasse, S., 1962. Recherches sur les vibrios marins. A propos de 44 souches isolees de Moules (Mytilus galloprovincialis) du littoral algerois. Bull. Soc. Pathol. Exot., 55, 260–275. Brooks, J.M., Kennicutt II, M.C., Fisher, C.R., Macko, S.A., Cole, K., Childress, J.J., Bidigare, R.R. & Vetter, R.D., 1987. Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources. Science, 238, 1138– 1142.
334
D.PRIEUR ET AL.
Brown, C., 1973. The effects of some selected bacteria on embryos and larvae of the American oyster, Crassostrea virginica. J. Invertebr. Pathol., 21, 215–223. Brown, C., 1974. A pigment-producing pseudomonad which discolors culture containers of embryos of a bivalve mollusk. Chesapeake Sci., 15, 17–21. Brown, C., 198la. A prodiginine pigment toxic to embryos and larvae of Crassostrea virginica. J. Invertebr. Pathol., 38, 281–293. Brown, C., 1981b. A study of two shellfish-pathogenic Vibrio strains isolated from a long island hatchery during a recent outbreak of disease. J. Shellfish Res., 1, 83–87. Brown, C. & Losee, E., 1978. Observations on natural and induced epizootics of vibriosis in Crassostrea virginica larvae. J. Invertebr. Pathol., 31, 41–47. Brown, C. & Roland, G., 1984. Characterization of exotoxin produced by a shellfish-pathogenic Vibrio sp. J. Fish. Dis., 7, 117–126. Brown, C. & Russo, D.J., 1979. Ultraviolet light disinfection of shellfish hatchery sea water. I. Elimination of five pathogenic bacteria. Aquaculture, 17, 17–23. Brown, C. & Tettelbach, L.P., 1988. Characterization of a nonmotile Vibrio sp. pathogenic to larvae of Mercenaria mercenaria and Crassostrea virginica. Aquaculture, 74, 195–204. Brown, L.D. & Dorn, C.R., 1977. Fish shellfish and human health. J. Food Prot., 40, 712–717. Bryan, F.L., 1973. Foodborne diseases from fish and shellfish. In, Microbial Safety of Fishery Products, edited by C.O. Chichester & H.D. Graham, Academic Press, New York, pp. 273–302. Bryan, F.L., 1980. Epidemiology of food borne diseases transmitted by fish, shellfish and marine crustaceans in the USA 1970–1978. J. Food Prot., 43, 859– 876. Buck, J.D., Bubucis, P.M. & Combs, T.J., 1977. Occurrence of human associated yeasts in bivalve shellfish from Long Island Sound. Appl. Environ. MicrobioL, 33, 370–378. Buestel, D., Cochard, J.C., Dao, J.C. & Gérard, A., 1982. Production artificielle de naissain de coquilles Saint Jacques Pecten maximus; premiers résultats en rade de Brest. Vie Marine, 4, 24–28. Buttiaux, R., 1961. Salmonella problems In, Fish as Food, Vol. 2, edited by G. Borgstrom, Academic Press, New York, pp. 503–519. Cabelli, V.J. & Heffernan, W.P., 1970a. Accumulation of Escherichia coli by the Northern Quahaug. Appl. Microbiol, 19, 239–244. Cabelli, V.J. & Heffernan, W.P., 1970b. Elimination of bacteria by the soft shell clam, Mya arenaria. J. Fish. Res. Board Can., 27, 1579–1587. Cabelli, V.J. & Heffernan, W.P., 1971. The elimination of bacteria by the northern quahaug; variability of the response of individual animals and development of criteria. Proc. Natl Shellfish Assoc., 61, 102–108. Cammen, L.M., 1980a. Ingestion rate: an empirical model for aquatic deposit feeders and detritivores. Oecologia (Berlin), 44, 303–310. Cammen, L.M., 1980b. The significance of microbial carbon in the nutrition of the deposit feeding polychaete Nereis succinea. Mar. Biol., 61, 9–20. Cammen, L.M. & Walker, S.A., 1982. Distribution and activity of attached and freeliving suspended bacteria in the bay of Fundy. Can J. Fish. Aquat. Sci., 39, 1655–1663. Carlson, D.J., Townsend, D.W., Hilyard, A.L. & Eaton, J.F., 1984. Effect of on intertidal mudflat on plankton of overlying water column. Can. J. Fish. Aquat. Sci., 41, 1523–1528. Carpenter, E.J. & Culliney, J.L., 1975. Nitrogen fixation in marine shipworms. Science, 187, 551–552. Cavanaugh, C.M., 1983. Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature (London), 302, 58–61.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
335
Cavanaugh, C.M., Levering, P.R., Maki, S.S., Mitchell, R. & Lidstrom, M. E., 1987. Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature (London), 325, 346–348. Certes, A., 1882. Note sur les parasites et les commensaux de l’huître. Bull. Soc. Zool. Fr., 7, 347–353. Chakroun, F., 1964. Contribution a l’étude des microflores bactériennes de la moule Mytilus galloprovincialis Lamarck. These 3ème cycle Océanogr. Biol., Paris, 110 pp. Cheng, T.C., 1976. Beta-glucuronidase in the serum and hemolymph cells of Mercenaria mercenaria and Crassostrea virginica (Mollusca: Pelecypoda). J. Invertbr. Pathol, 27, 125–128. Cheng, T.C., Bui, M.N., Howland, K.H., Schoenberg, D.A. & Sullivan, J.T., 1981. Effect of preinjection of Crassostrea virginica with bacteria on subsequent chemotactic responses by its hemocytes. J. Invertebr. Pathol., 38, 122–126. Cheng, T.C. & Downs, J.C.U., 1988. Intracellular acid phosphatase and lysozyme levels in subpopulations of oyster, Crassostrea virginica, hemocytes. J. Invertebr. Pathol., 52, 163–167. Cheng, T.C. & Howland, K.H., 1979. Chemotactic attraction between hemocytes of the oyster, Crassostrea virginica and bacteria. J. Invertebr. Pathol., 33, 204–210. Cheng, T.C. & Howland, K.H., 1982. Effects of colchicine and cytochalasin B on chemotaxis of oyster (Crassostrea virginica) hemocytes. J. Invertebr. Pathol., 40, 150–152. Cheng, T.C., Huang, J.W., Karadogan, H., Renwrantz, L.R. & Yoshino, T.P., 1980. Separation of oyster hemocytes by density gradient centrifugation and identification of their surfaces receptors. J. Invertebr. Pathol., 36, 35–40. Cheng, T.C., Rodrick, G.E., Foley, D.A. & Koehler, S.A., 1975. Release of lysozyme from hemolymph cells of Mercenaria mercenaria during phagocytosis. J. Invertebr. Pathol., 25, 261–265. Chia, F. S & Rice, M.E., 1978. Settlement and Metamorphosis of Marine Invertebrate Larvae. Elsevier, North-Holland, New York, 290 pp. Childress, J.J., Fisher, C.R., Brooks, J.M., Kennicut II, M.C., Bidigare, R. & Anderson, A.E., 1986. A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science, 233, 1306–1308. Chugh, T.D., 1985. Detection of R Plasmids in Salmonella isolated from clams and marine waters of Kuwait. Water, Air Soil Pollut., 26, 59–63. Clegg, F.L. & Sherwood, H.P., 1947. The bacteriological examination of Molluscan shellfish. J. Hyg., 45, 504–521. Cohen, R.D. H., Dresler, P.V., Phillips, E.J. P. & Cory, R.L., 1984. The effect of the Asiatic clam, Corbicula fluminea, on phytoplankton of the Potomax River, Maryland. Limnol. Oceanogr., 29, 170–180. Cole, J.J., Stuart, F. & Michael, L.P., 1988. Bacteria production in fresh and sea water ecosystems, a cross-system overview. Mar. Ecol. Prog. Ser., 43, 1–10. Cole, M.T., Kilgen, M.G., Reily, L.A. & Hackney, C.R., 1986. Detection of enteroviruses and bacterial indicators and pathogens in Louisiana oysters and their overlying waters. J. Food Prot., 49, 596–601. Colwell, R.R. & Liston, J., 1959. A bacteriological study of the natural flora of Pacific oysters (Crassostrea gig as) when transplanted to various areas in Washington. Proc. Natl Shellfish Assoc., 50, 181–188. Colwell, R.R. & Liston, J., 1960. Microbiology of Shellfish. Bacteriological study of the natural flora of Pacific oysters (Crassostrea gigas). Appl. Microbiol., 8, 104–109. Colwell, R.R. & Liston, J., 1962. The natural bacterial flora of certain marine invertebrates. J. Insect. Pathol., 4, 1, 23–33.
336
D.PRIEUR ET AL.
Colwell, R.R. & Sparks, A.K., 1967. Properties of Pseudomonas enalia, a marine bacterium pathogenic for the invertebrate Crassostrea gigas (Thunberg). Appl. Microbiol., 15, 980–986. Comar, P.G., Kane, B.E. & Jeffreys, D.B., 1979. Sanitary significance of the bacterial flora of the brackish water clam Rangia cuneata. Proc. Natl Shellfish Assoc., 69, 92–100. Comps, M., 1983. Infections rickettsiennes chez les mollusques bivalves des côtes françaises. Rapp. P.-V. Réun. Cons. Int. Explor. Mer., 182, 134–136. Cooke, M.D., 1976. Antibiotic resistance among coliform and fecal coliform bacteria isolated from sewage, seawater and marine shellfish. Antimicrob. Agents. Chemother., 9, 879–884. Coon, S.L., Bonar, D.B. & Weiner, R.M., 1985. Induction of settlement and metamorphosis of the Pacific oyster, Crassostrea gigas (Thunberg), by L. Dopa and cathecolamines. J. Exp. Mar. Biol. Ecol., 94, 211–221. Cooper-Willis, C.A., 1979. Changes in the acid phosphatase levels in the haemocytes and haemolymph of Patella vulgata after challenge with bacteria. Comp. Biochem. Physiol., 63A, 627–631. Corpe, W.A., 1970. Attachment of marine bacteria to solid surfaces. In, Adhesion in Biological systems, edited by R.S. Manley, Academic Press, New York, pp. 72– 87. Crisp, D.J. & Ryland, J.S., 1960. Influence of filming and of surface texture on the settlement of marine organisms. Nature (London), 185, 119. Cross, G., Forsyth, J., Greenberg, H., Harrison, J., Irving, L., Luke, R., Moore, B. & Schnal, R., 1979. Oyster associated gastroenteritis. Med. J. Aust., 1, 56–57. Cundell, A.M. & Young, R.R., 1975. Hind gut microflora from oil-polluted soft-shell clams. Mar. Pollut. Bull, 6, 134–136. Cutter, J.M. & Rosenberg, F.A., 1971. The role of cellulolytic bacteria in the digestive processes of the shipworm. 2-Requirement for bacterial cellulase in the digestive system of teredine borers. Proc. 2nd Intern. Biodeterioration Symp., 1–31. Dahlbäck, B. & Gunnarsson, L.A. H., 1981. Sedimentation and sulfate reduction under a mussel culture. Mar. Biol., 63, 269–275. Dame, R.F. & Dankers, N., 1988. Uptake and release of materials by a Wadden Sea mussel bed. J. Exp. Mar. Biol. Ecol., 118, 207–216. Dame, R.F., Zingmark, R.G. & Haskin, E., 1984. Oyster reefs as processors of estuarine materials. J. Exp. Mar. Biol. Ecol., 83, 239–247. Dame, R.F., Zingmark, R.G. & Nelson, D., 1979. Filter feeder coupling between the estuarine water column and benthic subsystems. In, Estuarine Perspectives, edited by V.S.Kennedy, Academic Press, New York, pp. 521–526. Dando, P.R. & Southward, A.J., 1986. Chemoautotrophy in bivalve molluscs of the genus Thyasira. J. Mar. Biol. Assoc. U.K., 66, 915–929. Dando, P.R., Southward, A.J. & Southward, E.C., 1986. Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proc. R. Soc. Lond. Ser. B, 227, 227–247. Dando, P.R., Southward, A.J., Southward, E.C., Terwilliger, N.B. & Terwilliger, R.C., 1985. Sulphur oxidizing bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar. Ecol. Prog. Ser., 23, 85–98. Dean, R.C., 1978. Mechanisms of wood digestion in the shipworm Bankia gouldi Bartsh: enzyme degradation of cellulose, hemicelluloses and wood cell walls. Biol. Bull. (Woods Hole, Mass.), 155, 297–316. De Burgh, M.E. & Singla, C.L., 1984. Bacterial colonization and endocytosis on the gill of a new limpet species from a hydrothermal vent. Mar. Biol., 84, 1–6. Delattre, J.M. & Delesmont, R., 1981. L’analyse des coquillages peut-elle servir au contrôle microbiologique du littoral. Rev. Int. Océanog. Méd., 43–44, 11–16. Denis, F.A., 1975. Contamination of shellfish with strains of Pseudomonas aeruginosa and specific bacteriophages. Can. J. Microbiol., 21, 1055–1057.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
337
DiSalvo, L.H., Blecka, J. & Zebal, R., 1978. Vibrio anguillarum and larval mortality in California coastal shellfish hatchery. Appl. Environ, Microbiol., 35, 219–221. Doering, P.H., Kelly, J.R., Oviatt, C.A. & Sowers, T., 1987. Effect of the hard clam Mercenaria mercenaria on benthic fluxes of inorganic nutrients and gases. Mar. Biol., 94, 377–383. Driscoll, E.G., 1975. Sediment-animal-water interaction, Buzzards Bay, Massachusetts. J. Mar. Res., 33, 275–302. Earampamoorthy, S. & Koff, R.S., 1975. Health hazards of bivalve mollusk ingestion. Ann. Intern. Med., 83, 107–110. Eliot, C., 1926. Observations on the colon-aerogenes group from the oyster. Am. J. Hyg., 6, 777. Elston, R., 1979. Economically important larvae diseases and their control. Riv. Ital. Piscic. Ittiop., 14, 47–54. Elston, R. & Leibovitz, L., 1980a. Detection of vibriosis in hatchery reared larval oysters: correlation between clinical, histological and ultrastructural observations in experimentally induced disease. Abstract, Proc. of the Nat. Shellfish Ass., 70, 122–123. Elston, R. & Leibovitz, L., 1980b. Pathogenesis of experimental vibriosis in larval American oysters, Crassostrea virginica. Can. J. Fish. Aquat. Sci., 37, 964– 978. Elston, R., Leibovitz, L., Relyea, D. & Zatila, J., 1981. Diagnosis of vibriosis in a commercial oyster hatchery epizootic: diagnostic tools and management features. Aquaculture, 24, 53–62. Elston, R.A., 1984. Prevention and management of infectious diseases in intensive mollusc husbandry. J. Wld. Maricult. Soc., 15, 284–300. Elston, R.A., Elliot, E.L. & Colwell, R.R., 1982. Conchiolin infection and surface coating Vibrio: shell fragility, growth depression and mortalities in cultured oysters and clams (Crassostrea virginica, Ostrea edulis and Mercenaria mercenarid). J. Fish. Dis., 5, 265–284. Elston, R.A. & Peacock, M.G., 1984. A rickettsiales-like infection in the Pacific razor clam, Siliqua patula. J. Invertebr. Pathol., 44, 84–96. Felbeck, H., 1983. Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacteria symbiosis. J. Comp. Physiol., 152, 3–11. Felbeck, H., Childress, J.J. & Somero, G.N., 1981. Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature (London), 293, 291–293. Fenchel, T., 1970. Studies on the decomposition of organic detritus derived from the turtle grass Thalassia testidinum. Limnol. Oceanogr., 15, 14–20. Fenchel, T., 1972. Aspects of decomposer food chains in marine benthos. Verh. Dtsch. Zool. Ges., 65, 14–22. Fenchel, T., 1988. Microfauna in pelagic food chains. In, Nitrogen Cycling in Coastal Marine Environments, edited by T.H. Blackburn & J. Sorensen, John Wiley & Sons, Chichester, pp. 59–65. Fenchel, T. & Blackburn, T.H., 1979. Bacteria and Mineral Cycling. Academic Press, London, 250 pp. Ferguson, R.L. & Rublee, P., 1976. Contribution of bacteria to standing crop of coastal plankton. Limnol. Oceanogr., 21, 19–27. Fergusson, J. C, 1982. A comparative study of the net metabolic benefits derived from the uptake and release of free amino acids by marine invertebrates. Biol. Bull. (Woods Hole, Mass.), 162, 1–7. Fiala-Médioni, A., 1984. Mise en évidence par microscopie électronique à transmission de l’abondance de bactéries symbiotiques dans la branchie de Mollusques bivalves de sources hydrothermales profondes. C.R. Acad. Sci. Paris, Ser. III, 17, 487–492.
338
D.PRIEUR ET AL.
Fiala-Médioni, A., Alayse, A.M. & Cahet, G., 1986. Evidence of in situ uptake and incorporation of bicarbonate and amino acids by hydrothermal vent mussel. J. Exp. Mar. Biol. Ecol, 96, 191–198. Fiala-Médioni, A. & Le Pennec, M., 1988. Structural adaptations in the gill of the Japanese subduction zone bivalves (Vesicomyidae) Calyptogena phaseoliformis and Calyptogena laubieri. Oceanologica Acta, 11, 185–192. Fiala-Médioni, A. & Métivier, C., 1986. Ultrastructure of the gill of the hydrothermal vent bivalve Calyptogena magnifica, with a discussion of its nutrition. Mar. Biol., 90, 215–222. Fisher, C.R. & Childress, J.J., 1986. Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi. Mar. Biol., 93, 59– 68. Fisher, C.R., Childress, J.J., Oremland, R.S. & Bidigare. R.R., 1987. The importance of methane and thiosulfate in the metabolism of the bacterial symbionts of two deep-sea mussels. Mar. Biol., 96, 59–71. Fisher, M.R. & Hand, S.C., 1984. Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol. Bull. (Woods Hole, Mass.), 167, 445–459. Fleet, G.H., 1978. Oyster depuration. A review. Food Technol Aust., 30, 444–454. Foley, D.A. & Cheng, T.C., 1977. Degranulation and other changes of molluscan granulocytes associated with phagocytosis. J. Invertebr. Pathol., 29, 321–325. Foote, C.J., 1895. A bacteriological study of oysters with special reference to them as a source of typhoid infection. Med. News, 66, 320. Foster-Smith, R.L., 1975. The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edule (L.) and Venerupis pullastra. J. Exp. Mar. Biol. Ecol., 17, 1–22. Fraiser, M.B. & Koburger, J.A., 1983. Incidence of Salmonella in clams, oysters, and mullet. J. Food Prot., 47, 343–345. Franca, S.M. C., Gibbs, D.L., Samuels, P. & Ichson, W.D., 1980. V. parahaemolyticus in Brazilian coastal waters. J. Am. Med. Assoc., 224, 587– 588. Frankenberg, D. & Smith, K.L., 1967. Coprophagy in marine animals. Limnol. Oceanogr., 12, 443–450. Friedl, F. & Alvarez, M., 1988. Cytometric studies on Mercenaria hemocytes. 3rd. Internal. Colloq. Pathol. Marine Aquacult., p. 115 only. Fuhrman, J.A. & Ammerman, J.W. & Azam, F., 1980. Bacterioplankton in the coastal euphotic zone: distribution, activity and possible relationship with phytoplankton. Mar. Biol, 60, 201–207. Fuks, D. & Filic, Z., 1977. Microbiological control of shellfish growing waters and bacteria elimination by Mussel Mytilus galloprovincialis. Acta Biol. Jugosl. Ser. E. IchthyoL, 9, 101–106. Galtsoff, P.S., 1964. The American oyster, Crassostrea virginica (Gmelin). U.S. Fish. Wildl Serv. Fish. Bull., 64, 1–80. Garland, C.D., Nash, G.V. & McMeekin, T.A., 1982. Absence of surface-associated microorganisms in adult oysters (Crassostrea gigas). Appl. Environ. Microbiol., 44, 1205–1211. Garland, C.D., Nash, G.V., Summer, C.E. & McMeekin, T.A., 1983. Bacterial pathogens of oyster larvae (Crassostrea gigas) in a Tasmanian hatchery. Aust, J. Mar. Freshwater Res., 4, 483–487. Geiger, J.C., Ward, W.E. & Jacobson, M.A., 1926. The bacterial flora of market oysters. J. Infect. Dis., 38, 273–280. Geldreich, E.E., 1965. Detection and significance of fecal coliform bacteria in stream pollution studies. J. Water Pollut. Control Fed., 37, 1722–1726. Gelli, D.S., Tachibana, T. & Sakuma, H., 1979. Occurrence of V. parahaemolyticus, E. coli and mesophilic bacteria in oysters. Rev. Inst. Adolfo Lutz., 39, 61–66.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
339
Gerba, C.P., Goyal, S.M., Cech, I. & Bogdan, G.F., 1980. Bacterial indicators and environmental factors as related to contamination of oysters by enteroviruses. J. Food Prot., 41, 99–101. Giere, O., 1985. Structure and position of bacteria and symbionts in the gill filaments of Lucinidae from Bermuda. Zoomorphology, 105, 296–301. Gieskes, W.W. & Kraay, G.W., 1986. Floristic and physiological differences between the shallow and the deep nanoplankton community in the euphotic zone of the open tropical Atlantic revealed by HPLC analysis of pigments. Mar. Biol., 91, 567–576. Glenn, A.R., 1976. Production of extra cellular protein by bacteria. Annu. Rev. Microbiol., 30, 41–62. Goldberg, E.G., 1975. The mussel watch: a first step in global marine monitoring. Mar. Pollut. Bull, 6, 111. Grassle, J.F., 1985. Hydrothermal vent animals: distribution and biology. Science, 229, 713–717. Greenberg, E.P., Duboise, M. & Palhof, B., 1982. The survival of marine vibrios in Mercenaria mercenaria. J. Food Saf., 4, 113–123. Griffin, M.R., Dalley, E., Fitzpatrick, M. & Austin, H., 1983. Campylobacter gastroenteritis associated with raw clams. J. Med. Soc. N.J., 80, 607–609. Grimes, D.J., Atwell, R.W., Brayton, P.R., Palmer, L.M., Rollins, D.M., Roszak, D.B., Singleton, F.L., Tamplin, M.L. & Colwell, R.R., 1986. The fate of enteric pathogenic bacteria in estuarine and marine environment. Microbiol Soc., 3, 324– 329. Grischkowsky, R.S. & Liston, J., 1974. Bacterial pathogenicity in laboratoryinduced mortality of the Pacific oyster (Crassostrea gigas, Thunberg). Proc. Natl. Shellfish. Assoc., 64, 82–91. Gross, J., 1910. Cristispira nov. gen., ein Beitrag zur Spirocheatenfrage. Mitt. Zool. Stat. Neapel, 20, 41–7. Guillard, R.R.L., 1959. Further evidence of the destruction of bivalve larvae by bacteria. Biol Bull. (Woods Hole, Mass.), 117, 258–266. Gulka, G. & Chang, P.W., 1984a. Pathogenicity and infectivity of a rickettsia-like organism in the sea scallop, Placopecten magellanicus. J. Fish. Dis., 8, 309–318. Gulka, G. & Chang, P.W., 1984b. Host response to rickettsial infection in blue mussel, Mytilus edulis L. J. Fish. Dis., 8, 319–323. Guzewich, J.J. & Morse, D.L., 1986. Source of shellfish in outbreaks of probable viral gastroenteritis implications for control. J. Food Prot., 49, 389–394. Hada, H.S., West, P.A., Lee, J.V., Stemmler, J. & Colwell, R.R., 1984. Vibrio tubiashii sp. nov., a pathogen of bivalve mollusks. Int. J. Syst. Bacterial., 34, 1– 4. Hargrave, B.T., 1976. DDT residues in benthic invertebrates and demersal fish in St Margarets Bay, Nova Scotia. J. Fish. Res., 33, 1692–1698. Harvey, R.W. & Luoma, S.N., 1984. The role of bacteria exopolymer and suspended bacteria in the nutrition of the deposit-feeding clam, Macoma balthica. J. Mar. Res., 42, 957–968. Haven, D.S. & Morales-Alamo, R., 1966. Aspects of biodeposition by oysters and other invertebrates filter-feeders. Limnol. Oceanogr., 11, 487–498. Haven, D.S., Perkins, F.O., Morales-Alamo, R. & Rhodes, M.W., 1977. Coliform depuration of Chesapeake Bay oysters. In, Proc. 10th Natl. Shellfish Sanitation workshop, pp. 49–59. Heffernan, W.P. & Cabelli, V.J., 1970. Elimination of bacteria by the northern quahaug Mercenaria mercenaria: environment parameters significant to the process. J. Fish. Res. Board Canada, 27, 1569–1577. Heffernan, W.P. & Cabelli, V.J., 1971. The elimination of bacteria by the northern quahaug: variability in the response of individual animals and the development of criteria. Proc. Natl. Shellfish Assoc., 61, 102–108.
340
D.PRIEUR ET AL.
Henriksen, K., Rasmussen, M.B. & Jensen, A., 1983. Effect of bioturbation on microbial nitrogen transformations in the sediment and fluxes of ammonium and nitrate to the overlaying water. Environ. Biogeogr. Ecol. Bull., 35, 193–205. Henry, M., Vicente, N. & Cornet, C., 1981. Analyse ultrastructurale du filament branchial d’un mollusque bivalve Cerastoderma glaucum Poiret 1789. Association particulière avec des microorganismes. Haliotis, 11, 101–104. Hernandez, J.F., Oger, C. & Delattre, J.M., 1984. Étude microbiologique des moules de la région Nord-Pas de Calais. IFREMER (Fr) Convention, No. 83/7214, 38 pp. Herry, A. & Le Pennec, M., 1987. Endosymbiotic bacteria in the gills of the littoral bivalve molluscs Thyasira flexuosa (Thyasiridae) and Lucinella divaricata (Lucinidae). Symbiosis, 4, 25–36. Hidaka, T. & Saito, K., 1956. Studies on the cellulose decomposing bacteria found in the digestive organs of Teredo (Teredo navalis sp.) II on the bacterial cellulase. Mem. Fac. Fish. Kagoshima Univ., 5, 172–177. Hidu, H. & Tubiash, H.S., 1963. A bacterial basis for the growth of antibiotic-treated bivalve larvae. Proc. Natl. Shellfish Assoc., 54, 25–39. Hily, A., Le Pennec, M. & Henry, M., 1986. Ultrastructure des diverticules digestifs d’un Mytilidae des sources hydrothermales du Pacific oriental. C.R. Acad. Sci. Paris, 302, Sér. III, 495–502. Hily, A., Le. Pennec, M., Prieur, D. & Fiala-Medioni, A., 1986. Anatomie et structure du tractus digestif d’un mytilidae des sources hydrothermales profondes de la ride du Pacifique oriental. Cah. Biol. Mar., 27, 235–241. Hinsch, G.W. & Hunte, M., 1988. Ultrastructure of phagocytosis in hemocytes of the American oyster. 3rd Int. Colloq. Pathol. Marine Aquacult., p. 147 only. Hobbie, J.E. & Lee, C., 1980. Microbial production of extracellular material: importance in benthic ecology. In, Marine Benthic Dynamics, edited by B.C. Coull & K.R. Tenore, University of South Carolina Press, Columbia, S.C., pp. 341–346. Hood, M.A., Ness, G.E. & Blake, N.J., 1983. Relationship among fecal coliforms E. coli and Salmonella in shellfish. Appl. Environ, Microbiol., 45, 1, 122–126. Hood, M.A., Ness, G.E. & Rodrick, G.E., 1981. Isolation of Vibrio cholerae serotype Ol from the eastern oyster Crassostrea virginica. Appl. Environ. Microbiol., 41, 559–560. Howland, K.H. & Cheng, T.C., 1982. Identification of bacterial chemoattractants for oyster (Crassostrea virginica) hemocytes. J. Invertebr. Pathol., 39, 123–132. Huchon, A., 1980. Infection d’allure typique due à Listeria monocytogenes après absorption d’huitres. La Nouvelle Presse Médicale, 9, 43–3281. Hunt, D.A. & Springer, S., 1978. Comparison of two rapid test procedures with the standard EC test for recovery of faecal coliform bacteria from shellfish growing waters. J. Assoc. Anal. Chem., 61, 1317–1323. Hunter, A.C. & Linden, B.R., 1923. An investigation of oyster spoilage. Am. Food J., 18, 538–540. Hussong, D., Colwell, R.R. & Weiner, R.M., 1981. Seasonal concentration of coliform bacteria by Crassostrea virginica the eastern oyster in Chesapeake Bay. J. Food Prot., 44, 201–203. Jacq, E. & Prieur, D., 1986. Les Associations bactéries-matière particulaire en milieu pélagique. In, Act. Coll. No. 3, 2nd Coll. Int. Bact. Mar. (Brest 1984), edited by GERBAM, IFREMER, CNRS, pp. 229–236. Janssen, W.A., 1973. Oysters: retention and excretion of three types of human waterborne disease bacteria. Health Lab. Sci., 11, 20–24. Jeanthon, C., Prieur, D. & Cochard, J.C., 1988. Bacteriological survey of antibiotictreated sea waters in a Pec ten maximus hatchery. Aquaculture, 71, 1–8. Jeffries, V.E., 1982. Three Vibrio strains pathogenic to larvae of Crassostrea gigas and Ostrea edulis. Aquaculture, 29, 201–226. Johnson, H.M., 1964. Human blood group A specific agglutinins of the butter clan. Saxidomus giganteus. Science, 146, 548–549.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
341
Johnson, P.W. & Sieburth, J. McN., 1979. Chrococcoid Cyanobacteria in the sea: a ubiquitous and diverse photo trophic biomass. Limnol. Oceanogr., 24, 928– 935. Johnson, P.W. & Sieburth, J. McN., 1982. In situ morphology and occurrence of eucaryotic phophotrophs of bacterial size in the picoplankton of estuarine and oceanic water. J. Phycol, 18, 318–327. Johnson, R.G., 1974. Particulate matter at the sediment-water interface in coastal environments. J. Mar. Res., 33, 313–330. Johnson, R.G., 1977. Vertical variation in particulate matter in the upper twenty centimeters of marine sediments. J. Mar. Res., 35, 273–282. Johnstone, J., 1910. Routine methods of shellfish examination with reference to sewage pollution. J. Hyg., 9, 412–440. Joint, I.R. & Pomroy, A.J., 1983. Production of picoplankton and small nanoplankton in the Celtic Sea. Mar. Biol., 77, 19–27. Jollès, P., 1969. Lysozymes: a chapter in molecular biology. Angew. Chem., 8, 227– 294. Jordan, T.E. & Valiela, I., 1982. A nitrogen budget of the ribbed mussel, Geukensia demissa and its significance in nitrogen flow in a New England salt marsh. Limnol. Oceanogr., 27, 75–90. Jørgensen, C.B., 1983. Fluid mechanical aspects of suspension feeding. Mar. Ecol. Prog. Ser., 11, 89–103. Joseph, S.N., Donta, S.T., Maneval, D.R., Kaper, J.B., Colwell, R.R. & Spira, W.N., 1984. An assessment of Non Ol V. cholerae virulence in the Yl mouse adrenal cell assay. In, Vibrios in the Environment, edited by R.R. Colwell, Wiley Interscience Publ., New York, pp. 123–143. Juniper, S.K. & Sibuet, M., 1987. Cold seep benthic communities in Japan subduction zones: spatial organization, trophic strategies and evidence for temporal evolution. Mar. Ecol. Prog. Ser., 40, 115–126. Kaneko, T., Colwell, R.R. & Hamons, F., 1975. Bacteriological studies of Wicomico river soft-cell clam (Mya arenaria) mortalities. Chesapeake Sci., 16, 1, 3–13. Kaper, J., Lockman, H., Colwell, R.R. & Joseph, S.W., 1979. Ecology serology and enterotoxin production of Vibrio cholerae in Chesapeake Bay. Appl. Environ. Microbiol, 37, 91–103. Kaspar, H.F., Gillespie, P.A., Boyer, I.C. & MacKenzie, A.L., 1985. Effects of mussel aquaculture on the nitrogen cycle and benthic communities in Kenepuru Sound, Marlborough Sounds, New Zealand. Mar. Biol., 85, 127–136. Kautsky, N. & Evans, S., 1987. Role of biodeposition by Mytilus edulis in the circulation of matter and nutrients in a Baltic coastal ecosystem. Mar. Ecol. Prog. Ser., 38, 201–212. Kelly, C.B. & Arcisz, W., 1954. Survival of enteric organisms in shellfish. U.S. Public Health Reports, 69, 1205–1210. Kelly, J.R. & Nixon, S.W., 1984. Experimental studies of the effect of organic deposition on the metabolism of a coastal marine bottom community. Mar. Ecol. Prog. Ser., 17, 157–169. Kemp, W.N. & Boynton, W.R., 1981. External and internal factors regulating metabolic rates of an estuarine benthic community. Oecologia (Berlin), 51, 19– 27. Kenk, V.C. & Wilson, B.R., 1985. A new mussel (Bivalvia, Mytilidae) from hydrothermal vents in the Galapagos rift zone. Malacologia, 26, 253–271. Kennicutt II, M.C., Brooks, J.M., Bidigare, R.R., Fay, R.R., Wade, T.L. & McDonald, T.J., 1985. Vent-type taxa in a hydrocarbon seep region on the Louisiana slope. Nature (London), 317, 351–353. Kiørboe, T., Møhlenberg, F. & Nøhr, O., 1980. Feeding, particle selection and carbon absorption in Mytilus edulis in different mixtures of algae and resuspended bottom material. Ophelia, 19, 193–205.
342
D.PRIEUR ET AL.
Kirchman, D., Graham, S., Reish, D. & Mitchell, R., 1982. Bacteria induce settlement and metamorphosis of Janua (Dexiopira) brasiliensis Grube (polychaeta: Spirorbidae). J. Exp. Mar. Biol. Ecol., 56, 153–163. Kirchman, D. & Mitchell, R., 1981. Biochemical interaction between microorganisms and marine fouling invertebrates. Biodeterioration, 5, 281–290. Kobayashi, T., Enomoto, R., Sakazaki, R. & Kuwahara, S., 1963. A new selective isolation medium for pathogenic vibrios: TCBS Agar. Jpn. J. Bacteriol., 18, 387– 391. Koburger, J.A. & Miller, M.L., 1986. Evaluation for a fluorogenic MPN procedure for determinating E. coli in oysters. J. Food Prot., 48, 244–245. Kokubo, Y., Matsushita, S., Kai, A., Yamada, M. & Konuma, H., 1978. Incidence of E. coli in raw oyster and enterotoxin productibility of the isolates. J. Food Hyg. Soc. Jpn., 19, 117–121. Kraeuter, I.N., 1976. Biodeposition by salt-marsh invertebrates. Mar. Biol., 35, 215– 223. Kueh, C.S.W. & Chan, K., 1985. Bacteria in bivalve shellfish with special reference to the oyster. J. Appl. Bacteriol., 59, 41–47. Kuenzler, E.J., 1961. Structure and energy flow of a mussel population in a Georgia salt marsh. Limnol. Oceanogr., 6, 191–204. Kulm, L.D., Suess, E., Moore, J. C, Carson, B., Lewis, B.T., Ritger, S.D., Kadko, D.C., Thornburg, T.M., Embley, R.W., Rugh, W.D., Massoth, G.J., Langseth, M.G., Cochrane, G.R. & Scamman, R.L., 1986. Oregon subduction zone: venting, fauna and carbonates. Science, 231, 561–566. Kurata, A., 1986. Production and consumption of B group vitamins in situ. In, Act. de Coll. No. 3, 2nd Coll. Int. Bact. Mar. (Brest 1984), edited by GERBAM, IFREMER, CNRS, pp. 169–174. Kusuki, Y., 1978. Relationship between quantities of faecal material produced and of the suspended matter removed by the Japanese Oyster. Bull. Jpn. Soc. Sci. Fish., 44, 1183–1185. Langdon, C.J., 1983. The effect of algal and artificial diets on the growth and growth studies with bacteria-free oyster (Crassostrea gigas) larvae fed on semi defined artificial diets. Biol Bull (Woods Hole, Mass.), 164, 227–235. Lartigue, D., Novak, A.F. & Fiegger, E.A., 1960. An evaluation of the indole and trimethylamine tests for oyster quality. Food Technol., 14, 109–112. Laubier, L., Ohta, S. & Sibuet, M., 1986. Découverte de communautés animates profondes durant la campagne franco-japonaise Kaiko de plongées dans les fosses de subduction autour de Japon. C.R. Acad. Sci. Paris, Sér. III, 303, 25–29. Le Gall, G., Chagot, D., Mialhe, E. & Grizel, H., 1988a. Branchial rickettsiales-like infection associated with a mass mortality of sea scallop Pecten maximus. Dis. Aquat. Org., 4, 229–232. Le Gall, G., Mialhe, E. & Grizel, H., 1988b. Epidemiology of a rickettsial disease of the bay scallop, Pecten maximus, in France. 3rd Int. Colloq. Pathol. Marine Aquacult., p. 97 only. Le Pennec, M., 1987. Alimentation et reproduction d’un Mytilidae des sources hydrothermales profondes du Pacifique oriental. Oceanologia Acta, Vol. spec. 8, 181–190. Le Pennec, M., Herry, A., Diouris, M., Moraga, D. & Donval, A., 1987. Chemoautotrophie bactérienne chez le mollusque bivalve littoral Lucinella divaricata (Linné). C.R. Acad. Sci. Paris, Sér. III, 305, 1–5. Le Pennec, M. & Hily, A., 1984. Observations sur la nutrition d’un Mytilidae des sites hydrothermaux du Pacifique oriental. C.R. Acad. Sci. Paris, Sér. III, 298, 493–497. Le Pennec, M. & Prieur, D., 1972. Développement larvaire de Mytilus edulis (L.) en présence d’antibiotiques. 1 ère partie: détermination des concentrations actives non toxiques de quatre antibiotiques: Auréomycine, Erythromycine, Chloramphénicol et Sulfamérazine. Rev. Int. Oceanogr. Méd., 28, 167–180.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
343
Le Pennec, M. & Prieur, D., 1977. Les antibiotiques dans les élevages de larves de bivalves marins. Aquaculture, 12, 15–30. Le Pennec, M. & Prieur, D., 1984. Observations sur la nutrition d’un mytilidae d’un site hydrothermal actif de la dorsal du Pacifique oriental. C.R. Acad. Sci. Paris, 298, Sér. III, 493–98. Le Pennec, M., Prieur, D. & Lucas, A., 1985. Studies on the feeding of hydro thermalvent mytilid from the east Pacific rise. In, Proceedings of the 19th European Marine Biology Symposium, edited by P.E. Gibbs, Cambridge University Press, Cambridge, pp. 159–166. Ledo, A., Gonzalez, E., Barja, J.L. & Toranzo, A.E., 1983. Effects of depuration systems on the reduction of bacteriological indicators in cultured mussels (Mytilus edulis). J.Shellfish Res., 3, 59–64. Leibovitz, L. & Elston, R., 1980. Detection of vibrosis in hatchery larval oyster cultures: study of the interrelationship of diagnosis and management variables in an experimental model. Proc. Natl. Shellfish. Assoc., 70, 123–125. Leippe, M. & Renwrantz, L., 1985. On the capability of bivalve and gastropod hemocytes to secrete cytotoxic molecules. J. Invertebr. Pathol., 46, 209–210. Leippe, M. & Renwrantz, L., 1988. Release of cytotoxic agglutinating molecules by Mytilus hemocytes. Dev. Comp. Immunol., 12, 297–308. Leung, C., Shortridge, K.F., Morton, B. & Wong, P.S., 1973. The seasonal incidence of faecal bacteria in the tissues of the commercial oyster Crassostrea gigas Thunberg 1973 correlated with the hydrology of Deep Bay-Hong Kong. In, Proc. Spec. Symp. Mar. Sci., Hong Kong, Pacif. Sci. Assoc., pp. 114–127.. Levine, M.M., Black, R. & Clement, M.L., 1984. Pathogenesis of enteric infections caused by Vibrio. In Vibrios in the Environment, edited by R.R. Colwell, Wiley Interscience Publ., New York, pp. 109–123. Levinton, J.S. & Lopez, G.R., 1977. A model of renewable resources and limitation of deposit-feeding benthic populations. Oecologia (Berlin), 31, 177–190. Li, W.K. W., Subba Rao, D.V., Harrison, W.G., Smith, J.C., Culler, J.J., Irwin, B. & Platt, T., 1983. Autotrophic picoplankton in the tropic ocean. Science, 219, 292–295. Lipovsky, V.P. & Chew, K.K., 1972. Mortality of Pacific oysters (Crassostrea gigas): the influence of temperature and enriched seawater on oyster survival. Proc. Natl Shellfish. Assoc., 62, 72–82. Liston, J., 1973. Vibrio parahaemolyticus. In, Microbial Safety of Fishery Products, edited by C.O. Chichester & H.D. Graham, Academic Press, New York, pp. 203–212. Lodeiros, C., Bolinches, J., Dopazo, C.P. & Toranzo, A.E., 1987. Bacillary necrosis in hatcheries of Ostrea edulis in Spain. Aquaculture, 65, 15–29. Lonsdale, P., 1977. Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep-sea Res., 24, 857–863. Loosanoff, V.L., 1954. New advances in the study of bivalve larvae. Am. Sci., 42, 607–624. Loosanoff, V.L. & Davis, C.H., 1963. Rearing of bivalve mollusks. Adv. Mar. Biol., 1, 1–136. Lopez, G.R., 1980. The availability of microorganisms attached to sediment as food for some marine deposit feeding molluscs, with notes on microbial detachment due to the crystalline style. In, Marine Benthic Dynamics, edited by K.R. Tenore & B.C. Coull, University of South Carolina Press, Columbia, S.C., pp. 387– 405. Lovelace, T.E., Tubiash, H. & Colwell, R., 1968. Quantitative and qualitative commensal bacterial flora of Crassostrea virginica in Chesapeake Bay. Proc. Natl Shellfish Assoc., 58, 82–87. MacDonald, B.A., 1988. Physiological energetics of Japanese scallop Patinopecten yessoensis larvae. J. Exp. Mar. Biol. Ecol., 120, 155–170.
344
D.PRIEUR ET AL.
Mackowiack, P.A., Caraway, C.T. & Portnoy, B.J., 1976. Oyster associated hepatitis. Lessons from Louisiana experience. Am. J. Epidemiol., 103, 181–191. Madden, R.H., Buller, H. & McDonell, D.N., 1986. Clostridum perfringens an indicator of hygienic quality of depurated shellfish. J. Food Prot., 49, 33–36. Maginot, M., Samain, J.F., Daniel, J.Y., Le Coz, J.-R. & Moal, J., in press. Kinetic properties of lysozyme from the digestive gland of Tapes philippinarum. Oceanis. Manahan, D.T. & Crisp, D.J., 1982. The role of dissolved organic material in the nutrition of pelagic larvae: aminoacid uptake by bivalve veligers. Am. Zool., 22, 635–646. Manahan, D.T. & Richardson, K., 1983. Competition on the uptake of dissolved organic nutrients by bivalve larvae (Mytilus edulis) and marine bacteria. Mar. Biol., 75, 241– 247. Mann, K.H., 1972. Macrophyte production and detritus food chains in coastal areas. Mem. Ist. Ital. Idrobiol., 29 (Suppl.) , 353–382. Marjori, L., Campello, C. & Crevatin, E., 1977. Salmonella pollution of the Gulf of Trieste. Rev. Int. Oceanogr. Med., 47, 181–191. Martin, Y., 1976. Importance des bactéries chez les mollusques bivalves. Haliotis, 7, 97– 103. Martin, Y. & Mengus, B., 1979. Utilisation de souches bactériennes sélectionnées dans l’alimentation des larves de Mytilus galloprovincialis LMK (mollusque bivalve) en é’evages expérimentaux. Aquaculture, 10, 253–262. Martin, Y. & Vicente, N., 1975. Action des antibiotiques sur les cultures des larves de mollusques bivalves. Essais sur Mytilus galloprovincialis (Lmk). Rev. Int. Océanogr. Méd., 39–40, 53–69. Martin-Bouyer, G., 1978. Techniques épidémiologiques dans la mesure des risques. Rev. Int. Océanogr. Méd., 50, 69–81. Martinez, J.C., 1984. Étude comparative entre la microflore de l’appareil digestif de Teredo navalis L. (Teredinidae Bivalvia) et les populations bactériennes de son environnement. CNEXO: Ed. Act. Coll., 13, 91–96. Martinez, J.C. & Trique, B., 1986. Relations entre les microflores bactériennes et la cellulolyse dans l’appareil digestif et l’environnement de Teredo navalis L. (Teredinidae, bivalvia). In, Act. Coll. No. 3, 2nd Coll. Int. Bact. Mar. (Brest 1984), edited by GERBAM, IFREMER, CNRS, pp. 435–43. Mattsson, J. & Lindén, 1983. Benthic macrofauna succession under mussels, Mytilus edulis L. (Bivalvia), cultured on hanging long-lines. Sarsia, 68, 97–102. Mayasich, S.A. & Smucker, R.A., 1987. Role of Cristispira sp. and other bacteria in the chitinase and chitobiase activities of the crystalline style of Crassostrea virginica (Gmelin). Microb. Ecol., 14, 157–166. Mazieres, J., Richard, B. & Mazieres, S., 1980. Une méthode de recherche rapide des coliformes fécaux dans les eaux de mer et les coquillages. Rev. Trav. Inst. Pêches Marit., 44, 289–293. McHenery, J.G. & Birkbeck, T.H., 1979. Lysozyme of the mussel Mytilus edulis. Mar. Biol. Lett., 1, 111–119. McHenery, J.G. & Birkbeck, T.H., 1982. Characterisation of the lysozyme of Mytilus edulis (L.). Comp. Biochem. Physiol., 71B, 583–589. McHenery, J.G. & Birkbeck, T.H., 1985. Uptake and processing of cultured microorganisms by bivalves. J. Exp. Mar. Biol. Ecol., 90, 145–163. McHenery, J.G. & Birkbeck, T.H., 1986a. Distribution of lysozyme-like activity in 30 bivalve species. Comp. Biochem. Physiol., 85B, 581–584. McHenery, J.G. & Birkbeck, T.H., 1986b. Inhibition of filtration in Mytilus edulis L. by marine vibrios. J. Fish Dis., 9, 257–261. McManus, G.B. & Peterson, W.T., 1988. Bacterioplankton production in the nearshore zone during upwelling off central Chile. Mar. Biol. Ecol. Prog. Ser., 43, 11–17. Metcalf, T.G., 1974. Evaluation of shellfish sanitary quality by indicators of sewage pollution. In “Discharge Sewage from Sea Outfalls”. Pergamon Press, London, pp. 75–82.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
345
Metcalf, T.G., Slanetz, L.W. & Bartley, C.H., 1973. Enteric pathogens in estuary waters and shellfish. In, Microbial safety of fishery products, edited by C.O. Chichester & H.G.Graham, Academic Press, New York, 215–234. Meyer-Reil, L.A., 1977. Bacterial growth rates and biomass production. In, Microbial Ecology of a Brackish Water Environment, edited by G.Rheinheimer, Springer, Berlin, Ecol. Studies, 25, 223–243. Meyer-Reil, L.A., Dawson, R., Liebezeit, G. & Tiedge, H., 1978. Fluctuation and interactions of bacterial activity in sandy beach sediments and overlying water. Mar. Biol., 48, 161–171. Meyers, T.R., 1981. Endemic diseases of cultured shellfish of Long Island, New York: adult and juvenile American oysters (Crassostrea virginica) and hard clams (Mercenaria mercenaria). Aquaculture, 22, 305–330. Mialhe, E., Chagot, D., Boulo, V., Comps, M., Ruano, F. & Grizel, H., 1987. An infection of Ruditapes decussatus (Bivalvia) by Rickettsia. Aquaculture, 67, 258–259. Millar, R.H. & Scott, J.M., 1967. Bacteria-free culture of oyster larvae. Nature (London), 216, 1139–1140. Minet, J., Barbosa, T., Prieur, D. & Cormier, M., 1987. Mise en evidence du processus de concentration des bactéries par la moule, Mytilus edulis (L.). C.R. Acad. Sci. Paris Ser. III, 305, 351–354. Mitchell, R. & Young, L., 1972. The role of microorganisms in marine fouling. Off. Nav. Res. Contract 00014–67–A–0298–0026–NR-306–025. U.S. Office of Naval Research, Washington, D.C., 23 pp. Mohandas, A. & Cheng, T. C, 1985. An electron microscope study of the structure of lysosomes released from Mercenaria mercenaria granulocytes. J. Invertebr. Pathol., 46, 332–334. Møhlenberg, F. & Riisgård, H.U., 1978. Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia, 17, 239–246. Moore, B., 1970. The present status of diseases connected with marine pollution. Rev. Int. Oceanogr. Med., 18–19, 193–223. Moore, M.N. & Lowe, D.M., 1977. The cytology and cytochemistry of the hemocytes of Mytilus edulis and their responses to experimentally injected carbon particles. J. Invertebr. Pathol., 29, 18–30. Mori, K., Nakamura, M. & Nomura, T., 1988. H O production by hemocytes as a 2 2 practicable means of evaluating the defensive capacity of scallops under culture. 3rd Int. Colloq. Pathol. Marine Aquacult., p. 117 only. Morita, R.Y., 1985. Starvation of heterotrophs. In, Bacteria in their Environments, edited by M. Fletcher & G.D. Floodgate, Academic Press, New York, pp. 111–130. Morrison, C. & Shum, G., 1982. Chlamydia-like organisms in the digestive diverticula of the bay scallop, Argopecten irradians (Lmk). J. Fish Dis., 5, 173–184. Morrison, C. & Shum, G., 1983. Rickettsias in the kidney of the bay scallop, Argopecten irradians (Lamarck). J. Fish Dis., 6, 537–541. Morton, B., 1978. Feeding and digestion in shipworms. Oceanogr. Mar. Biol. Annu. Rev., 16, 108–144. Morton, B., 1983. Feeding and digestion in bivalvia. In, The Mollusca, Vol. 5, Physiology, edited by A.S.M. Saleuddin & K.M.Wilbur, Academic Press, London, pp. 65–147. Murchelano, R.A. & Bishop, J.L., 1969. Bacteriological study of laboratory reared juvenile American oysters (Crassostrea virginica). J. Invertebr. Pathol., 14, 321– 327. Murchelano, R.A. & Brown, C., 1968. Bacteriological study of the natural flora of the eastern oyster, Crassostrea virginica. J. Invertebr. Pathol., 11, 520–521. Murphy, L.S. & Haugen, E.M., 1985. The distribution and abundance of phototrophic ultraplankton in the North Atlantic. Limnol. Oceanogr., 30, 47–58. Nair, N.B. & Saraswathy, M., 1971. The biology of the wood-boring tereinid molluscs. Adv. Mar. Biol., 9, 336–509.
346
D.PRIEUR ET AL.
Nakamura, M., Mori, K., Inooka, S. & Nomura, T., 1985. In vitro production of hydrogen peroxide by the amoebocytes of the scallop Patinopecten yessoensis (Jay). Dev. Comp. Immunol, 9, 407–417. Narain, A.S., 1973. The ameobocytes of lamellibranch molluscs, with special reference to the circulating amoebocytes. Malacol. Rev., 6, 1–12. Newell, R., 1965. The role of detritus in the nutrition of two marine deposit feeders, the prosobranch Hydrobia ulvae and the bivalve Macoma balthica. Proc. Zool. Soc. London, 144, 25–45. Newell, R.C. & Field, J.G., 1983. The contribution of bacteria and detritus to carbon and nitrogen flow in a benthic community. Mar. Biol. Lett., 4, 23–26. Newell, R.C., Field, J.G. & Griffiths, C.L., 1982. Energy balance and significance of microorganisms in a kelp bed community. Mar. Ecol. Prog. Ser., 8, 103–113. Newell, R.C., Lucas, M.I. & Linley, E.A. S., 1981. Rate of degradation and efficiency of conversion of phytoplankton debris by marine microorganisms. Mar. Ecol. Prog. Ser., 6, 123–136. N’Guyen Thi Son & Fleet, G.H., 1980. Behavior of pathogenic bacteria in the oyster Crassostrea gigas, during depuration, relaying and storage. Appl. Environ. Microbiol., 40, 994–1002. Nichols, F.H., 1985. Increased benthic grazing: an alternative explanation for low phytoplankton biomass in Northern San Francisco Bay during the 1976–1977 drought. Estuarine Coastal Shelf Sci., 21, 379–388. Nicolas, J.L. & Cochard, J.C., 1987. Aquaculture de mollusques: la palourde. Mise en evidence d’une maladie spécifique des élevages larvaires de la palourde. Equinoxe, 15, 32–35. Nienhuis, P.H., 1981. Distribution of organic matter marine organisms. In, Marine Organic Chemistry, edited by E.K. Duursma & R. Dawson, Elsevier Oceanography Series, 31, pp. 31–69. Nishio, T., Nakamori, J. & Miyazaki, K., 1981. Survival of Salmonella typhi in oysters. Zentralbl. Bakt. Mikrobiol Hyg., 172, 415–26. Nixon, S.W., Oviatt, C.A., Garber, J. & Lee, V., 1976. Diel metabolism and nutrient dynamics in a salt marsh embayment. Ecology, 57, 740–750. Nolan, C.M., Ballard, J., Kaysner, C.A., Litja, J.L., Williams, L.P. & Tenover, F. C., 1984. Vibrio parahaemolyticus gastroenteritis: an outbreak associated with raw oysters in the Pacific Northwest. Diagn. Microbiol. Infect. Dis., 2, 119–128. Nottage, A.S. & Birkbeck, T.H., 1986. Toxicity to marine bivalves of culture supernatant fluids of the bivalve-pathogenic Vibrio strain MCNB 1338 and other marine vibrios. J. Fish Dis., 9, 249–256. Nottage, A.S. & Birkbeck, T.H., 1987a. Purification of a proteinase produced by the bivalve pathogen Vibrio alginolyticus NCMB 1339. J. Fish Dis., 10, 211–220. Nottage, A.S. & Birkbeck, T.H., 1987b. Production of proteinase during experimental infection of Ostrea edulis L. larvae with Vibrio alginolyticus NCMB 1339 and the antigenic relationship between proteinase produced by marine vibrios pathogenic for fish and shellfish. J. Fish Dis., 10, 265–273. Nottage, A.S. & Birkbeck, T.H., 1987c. The role of toxins in Vibrio infections of bivalve molluscs. Aquaculture, 67, 244–246. Novak, A.F., Fieger, E.A. & Stolzle, K.A., 1960. In vitro effects of chlortetracycline on bacteria indigenous to gulfshrimp and oysters. Food Technol., 14, 585–586. Odum, W.E., Kirk, P.W. & Zieman, J.C., 1979. Non-protein nitrogen compounds associated with particles of vascular plant detritus. Oikos, 32, 363–367. Okutani, T. & Métivier, B., 1986. Description of three new species of Vesicomyid bivalves collected by the submersible nautile from abyssal depths off Honshu, Japon. Venus, 45, 147–160. Oppenheimer, C.H. & ZoBell, C.E., 1952. The growth and viability of sixty three species of marine bacteria as influenced by hydrostatic pressure. J. Mar. Res., 11, 10–18.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
347
Owen, G., 1978. Classification and the bivalve gill. Phil. Trans. R. Soc. London Ser. B, 284, 377–386. Owen, G. & McCrae, J.M., 1976. Further studies on the latero-frontal tracts of bivalves. Proc. R. Soc. London Ser. B, 194, 527–544. Page, A. & Cutlip, R.C., 1982. Morphological and immunological confirmation of the presence of chlamydiae in the gut tissues of the Chesapeake Bay Clam, Mercenaria mercenaria. Curr. Microbiol., 7, 297–300. Paoletti, A., 1968. Organismes predateurs dans l’autoépuration des eaux de mer polluées. Essais d’étude avec des bactéries radioactives et autrement marquées. Rev. Int. Oceanog. Med., 10, 229–247. Paull, C.K., Hecker, B., Commeau, R., Freeman-Lynde, R.P., Neumann, C., Corso, W.P., Golubic, S., Hook, J.E., Sikes, E. & Curray, J., 1984. Biological communities at the Florida escarpment resemble hydro thermal vent taxa. Science, 226, 965–967. Peixotto, S.S., Finne, G., Hanna, M.O. & Vanderzant, C, 1979. Presence, growth and survival of Yersinia enterolitica in oysters, shrimp and crab. J. Food Prot., 42, 974–981. Perkins, F.O., Haven, D.S., Alamo, R.M. & Rhodes, M.W., 1980. Uptake and elimination of bacteria in shellfish. J. Food Prot., 43, 124–126. Pinot, M., Riou, F. & Chaperon, J., 1988. Impact sanitaire de la consommation de coquillage bivalves filtreurs. Rapport IFREMER, Contract No. 87/2/430421. Plusquellec, A., Beucher, M. & Le Gal, Y., 1983. Enumeration of the bacterial contamination of bivalves in monitoring the marine bacteria pollution. Marine Pollut. Bull., 14, 260–263. Plusquellec, A., Beucher, M. & Le Gall, Y., 1986. Bivalves indicateurs de pollution microbienne des eaux littorales. In, Act. Coll. No. 3, 2nd Coll. Int. Bact. Mar.) (Brest 1984), edited by GERBAM, IFREMER, CNRS, pp. 541– 548. Plusquellec, A., Beucher, M., Prieur, D. & Le Gal, Y., in press. Contamination of the mussel by enteric bacteria. J. Shellfish Res., 9, in press. Popham, J.D. & Dickson, M.R., 1973. Bacterial associations in the Teredo Bankia australis (Lamellibranchia: mollusca). Mar. Biol., 19, 338–340. Portnoy, B.C., 1975. Oyster associated hepatitis: failure of shellfish certification programs to prevent outbreaks. J. Am. Med. Assoc., 3, 1065–1068. Presnell, M.W., Miescier, J.J. & Hill, W.F., 1967. Clostridium botulinum in marine sediments and in the oyster Crassostrea virginica from Mobile Bay. Appl. Microbiol., 15, 668–669. Prieur, D., 198la. Experimental studies of trophic relationships between marine bacteria and bivalve molluscs. Kiel. Meeresforsch., (Sondh.), No. 5, 376–383. Prieur, D., 1981b. Les relations entre mollusques bivalves et bactéries hétérotrophes en milieu marin. Étude analytique et experiment ale. Thèse Doct. Etat. Sci. Nat. Brest, 266 pp. Prieur, D., 1987. Étude préliminaire de communautés bactériennes hétérotrophes associées à des invertébrés des sources hydrothermales profondes. Oceanologica Acta, spec. 8, 139–145. Prieur, D. & Carval, J.P., 1979. Bacteriological and physico-chemical analysis in a bivalve hatchery: techniques and preliminary results. Aquaculture, 17, 359– 374. Prieur, D. & Jeanthon, C., 1987. Preliminary studies of heterotrophic bacteria isolated from deep-sea hydro thermal vent invertebrates. Symbiosis, 4, 87–98. Quadri, R.B., Buckle, K.A. & Edwards, R.A., 1974. Rapid method for the determination of faecal contamination in oysters. J. Appl. Bacteriol., 37, 7–14. Rajagopalan, K. & Sivalingam, P.M., 1978. Bacterial flora of a green mussel (Mytilus viridis Linnaeus) and a naturally occurring rock oyster (Crassostrea cuculata). Mal. Appl. Biol, 7, 43–47.
348
D.PRIEUR ET AL.
Rasmussen, L.P. D., Hage, E. & Karlog, O., 1985. An electron microscope study of the circulating leucocytes of the marine mussel, Mytilus edulis. J. Invertebr. Pathol., 45, 158–167. Rau, G.H., 198la. Low 15 N/ 14N in the hydrothermal vent animal: ecological implications. Nature (London), 289, 484–485. Rau, G.H., 1981b. Hydrothermal vent clam and tube worm 13C/12C: further evidence of non photosynthetic food sources. Science, 213, 338–340. Rau, G.H. & Hedges, J. L, 1979. Carbon-13 depletion in a hydrothermal vent mussel: suggestion of chemosynthetic food source. Science, 203, 648–649. Reid, R.G. B., 1966. Digestive tract enzymes in the bivalves Lima hians Gmelin and Mya arenaria L. Comp. Biochem. Physiol., 17, 417–433. Reid, R.G. B., 1978. The systematic, adaptative and physiological significance of proteolytic enzyme distribution in bivalves. Veliger, 20, 260–265. Reid, R.G. B. & Brand, D.G., 1986. Sulfide-oxidizing symbiosis in lucinaceans: implications for bivalve evolution. Veliger, 29, 3–24. Renwrantz, L., Daniels, J. & Hansen, P.D., 1985. Lectine-binding to hemocytes of Mytilus edulis. Dev. Comp. Immunol., 9, 203–210. Renwrantz, L. & Stahmer, A., 1983. Opsonizing properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis. J. Comp. Physiol., 149, 535–546. Renwrantz, L., Yoshino, T., Cheng, T. & Auld, K., 1979. Size determination of hemocytes from the American oyster, Crassostrea virginica, and the description of a phagocytosis mechanism. J. Physiol. Zool., 83, 1–12. Rhoads, D.C., 1973. The influence of deposit-feeding benthos on water turbidity and nutrient recycling. Am. J. Sci., 273, 1–22. Rhoads, D.C., 1974. Organism-sediment relations on the muddy sea floor. Oceanogr. Mar. Biol. Annu. Rev., 12, 263–300. Rhoads, D.C. & Young, D.K., 1970. The influence of deposit-feeding organisms on sediment stability and community trophic structure. J. Mar. Res., 28, 150–178. Rice, C.E., 1929. The decomposition of clam muscle in acid solutions. Contrib. Can. Biol. Fisheries, 4, 97–105. Rice, M.A., Wullis, M. & Stephens, G.C., 1980. Influx and net flux of amino acids into larval and juvenile European flat oyster, Ostrea edulis. J. Exp. Mar. Biol. Ecol., 48, 51–59. Riisgård, H.U., 1988. Efficiency of particle retention and filtration rate in 6 species of the Northeast American bivalves. Mar. Ecol. Prog. Ser., 45, 217–223. Rodhouse, P.G., Roden, C.M., Hensey, M.P. & Ryan, J.H., 1985. Production of mussels, Mytilus edulis, in suspended culture and estimates of carbon and nitrogen flow: Killary harbour, Ireland. J. Mar. Biol. Ass. U.K., 65, 55–68. Rodrick, G.E., Blake, N.J., Tamplin, M., Cornette, J.E., Cuba, T. & Hood, M.A., 1984. The relationship between fecal coliform levels and the occurence of Vibrio in Apalachicola Bay (Florida). In, Vibrios in the Environment, edited by R.R. Colwell, Wiley Interscience Publ., New York, pp. 567–575. Rodrick, G.E. & Ulrich, S.A., 1984. Microscopical studies on the hemocytes of bivalves and their phagocytic interaction with selected bacteria. Helgol. Meeresunters., 31, 167–176. Rosenberg, F.A. & Cutter, J., 1973. The role of cellulolytic bacteria in the digestive processes of the shipworm. In, Proc. 3rd Int. Congr. Marine Corrosion and Fouling, Northwestern University Press, Evanston, pp. 778–796. Rowse, A.J. & Fleet, G.H., 1984. Effects of water temperature and salinity on elimination of Salmonella charity and E. coli from Sydney rock oysters (Crassostrea commercialis). Appl. Environ. Microbiol., 48, 1061–1063. Ruddel, C.L., Dunlap, T., Okazaki, R.K. & Munn, R., 1978. The effect of selected basic dyes on the blood cells, in particular, the basophils, of the Pacific oyster, Crassostrea gigas. J. Invertebr. Pathol., 31, 313–323.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
349
Russell-Hunter, W.D., 1970. Aquatic Productivity. MacMillan, New York, 147 pp. Salton, M.R. J., 1957. The properties of lysozyme and its action on microorganisms. Bacteriol Rev., 215, 67–89. Samain, J.F., Cochard, J.C., Chevelot, L., Daniel, J.Y., Jeanthon, C., Le Coz, J. R., Marty, Y., Moal, J., Prieur, D. & Salaun, M., 1987. Effet de la qualité de 1’eau sur la croissance larvaire de Pecten maximus en écloserie: observations préliminaries. Haliotis, 16, 363–381. Sanders, H.L. & Hessler, R.R., 1969. Ecology of the deep sea benthos. Science, 163, 1419–1424. Scheltema, R.S., 1974. Biological interactions determining larval settlement of marine invertebrates. Thalassia Jugosl., 10, 263–296. Schubert, H., Shiewer, U. & Tschirner, E., 1989. Fluorescence characteristics of cyanobacteria (blue-green algae). J. Plankton Res., 11, 353–359. Schweimanns, M. & Felbeck, H., 1985. Significance of the occurrence of chemoautotrophic bacterial endosymbionts in Lucinid clams from Bermuda. Mar. Ecol. Prog. Ser., 24, 113–120. Seiderer, L.J., Davis, C.L., Robb, F.T. & Newell, R. C, 1984. Utilisation of bacteria as nitrogen resource by kelp-bed mussel, Choromytilus meridionalis. Mar. Ecol. Prog. Ser., 15, 109–116 Seiderer, L.J. & Newell, R.C., 1985. Relative significance of phytoplankton, bacteria and plant detritus as carbon and nitrogen resources for the kelp bed filter-feeder Choromytilus meridionalis. Mar. Ecol. Prog. Ser., 22, 127–139. Shear, C.L. & Gottlieb, M.S., 1980. Shellfish borne disease control in the United States. A commentary. Med. Hypoth., 6, 315–327. Sherr, B.F., Sherr, E.B. & Newell, S.Y., 1984. Abundance and productivity of heterotrophic nanoplankton in Georgia coastal waters. J. Plankton Res., 6, 195– 203. Shumway, S.D., Cucci, T.L., Newell, R.C. & Yentsch, C.M., 1985. Particle selection, ingestion and absorption in filter-feeding bivalves. J. Exp. Mar. Biol. Ecol., 91, 77–92. Sieburth, J., McN., Smetacek, V. & Jürgen, L., 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr., 23, 1256–1263. Sigerfoos, C.P., 1908. Natural history, organisation and late development of the Teredinidae, or shipworms. Bull. Bur. Fish., Wash., 37, 191–231. Slanetz, L.W., Bartley, C.H. & Stanley, K.W., 1968. Coliforms, fecal streptococci and Salmonella in seawater and shellfish. Health Lab. Sci., 5, 66–78. Sobsey, M.D., Hackney, C.A., Carrick, R.J., Beber, R. & Speck, M.L., 1980. Occurence of enteric bacteria and viruses in oysters. J. Food Prot., 43, 111–113. Sorokin, Y. L, 1971. Bacterial population as components of oceanic ecosystems. Mar. Biol., 11, 101–105. Sorokin, Y. L, 1978. Decomposition of organic matter and nutrient regeneration oxygenation. In, Marine Ecology, IV, Dynamics, edited by O. Kinnie, Chichester, Wiley, pp. 501–516. Sorokin, Y. L, 1981. Microheterotrophic organisms in marine ecosystems. In, Analysis of Marine Ecosystems, edited by H.R. Longhurst, Head Press, New York, pp. 293–342. Southward, E.C., 1986. Gill symbionts in thyasirids and other bivalve molluscs. J. Mar. Biol. Assoc. U.K., 66, 889–914. Soyer, J., Soyer-Gobillard, M.O., Thiriot-Quiévreux, C., Bouvy, M. & Cahet, C., 1987. Chemoautotrophic bacterial endosymbiosis in Spisula subtruncata (Bivalvia, Mactridae). Ultrastructure metabolic significance and evolutionary implications. Symbiosis, 3, 301–314. Spiro, B., Greenwood, P.R., Southward, A.J. & Dando, P.R., 1986. 13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutritional
350
D.PRIEUR ET AL.
importance of chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser., 28, 233–240. Spite, G.T., Brown, D.F. & Twedt, R.M., 1978. Isolation of an enteropathogenic kanagawa positive strain of V. paraheamolyticus from seafood implicated in an acute gastroenteritis. Appl. Environ. Microbiol., 35, 1226–1227. Srna, R.F. & Baggaley, A., 1976. Rate of excretion of ammonia by the hard clam Mercenaria mercenaria and the American Oyster, Crassostrea virginica. Mar. Biol., 36, 251–258. Stahl, D.A., Lane, D.J., Olsen, G.J. & Pace, N.R., 1984. Analysis of hydrothermal vent-associated symbionts by ribosomal RNA sequences. Science, 224, 409–411. Stephens, G.C., 1982. Dissolved organic material and the nutrition of marine bivalves. In, Proc. 2nd Int. Conf. on Aquaculture, Nutrition, Biochemical and Physiological Approaches to Shellfish Nutrition, edited by G.D. Druder et al., Louisiana State University Press, Delaware, pp. 338–357. Stevens, S.A., 1983. Ecology of intertidal oyster reefs: food, distribution and carbon nutrient flow. Ph.D. Thesis, Univ. Georgia, 1–195. Steward, M.G., 1979. Absorption of dissolved organic nutrients by marine invertebrates. Oceanogr. Mar. Biol. Annu. Rev., 17, 163–192. Stuart, V. & Klumpp, D.W., 1984. Evidence for food-resource partitioning by kelpbed filter feeders. Mar. Ecol. Prog. Ser., 16, 27–37. Stuart, V., Newell, R.C. & Lucas, M. L, 1982. Conversion of kelp debris and faecal material from the mussel Aulacomya ater by marine microorganisms. Mar. Ecol. Prog. Ser., 7, 47–57. Sugita, H., Tanaami, H., Kobashi, T. & Deguchi, Y., 1981. Bacterial flora of coastal bivalves. Bull. Jpn. Soc. Scient. Fish., 47, 655–661. Symons, J.L., 1921. Some bacterial organisms occurring in the clam (Mya arenaria) which may produce “blackening” in tins. Contrib. Can. Biol., 1, 3–14. Tanikawa, E., 1937. Bacteriological examination of oysters stored at low temperatures. Zentr. Bakteriol. Parasitol, 97, 133–147. Tenore, K.R., 1988. Nitrogen in benthic food chains. In, Nitrogen Cycling In Coastal Marine Environments, edited by T.H. Blackburn & J. Sorensen, John Wiley & Sons, Chichester, pp. 85–123. Tenore, K.R., Boyer, L.F., Cal. R.M., Corall, J., Garcia-Fernandez, C., Gonzalez, N., Gonzalez-Gurriaran, E., Hanson, R.B., Iglesias, J., Krom, M., Lopez-Jamar, E., McClain, J., Pamatmatt, M.M., Perez, A., Rhoads, D.C., de Santiago, G., Tietjen, J., Westrich, J. & Windom, H.L., 1982. Coastal upwelling in the Rias Bajas, NW Spain: contrasting the benthic regimes of the Rias de Arosa and de Muros. J. Mar. Res., 40, 701–772. Tenore, K.R. & Dunstan, W.M., 1973a. Comparison of rates of feeding and biodeposition of the American oyster, Crassostrea virginica Gmelin fed different species of phytoplankton. J. Exp. Mar. Biol. Ecol., 12, 19–26. Tenore, K.R. & Dunstan, W.M., 1973b. Comparison of feeding and biodeposition of three Bivalves at different food levels. Mar. Biol., 21, 190–195. Theede, H., 1981. Studies on the role of benthic animals of the western Baltic in the flow of energy and organic material. Kiel. Meeresforsch. (Sondh.), No. 5, 434– 444. Thomas, K.C. & Jones, A.M., 1971. Comparison of methods on estimating the number of E. coli in edible mussels and the relationship between the presence of Salmonella and E. coli. J. Appl. Bacteriol, 34, 717–725. Thompson, W.K. & Trenholm, D.A., 1971. The isolation of Vibrio parahaemolyticus and related halophilic bacteria from Canadian Atlantic shellfish. Can. J. Microbiol, 17, 545–549. Timoney, J.F. & Abston, A., 1984. Accumulation and elimination of E. coli and Salmonella typhimurium by hard clams in an in vitro system. Appl. Environ. Microb., 47, 986–988.
INTERACTIONS BETWEEN BIVALVE MOLLUSCS AND BACTERIA
351
Tison, D.L. & Seidler, R.J., 1983. Vibrio aestuarianus: a new species from estuarine waters and shellfish. Int. J. Syst. Bacteriol., 33, 699–702. Tripp, M.R., 1966. Hemagglutinin in the blood of the oyster Crassostrea virginica. J. Invertebr. Pathol, 8, 478–84. Tritar, S., 1987. Étude expérimentale du rôle du film bactérien dans l’initiation de la métamorphose des larves de bivalves. These. Doctorat, Université de Brest, 167 pp. Trollope, D.R., 1982. Faecal contamination of the common mussel. In, Source Book of Experiments for the Teaching of Microbiology, edited by P.Wardlaw, Academic Press, New York, pp. 531–539. Trollope, D.R., 1984. Use of molluscs to monitor bacteria in water. In, Microbiological Methods for Environmental Microbiology, Society for Applied Bacteriology, pp. 393–408. Trollope, D.R. & Al Salihi, S.B.S., 1984. Sewage derived bacteria monitored in a marine water column by means of captive mussels. Mar. Environ. Res., 12, 311–322. Trytek, R.E. & Allen, W.W., 1980. Synthesis of essential amino acids by bacterial symbionts in the gills of the shipworm Bankia setacea. Comp. Biochem. Physiol., 67A, 419–427. Tsuchiya, M. 1980. Biodeposit production by the mussel Mytilus edulis L. on rocky shores. J. Exp. Mar. Biol. Ecol, 47, 203–222. Tsuchiya, M., 1981. Biodeposit production and oxygen uptake by the Japanese common scallop Patinopecten yessoensis (Jay). Bull. Mar. Biol. Stn. Asamushi, Tohoku Univ., 17, 1–15. Tubiash, H.S., 1972. Bacterial pathogens associated with cultured bivalve mollusk larvae. In, Culture of Marine Invertebrate Animals, edited by W.L. Smith & M. H.Chanley, Plenum Publ. Co., New York, pp. 61–71. Tubiash, H.S., 1974. Single and continuous exposure of the adult American oyster, Crassostrea virginica, to marine vibrios. Can. J. Microbiol., 20, 513–517. Tubiash, H.S., Chanley, P.E. & Leifson, E., 1965. Bacillary necrosis, a disease of larval and juvenile bivalve mollusks. J. Bacteriol., 90, 1036–1044. Tubiash, H.S., Colwell, R.R. & Sakazaki, R., 1970. Marine vibrios associated with bacillary necrosis, a disease of larval and juvenile bivalve mollusks. J. Bacteriol., 103, 271–272. Tubiash, H.S., Otto, S.V. & Hugh, R., 1973. Cardiac edema associated with Vibrio anguillarum in the American oyster. Proc. Natl. Shellfish Assoc., 63, 39–42. Twedt, R.M., Madden, J.M., Hunt, J., Francis, D.W., Peeler, J.T., Duran, A.P., Hebert, W.O., McCay, S.G. & Roderick, C.N., 1981. Characterization of V. cholerae isolated from oysters. Appl. Environ, Microbiol., 41, 1475–1478. Valiela, I., 1984. Marine Ecological Processes. Springer-Verlag, New York, 250 pp. Van den Broek, M.J. M., Mossel, D.A.A. & Eggenkan, A.E., 1979. Occurrence of V. parahaemolyticus in Dutch mussel. Appl. Environ, Microbiol., 37, 438– 442. Vasconcelos, G.J. & Lee, J.S., 1972. Microbiol. flora of Pacific oysters (Crassostrea gigas) subjected to ultraviolet irradiated seawater. Appl. Microbiol., 23, 11–16. Vasta, G.R., 1982. A cell membrane-associated lectin of the oyster hemocytes. J. Invertebr. Pathol, 40, 367–377. Vasta, G.R., Cheng, T.C. & Marchalonis, J.J., 1984. A lectin of the hemocytes membrane of the oyster (Crassostrea virginica). Cell. Immunol, 88, 475–488). Vaughn, J.M. & Metcalf, T.G., 1975. Coliphages as indicators of enteric viruses in shellfish raising estuarine waters. Water Res., 9, 613–616. Verwey, J., 1954. On the ecology of distribution of cockle and mussel in the Dutch waddensea, their role in sedimentation and the source of their food supply. Arch. Néerl. Zool, 10, 171–239. Vetter, R.D., 1985. Elemental sulfur in the gills of three species of clams containing chemoautotrophic bacteria: a possible inorganic energy storage compound. Mar. Biol., 88, 33–2.
352
D.PRIEUR ET AL.
Walne, P.R., 1956. Experimental rearing of the larvae of Ostrea edulis L. in the laboratory. Fish. Invest., London Ser. II, 20, 1–23. Wangersky, P.J., 1977. The role of particulate matter in the productivity of surface waters. Helgol. Wiss. Meeresunters., 30, 546–564. Waterbury, J.B., Turner, R.D. & Calloway, C.B., 1983. A cellulolytic nitrogen-fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia, Teredinidae). Science, 221, 1401–1403. Weagant, S.D. & Kaysner, C.A., 1982. The incidence and seasonal distribution of Yersinia enterocolitica and Vibrio parahaemolyticus in a Puget sound commercial oyster bed. J. Shellfish Res., 2, 122–123. Weiner, R.M. & Colwell, R.R., 1982. Induction of settlement and metamorphisis in Crassostrea virginica by a melanin-synthesizing bacterium. Tech. Rep. Maryland Sea Grant Program 1124 H.J. College Park, Maryland 20742 (USA), Publ. No. UM-SG-TS-92–05, 44 pp. Weiner, R.M., Segall, A.M. & Colwell, R.R., 1985. Characterization of a marine bacterium associated with Crassostrea virginica (the eastern oyster). Appl. Environ. Microbiol, 49, 83–90. Whittenburry, R. & Dalton, H., 1981. The methylotrophic bacteria. In, The Prokaryotes, edited by M.P. Starr, Springer Verlag, Berlin, pp. 895–902. Wilkinson, C.R., 1984. Immunological evidence for the precambrian origin of bacterial symbioses in marine sponges. Proc. R. Soc. London, Ser. B, 230, 79–147. Wilson, J.H., 1980. Particle retention and selection by larvae and spat of Ostrea edulis in algal suspension. Mar. Biol., 57, 135–145. Wilson, R., Lieb, S., Roberts, A., Stryker, S., Janoweski, H., Gunn, R., Davis, B., Riddle, C.F., Barret, T., Morris, J.G. & Blake, P.A., 1981. Non 01 Vibrio cholerae gastroenteritis associated with eating raw oysters. Am. J. Epidemiol., 114, 293–298. Wittke, M. & Renwrantz, L., 1984. Quantification of cytotoxic hemocytes of Mytilus edulis using a cytotoxicity assay in agar. J. Invertebr. Pathol, 43, 248–253. Wojtowicz, M.B., 1972. Carbohydrases of the digestive gland and the crystalline style of the Atlantic deep-sea scallop (Placopecten magellanicus, Gmelin). Comp. Biochem. Physiol., 43A, 131–141. Wood, A.P. & Kelly, D.P., 1989. Methylotrophic and autotrophic bacteria isolated from lucinid and thyasirid bivalves containing symbiotic bacteria in their gills. J. Mar. Biol. Assoc. U.K., 69, 165–179. Wood, P.C., 1957. Factors affecting the pollution and self purification of molluscan shellfish. J. Cons., Cons. Int. Explor. Mer, 22, 202–208. Wood, P.C., 1975. Fish and shellfish hygiene. Lancet, Issue 7922, 1422 only. Wright, R.T., Coffin, R.B., Persing, C. & Pearson, D., 1982. Field and laboratory measurements of bivalve filtration of natural marine bacterioplankton. Limnol. Oceanogr., 27, 91–98. Yoovidhya, T. & Fleet, G.H., 1981. An evaluation of the Al MPN and the Anderson and Baird Parker Plate Count Methods for enumerating E. coli in the Sydney rock oyster. J. Appl. Bacteriol, 50, 519–528. Yoshino, T.P. & Tuan, T.L., 1985. Soluble mediators of cytolytic activity in hemocytes of the Asian clam, Corbicula fluminea. Dev. Comp. Immunol., 9, 515–522. ZoBell, C.E., 1935. The significance of marine bacteria in the fouling of submerged surfaces. J. Bacteriol., 29, 239, 251. ZoBell, C.E. & Feltham, C.B., 1937. Bacteria as food for certain marine invertebrates. J. Mar. Res., 1, 312–327.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 353–379 Margaret Barnes, Ed. Aberdeen University Press
THE FUNDAMENTALS OF INSEMINATION IN CIRRIPEDES WALTRAUD KLEPAL Institut für Zoologie der Universität Wien, Althanstraße 14, A-1090 Wien, Österreich
ABSTRACT Current knowledge of males in various stages of reduction and of the fundamentals of insemination in cirripedes is reviewed. Anatomical data (based on light and electron microscopy) as well as behavioural and theoretical aspects of reproduction are discussed. Interest focuses on the Cirripedia sensu stricto but Rhizocephala are also considered. Cirripedes are aberrant in having a penis which is not just a tube for the transfer of semen. It is a highly sensitive organ first involved in the search of the functional female, into whose mantle cavity the semen is then deposited. This process is called pseudo-copulation after which the penis degenerates in some species (Thoracica), while in others the male itself deteriorates (Thoracica, Acrothoracica). At the new breeding season the penis regenerates or new males become active, respectively. The cirrepede spermatozoon is unusual in having an elongate nucleus alongside the flagellum, a single mitochondrion, and a single centriole. An accessory droplet, species-specific in its structure, presumably assumes the function of multiple mitochondria in other spermatozoa. The question of whether hermaphroditism or gonochorism is the original type of reproduction in cirripedes is still a matter of discussion. Two possible pathways for the evolution of sexuality in cirripedes are discussed.
INTRODUCTION Adult Cirripedia are exclusively sessile Crustacea. They are considered to consist of three Orders: the parasitic Rhizocephala and the cirral setosefeeders Thoracica and Acrothoracica (Newman, 1982). Although it now appears that the Rhizocephala may not be Cirripedia in the strict sense (Newman, 1987; Høeg, in press) they will be considered here and notes on Ascothoracida, a probable sister group of cirripedes within the Maxillopoda (Grygier 1983, 1987c; Newman, 1987), will be included for comparison whenever appropriate. Although there are a number of papers on the sexuality of cirripedes (such as Darwin, 1873; Laloy, 1903; Smith & Weldon, 1920; Witschi, 1935; Callan, 1941; Barnes & Crisp, 1956; Ichikawa & Yanagimachi, 1958, 1960; Yanagimachi, 1961; Henry & McLaughlin, 1965, 1967; Tomlinson, 1966; Yanagimachi & Fujimaki, 1967; Walley, White & Brander, 1971; McLaughlin & Henry, 1972; Klepal, Barnes & Barnes, 1975, 1977; Klepal & Barnes, 1977; Walker, 1980; Crisp, 1983; Foster,
354
WALTRAUD KLEPAL
1983; Svane, 1986; Høeg, 1987) and a review of the comparative anatomy of the males (Klepal, 1987) there is no comprehensive study of the fundamentals of the sexual biology of the cirripedes. It is the aim of this review to fill this gap and to supplement it by some behavioural and theoretical aspects of reproduction. The following subjects will be considered: type of reproduction, pseudo-copulation, anatomy and morphology of the males, anatomy and function of the penis, fate of the penis after copulation, spermatozoa and prospects of evolution. In conclusion, directions for future research will be suggested.
TYPE OF REPRODUCTION Males, as distinct from females and/or hermaphrodites, are found in all three Orders of cirripedes: Acrothoracica, Thoracica and Rhizocephala. Whilst the Acrothoracica and Rhizocephala are strictly gonochoristic, the Thoracica are either hermaphrodites, hermaphrodites accompanied by complemental males, or gonochorists with dwarf males. The hermaphrodites are protandric and thus preadapted to the production of complemental males (Newman, 1980). The males in the Thoracica seem to develop from normal cyprids which are arrested in growth except for the male reproductive system which is well developed. A sequence of this progressive specialisation may be seen in Calantica and Scillaelepas (Newman, 1980). The subrostral peduncular scales of the hermaphrodites become enlarged as in Scillaelepas s.str. Specially formed scales are then incorporated into the capitulum as in Gruvelialepas, and the capitular subrostrum is developed as in Aurivillialepas. Finally, the male is transferred from the subrostral to the suprarostral position between the scutal plates as in Calantica. As this sequence proceeds, the males become more and more degenerate until they are merely bags of sperms attached in special pockets in the scuta, as in Acroscalpellum. Thus, the hermaphrodite supports the progenetic reduction of the male by providing it with protection. The Acrothoracica are burrowing cirripedes, previously thought to have evolved from the Lepadomorpha (Newman, Zullo & Withers, 1969; Tomlinson, 1969; Newman, 1982), but now considered to have evolved from a prethoracican ancestor (Newman, 1987). Their males are fixed to the outside of the female, usually close to the attachment disk or they are buried within a pocket in the mantle tissue of the female in the immediate area of the ovary (Tomlinson & Newman, 1960). Because the males are non-feeding they depend on larval food reserves. The supposedly most primitive Rhizocephala, the Chthamalophilidae, first thought to be self-fertilising hermaphrodites (Bocquet-Védrine, 1961) are now known to have separate sexes (Bocquet-Védrine & Bourdon, 1984). Among more advanced Rhizocephala, Lützen (1984) and Walker (1985) consider the European Sacculina carcini gonochoristic, although it was previously thought to be hermaphroditic (Bocquet-Védrine, 1972).
COPULATION In the Thoracica the spermatozoa are not deposited in structures associated with the terminal part of the female reproductive tract, but in the mantle cavity. Many people,
INSEMINATION IN CIRRIPEDES
355
therefore, prefer the term pseudo-copulation for the sperm transfer. It is often, however, referred to as copulation. Walley (1965) pointed out that “receptive” females have greatly swollen oviducal glands and their oocyte nuclei are in the metaphase of the first meiotic division. In “non-receptive” females the oviducal glands are less swollen and the oocyte nuclei are at interphase. Semen is deposited in the mantle cavity of the receptive female shortly before the eggs are laid. The oocytes enter a sac formed by the oviducal gland in which they are fertilised. Oviposition may be induced by the stimulatory action of the semen (Walley, 1965; Walley et al., 1971) of which a large quantity is produced at copulation. The first indication of copulation in Balanomorpha is penis activity. The cause of the initiation of this may be ascorbic acid (Collier, Ray & Wilson, 1956). All animals of a restricted population, e.g. on a single stone, are in a similar state and will often show copulatory activity at the same time. The stimulus to copulation may well be synchronised and entirely endogenous. At the time of copulation the penis, even in its relaxed state, is extremely long (Crisp & Patel, 1960; Klepal et al., 1975). Southward (1955) pointed out that some cirral activity normally precedes extrusion of the penis. An animal about to behave as a functional female will not show any “normal” cirral activity (Crisp & Southward, 1961). The operculum of the functional male is raised to a high level, thereby increasing the volume of the mantle cavity. The cirri are protruded and thrust further back against the carina than in a normal extension and the penis gives the appearance of being “unrolled” by high hydrostatic pressure. Subsequent searching movements over virtually 360 degrees in the horizontal plane and with considerable vertical movement is brought about by the activity of the muscles of the penis and pedicel with variations in the hydrostatic pressure allowing changes in extension. During the search for a functional female the penis is repeatedly bent downwards to touch the substratum in an apparent “testing” action. This searching appears to be random rather than immediately directed towards a functional female. Even when a second penis is accepted during copulation the second functional male still appears to locate the female already in copula by random searching activity. A functional female will remain with its opercular valves wide open, facilitating entry of the penis into its mantle cavity; this implies some recognition of the penis, presumably by the sensory structures on the lips of the opercular valves (Foster & Nott, 1969). The functional male, on the other hand, receives the stimulus, possibly caused by some product of the completely ripe ovary of the functional female, via the penis setae (Munn, Klepal & Barnes, 1974). Chemoreception is also suggested by multiple insemination of one individual (the acceptance of up to six penes has been seen), when other potentially functional females are present in large numbers. The animal in copula is particularly “attractive” (Barnes, Barnes & Klepal, 1977). Mutual copulation has never been observed (Barnes & Barnes, 1956)—an animal acting as a functional male is unable to accept the penis of a functional male. A single insertion of the penis may last 90 s. A maximum of 10 insertions taking place over 100 min has been observed but 6–8 insertions over 30–90 min are more common. The force required to expel the semen is obtained by the muscular activity of the walls of the vesiculae seminales. During the whole of the copulatory activity virtually all the semen of the functional male is transferred. This may amount to a considerable proportion of the total mass of the body at this time (Barnes, Barnes & Finlayson,
356
WALTRAUD KLEPAL
1963). Any given spermatozoon spends about 12 s passing through the penis (Barnes, Klepal & Munn, 1971; Barnes et al., 1977). When copulation is completed the penis is finally withdrawn and the functional male soon behaves normally—beating and closing at intervals (Barnes et al., 1977). The functional female remains with its valves raised for about 20 min during which time there are marked rocking movements of the valves which either remain open or closed and open at intervals, the cirri being still visible within the mantle cavity but never protruded. The animal then closes and remains so for 10–30 min after which spermatozoa are expelled via the mantle cavity current at intervals during a pumping beat. Normal cirral activity is at first impeded by the mass of coagulated semen sticking to the cirri. It may take 60 min before the cirri are completely free and capable of resuming a fully normal cirral beat. In Acrothoracica neither mating behaviour nor copulation has been observed but some species have males with a probiosciform penis which presumably functions in a similar way to the thoracican penis. In the Rhizocephala several patterns of sexual systems can be distinguished (see Høeg, in press). Either male cyprids settle on a juvenile female and metamorphose into trichogons (Høeg, 1987), which are implanted into a pair of receptacles in the female (as in the Peltogasteridae, Lernaeodiscidae, and Sacculinidae), or the male cyprid uses antennular penetration to implant spermatogonia into a juvenile female, where spermatogenesis takes place in a single receptacle (as in Clistosaccus) or within the ovary (as in Sylon). In other rhizocephalans spermatogenesis takes place in so-called “spermatogenic islands”.
ANATOMY AND MORPHOLOGY OF THE MALES The comparative anatomy of males in cirripedes has been dealt with in detail by Klepal (1987). Dwarf males (associated with females) and complemental males (associated with hermaphrodites) may be distinguished (Darwin 1851). Crisp (1983) introduced the term “apertural” male for potential hermaphrodites which stopped in their development at the protandric stage. Henry & McLaughlin (1965) found complemental males in the balanoid genus Solidobalanus. The males are degenerate, without a mouth. They have vestigial cirri and the typical cyprid antennules, while the reproductive organs are well developed. Since 1965 four species of Balanus s.l. have been shown to have complemental males: Conopea masignotus, C. galeatus, C. merilli, and C. calceolus (Henry & McLaughlin, 1967; McLaughlin & Henry, 1972). The external morphology of all balanoid males found so far is similar (Fig 1). C. calceolus differs in having separated scuto-tergal valves and raised opercular lips. The males have a penis-thorax, the setation of which varies. The more setae there are on the penis the more vestigial are the cirri. The degree of reduction varies in the males of the four balanoid species. A progressive degeneration in cirral structure and mouthparts may be traced from C. calceolus (Fig 1B) through C. masignotus (Fig 1C) to C. galeatus (Fig 1D), and C. merilli (Fig 1E). Usually the vesicula seminalis is paired. The testis is in most cases a diffuse bilobed structure.
INSEMINATION IN CIRRIPEDES
357
Fig 1. —Morphology of males in Balanomorpha (after McLaughlin & Henry, 1972). A, generalised male with a semi-globular basis, a narrow lateral band and the opercular surface with prominent scuta and terga and opercular lips. Scale bar=0.1 mm. B-E, the males of all species found so far have a penisthorax with setae; cirri and mouthparts are reduced to a variable degree. Scale bars=0.05 mm.
358
WALTRAUD KLEPAL
In Bathylasma corolliforme and B. alearum (Foster, 1983) small individuals acting as males are found on the opercular valves of hermaphrodites (see Fig 3D in Klepal, 1987). Their mouthparts, cirri, and penis are well developed as are the reproductive organs. A complemental male, looking like a small hermaphrodite, is also known in Chionelasmus darwini (Hui & Moyse, 1984; see Fig 3E in Klepal, 1987). Chelonibia patula (called Chelonobia patula by Crisp, 1983) is a protandric hermaphrodite, with so called “apertural” males (see Fig 3F,G in Klepal, 1987) that settle in the region of the opercula (Crisp, 1983). Probably ‘orificial’ males would have been a more appropriate term. As in all the males described above (except those of Conopea) the males in Chelonibia patula can feed and grow, and they retain the potential to develop into hermaphrodites. Individuals smaller than 2 mm are sexually immature and lack a penis. Those between 2 and 4 mm are protandric hermaphrodites. They lack an ovary but have testes, vesiculae seminales, and a developed penis, so they can presumably fertilise the hermaphrodites (see Fig 3H in Klepal, 1987). C. patula individuals with a basal diameter greater than 7 mm are simultaneous hermaphrodites. No separate males have yet been found in the Verrucomorpha. Within the Lepadomorpha there are many dwarf and complemental males. Pilsbry (1908) suggested that the characters of the males should be considered just as those of the females and the hermaphrodites for the elucidation of the systematic position of the various scalpelliform species. With reference to males Pilsbry distinguished four different genera by the plates, the degree of separation between capitulum and peduncle, the presence of a mouth and alimentary system, and the condition of the cirri. The genera Calantica and Smilium have the least reduced complemental males (Fig 2A). They look like juveniles with capitulum and peduncle well distinguished from each other. They have large, primary capitular plates, and a number of small latera so that altogether there may be 15 plates on the capitulum. The males of both genera have six pairs of articulated cirri, equally spaced, and at least in Calantica there is a long, extensible penis that may be beset with setae as in C. trispinosa. The penis is relatively longer than in a juvenile hermaphrodite of the same size, e.g. as described by Foster (1978) in C. villosa. The digestive tract is functional (Nilsson-Cantell, 1931). In general males are rare in Calantica, but up to 16 have been found between the scuta of large hermaphrodites of C. spinilatera (Foster, 1978). Euscalpellum has more degenerate males (Fig 2B). They are saclike, not distinctly divided into a capitulum and peduncle and they have only five plates, the scuta being larger than in Scalpellum. They have six pairs of articulated cirri and a mouth. Males of Scalpellum are very degenerate, sac-like without a peduncle or mouth, vestigial cirri or digestive tract (Fig 2C). The wall plates are absent and the scuta and terga are extremely small. Within the genus Scalpellum Pilsbry (1908) distinguishes three groups: (1) Group of S. scalpellum. (2) Group of S. californicum. (3) Group of S. stroemii. Many species of Scalpellum are known but even when males have been found they have often only been described very superficially (Table I; see also Table I in Klepal, 1987).
INSEMINATION IN CIRRIPEDES
359
Fig 2. —Males of Lepadomorpha at various stages of reduction. In Scalpellum peronii (A) (after Krüger, 1914) capitulum and peduncle are well separated. There are six large plates (sometimes additional smaller ones as in Calantica villosa) on the capitulum. In Euscalpellum rostratum (B) (after Pilsbry, 1908) capitulum and peduncle can hardly be distinguished. There are only five plates on the capitulum. Six pairs of cirri are developed in all species mentioned above. In Scalpellum wood-masoni (C) (after NilssonCantell, 1932) the male is sac-like, the capitulum and peduncle cannot be distinguished, there are only four rudimentary plates around the mantle opening and there are minute spines on the surface. Scale bars in B and D=0.5 mm. Scale bars of other species not shown in the original papers.
There are a number of species whose males have a distinct capitulum with six plates and a peduncle. They have six pairs of cirri with a space between the first pair and the rest. Their alimentary canal is open and functional and their penis is sometimes extensible (see * in Table I). In the males of many other species the capitulum and peduncle are not distinct and usually there are fewer than six plates on the capitulum. Often the plates are reduced in size. There may be six pairs (or less) of reduced cirri. The alimentary canal may be open and functional, but often there is no information or the information available is doubtful. A penis may be present; again the information is often doubtful (see † in Table I).
360
WALTRAUD KLEPAL
TABLE I Males of Scalpellum in various stages of reduction and some of the most important papers containing their description. Al.c.=Alimentary canal, Cap.=Capitulum, Ped.=Peduncle, cm=complemental male, dm=dwarf male, d=distinct, e=extensible, jd=just distinct, nd=not distinct, of=open and functioning, P=plates well developed, p=plates reduced, r=reduced, 1/2–6=space between first cirrus and the rest, +=present, — =no information,? =doubtful. For definition of * and † see text, pp. 359, 360.
S. rostratum has a special position in having a distinct capitulum and peduncle, an open and functional alimentary canal, and six pairs of cirri with a space between the first cirrus and the rest. There is also a penis but the plates on the capitulum are reduced in number and size and the caudal appendages are
INSEMINATION IN CIRRIPEDES
361
small. There need not be morphological concordance between the males and the hermaphrodites of two species: in S. squamuliferum and S. bengalense the hermaphrodites resemble each other closely, while the males of the same two species differ widely. It is apparent that much more information is needed before the evolutionary development and/or reduction of the males in this genus can be followed with any certainty. The anatomy of the males of some Iblidae is well known. Darwin (1851) described the anatomy of the males of Ibla cumingi and I. quadrivalvis. Stewart (1911) gave a general outline of the various organ systems of the males, without going into any detail. Klepal (1985) described the anatomy of the female and the male of I. cumingi and compared it with other species described so far. The muscular system in the male of I. cumingi is very complex (Fig 3). Several muscles in the male are identical with corresponding ones in the female. In general the muscles are smaller (less well developed) in the male than in the female. Both male and female have muscles not present in the other sex, e.g. those associated with the excretory system of the male. The cement cells of the male are arranged in a grape-like fashion and hence are very different from
Fig 3. —Dwarf male of Ibla cumingi. A, general view, scale bar=0.5 mm. B, schematic representation of the anatomy on the left. All organ systems are well developed. The muscles for the movement of the body and for the excretory system are complex. (Modified from Klepal, 1985).
362
WALTRAUD KLEPAL
those of the female. The genital system of the male of Ibla consists of two testes and two tube-shaped and coiled vesiculae seminales, the front parts of which are widened and may be fused into one pouch (as in I. cumingi). From there two ducti ejaculatorii lead to one genital pore in front of the anus on the ventral side of the animal. The size of the testes depends on the stage of maturity of the animal. In the Acrothoracica the males may only be a tenth the size of the females and they may be even smaller than the cypris larva from which they develop. Their size and morphology may change with age (Turquier, 1985). Within the Lithoglyptidae—supposedly the most primitive family of Acrothoracica (Tomlinson & Newman, 1960)—three types of males may be distinguished (see Figs 1, 2 in Klepal, 1987). (1)
(2)
(3)
Pear-shaped males with a penis homologous to the thorax of the cyprid. There are no special modifications of the larval antennae for attachment (e.g. Weltneria, Lithoglyptes). Polygonal males of variable shape with a well-developed annulated penis that may be contractile, as in Berndtia purpurea (Utinomi, 1961). The attachment organ is specialised: either a long and thin peduncle as in Kochlorine hamata or an orchid lobe as in K. floridana. Males without a penis as in K. bocqueti or K. ulula (Tomlinson, 1973).
The males may have a single testis and a single vesicula seminalis, or the presence of a penis may be doubtful, as in some species of Lithoglyptes. When a penis is developed it may lie in a channel which is supposedly a rudiment of the mantle cavity (e.g. in Weltneria exargilla) or in a specialised lacunar channel in the body tissue (e.g. in Berndtia purpurea, see Figs 1, 2 in Klepal, 1987). The males of Lithoglyptes are similar to those of Alcippe (=Trypetesa) and lack appendages. Information on the males of Cryptophialus and Australophialus (Fig 4) is very scarce. In several species there is no penis, in others the penis is formed late in life, others have a long penis and some a very short one (Tomlinson, 1960). In species with a well-developed penis, it may be several times the length of the male and annulated throughout its length. The sexes cannot be distinguished in the cyprid stage. When an apparently undifferentiated cypris larva of Trypetesa lateralis settles on a female the larval organs atrophy and it develops into a dwarf organism of very simple anatomy (Tomlinson, 1955). It loses its carapace, becomes rounder and gets progressively smaller and wrinkled, with greatly enlarged gonads. The mature male is variable in shape and is a highly specialised organism with a single testis and a single vesicula seminalis. It does not have a penis (Turquier, 1971). In the male, evolution of the genital apparatus is clearly accelerated; the male is able to reproduce about two weeks after hatching from the nauplius (the female matures only after several months). The males of the Rhizocephala are highly reduced. They develop from large eggs via large, non-feeding nauplii and cyprids. Species with a kentrogon (Peltogasteridae, Lernaeodiscidae, and Sacculinidae) form a post-cypris male larva, the trichogon (Høeg, 1987). This penetrates the mantle cavity of the female where it enters a receptacle; here spermatogenesis begins. The trichogon is the most reduced larval stage within the Crustacea. It is worm-shaped, without any sign of segmentation and does not have any appendages or internal organs. There
INSEMINATION IN CIRRIPEDES
363
Fig 4. —Males of Acrothoracica. The males are of variable shape and they are in different stages of reduction (even within one genus as in Trypetesa (=Alcippe). In Cryptophialus wainwrighti (A) the larval attenules and a long penis are obvious (after Tomlinson, 1969; scale bar not given in the original paper). Trypetesa habei (B) has antennules and a long penis sheath (after Tomlinson, 1969; scale bar=0.1 mm). The male of T. spinulosa (C) has prominent lobes for attachment and a long penis sheath (after Turquier, 1976; scale bar=0.2 mm). In T. nassarioides (D) antennules and genital apparatus are well developed (after Turquier, 1971; scale bar=0.2 mm). The male of Australophialus turbonis (E) has a pair of antennules and a long and coiled penis (after Tomlinson, 1969; scale bar=50 µm).
are only four cell-types in the male: the dorsolateral, the ventral epidermis, the inclusion cells and the postganglion cells. The implanted male is retained for the entire life span of the female parasite. In other species of rhizocephalans the development of the male is arrested in the cypris stage and they either adopt the “antennular penetration system” (e.g. in the Sylonidae and Clistosaccidae) or they give rise to “spermatogenic islands” (e.g. in the Chthamalophilidae) as described by Høeg (in press).
ANATOMY AND FUNCTION OF THE PENIS In many invertebrates and vertebrates the penis simply acts as a ductus for the transfer of semen, together with the secretions of auxiliary glands, during
364
WALTRAUD KLEPAL
copulation. In hermaphroditic balanoid barnacles immediate pre-copulatory activity is confined to the search for a functional female by the penis of a functional male and the acceptance of the penis prior to the transfer of semen. The penis consists of a pedicel and the penis proper. The pedicel arises between the paired sixth cirri. It consists of a basal and a distal part, which when fully developed, are set at an angle to each other. The pedicel is variously thickened by bands of chitin which may
Fig 5. —Thickened structures on the penis pedicel, a useful taxonomic character. In Verruca stroemia a true pedicel is absent. In Lepas fascicularis no distinct structures other than a slight thickening corresponding to the girdle can be recognised. In Lithotrya dorsalis there is an indistinct girdle and only just an indication of lateral processes. From the girdle weakly developed, broad, upwardly directed processes arise which may correspond to the carinal processes. In Pollicipes polymerus the girdle is incomplete and the shield and lateral processes are developed. There are no carinal processes. In Chthamalus stellatus the girdle and lateral processes are well developed. When seen in lateral view they form a distinct, continuous, S-shaped curve. Balanus balanus has very short lateral processes, but well defined lateral areas; a horn, which may be an advanced character, is well developed. In Semibalanus balanoides the girdle is thin carinally, the lateral processes are short, and the lateral area and shield are well developed (after Barnes & Klepal, 1971).
INSEMINATION IN CIRRIPEDES
365
Fig 6. —Schematic representation of penis of Balanus balanus. A, longitudinal section showing longitudinal muscles attaching at basis of each annulation. Strands of connective tissue traverse the lacunae near the tip. Circular muscle bands surround gland cells near the tip of the penis. B, cross section through penis proper showing arrangement of logitudinal muscles, nerves and lacunae. C, pedicel and part of penis cut open to show complex musculature inserting on thickened exoskeleton (e.g. girdle and shield). The ductus ejaculatorius is surrounded by connective tissue. Four strands of longitudinal muscles, four nerves and four lacunae are seen in the penis proper (after Klepal et al., 1972).
be used in taxonomy (Barnes & Klepal, 1971). The Balanomorphoidea show the most complex pedicel structures (Fig 5). The thickened parts in their most complete form consist of the girdle, two lateral processes, an upward projecting process, two carinal processes, and the shield. The extent of the thickening varies with size. The complex musculature of the pedicel and the longitudinal muscles of the penis proper (Fig 6) allow the extended penis to explore a considerable area around the functional male. The pedicel is supplied with a series of paired muscles, which run from the carinal processes downwards into the body (Fig 6). Longitudinal muscles are a conspicuous feature of the penis proper and their arrangement, and the presence and extension of the lacunae, depend on the size of the animal and also on the size of the penis (Klepal, Barnes & Munn, 1972). In small, but mature Semibalanus balanoides and Balanus balanus there are four groups of longitudinal muscles basally in the penis (Fig 6), surrounded by connective tissue and the lacunae are small. More distally there are eight groups of muscles, which are arranged peripherally near the tip. Here the lacunae are larger. The longitudinal muscles of the penis are attached proximally within the pedicel and distally to the exoskeleton at the bottoms of the annulations. In the
366
WALTRAUD KLEPAL
pedicel there are paired nerves which give rise to four in the penis proper and these correspond to the four groups of radially arranged setae (Fig 6), which are believed to be mechano- and chemosensory. There may be up to 12 setae in each group. Three to four dendrites enter each seta. Prior to copulation the mature penis of Semibalanus balanoides has subterminal setae that are somewhat longer than the terminal setae. At this stage the most proximal setae, each relatively thick and short, may only be present in groups of two or three. The penis is covered by a chitinous exoskeleton about 1.3 µm thick. Under the action of turgor pressure the articulated form allows an extension during searching activity and copulation of up to three to four times the resting length. At the tip of the penis there are multicellular epidermal glands opening to the exterior and surrounded by circular muscle bands. The mature, relaxed penis is extremely long relative to body size and lies rostrally in front of the cirri on one side and then, curls carinally behind all the cirri, and comes to lie along the surface of the prosoma. Prior to copulation and with the body raised in the mantle cavity, the action of blood pressure unrolls the penis. At the same time, contraction of the muscles of the pedicel will rotate the penis carinally and together with the relaxation of the appropriate longitudinal muscles allow the penis to turn upon itself and pass between the sixth cirri to project carinally. This is the posture before the initiation of the searching movements. Data on the morphology of the penis of Acrothoracica are scarce. The following results were collected by Tomlinson (1969). The penis is only developed in mature individuals. It is of different length in the various species and its function is not always clear. In Lithoglyptes indicus the penis is very long. It must be extended to the outside through the opening left in the mantle and it must have enormous capability of control. In some species there is only a penis sheath but no penis, as in Trypetesa habei (Fig 4B). The penis may be annulated as in Kochlorine floridana, and there seems to be a penis retractor muscle connected to one of three lobes projecting from the main body of the male. In Cryptophialus newmani, on the other hand, the penis does not show much annulation but it seems to have a chitinous tip. In the Rhizocephala a whole male organism, which is reduced to a “gonad”, is accommodated within the receptacles, and is nourished and controlled by the female (Høeg, in press).
FATE OF PENIS AFTER COPULATION Normal development of the penis of the Thoracica seems to be under the control of an androgen secreted by the gonad and is inhibited by light period and temperature (Barnes & Stone, 1972). It is also possible that both gonad and penis development are stimulated by a common hormone. In Semibalanus balanoides subsequent to copulation the vesiculae seminales and the testes regress and the penis tissue is apparently not renewed; this may be ascribed to the absence of such a hormone and may result in the penis being lost. The penis shrinks and normal turgor pressure is lost. The tissues of the penis distal to the pedicel degenerate. The connective tissue cells within the pedicel form a condensed transverse layer. Many of the cells within this layer undergo division and the layer increases in
INSEMINATION IN CIRRIPEDES
367
thickness, with the cells embedded among fibres and orientated parallel to the direction of stress (Le Gross Clark, 1971; Klepal, Barnes & Barnes, 1975). The strands of the condensed layer eventually separate into two layers with structureless material in between; the separation then extends across the whole penis. The proximal part seals the pedicel, while the distal part of the fibrous layer is contained in the exuvia at the base of the degenerate penis tissue. The terminal cells become continuous with the new epithelium and so enclose the whole primordium. The cells in the remaining “stump” de-differentiate to form the penis primordium. At the next ecdysis the pedicle exuvia is lost and some remains of the fibrous layer give the end of the exuvia a thickened appearance (Fig 7). When the penis is only partially lost and exuvia contains only part of the penis tissue, both the remainder of the penis and the exuvia are annulated. Degeneration is causally related to the extreme distension of the penis during copulation and proceeds more rapidly at the tip (Fig 7). Histologically, at the light microscope level, connective tissue cells not in contact with specific organs tend to degenerate first. The cytoplasm of the cells becomes reduced to a thin layer surrounding the nucleus and the fibrous membranes of this tissue break into small pieces. The cells lose their stainability and ultimately many of them disappear. The basement membrane of the ductus ejaculatorius becomes particularly distinct in the degenerating penis. The longitudinal muscles nearest to the ductus disappear first. Later the outer
Fig 7. —Stages of penis degeneration in Semibalanus balanoides. A, degenerate tissue fills the whole of the annulated part of the penis and there is dedifferentiated tissue in the pedicel. When the exuvia is shed, remains of degenerating tissue may be left on the pedicel as seen in B or the degenerating tissue is given off completely as seen in C. D, alternatively, the exuvia may contain a variable amount of degenerate tissue, which appears darkened at the tip. On the body a “part-penis” remains attached to the animal. A, B, and C may be successive stages. The alternative is A followed by D and C. (After Klepal et al., 1975).
368
WALTRAUD KLEPAL
muscles break away from their attachments to the exoskeleton. The muscles first lose their striations and then their individual fibres are lost (Klepal et al., 1972). Eventually the muscle bands break up into structureless blocks. The sheaths of the longitudinal nerves are lost, and sometimes they break up longitudinally. The whole nerve bundle loses its structure and forms a homogeneous mass, which does not stain. The epithelial cells are the last to degenerate. The plasma membranes break down, so that in places the exoskeleton appears to be underlain by a thin layer of plasma to which any remaining nuclei give a beaded appearance (Klepal et al., 1975). There is a slight possibility that the epidermal cells have simply shrunk. To verify one or the other alternative TEM investigations are necessary. Animals which copulate early are the first to lose their penis. This is true no matter whether the time difference arises from geographical distribution (Barnes & Barnes, unpubl.), from different levels on the shore (Crisp & Patel, 1960) or from different treatments of experimental animals. The period of reproductive anecdysis may be shortened by feeding but the penis, in part or whole, is still lost at the first ecdysis after copulation. It is possible that copulation itself may, by some feedback process, inhibit the production of sex hormones. Regeneration of the penis depends on a stimulus from the new testis. In S. balanoides the penis is regenerated each year. Some regeneration also takes place in Balanus balanus. Development is at first slow, followed by a rapid increase in length during the summer and autumn. The development of the penis throughout a population may be variable. With successive ecdyses the penis lengthens and reaches its maximum length at the time of copulation (Barnes & Stone, 1972). The penis primordium left after the loss of the degenerated penis contains a uniform mass of mesenchyme cells (Fig 8A). The exoskeleton is lined by epidermis which, as seen by light microscopy, lacks a basement membrane at this stage. Striated, thickened areas of chitin are evident over what will become the pedicel (Fig 8B-D). As the pedicel takes on its characteristic form these areas become thicker centrally and processes become apparent. The penis proper lengthens, assumes the characteristic angle to the pedicel, and becomes annulated. At an early stage combs are present on the pedicel and it may carry a pair of setae on the upper surface as in Semibalanus balanoides (Klepal & Barnes, 1974). The organisation and development of the tissues is first seen within the pedicel and then extends distally into the penis (Klepal & Barnes, 1974). Within the pedicel the ductus ejaculatorius differentiates. It is lined by epithelium and is surrounded by connective tissue fibres. The myoblasts of the longitudinal muscles dedifferentiate and become attached to the cuticle by fibres of connective tissue. Paired nerves are present within the pedicel and the outer epithelium now has a welldefined basement membrane. The penis becomes annulated and the most distal part still contains some mesenchyme. Small setae are present on the annulations. The lacunae, which in early stages of development run for a considerable length of the penis, later tend to form ramifying channels. The outer, upper longitudinal muscles are the first to become well defined. Then other longitudinal muscles are formed and these increase in number and size until they are disposed as seen in sections of the mature penis. With growth and with an increasing number of annulations more setae are formed. The setae increase in length but their most marked increase in size takes place at the same time as the penis length increases.
INSEMINATION IN CIRRIPEDES
369
Fig 8. —Schematic representation of penis regeneration in Semibalanus balanoides. A, penis primordium containing mesenchyme, showing a space which will become the ductus ejaculatorius. B, on the outside of the primordium lateral thickenings appear as separate parts. C, the separate parts of the thickenings fuse and they become larger. Two setae are characteristic on the pedicel of this species. D, the penis proper begins to grow and assumes the angle of the mature penis to the pedicel. The exoskeleton invaginates to form the terminal part of the ductus. E, the typical thickenings of the pedicel are formed, the two setae have disappeared, the penis proper is annulated. (After Klepal & Barnes, 1974).
Nothing is known about the fate of the penis after copulation in the Acrothoracica.
SPERMATOZOA The cirripede spermatozoon is filiform, motile and flagellate. Its diameter is about 0.5 µm at the widest point and the length varies between 20 and 100 µm, depending on the species. Its fine structure has been investigated by several workers (Fig 9); results of more recent work were not available at the time of writing this review. Each spermatozoon consists of an acrosomal region, the axoneme, the nucleus, which is kidney-shaped in cross section, alongside three quarters of the axoneme and a single mitochondrion just behind the nucleus. The acrosome of all cirripede spermatozoa so far investigated by electron microscopy is conical (Fig 9) (e.g. of Pollicipes cornucopia, Balanus perforates, B. balanus,
370
WALTRAUD KLEPAL
Semibalanus balanoides, and Trypetesa (=Alcippe) nassarioides). A collar is attached to the base of the acrosome and the anterior end of the axial filament complex. It sheathes the anterior part of the axoneme. The axoneme itself has the typical (9×2)+2 structure. The central microtubules arise just short of the disk portion of the collar and terminate just before the outer doublets. The cristae of the mitochondrion may appear tubular as in Semibalanus balanoides (Munn & Barnes, 1970), which is unusual in spermatozoa. The single centriole present in Balanus perforatus carries the flagellum and is situated under the acrosome from which it is separated by a thin nuclear disk (Bocquet-Védrine & Pochon-Masson, 1969). The proximal centriole is lost during spermatogenesis and is never found in the spermatozoon. There is an accessory droplet behind
Fig 9. —Schematic representation of the cirripede spermatozoon. A, longitudinal section through anterior end of spermatozoon showing the conical acrosome, the longitudinal nucleus, the disk separating the acrosome from the nucleus and the flagellum (after Turquier & Pochon-Masson, 1969). B, cross section showing nucleus, flagellum, and accessory droplet with cisternae and rods (after Klepal, 1985). C, rnature filiform spermatozoon as seen at the light microscope level (after Barnes, Klepal & Munn, 1971). D, longitudinal section of developing spermatozoon with acrosome, nucleus, accessory droplet, and a single mitochondrion (after Pochon-Mason, Bocquet-Védrine & Turquier, 1970).
INSEMINATION IN CIRRIPEDES
371
and to the side of the centriolar complex during most of the development of the spermatozoon. Its form varies somewhat from species to species and depends on the stage of development (Barnes, Klepal & Munn, 1971). It seems that its size and situation can be used as a basis for cirripedian taxonomic identification (Azevedo & Corral, 1982). Its formation begins in the early spermatid as a vesicle on the concave side of the nucleus (Azevedo & Corral, 1982). At this stage it is a pro-accessory droplet containing a light matrix with a central, longitudinal dense core. The centre of the droplet is refringent under phase contrast (Barnes et al., 1971). There is paracristalline material of variable shape in the accessory droplet matrix (Bocquet-Védrine & Pochon-Masson, 1969; Azevedo & Corral, 1982). In later spermatids the accessory droplet attains its maximum length, the matrix becomes denser and thinner and there is rarely any refringent material. Bocquet-Védrine & Pochon-Masson (1969) showed that in the Balanomorpha this droplet is not just a cytoplasmic relict but a very specialised inclusion variously transformed during spermiogenesis. Changes can be quite abrupt (Barnes et al., 1971) or gradual (Bocquet-Védrine & Pochon-Masson, 1969). The droplet, ovoid in most species so far investigated, seems to shrink from anterior to posterior and then to collapse. In Semibalanus balanoides, Balanus balanus, B. perforatus, B. crenatus, B. eburneus, B. amphitrite amphitrite, Chthamalus stellatus, and Elminius modestus this results in a ‘grey’ droplet (as observed under the light microscope) with no refringent centre on an otherwise completely filiform spermatozoon, which then often swims away. In Verruca stroemia the highly refringent centre may remain in an ovoid or ellipsoidal droplet even when the latter has turned grey. In this species the centre may separate into two or three parts. After the change, the axial complex and refringent crystalloid corpuscle (probably protein) persist while osmophilic (presumably lipoprotein) material is lost. The droplet may serve as a metabolic substrate during development and/or contain essential enzymes or reserve materials during the later stages of spermiogenesis and storage in the vesiculae seminales. Motility in cirripede spermatozoa is largely a function of the physiological state of the gamete and is not determined by physical characteristics such as the size of the droplet. The accessory droplet may possibly take the place of the chondriome in providing the energy necessary for the penetration of the ova (Barnes et al., 1971). The accessory droplet of Ibla (Klepal, 1985) is reminiscent of the “Nebenkern” of the spermatids of other crustaceans and insects, although the resemblance to a mitochondrion is only superficial (Szöllösi, 1975). So far no “Nebenkern” was found in any cirripede spermatozoon. Presumably the spermatozoon is only completely mature when it assumes a filiform appearance (Fig 9C), which never occurs in the vesicula seminalis. Spermatozoa with accessory droplets were rarely motile. The spermatozoa mostly get their accessory droplet in the testis before they pass into the vesiculae seminales. Spermatozoa with accessory droplets show vibratory movements whereas marked translatory movements have only rarely been observed. The velocity of the translatory movement increases nearer the time of fertilization; e.g. if it is 30 µm·s -1 initially it may be 70 µm·s -1 eventually. In Balanus balanus the velocity of filiform spermatozoa is 100 µm·s -1 on average (Barnes et al., 1971). From the pore size in the oviducal sac (diameter about 0.5 µm) and the diameter of the widest part of the mature, filiform
372
WALTRAUD KLEPAL
spermatozoon (about 0.4 µm) it is evident that the accessory droplets of the spermatozoa (diameter about 1.0 µm) must be lost before they can pass through the pores of the oviducal sac. Thus, any function of the droplet must be sought in the earlier stages of maturation of the spermatozoon. If the number of sperm cells that enter a sac of about 1.5 mm diameter is calculated and if one assumes that there are pores on 90% of the sac surface, there will be about 276 sperm cells available per ovum (Klepal, Barnes & Barnes, 1977). There is some evidence that the spermatozoa enter the sac before the oocytes do. Indeed sometimes sacs may be found, white and full of spermatozoa, with no eggs inside (M. Barnes, pers. comm.; Klepal et al., 1977). Another suggestion (Walley, 1965) is that secretory material is released into the lumen of the oviducal glands of Semibalanus species before the ovisacs begin to form. As each ovisac distends with eggs the secretion is likely to be forced out through the pores in the ovisac wall. Thus it may attract motile sperm and aid them to locate pores. Walker (1980) agreed with Walley (1965) and suggested that the pores in the ovisac wall become enlarged when the ovisac contains relatively few eggs. This should ease passage of the sperm cells through the wall. Then the pressure of the incoming eggs and secretions stretch the ovisac wall and supposedly close the pores. Spermatozoa of S. balanoides are activated in the mantle cavity by oviducal gland fluid (Walley, White & Brander, 1971) and remain active for only 5 to 6 min (Walker, 1977a,b). Turquier & Pochon-Masson (1969) investigated the spermatozoa of the acrothoracican Trypetesa nassaroides. These closely resemble those of the Thoracica. There is only one centriole in the mature spermatozoon. The flagellum has the (9×2)+2 structure but there is a rigid formation on it which may reduce or weaken the flagellar movement. This “structure” may be a site of important metabolic activity. The mitochondrial apparatus is reduced. Spermatogenesis in rhizocephalans is cyclic within the receptacles and synchronised with oogenesis (Høeg, in press).
PROSPECTS OF EVOLUTION Dioecy (separate sexes) is characteristic of burrowing cirripedes (Tomlinson, 1953, 1969) and the parasitic cirripedes (Newman, 1982). In the Thoracica hermaphroditism is the rule. There are, however, a few cases of androdioecy (hermaphrodites with complemental males, see Charnov, 1987) and some dioecious species (females with dwarf males). In the Cirripedia reproductive success depends on the distribution and the gregariousness of both sexes. This may take the form of individuals being hermaphrodites and settling close together so that cross-fertilisation is ensured. The other possible way of ensuring reproduction is gonochorism with the males settling close to or on the females. Originally males and females were presumably of equal size (Foster, 1983). It is well known in cirripedes that individuals settle on each other (e.g. Klepal, 1971). Therefore males presumably soon (in evolutionary terms) began to settle on females. When males settled near to the mantle opening of the female they became reduced in size. At the same time the energy necessary to maintain a large body was saved. This condition is found in some species of Scalpellum.
INSEMINATION IN CIRRIPEDES
373
Fertilisation is even easier when the male moves inside the mantle cavity of the female and such a move causes major changes of the male. Valve plates on the capitulum and plates or spines on the peduncle are no longer necessary for the protection of the male and may even be disturbing to the female. There is no room for the male to use a cirral net, so the male cirri become reduced. As a consequence, the mode of feeding has to change followed by reduction of the thorax; the penis may also disappear. This stage of development of a reduced male is seen in Ibla cumingi and I. quadrivalvis, where the male genital opening can be brought into direct contact with the oviducal sac of the female. Therefore this stage of development is especially favourable for fertilisation. The next step is a further reduction of the size of the male with a reduction of the digestive tract. The male must then depend on reserve material within its body and is thus short-lived. This stage of development may be represented in the male of I. idiotica (Batham, 1945). A further step and an alternative to the short-lived male is the development of absorptive processes and thus endoparasitism within the mantle cavity of the female, as seen in the Ascothoracida (Vaghin, 1946). Male subordination could be cryptogonochorism (Ghiselin, 1969) with a hyperparasitic larval male. The contents of the male cyprid are released into the female where the male cells develop into spermatozoa (Ichikawa & Yanagimachi, 1958, 1960). The functioning of the implanted male gonad is controlled by the female (Bresciani & Lützen, 1972), simulating a truly hermaphroditic condition. This ‘pseudo-hermaphrodite’ may then become a true hermaphrodite. Occasionally males remain associated with the latter as in I. quadrivalvis. The other hypothetical pathway of the development of sexual systems could have begun with sessile protandric hermaphrodites. If in a hermaphrodite the development of the female gonad were retarded, pure males could develop besides hermaphrodites; this is the case in I. quadrivalvis. In a hermaphrodite with a complemental male the male gonad is reduced (Darwin, 1854), and further reduction of the male gonad and the secondary male organs could result in a pure female and a gonochoristic condition, as in I. cumingi. This tendency towards reduction of the male ‘part’ in a hermaphrodite is also seen in the balanomorph barnacle Semibalanus balanoides, which loses its penis after each reproductive season (Klepal, Barnes & Barnes, 1975). The male reproductive organs are developed anew for each “breeding season”. Although there does not seem to be any correlation between the occurrence of dwarf or complemental males in cirripedes and the macrohabitat, Crisp (1983) came to the conclusion that the development of the complemental males could be induced by conditions in the microhabitat. An attached and/or isolated species is more successful when it is hermaphroditic than when it is gonochoristic. Some hermaphroditic barnacles are thought to be facultatively capable of self-fertilisation (Barnes & Crisp, 1956), although no barnacle is known to be a usual “selfer” (Charnov, 1987). Biochemical and genetic studies also suggest that ‘selfing’ is rare (Dando, 1987). Self-fertilisation is useful where the population densities are low (Tomlinson, 1966). In the case of scarce mates, sperm production by hermaphrodites will be small (Charnov, 1987). Thus, in the deep sea and on noncontiguous substrata it benefits the large individuals to have small males present (Ghiselin, 1969; Newman, 1980; Crisp, 1983). Each individual is thus
374
WALTRAUD KLEPAL
capable of initiating a new colony. Because inbred offspring show low fitness there is selection for out-crossing (Maynard-Smith, 1978). Hermaphrodites with complemental males have the advantage of self-fertilisation and/or cross fertilisation with their complemental males. Dwarf males and complemental males which are offspring of different individuals than those in whose mantle cavity they settle entail great advantage for the species, and they may allow an escape from self-fertilisation (Charnov, 1987). If several males successfully inseminate a female, gene flow is even further enhanced.
CONCLUSIONS AND DIRECTIONS OF FUTURE RESEARCH The cirripedes are outstanding in having manifold reproductive systems. This is partly due to the Rhizocephala still belonging to the cirripedes, although there is an increasing tendency to separate that Order from the Cirripedia (Newman, 1982). It may be reasonable to consider the Rhizocephala a sister group to the Cirripedia sensu stricto (Høeg, pers. comm.). This is suggested by the development of the kentrogon from the oral cone and by an analysis of larval characters. A free-living urcirripede, an ascothoracid-like form may have given rise to the Rhizocephala and to the Thoracica (Newman, 1982). The Cirripedia Thoracica have a complex penis which is responsible for finding a functional female, apart from its usual function of the transfer of semen. After copulation the penis degenerates in some species and regenerates again for the next breeding season. More information is still needed on the anatomy, function, and fate of the penis after copulation in the Acrothoracica. The spermatozoon of cirripedes is unusual in having an elongate nucleus alongside the flagellum, a single mitochondrion, and a single centriole. An accessory droplet, presumably species-specific, takes the function of mitochondria in other spermatozoa. Further investigations, which may already be underway, on spermatogenesis and spermiogenesis of several cirrepede species would add to a better understanding of the phylogenetic relationship of the species within the Acrothoracica, Thoracica, and Rhizocephala and between the three Orders. It was mainly on the basis of the structure of the spermatozoa that the Ascothoracida was separated from the Cirripedia and on that and other grounds is now considered a superorder co-ordinate with the Cirripedia within the Maxillopoda (Grygier, 1987a,c). The spermatozoa of the Ascothoracida differ from those of the Cirripedia in having a flagellum posterior to the elongated head and midpiece (Grygier 1981, 1982). At least some species have several mitochondria in the midpiece. By their prehensile first and reduced second antenna, a bivalved carapace, and the position of the genital apertures, the Ascothoracida is, however, closer to the Cirripedia or to the Cirripedia + Facetotecta (Grygier, 1987c) than to any other maxillopodan group (Newman, 1982). The question of whether hermaphroditism or gonochorism is the original type of reproduction in cirripedes is still a matter of discussion. Hermaphroditism, hermaphroditism with complemental males and gonochorism are common. The males are usually considerably smaller than the females or hermaphrodites. Most Ascothoracida are thought to have dwarf or complemental males with a long, but
INSEMINATION IN CIRRIPEDES
375
not very extensible penis (Moyse, 1983). Grygier (1987b) states that most ascothoracid species seem to have separate sexes from the start of ontogeny. A comprehensive study on the comparative anatomy of the cirripede males will provide further insight into the different stages of their reduction. At the same time it may be possible to answer the question of how sexuality evolved within the cirripedes, and (by making appropriate comparisons with their males) in the closely related ascothoracids. Thus, by examining the reproductive system of cirripedes more closely insight into a number of general biological problems may be gained.
ACKNOWLEDGEMENTS Thanks are due to Dr M.Barnes and Dr J.Høeg for helpful suggestions during the preparation of the final version of the manuscript, and to S. Neulinger, who made the drawings. The efforts of especially one anonymous referee on an early version of the manuscript are gratefully acknowledged. Part of this work was supported by the Projekt P7438-BIO des Fonds zur Förderung der wissenschaftlichen Forschung in Österreich.
REFERENCES Annandale, N., 1910. The Indian barnacles of the subgenus Smilium with remarks of the classification of the genus Scalpellum. Rec. Ind. Mus., 5–6: 145–155. Azevedo, C. & Corral, L., 1982. Ultrastructural study of spermatozoon and spermiogenesis of Pollicipes cornucopia (Crustacea; Cirripedia), with special reference to nucleus maturation. J. Submicrosc. Cytol., 14, 641–654. Barnes, H. & Barnes, M., 1956. The formation of the egg mass in Balanus balanoides (L.). Arch. Soc. ‘Vanamo’, 11, 11–16. Barnes, H., Barnes, M. & Finlayson, D.M., 1963. The seasonal changes in body weight, biochemical composition, and oxygen uptake of two common boreoarctic cirripedes, Balanus balanoides and B. balanus. J. Mar. Biol. Assoc. U.K., 43, 185–211. Barnes, H., Barnes, M. & Klepal, W., 1977. Studies on the reproduction of cirripedes. I. Introduction: copulation, release of oocytes, and formation of the egg lamellae. J. Exp. Mar. Biol. Ecol., 27, 195–218. Barnes, H. & Crisp, D.J., 1956. Evidence of self-fertilization in certain species of barnacles. J. Mar. Biol. Assoc. U.K., 35, 631–639. Barnes, H. & Klepal, W., 1971. The structure of the pedicel of the penis in cirripedes and its relation to other taxonomic characters. J. Exp. Mar. Biol. Ecol., 7, 71– 94. Barnes, H., Klepal, W. & Munn, E.A., 1971. Observations on the form and changes in the accessory droplet and motility of the spermatozoa of some cirripedes. J. Exp. Mar. Biol. Ecol., 7, 173–196. Barnes, H. & Stone, R.L., 1972. Suppression of penis development in Balanus balanoides (L.). J. Exp. Mar. Biol. Ecol., 9, 303–309. Batham, E.J., 1945. Description of female, male and larval forms of a tiny stalked barnacle, Ibla idiotica n. sp. Trans. R. Soc. N.Z., 75, 347–356. Bocquet-Védrine, J., 1961. Monographic de Chthamalophilus delagei J. BocquetVédrine, Rhizocéphale parasite de Chthamalus stellatus (Poli.). Cah. Biol. Mar., 2, 455–593.
376
WALTRAUD KLEPAL
Bocquet-Védrine, J., 1971. Redescription du cirripede pédonculé Calantica calyculus (Aurivillius) et analyse de ses rapports avec Scalpellum pilsbryi Gruvel. Arch. Zool. Exp. Gén., 112, 761–770. Bocquet-Védrine, J., 1972. Les Rhizocéphales. Cah. Biol. Mar., 13, 615–626. Bocquet-Védrine, J. & Bourdon, R., 1984. Cryptogaster cumacei n. gen., n. sp., premier rhizocéphale parasite d’un cumacé. Crustaceana 46, 261–270. Bocquet-Védrine, J. & Pochon-Masson, J., 1969. Cytodifférenciation d’une vésicule de sécrétion au cours de la spermiogenèse chez Balanus perforatus Brug. (Crustacé Cirripède). Arch Zool. Exp. Gén., 110, 595–616. Bresciani, J. & Lützen, J., 1972. The sexuality of Aphanodomus (parasitic copepod) and the phenomenon of cryptogonochorism. Vidensk. Medd. Dan. Naturhist. For en. Khobenhavn, 135, 7–20. Callan, H.G., 1941. Determination of sex in Scalpellum. Nature (London), 148, 258only. Charnov, E.L., 1987. Sexuality and hermaphroditism in barnacles: a natural selection approach. In, Barnacle Biology. Crustacean Issues 5, edited by A.J. Southward, A.A. Balkema, Rotterdam, pp. 89–103. Collier, A., Ray, S. & Wilson, W.B., 1956. Some effects of specific organic compounds on marine organisms. Science, 124, 220only. Crisp, D.J., 1983. Chelonobia patula (Ranzani), a pointer to the evolution of the complemental male. Mar. Biol. Lett., 4, 281–294. Crisp, D.J. & Patel, B.S., 1960. The moulting cycle in Balanus balanoides L. Biol. Bull. (Woods Hole, Mass.), 118, 31–47. Crisp, D.J. & Southward, A.J., 1961. Different types of cirral activity of barnacles. Phil. Trans. R. Soc. London Ser. B, 243, 271–307. Dando, P.R., 1987. Biochemical genetics of barnacles and their taxonomy. In, Barnacle Biology. Crustacean Issues 5, edited by A.J. Southward, A.A. Balkema, Rotterdam, pp. 73–87. Darwin, C., 1851. A Monograph on the Sub-class Cirripedia, with Figures of all the Species. The Lepadidae; or, Pedunculated Cirripedes. Ray Society, London, 400 pp. Darwin, C., 1854. A Monograph of the Sub-class Cirripedia, with Figures of all the Species. The Balanidae, the Verrucidae. Ray Society, London, 684 pp. Darwin, C., 1873. On the males and complemental males of certain cirripedes, and on rudimentary structures. Nature (London), 8, 431–32. Foster, B.A., 1978. The Marine Fauna of New Zealand: Barnacles Cirripedia: Thoracica). N.Z. Oceanogr. Inst., Mem. No. 69, 160 pp. Foster, B.A., 1983. Complemental males in the barnacle Bathylasma alearum (Cirripedia: Pachylasmidae). Aust. Mus. Mem., 18, 133–139. Foster, B.A. & Nott, J.A., 1969. Sensory structures in the opercula of the barnacle Elminius modestus. Mar. Biol., 4, 340–344. Ghiselin, M.T., 1969. The evolution of hermaphroditism among animals. G. Rev. Biol., 44, 189–208. Gruvel, A., 1900. Étude du mâle complémentaire du Scalpellum vulgare. Arch. Biol. Belg., 16, 27–47. Grygier, M.J., 1981. Sperm of the ascothoracican parasite Dendrogaster, the most primitive found in Crustacea. Int. J. Invertebr. Reprod., 3, 65–73. Grygier, M.J., 1982. Sperm morphology in Ascothoracida (Crustacea: Maxillopoda): confirmation of generalized nature and phylogenetic importance. Int. J. Invertebr. Reprod., 4, 323–332. Grygier, M.J., 1983. Ascothoracida and the unity of Maxillopoda. In, Crustacean Phytogeny. Crustacean Issues 1, edited by F.R. Schram, A.A. Balkema, Rotterdam, pp. 73–104. Grygier, M.J., 1987a. Classification of the Ascothoracida (Crustacea). Proc. Biol. Soc. Wash., 100, 452–458. Grygier, M.J., 1987b. Reappraisal of sex determination in the Ascothoracida. Crustaceana, 52, 149–162.
INSEMINATION IN CIRRIPEDES
377
Grygier, M.J., 1987c. New records, external and internal anatomy and systematic position of Hansen’s Y-larvae (Crustacea: Maxillopoda: Facetotecta). Sarsia, 72, 261–278. Henry, D.P. & McLaughlin, P.A., 1965. Unique occurrence of complemental males in a sessile barnacle. Nature (London), 207, 1107–1108. Henry, D.P. & McLaughlin, P.A., 1967. A revision of the subgenus Solidobalanus Hoek (Cirripedia Thoracica) including a description of a new species with complemental males. Crustaceana, 12, 43–58. Høeg, J.T., 1987. Male cyprid metamorphosis, and a new male larval form, the trichogon, in the parasitic barnacle Sacculina carcini (Crustacea: Cirripedia: Rhizocephala). Philos. Trans. R. Soc. London, Ser. B, 37, 47–63. Høeg, J.T., in press. Functional and evolutionary aspects of the sexual system in the Rhizocephala (Crustacea: Thecostraca: Cirripedia). In, Crustacean Sexual Biology, edited by R.Bauer & J.Martin, Columbia University Press, New York, in press. Hoek, P.P. C, 1884. Report on the Cirripedia collected by H.M.S. Challenger during the years 1873–76. Anatomical Part, Rep. Sci. Res. Voy. Challenger, Zool., 10, Part III, 47 pp. Hui, E. & Moyse, J., 1984. Complemental male in the primitive balanomorph barnacle, Chionelasmus darwini. J. Mar. Biol. Assoc. U.K., 64, 91–97. Ichikawa, A. & Yanagimachi, R., 1958. Studies on the sexual organization of the Rhizocephala. I. The nature of the “testes” of Peltogasterella socialis Krüger. Annot. Zool. Jpn., 31, 82–96. Ichikawa, A. & Yanagimachi, R., 1960. Studies on the sexual organization of the Rhizocephala. II. The reproductive function of the larval (cyrpris) males of Peltogaster and Sacculina. Annot. Zool. Jpn., 33, 42–56. Klepal, W., 1971. Chthamalus stellatus (Poli) und C. depressus (Poli) in der Adria. J. Exp. Mar. Biol. Ecol., 7, 271–294. Klepal, W., 1985. Ibla cumingi (Crustacea, Cirripedia)—a gonochoristic species (anatomy, dwarfing and systematic implications). P.S.Z.N.I. Mar. Ecol., 6, 47–119. Klepal, W., 1987. A review of the comparative anatomy of the males in cirripedes. Oceanogr. Mar. Biol. Annu. Rev., 25, 285–351. Klepal, W. & Barnes, H., 1974. Regeneration of the penis in Balanus balanoides (L.). J. Exp. Mar. Biol. Ecol., 16, 205–211. Klepal, W. & Barnes, H., 1977. Studies on the reproduction of cirripedes. V. Pollicipes cornucopia Leach and Balanus balanus (L.); an electron microscope investigation of the structure of the oviducal sacs. J. Exp. Mar. Biol. Ecol., 27, 261–287. Klepal, W., Barnes, H. & Barnes, M., 1975. Variability in the ‘loss’ of the penis in Balanus balanoides (L.) under natural and experimental conditions and histology of degeneration. In, Proc. 9th Europ. Mar. Biol. Symp., edited by H. Barnes, Aberdeen University Press, Aberdeen, pp. 275–286. Klepal, W., Barnes, H. & Barnes, M., 1977. Studies on the reproduction of cirripedes. VI. Passage of the spermatozoa into the oviducal sac and closure of pores. J. Exp. Mar. Biol. Ecol., 27, 289–304. Klepal, W., Barnes, H. & Munn, E.A., 1972. The morphology and histology of the cirripede penis. J. Exp. Mar. Biol. Ecol., 10, 243–265. Krüger, P., 1914. Die Fauna Südwest-Australiens. Cirripedia. 4, lfg. 11, 429–41. Laloy, L., 1903. Les cirripèdes. Notions nouvelles sur leur phylogénie et leur évolution sexuelle. Rev. Sci., 4th Ser., 19, 360–366. Le Gross Clark, W.E., 1971. The Tissues of the Body. An Introduction to the Study of Anatomy. Claredon Press, Oxford, 6th edition, 424 pp. Lützen, J., 1984. Growth, reproduction, and life span in Sacculina carcini Thompson (Cirripedia: Rhizocephala) in the Isefjord, Denmark. Sarsia, 69, 91–106. Maynard-Smith, J., 1978. Evolution of Sex. Cambridge University Press, Cambridge, 222 pp. McLaughlin, P.A. & Henry, D.P., 1972. Comparative morphology of complemental males in four species of Balanus (Cirripedia Thoracica). Crustaceana, 22, 13–30.
378
WALTRAUD KLEPAL
Moyse, J., 1983. Isidascus bassindalei gen. nov., sp. nov. (Ascothoracida: Crustacea) from north-east Atlantic with a note on the origin of barnacles. J. Mar. Biol. Assoc. U.K., 63, 161–180. Munn, E.A. & Barnes, H., 1970. The fine structure of the spermatozoa of some cirripedes. J. Exp. Mar. Biol. Ecol, 4, 261–268. Munn, E., Klepal, W. & Barnes, H., 1974. The fine structure and possible sensory functions of the sensory setae of the penis of Balanus balanoides (L.). J. Exp. Mar. Biol. Ecol., 14, 89–98. Newman, W.A., 1980. A review of extant Scillaelepas (Cirripedia: Scalpellidae) including recognition of new species from the north Atlantic, western Indian Ocean and New Zealand. Téthys, 9, 379–398. Newman, W.A., 1982. Cirripedia. In, The Biology of Crustacea, Vol. 1, edited by L. Abele, Academic Press, New York, pp. 197–221. Newman, W.A., 1987. Evolution of cirripedes and their major groups. In, Barnacle Biology. Crustacean Issues 5, edited by A.J. Southward, A.A. Balkema, Rotterdam, pp. 3–42. Newman, W.A., Zullo, V.A. & Withers, T.H., 1969. Cirripedia. In, Treatise on Invertebrate Paleontology, Part R, Arthropoda 4, Vol. 1, edited by R.C. Moore, Geol. Soc. Am. University of Kansas Press, pp. R206-R295. Nilsson-Cantell, C.A., 1921. Cirripeden-Studien. Zur Kenntnis der Biologie, Anatomie und Systematik dieser Gruppe. Zool. Bidr. Uppsala, 7, 75–395. Nilsson-Cantell, C.A., 1928. Studies on cirripeds in the British Museum (Natural History). Ann. Mag. Nat. Hist., Ser. 10, 2, 1–39. Nilsson-Cantell, C.A., 1932. Cirripeds from the Indian Ocean and Malay Archipelago in the British Museum (Nat. Hist.) London. Ark. Zool, 23(A), No. 18, 1–12. Pilsbry, H.A., 1908. On the classification of scalpelliform barnacles. Proc. Acad. Nat. Sci. Philadelphia, 60, 104–111. Pochon-Masson, J., Bocquet-Védrine, J. & Turquier, Y., 1970. Contribution à 1’étude du spermatozoïde des Crustacés Cirripèdes. In, Comparative Spermatology, edited by B. Baccetti, Accad. Naz. Lincei, 137, 205–219. Smith, G. & Weldon, W.F. R., 1920. Crustacea (continued): Cirripedia—Phenomena of growth and sex—Ostracoda. Order III, Cirripedia. In, The Cambridge Natural History, Vol. IV, edited by S.F. Harmer & A.E. Shipley, Macmillan & Co. Ltd., London, pp. 79– 109. Southward, A.J., 1955. On the behaviour of barnacles. I. The relation of cirral and other activities to temperature. J. Mar. Biol. Assoc. U.K., 34, 403–422. Stewart, F.H., 1911. Studies in post-larval development and minute anatomy in the genera Scalpellum and Ibla. Mem. Indian Mus., 3, 33–51. Svane, I., 1986. Sex determination in Scalpellum scalpellum (Cirripedia: Thoracia: Lepadomorpha), a hermaphroditic goose barnacle with dwarf males. Mar. Biol., 90, 249–253. Szöllösi, A., 1975. Electron microscope study of spermiogenesis in Locusta migratoria (Insect Orthoptera). J. Ultrastruct. Res., 50, 322–346. Tomlinson, J., 1966. The advantages of hermaphroditism and parthenogenesis. J. Theoret. Biol., 11, 54–58. Tomlinson, J.T., 1953. A burrowing barnacle of the genus Trypetesa (Order Acrothoracica). J. Wash. Acad. Sci., 43, 373–381. Tomlinson, J.T., 1955. The morphology of an acrothoracian barnacle, Trypetesa lateralis. J. Morphol, 96, 97–121. Tomlinson, J.T., 1960. Cryptophialus coronatus, a new species of acrothoracican barnacle from Dakar. Bull. Inst. Fran. Afr. Noire, Ser. A, 22, 402–10. Tomlinson, J.T., 1969. The burrowing barnacles (Cirripedia: Order Acrothoracica). U.S. Natl. Mus. Bull, 296, 162 pp. Tomlinson, J.T., 1973. Distribution and structure of some burrowing barnacles, with four new species (Cirripedia: Acrothoracica). Wasmann J.Biol., 31, 263–288.
INSEMINATION IN CIRRIPEDES
379
Tomlinson, J.T. & Newman, W.A., 1960. Lithoglyptes spinatus, a burrowing barnacle from Jamaica. Proc. U.S. Nat. Mus., 112, 517–526. Turquier, Y., 1971. Recherches sur la biologie des Cirripèdes Acrothoraciques. IV. La métamorphose des cypris mâles de Trypetesa nassarioides et de Trypetesa lampas (Hancock). Arch. Zool. Exp. Gén., 112, 301–348. Turquier, Y., 1976. Étude de quelques cirripedes acrothoraciques de Madagascar. II. Description de Trypetesa spinulosa n. sp. Bull. Soc. Zool. Fr., 101, 559–574. Turquier, Y., 1985. Cirripèdes acrothoraciques des côtes occidentales de la Méditerranée et de 1’Afrique du nord. I. Cryptophialidae. Bull. Soc. Zool. Fr., 110, 151–168. Turquier, Y. & Pochon-Masson, J., 1969. L’infrastructure du spermatozoïde de Trypetesa (=Alcippe) nassarioides Turquier (Cirripède acrothoracique). Arch. Zool. Exp. Gén., 110, 453–470. Utinomi, H., 1961. Studies on the Cirripedia Acrothoracica. III. Development of the female and male of Berndtia purpurea Utinomi. Publ. Seto Mar. Biol. Lab., 9, 413–446. Vaghin, V.L., 1946. On males of Dendrogasteridae (Entomostraca, Ascothoracica). C.R. Acad. Sci. Moscow, 25, 273–276. Walker, G., 1977a. Observations by scanning electron microscope (S.E.M.) on the oviducal gland sacs of Balanus balanoides at egg-laying. J. Mar. Biol. Assoc. U.K., 57, 969–972. Walker, G., 1977b. Sperm activation in Balanus balanoides (Crustacea: Cirripedia). Experientia, 33, 1603–1604. Walker, G., 1980. A study of the oviducal glands and ovisacs of Balanus balanoides (L.), together with comparative observations on the ovisacs of Balanus hameri (Ascanius) and the reproductive biology of the two species. Phil. Trans. R. Soc. London Ser. B., 291, 147–162. Walker, G., 1985. The cypris larvae of Sacculina carcini Thompson (Crusacea: Cirripedia: Rhizocephala). J. Exp. Mar. Biol. Ecol, 93, 131–145. Walley, L.J., 1965. The development and function of the oviducal gland in Balanus balanoides. J. Mar. Biol. Assoc. U.K., 45, 115–128. Walley, L.J., White, F., Brander, K.M., 1971. Sperm activation and fertilization in Balanus balanoides. J. Mar. Biol. Assoc., U.K., 51, 489–494. Witschi, E., 1935. The chromosomes of hermaphrodites. I. Lepas anatifera L. Biol. Bull. (Woods Hole, Mass.), 68, 263–267. Yanagimachi, R., 1961. Studies on the sexual organization of the Rhizocephala. III. The mode of sex-determination in Peltogasterella. Biol. Bull. (Woods Hole, Mass.), 120, 272–283. Yanagimachi, R. & Fujimaki, N., 1967. Studies on the sexual organization of the Rhizocephala. IV. On the nature of the “testis” of Thompsonia. Annot. Zool. Jpn., 40, 98–104.
Oceanogr. Mar. Biol. Annu. Rev., 1990, 28, 381–96 Margaret Barnes, Ed. Aberdeen University Press
THE ECOLOGY OF TROPICAL SOFT-BOTTOM BENTHIC ECOSYSTEMS* DANIEL M.ALONGI Australian Institute of Marine Science, PMB 3, Townsville MC, Queensland 4810, Australia
ABSTRACT The structure and function of tropical soft-bottom benthic ecosystems are reviewed and compared with seafloor ecosystems of higher latitudes. Diversity of benthic habitats peaks in the tropics. Variations in climate have led to the development of unique sedimentary features and sea-floor habitats such as mangroves, coral reefs, stromatolites, mixed terrigenous-carbonate shelves, fluid mud-banks and hypersaline lagoons. Temporal and spatial patterns of benthos in all latitudes are determined by primary production in the water column and by sediment type and associated physicochemical conditions. In the tropics, however, control of benthic communities is vested in monsoonal rains, high temperatures, hypersaline conditions, carbonate sedimentation and compaction, low and variable oxygen and dissolved nutrient concentrations, chemical defenses by plants, smothering by massive riverine sedimentation, erosion of mudbanks and by anoxia caused by impingement and stratification of water masses. The widest variations in faunal densities and species richness occur in the tropics, coinciding with the great variety of habitats and environmental conditions. Energetically, there is some evidence of higher rates of microbial growth and invertebrate production in the tropics, but pelagic and demersal fish yields to man seem to be equivalent to those in higher latitudes. At the ecosystems level, variations in energy fluxes are as great within a given latitude as they are among latitudes, obfuscating some real differences with latitude. It is clear that the tropics are not a uniform or benign milieu but offer climatic and environmental conditions as inimical to benthic assemblages as the supposedly, more inhospitable, boreal and temperate latitudes.
INTRODUCTION Nearly 40% of the total open ocean area and 30% of the total area of the world’s continental shelves lie within the tropics (see Table I). Study of the tropical biosphere is increasing and several aspects of the ecology of tropical marine systems have been reviewed recently (fish yields, Jones, 1982; wetlands, De la Cruz, 1986; general ecology, Longhurst & Pauly, 1987; mangroves and coral reefs, Alongi, * Contribution No. 483 from the Australian Institute of Marine Science.
382
DANIEL M.ALONGI
1989a,b; pollution and management, Hatcher, Johannes & Robertson, 1989). All of these overviews have considered at least a few aspects of the role of soft-bottom communities, but a large proportion of the tropical soft-bottom literature has not been considered. This review addresses the structural and functional aspects of tropical soft-bottom benthos, emphasising differences with the ecology of benthos in higher latitudes. While the same ecological factors (e.g., competition, predation, food supply) must regulate benthic communities worldwide, there are differences both at the climatic and oceanographic levels which form the basis for comparing benthic ecosystems of different latitudes. There is no simple definition of the tropics. It is not, as commonly supposed, a benign and uniform region of the earth. The ecological boundaries of the tropics are somewhat fluid as tropical climatic conditions may reach well beyond the Tropics of Cancer and Capricorn (23.5° north and south of the Equator; Fig 1). In this review, the delimitation of the tropics as suggested by Deshmukh (1986) is accepted, being defined on land by the ecological boundaries between the tropical and extratropical vegetation types, and on the sea by the 18°C mean isotherm at sea level for the coolest month, as modified from Nieuwolt (1977), Bolin, Begins, Kempe & Ketner (1979) and Walter (1979). Variations in temperature and rainfall are large in the tropics. For instance, daily thermal changes increase both away from the Equator and with elevation on land. Over the tropical seas, climatic variations are smaller, but rainfall patterns differ greatly. The western boundaries of the oceans are warmer, wetter, and more stable climatically than the eastern margins. These differences are of great ecological significance because the distribution of tropical shallow-water habitats, especially mangroves and coral reefs, and their associated vegetation, is a reflection of these climatological variations. These climatic differences are caused by the assymetrical form and unequal size of the oceanic margins, which strongly influence sea-surface temperatures, currents, and nutrient regimes (see the comprehensive reviews of tropical climatology and oceanography by Nieuwolt, 1977; Cane & Sarachik, 1983; Knox & Anderson, 1985; Philander, 1985). The diversity of marine habitats peaks in the tropics. Many are dominant or unique, such as mangroves, coral reefs, stromatolites, and hypersaline lagoons (Longhurst & Pauly, 1987). It is interesting to note, however, that the tropical
Fig 1. —Global map (40°N to 40°S) delimiting the boundaries of the tropics. The dashed lines depict the 18° mean isotherm at sea level; the solid lines delineate the limits of tropical vegetation. Code numbers of major tropical rivers are shown and correspond with listing in Table II. Modified from Deshmukh (1986).
TROPICAL BENTHIC ECOSYSTEMS
383
marine biosphere is but a comparatively thin shell covering a generally cold ocean mass. Even in the tropics, sea temperatures rapidly decrease below the thermocline to temperatures identical (or nearly so) at equivalent depths in higher latitudes, indicating that the oceanic environment of the deep sea (below 200 m) is similar worldwide. This review will therefore focus mainly on benthic ecosystems from the intertidal to the edge of the continental shelves. Little benthic work has been conducted in the tropics compared with higher latitudes, so why review the tropical benthos? As pointed out by Hatcher, Johannes & Robertson (1989), pollution, urbanisation, and human population growth are increasing along tropical coastlines at an alarming rate, and most developing countries have yet to formulate effective plans of management and conservation; the failure is due as much to the lack of scientific research as to political awareness and financial problems. These factors alone necessitate a review of the widely scattered, tropical benthic literature, not to mention the probable harm to advances in benthic ecology if this information continues to be ignored. Previous reviews and books on benthic community ecology (Thorson, 1957; Tenore & Coull, 1980; Gray, 1981 and references therein) reflect temperate and boreal biases which have been responsible, in part, for exhaustive arguments on topics such as species diversity and discrete compared with clinal community organisation. It is tempting to suggest that these concepts would have evolved more clearly and with less rancour if tropical habitats had been examined earlier and in more detail. A clear understanding of the origins of marine benthic biota may eventually shed some light on controversies such as patterns of species diversity (Vermeij, 1978). Discontinuities exist in the latitudinal distribution of benthic invertebrates; similarity is greater between tropical and subtropical faunas than between the subtropical and high latitude faunas (Menzies, George & Rowe, 1973). Ekman (1953) noted that within the warm-water benthic fauna there is a considerable degree of longitudinal homogeneity, attributed to the origins of most benthic lifeforms in the circumtropical Téthys Sea and their eventual radiation to more marginal, high latitude environments. Expansion of the tropical fauna probably ended during global cooling in the Tertiary period (Valentine, 1971). An IndoWest Pacific and an Atlantic-East Pacific fauna are the two principal elements of the zoogeography of the benthic warm-water fauna, with the former region faunistically more diverse. Within regions, the western margins appear to have a more diverse fauna than the eastern margins, underscoring the long-term, but frequently overlooked, importance of climatological and environmental variations of the world oceans.
ENVIRONMENTAL CHARACTERISTICS Many environmental characteristics are unique to the tropics or differ from high latitudes to varying degrees (Table I). A complete analysis of the chemical and physical oceanographic conditions of the tropical oceans is beyond the scope of this review (see Cane & Sarachik, 1983; Knox & Anderson, 1985; Philander, 1985). Several environmental aspects relevant to the structure and function of tropical benthic communities are briefly assessed in this section: (1) major climatic zones,
384
DANIEL M.ALONGI
TABLE I Some major environmental characteristics peculiar to or dominant in tropical oceans. See references in text and Hatcher et al. (1989).
(2) monsoons, (3) patterns of river discharge and effects on hydrography, (4) upwelling, and (5) sedimentary patterns and nutrients.
CLIMATOLOGICAL AND HYDROLOGICAL CONDITIONS
TROPICAL BENTHIC ECOSYSTEMS
385
On the basis of climate, the tropics are divided into four regions: (1) Africa, (2) tropical South and Central America, including the Caribbean islands, (3) tropical regions of the Indian, Atlantic and Pacific Oceans, and (4) southeast Asia and northern Australia (see Fig 1). Patterns of monsoonal rainfall in Africa vary greatly with the vast expanse of the continent within the tropics. In northern Australia and southeast Asia, three monsoonal patterns control climate: (1) equatorial monsoons where winter and summer monsoons are wet (Papua New Guinea and Indonesia); (2) dry and wet monsoons where one season is wet and one dry (dry winter and wet summer in Thailand and Australia; wet winter and dry summer in eastern Philippines, eastern India and Bay of Bengal); and (3) the dry tropics (where rainfall is less than 400 mm per year) in Pakistan, central Australia, northwest India and Saudi Arabia, where monsoons are rare because large-scale disturbances are inhibited by short ocean distances between land masses. Rainfall is greatest in southeast Asia. Nieuwolt (1977) provides a comprehensive treatment of climate in the tropics. Considering the regional variability of precipitation and high solar insolation in the tropics it is not surprising that very sharp gradients in temperature, salinity, and some other properties, such as dissolved nutrients, are exhibited in tropical waters. Sharp thermoclines and haloclines coincide in most tropical regions with strong vertical discontinuity maintained throughout most of the year, except where equatorial upwellings force cooler water to the surface, or where waters from central oceanic gyres intrude into humid regions to become warmer and more dilute. Lower salinities are characteristic of surface waters in the humid tropics, and conversely, surface waters in arid tropical seas are very salty. Three types of surface water were recognised by Wyrtki (1964) in the tropics: tropical surface water (25–28°C; 33–34‰), equatorial surface water (20–28°C, 34–35‰), and subtropical surface water (19–28°C, 35–36.5‰). This classification is not accepted by all oceanographers but it is generally agreed that great variability in salinity and its ability to adjust rapidly to changes in wind-induced motion and temperature characterises tropical surface waters (Cane & Sarachik, 1983; Philander, 1985). Surface water masses in the tropics are greatly influenced by river run-off and dilution by monsoonal rains, particularly on most continental shelves (Wytrki, 1964). Longhurst & Pauly (1987) call this phenomenon “estuarisation”, in which the inner portions of continental shelves consist of low salinity waters or exhibit discrete plumes of discharged river water. Estuarisation is important in the Bay of Bengal, Gulf of Panama, the South China Sea, and in the Gulf of Guinea. River plumes are most discernible in proximity to major rivers such as the Zaire (formerly Congo), Amazon, and Fly in Papua New Guinea (Table II). The Brazilian shelf and Bay of Bengal are the best known sites of shelf estuarisation. Subsurface water masses below the thermocline in the tropical oceans frequently contain an oxygen minimum layer. Several explanations have been offered to account for this poorly understood phenomenon, including minimal circulation or mixing of water to replenish oxygen consumed or that detritus accumulates in stagnant areas because of increases in water density with depth leading to the depletion of oxygen (Philander, 1985). Irrespective of the cause, low oxygen concentrations have important consequences for demersal fishes and the benthic fauna in some regions. For instance, along the west coast of India, coastal upwelling results in the placement of subsurface waters of low oxygen
386
DANIEL M.ALONGI
TABLE II Estimates of water and suspended sediment discharge from major tropical and subtropical rivers. Numbers in parentheses indicate ranking of top ten rivers on basis of water discharge and correspond with code numbers in Fig 1. Sources: UNESCO (1979), Milliman & Meade (1983), Ittekkott (1988), and Ok Tedi Mining Ltd, Papua New Guinea (unpubl. data)
content onto the continental shelf, displacing many demersal fishes and epibenthic crustaceans (Banse, 1968). Small rivers, creeks, and estuaries in many areas are also characterised by waters of low oxygen content with presumably similar biological consequences (Malabar, India, Seshappa, 1953; Australian mangrove creeks, Boto & Bunt, 1981). Changes in water mass characteristics induced by excessive evaporation may lead to changes in faunal distributions and abundances or to the development of a unique fauna such as in the hypersaline lagoons of the Red Sea (Fishelson, 1971; Jones, Price & Hughs [sic], 1978). During the hot dry season in northern Australia, salinity maximum zones form at the mouths of rivers as a result of evaporation (Wolanski, 1986). The mixing of estuarine and ocean waters is, in some cases, inhibited by this high salinity plug so that fresh water does not leave
TROPICAL BENTHIC ECOSYSTEMS
387
the estuary. Export of salt and nutrients from some tidal flats bordering these estuaries fortifies the salinity maximum zone, further isolating the rivers from adjacent coastal waters (Ridd, Sandstrom & Wolanski, 1988). Trapping of estuarine waters also occurs in estuaries lined with mangrove forests, the prop roots and tidal structure of which lead to noticeable time lags in tidal flushing and current mixing (Wolanski & Ridd, 1986). Strong tidal currents in tropical coastal waters frequently lead to the formation of tidal fronts, where tidal mixing overcomes buoyancy. The phenomenon is common in areas such as the northern Bay of Bengal, from the Philippines to Papua New Guinea, Gulf of Panama, Guianas to northern Brazil, the Malacca Strait, southern India, the Persian Gulf, and the Gulf of Carpentaria (Philander, 1985). In some shallow areas, particularly during the dry season, vertical gradients of buoyancy develop, inhibiting vertical mixing and resulting in the formation of a lutocline (fluid mud layer) separating clear surface water from sediment-laden bottom waters (e.g. Gulf of Carpentaria, Wolanski, Chappell, Ridd & Vertessy, 1988). Fluidisation of mud and the migration of mudbanks are not uncommon in other areas such as off the Malabar coast of India (Sesheppa, 1953) and off the coast of French Guiana (Froidefond, Pujos & Andre, 1988). Coastal upwelling is another major feature in the tropical oceans. Such events occur in all latitudes, but within subtropical and tropical latitudes, physicochemical differences between upwelled and surface water masses are greatest. Upwelling is dominant along the subtropical-tropical boundary coasts of Peru-Chile (Peru Current), Morocco-Mauritania (Canary Current), AngolaNamibia (Benguela Current), and California-Mexico; minor upwelling occurs on the Malabar coast of India, off the Andaman Islands, off western Australia, the Gulf of Panama (the “Costa Rica Dome”), the Gulf of Nicoya and Tehuan-tepec, off northeast Venezuela and Brazil south of Cabo Frio, from Ghana to Togo (Gulf of Guinea), on the Somali coast, and off southern Arabia (Cushing, 1988). Not all upwellings occur off eastern boundaries of continents, as some upwelling events are driven by events an entire ocean away. For example, in the Gulf of Guinea or along the Somali coast of Africa, a diversity of mechanisms drives regional coastal upwellings. Seasonality of upwelling in the tropics is a welldescribed phenomenon, but the actual circulatory patterns are poorly understood. Seasonal changes in current patterns occur, driven mainly by the movement of the Intertropical Convergence Zone (ITCZ) across the Equator every six months. Upwelling events and monsoons are thus ultimately linked to seasonal changes in the equatorial climate. It has been suggested that between-year variations are greater than within-year variations within the tropical oceans. Complete support for this concept awaits the acquisition of long-term oceanographic data, but the phenomenon of the El NiñoSouthern Oscillation (ENSO) emphasises the fact that atmospheric variations can mediate changes in the environment on a global scale with major biological consequences. El Niño is now seen to result from a periodic oscillation of atmospheric pressure between the Indian and Pacific Oceans (the Southern Oscillation). Effects of the ENSO events are felt worldwide, resulting in anomalous sea-surface temperatures throughout the tropical oceans. Major changes in the environment induced by ENSO have been shown to have profound consequences for the oceanic and coastal ecosystem off Peru-Chile and latitudinally along the entire eastern Pacific Ocean margin (Glynn, 1988).
388
DANIEL M.ALONGI
In summary, tropical and subtropical ocean regions are greatly influenced by high rates of evaporation and precipitation, and by coastal upwelling. These events can destroy the permanently stratified thermocline in many low-latitude shelf areas, unlike in temperate and polar oceans where water masses turn over by cooling in autumn and winter. Tidal currents induced mainly by monsoonal rains can, when sufficiently strong, also destroy stratification or prevent its formation. Such estuarisation on many tropical shelves is seasonal, depending on the onset of monsoonal disturbances, and the transition from unstratified to stratified conditions is usually sharp, delimited as a tidal front. North of the Equator, the eastern Pacific and eastern Atlantic Oceans are eddy-dominated, with countercurrents impinging upon estuaries fed by major rivers and fairly wide shelf areas. To the south, the coastlines are dominated by subtropical transition zones strongly seasonal in thermal and faunal characteristics (see Sharp, 1988, and references therein). In the eastern Indian Ocean and southeast Asia, the water masses are monsoon-dominated and warm year-round. The main systems in tropical and subtropical seas are, however, the upwelling areas, where biological production can exceed the productivity of higher latitude ecosystems (Cushing, 1988).
SEDIMENTARY PATTERNS
The frequency of climatic disturbances in the tropics leads to a dis-proportionate amount of the world’s freshwater and sediment discharge to the oceans occurring from tropical rivers (see Table II, Fig 1). The Amazon, Zaire, Orinoco, and Brahmaputra Rivers alone contribute approximately 51% and 39% of freshwater and sediment discharge from the world’s rivers, respectively. When all major tropical and subtropical rivers are included, the proportions rise to 70% of freshwater run-off and 74% of sediment discharge (Table II). There is considerable error in these estimates, but it is clear that most water, solids and dissolved materials drained from the continents are transported to the tropical oceans (Milliman & Meade, 1983). Ittekkot (1988) has estimated the contribution of organic carbon from the world’s rivers to the global carbon cycle, differentiating between labile and refractory fractions. His estimates indicate that 35% of the total organic carbon in river suspensions (2.3×10 14 gC·yr -1 ) is labile and probably oxidised within the rivers, estuaries, and nearshore marine habitats. The remainder (1.5×10 14 gC·yr -1) is very refractory and thus the bulk of suspended organic matter entering subtropical and tropical seas is highly degraded and may thus accumulate in marine sediments, although this remains to be substantiated. The distribution of sediment types on inner continental shelves reflects the influence of sediment run-off from the continents. Hayes (1967) compiled the available sedimentary data and correlated coastal climate with sediment type indicating that the major climatic factors responsible for the global patterns were weathering, the presence or absence of major rivers, glaciation, and ice-rafting. Mud and coral are most abundant in the tropics, whereas sand is globally abundant, decreasing with higher latitudes to be proportionately displaced by gravel and rock (Fig 2). The distribution of relict shell is not related to climate. The latitudinal pattern of inner shelf sediment types is somewhat deceptive because a large proportion of mud in the tropics occurs in proximity to the major
TROPICAL BENTHIC ECOSYSTEMS
389
Fig 2. —Latitudinal distribution of sediment types on the world’s inner continental shelves (modified from Hayes, 1967).
rivers, particularly the deltaic systems of the Amazon, Orinoco, Mekong, Ganges, and Brahmaputra Rivers. Muds along coastlines near major river plumes are stirred up sufficiently during monsoons to disrupt wave trains and to form mudbanks. This phenomenon occurs predominantly in the tropics, and is well documented along the coasts of southwest India (Seshappa, 1953; Gopinathan & Qasim, 1974; Jacob & Qasim, 1974) and northern South America (Wells & Coleman, 1981; Froidefond et al., 1988). On the southwest (Kerala) coast of India, certain inshore areas produce zones of calm water by dampening wave action. The large quantity of riverine-derived matter in colloidal suspension leads to the dissipation of wave energy. These mudbanks, locally known as “chakara”, extend over areas of at least 25 km 2 , and are characterised by siltyclay sediments, oxygen-deficient waters and, possibly, by generation of gases. The mud is generally 1 to 2 m thick and thixotropic. Formation and migration of the Kerala coast mudbanks are closely associated with high period waves and their refraction pattern along the sea bottom. The size of each bank is determined by the location of converging intertidal currents and offshore flow. The mudbank is supplied continuously with mud from both directions and compensates for losses due to settlement and from mudbanks disappear owing to the decrease in wave activity and increased settlement. Particulate nutrient (C, P) concentrations in mudbank deposits export by currents moving offshore. During the post-monsoon periods, the are generally high and positively correlated with decreasing grain size. Carbohydrate and plant phaeopigment values are very low, suggesting that the mud is nutritionally poor.
390
DANIEL M.ALONGI
Jacob & Qasim (1974) examined the guts of fish and prawns caught in the mudbank areas and found large quantities of mud, and suggested that it served as an alternative food supply during the monsoon season when other food items are not available. The coast of the Guianas (French Guiana, Surinam, British Guiana) of South America is also characterised by migrating mudbanks (Wells & Coleman, 1981; Froidefond et at., 1988). The coast is bordered by the sources of mud in the region, in the east by the mouth of the Amazon and in the west by the Orinoco River. Mudbanks attached to the shore are gigantic (about 200 km 2 ) and are composed of thixotropic fluid mud, forming a temporary storage for silt and clay. As off the southwest coast of India, the subtidal nearshore sea bed is shallow, gently sloped, and backed by mangrove forests, leading to similar wave and tidal current patterns which foster accretion and migration of fluid mud (Wells & Coleman, 1981). These linear mud shoals change rapidly in space and time, and are transported westward by wave-induced currents on the inner shelf and by the Guiana Current on the outer shelf. Tropical coastlines characterised by migrating mudbanks are the exception, rather than the rule. Excluding these areas and other regions such as off Peru and the Bight of Biafra where highly reduced, sulphidic blue mud persists (Longhurst, 1957a), most tropical shelves are sand-dominated, several by carbonates and in many instances, bordered landward by mangroves or fringed seawardly by coral reefs (Sellwood, 1986). Modern carbonate shelves in the subtropics and tropics fall into two categories: (1) protected shelf lagoons (Bahamas, Florida, Belize, Cuba, and the Great Barrier Reef), and (2) open shelves (Yucatan, western Florida along the Gulf of Mexico, the Persian Gulf and northern Australia). Shelf lagoons are characterised by the presence of fringing barrier reefs, islands, and shoals, and commonly have acrossshelf gradients of mixed terrigenous-carbonate facies. On the Belize shelf (Wantland & Pusey, 1975), the Grand Bahama Bank (Newell, Imbrie, Purdy & Thurber. 1959) and on the Great Barrier Reef (Alongi, 1989c), the lagoons of these regions consist of gradients of inshore terrigenous quartz sand and mud, eventually changing to mainly carbonate sand and mud out to the shelf break. Carbonate shelves are not limited to the warmer latitudes, but rimmed (protected) shelves are latitudinally restricted because only in this climatic region has the production of carbonate at the shelf margin been able to keep pace with the rise of Holocene sea level. Thus, on many tropical shelves, soft sandy-mud deposits derived from continental drainage dominate the inshore areas with varying mixtures of quartz and carbonate sand deposits dominating the middle and outer shelf areas, the extent of which vary with shelf width. Many coastal lagoons which formed behind barrier islands are either hypersaline in arid regions due to excessive evaporation (e.g. Persian Gulf) or form gigantic interconnecting waterways in the humid tropics, as along the eastern Gulf of Guinea. Sediment composition varies greatly among lagoons depending upon their openness to the sea and the presence or absence of rivers and coastal vegetation (Webb, 1958a,b). Lagoons in highly arid regions are characterised by cemented dunes (caused by precipitation of calcium carbonate) or “sabkha”, behind which biogenic material is rapidly produced. Microbial stromatolites develop particularly in arid Indo-Pacific areas (e.g. Shark Bay, Western Australia) where other biota are excluded by accretion of precipitated inorganic carbonates (Moriarty, 1983). The formation of cyanobacterial mats
TROPICAL BENTHIC ECOSYSTEMS
391
constitutes the final stages in the formation of coastal gypsum lakes (Jones, Price & Hughs [sic], 1978). In summary, wide variations in tropical rainfall lead to the formation of many sedimentary facies and habitats peculiar to the tropics. Mudbanks, green and blue anoxic mud regions, mixed terrigenous-carbonate bedforms, hypersaline lagoons, stromatolites and, more generally, mangroves, coral reefs, and extensive carbonate shelves are characteristic of shallow, tropical seas. These phenomena are created, influenced, and altered by processes peculiar to themselves, linked to climate, oceanographic factors, and the rate of terrigenous sedimentation.
PARTICULATE AND DISSOLVED SEDIMENTARY NUTRIENTS
Organic carbon and nitrogen The global distribution of sedimentary organic carbon and nitrogen is not related to latitude, but dependent upon water depth, grain size, terrestrial run-off, and hydrography (Romankevich, 1984). The highest concentrations of organic matter in sediments are in regions of upwelling and in proximity to rivers, and more generally, relate to the patterns of pelagic primary production. It is interesting to note, however, that while there are no clear latitudinal trends in the distribution of sedimentary organic carbon and nitrogen, the lowest and highest values yet recorded are found in the tropics (Table III). The highest concentrations, particularly of carbon, in intertidal sediments have been found in mangroves on Cape York Peninsula in Australia, whereas highest values in subtidal sediments have been found on the inner shelf off the east and west coasts of India, where mudbanks occur, and where organic pollution prevails. It is not unusual to measure carbon concentrations greater than 5% and nitrogen levels greater than 1% by dry weight in some tropical muds. Total phosphorus concentrations are also frequently high (>1 mg·g -1 ) particularly in areas near domestic waste (Sankaranarayanan & Panampunnayil, 1979). Seasonal variations in particulate organic matter, particularly in estuaries, are greatly influenced by monsoonal rains. In the Vellar estuary (Porto Novo) in India (Sivakumar, Thangaraj, Chandran & Ramamoorthi, 1983) and in estuaries along the Cape York Peninsula of Australia (Alongi, 1987a), total organic matter and organic carbon and nitrogen levels decrease during the monsoon season as a result of increased river discharge and scouring of surface silts and clays and associated organic matter. In dry tropical areas, organic matter concentrations do not appear to vary seasonally (Alongi, 1987a). Lowest organic nutrient concentrations recorded in the tropics are found mainly in carbonate sediments (see references in Alongi, 1989a; Table III) where organic sedimentation is generally low and concentrations are generally lower than in quartz sand and mud of equivalent grain size in temperate areas (Premuzic, Benkovitz, Gaffney & Walsh, 1982). C/N and N/P ratios vary greatly in tropical sediments as in other latitudes. Variations in these ratios reflect the relative importance of terrestrial compared with marine origin of the deposited organic matter as C/N ratios generally less than 8 indicate a marine origin, whereas higher values suggest some terrestrial input (Premuzic et al., 1982).
392
DANIEL M.ALONGI
TABLE III Range of organic carbon and nitrogen concentrations (% by dry weight) in some tropical intertidal and shallow (< 50 m) estuarine and marine sediments. References: 1 NicholsDriscoll, 1976; 2 Nichols & Rowe, 1977; 3 Sankaranarayanan & Panampunnayil, 1979; 4 Harkantra et al., 1980; 5 Rosenberg et al., 1983; 6 Ansari, Parulekar & Jagtap, 1980; 7 Aller & Aller, 1986; 8 Alongi, 1987a; 9 Hansen et al., 1987; 10 Alongi, 1988b; 11 Riddle, 1988; 12 Alongi, 1989c; 13 Alongi et al., 1989. a=not measured; *=mean only
Dissolved inorganic nutrients Concentrations of the principal dissolved inorganic nutrients (, , , Si(OH) , ) 4 are normally lower in tropical interstitial waters (Hartwig, 1976; Ullman & Sandstrom, 1987; Williams, Gill & Yarish, 1985; Corredor & Capone, 1985; Camacho-Ibar & Alvarez-Borrego, 1988; Alongi, 1989c; Corredor & Morell, 1989) than in pore waters of sediments in higher latitudes (see review of Reeburg, 1983, for temperate references). In tropical sediments, ammonium and silicate are usually in greatest concentration, followed by phosphate and nitrate with concentrations within the µM range. Concentrations of these nutrients are usually within the mM range in sediments at higher latitudes. One characteristic of tropical sediments is the frequent presence of nitrite () in the pore waters, which is an intermediate product of nitrification (eventual reduction of to ), and generally an indication of moderate anaerobic conditions. Nitrite is found in temperate sediments but occurs most commonly in moderately anaerobic, calcareous sediments in shallow waters of the tropics. Figure 3 depicts the vertical sedimentary profiles of the major dissolved inorganic nutrients in terrigenous, mixed terrigenous-carbonate, and carbonate deposits
TROPICAL BENTHIC ECOSYSTEMS
393
across the central Great Barrier Reef continental shelf (Alongi, 1989c). At most stations, nutrient concentrations did not change significantly with sediment depth and there were no clear trends in relation to sediment type. This shelf, like most other tropical shelves, is shallow (<80 m) and frequently disturbed by storms and by demersal fish and prawn trawling. Note that subsurface maxima are common, probably caused by the presence of some buried pieces of plant detritus. Water content of tropical sediments containing various amounts of carbonate is generally low (<50%) because carbonates tend to compact more readily than terrigenous material and lithify into limestone (see Sellwood, 1986). Mud and muddy sand deposits in mangrove forests of northeastern Australia and in subtidal muds off Goa, India, have low water content, frequently containing less than 50% water (Ansari, Parulekar & Jagtap, 1980; Alongi, 1987a). Whether low water content is a characteristic of most tropical marine sediments requires further information from other areas. Intertidal sediments in the arid tropics and during the dry season in other areas generally contain more silt than clay, and undergo desiccation with corresponding increases in pore-water salinity (Alongi, 1987a,b). Regeneration of nutrients across the sediment-water interface is significantly lower in the tropics than in temperate sediments of identical grain size and at similar temperatures (Table IV; see Table II in Ullman & Sandstrom, 1987), despite a sharp gradient in nutrient concentrations between the overlying waters and sediment. Fluxes are dominated by silicate and ammonium regeneration followed by low rates of and release. Several reasons can be cited for the low rates of nutrient release: low rates of plankton production and sedimentation of dead phytoplankton cells, and relatively high rates of bacterial growth. As in terrestrial ecosystems in the tropics, it is likely that nutrients in tropical marine systems are tied up in living plant and microbial biomass.
BENTHIC STANDING STOCKS, DISTRIBUTION AND COMMUNITY STRUCTURE
INTERTIDAL HABITATS
Sandy beaches (quartz, carbonate or mixed), mud and sand flats, seagrass beds (mainly Halodule spp. and Thalassia spp.), salt marshes, mangroves, and coral reefs comprise the great variety of littoral habitats found along tropical and subtropical coastlines. Many reef shoals also foster the development of mixed vegetation types, including low wooded islands (e.g., northern Great Barrier Reef lagoon, Gibbs, 1978); coral cays are frequently colonised by patches of saltresistant plants and mangroves in creeks and sheltered areas. In many instances, littoral fringes are inhabited by calcareous algae (e.g. Halimeda) and sparse seagrass beds (Taylor, 1968; Grelet et al., 1987). The sediments of these areas are usually a mixture of carbonate and terrigenous sand. Tables V and VI provide comprehensive, but not exhaustive, compilations of meiofaunal and macrofaunal densities in tropical intertidal habitats. A number of early studies are not included because only qualitative species lists were provided
394
DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
395
TABLE IV Ranges of dissolved inorganic nutrient fluxes (µmol·m-2·day-1) across the sediment-water interface in some tropical estuarine and marine sediments. References: 1 Hartwig, 1976; 2 Balzer et al., 1985; 3 Hines, 1985; 4 Hansen et al., 1987; 5 Ullman & Sandstrom, 1987; 6 Alongi, 1989c; 7 Alongi, 1989a and unpubl. data; 8 Corredor & Morell, 1989. a=not measured; b=total nitrogen
(e.g., Rodriguez, 1959; MacNae & Kalk, 1962; Berry, 1964; Rao & Ganapati, 1968); other studies provided only biomass data or did not specify how samples were taken to assess densities per unit area (e.g., Moore et al., 1968). Heterotrophic bacterial communities have rarely been examined in tropical littoral zones and most workers have used antiquated techniques, such as plate counts, to measure microbial biomass and activity (Achuthankutty et al., 1978; Nair & Loka Bharathi, 1980). Protozoan assemblages, mostly ciliates, have been examined by several workers in the tropics, but nearly all studies are composed of species lists or are taxonomic (Ganapati & Rao, 1958; Aladro Lubel, 1984; and references therein), and as for bacteria, will not be reviewed here. One problem associated with benthic protists at all latitudes is their efficient removal from the sediments and associated debris. Alongi (1986) compared various extraction techniques in tropical sediments and found that a Percoll-sorbitol mixture (silica gel) yielded consistently greater densities than other, older extraction methods. On an areal basis, ciliate and flagellate densities in various habitats within the Great Barrier Reef lagoon range from 10 4 to 10 6 ·m -2 and from 10 5 –10 7 ·m -2 , respectively. Highest densities are usually found associated with coral reef habitats (Hansen, Alongi, Moriarty & Pollard, 1987).
Fig 3. —Vertical distribution of dissolved inorganic nutrients in pore water in sediments of varying carbonate content across the central Great Barrier Reef shelf. Arrows depict concentrations in overlying bottom water. See map in Fig 12 (top, see p. 462 ) for location of stations. Adapted from Alongi (1989c).
Community structure of macrofauna in some tropical intertidal habitats (excluding mangroves and coral reefs). B=bivalve; I=isopod; A=amphipod; P=polychaete; G=gastropod; D=decapod; AC=actinarian; *=range only; **=mean only
TABLE V
396 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
397
DANIEL M.ALONGI
TABLE V—continued
398
TROPICAL BENTHIC ECOSYSTEMS
399
Data do exist on tropical microalgal abundances (as chlorophyll a), but most of the information is not comparable because of a lack of standardised units (e.g. µg Chl a per g sediment dry weight, sediment wet weight, wet cc, dry cc, per cm 2). The data that are comparable, mostly from mangroves and coral reefs, indicate low (< 10 µg Chl a·g-1 DW) densities of microautotrophs (see review of Alongi, 1989a and p. 455 in this review). Quantitative data compiled in Tables V and VI (and several of the later tables) must be treated with caution considering the different sampling techniques and sieve sizes used, different sediment depths, and the general lack of season and site replication. Nevertheless, it is reasonably clear that faunal densities in tropical intertidal regions are not greatly different from those in analogous temperate habitats; highest faunal densities generally occur in moderately exposed and sheltered habitats, whereas lowest densities are found on exposed, coarse sandy beaches, where most tropical intertidal studies have been conducted. Many of the studies indicate that faunal density patterns are not uniform with tidal elevation; patterns vary greatly among geographical regions and habitats. Faunal abundances in mangrove and coral reef benthos have not been included in Tables V and VI because they have been comprehensively reviewed earlier by Alongi (1989a). Briefly, densities of meiofauna and small (< 5 mm) infauna are generally lower in mangroves (usually < 500 individuals·10 cm -2 and < 1000 animals·m -2, respectively) than in other tropical intertidal habitats, including coral reefs. A variety of factors is thought to be responsible for the lower densities in mangroves: negative effects of polyphenolic acids derived from mangrove roots, bark and detrital matter, low water content, and generally low concentrations of interstitial oxygen and surface microalgae. In contrast, abundances of meiofauna and macrobenthos are high in coral reefs, particularly in lagoons where sediments are less physically disturbed and rich in micro- and macroalgae and plant detritus (Grelet et al., 1987; Chardy & Clavier, 1988; Riddle, 1988; Gourbault & Renaud-Mornant, 1989). Riddle (1988) recently found high densities (3115–13690 individuals·m -2) of infauna in a comprehensive study among inner, middle, and outer reefs within the central Great Barrier Reef. Polychaetes and crustaceans, mainly amphipods, constituted most of the fauna, with low densities of molluscs. His results are typical of the numerically rich and diverse fauna found in most coral reef lagoons (Grelet et al., 1987; Alongi, 1989a). The most comprehensive studies of the ecology of tropical intertidal habitats were conducted during the Scottish-Indian IBP (International Biological Programme) project over the five years between 1968 and 1973. The purpose of the programme was to compare the productivity of temperate sandy beaches in Scotland with tropical sandy beaches on the west coast of India. The published papers of the project (Ansell & Trevallion, 1969; Edwards et al., 1970, 1971; Trevallion, Ansell, Sivadas & Narayanan, 1970; Ansell et al., 1972a,b, 1973; McLusky, Nair, Stirling & Bhargava, 1975; McLusky & Stirling, 1975; Stirling, 1975; Steele, 1976) suggested that the temperate beaches showed greater faunal diversity, greater tidal range, lower temperature and fewer fluctuations in salinity, higher levels of chlorophyll, less organic carbon, longer lived species, and greater stability of faunal composition than the tropical beaches.
Densities of meiobenthos (no. individuals·10 cm-2) and dominant taxa in some tropical intertidal habitats (excluding mangroves and coral reefs). *=archiannelid
TABLE VI
400 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
401
402
DANIEL M.ALONGI
Seasonality Temporal patterns of intertidal populations depend greatly upon distance from the Equator, and whether or not the habitat in question lies in the wet or dry tropics. In the wet tropics, most benthic communities suffer increased mortality or migrate during monsoons to escape sediment erosion and low salinities. In the dry tropics, population densities of most benthic organisms vary in response to seasonal changes in temperature, high salinity and desiccation.
Wet tropics Most seasonal studies in the monsoon-influenced areas of the tropics have been conducted in India, where winter monsoons occur on the east coast and summer monsoons on the west coast. The detrimental effects of the monsoons in India on benthic microbes (Achuthankutty et al., 1978; Nair & Loka Bharathi, 1980), meiofauna (Ganapati & Rao, 1962; Govindan Kutty & Nair, 1966; Siva Rama Sarma & Chandra Mohan, 1981; Ansari, Chatterji & Parulekar, 1984a; Kondalarao & Ramana Murty, 1988) and macroinfauna (Ansell et al., 1972a, b, c; Dwivedi, Ayyappan Nair & Rahim, 1973; Achuthankutty, 1976; Nandi & Choudhury, 1983) are well documented. Negative effects of torrential rains on tropical and subtropical intertidal fauna have also been documented for macroinfauna in Malaysia (Broom, 1982) and in Australia (Green, 1968), and for meiofauna in Florida (Bush, 1966). The response of sedimentary bacteria to prolonged torrential rains is not clear but probably varies at the species level. On sandy beaches in Goa, India, Achuthankutty et al. (1978) found that total bacterial populations (measured using plating techniques) varied in relation to organic carbon, but not to changes in salinity. The results of Nair & Loka Bharathi (1980) suggest that different morphological-functional types respond differently to salinity fluctuations. Unfortunately, the methodology used was not sensitive enough to detect clear differences among the halotolerant and limnotolerant forms. Both forms correlated positively to changes in organic carbon suggesting removal of sedimentary bacteria with erosion. Using epiflorescence microscopy to monitor bacterial numbers and tritiated thymidine uptake to measure rates of bacterial growth, Alongi (1988a) found that increased freshwater run-off in four estuaries in tropical northeastern Australia eroded intertidal silts and clays, and the associated bacterial flora in summer. Specific rates of growth of the remaining flora were, however, higher compared with growth rates during the winter dry season, suggesting a positive correlation between sediment temperature and bacterial growth. The responses of meiobenthic organisms to monsoonal rains are reasonably clear, with most studies indicating a rapid decline in numbers with the onset of the monsoons followed by rapid recovery within several weeks. Reduction of meiofaunal densities is due either to vertical migration deeper into the sediment to avoid the low salinity (Bush, 1966) and erosion, or to subsequent resuspension, or to mortality. The first two modes of depopulation are also natural pathways for recolonisation. Thus, rapid recovery coupled with the naturally high resilience of most meiobenthic organisms to disturbance is predictable in all latitudes. Rapid recovery does not necessarily equate with the return of all taxa and species to pre-monsoon community structure. Govindan Kutty & Nair (1966) noted that the maximum occurrences of respective taxa differed with season on
TROPICAL BENTHIC ECOSYSTEMS
403
sandy beaches in southwest India. Foraminiferans, ciliates, turbellarians, nematodes, copepods, and oligochaetes attained peak abundances in the premonsoon season. During the monsoon period, archiannelids, polychaetes, isopods, kinorhynchs, and gastrotrichs exhibited population maxima, whereas no group dominated after the monsoon. Several studies have indicated that oligochaetes and gastrotrichs increase proportionately during monsoon seasons (Siva Rama Sarma & Chandra Mohan, 1981; Ansari et al., 1984a; Alongi, 1987a). Oligochaetes in particular are well adapted to withstand fluctuating environmental conditions as they are usually found in high abundance in freshwater and estuarine habitats. It is less clear what effect monsoons have on meiofaunal species, as only two intertidal studies have documented changes at the species level (Alongi, 1987b; Kondalarao & Ramana Murty, 1988). In several mangrove estuaries along the north Queensland coast of Australia, seasonal variations in nematode species composition vary greatly (35 to 90%), probably in relation to the duration and intensity of monsoonal rains (Alongi, 1987a,b). The dominant species found in these estuaries, Terschellingia longicaudata, Metalinhomoeus setosus, Anoplostoma viviparum, Paracomesoma dubium, and Trissonchulus oceanus, are common inhabitants of intertidal sediments in subtropical and temperate regions, and are capable of surviving large fluctuations in physicochemical conditions. In eastern India, the species composition of harpacticoid copepods changes during flood periods in mangrove muds and in neighbouring sandflat habitats (Kondalarao & Ramana Murty, 1988). Population densities of Halectinosoma curticorne, Tachidius discipes, Stenhelia longifurca, S. madrasensis, Pseudostenhalia secunda, Nitocra spinipes, Enhydrosoma buecholtzi, and Nannopus palustris decrease, and many other species disappear completely during the monsoons. The diversity of copepods decreased at all sites during the rainy season and increased in post-flood and summer periods. A few species, such as the interstitial dweller, Laophontopsis secunda, increased significantly in abundance during the monsoon season, indicating that a few harpacticoid species thrive under low salinity conditions. Epibenthic and infaunal macrobenthic communities also respond negatively to the onset of monsoonal rains. Most data on the role of monsoons in influencing seasonal variations of macrobenthos came from the Scottish-Indian IBP project. The most stable physical and chemical conditions on the southwest Indian beaches are reached in the pre-monsoon months when species richness peaks (Ansell et al., 1972a). Beach erosion takes place during the monsoon, and only species capable of migrating persist. This scenario is identical to other monsoonal regions. For instance, on a sandy beach at Calangate Goa in India, erosion and accretion processes displace and bury infauna in the more inclined, high intertidal sands. Other studies have observed the devastating effects of the prolonged torrential rains on intertidal fauna in Goa (Achuthankutty, 1976; Harkantra & Parulekar, 1985) and in Sunderbans in India (Nandi & Choudhury, 1983). In other regions where erosion is not the primary result of monsoonal rains, it is reasonably clear that faunal responses are, in many instances, speciesspecific, and the total community response is dependent upon the frequency and intensity of climatic disturbance as well as the time of year in which it occurs. There is some evidence of seasonality on mudflats in Malaysia (Broom, 1982) being attributed to spawning triggered by the depressed interstitial salinities in October-November when the northeast monsoon arrives. The fall in salinity
404
DANIEL M.ALONGI
appears to be responsible for the increased reproductive output of species with a planktonic larval stage, such as the dominant bivalves Anadara granosa and Pelecyora trigona. Seasonal cues triggering spawning can also be inferred from the results of Vargas (1988) on a mudflat on the Pacific coast of Costa Rica. Four abundance patterns were observed among the 25 most abundant species: peaks of abundance coinciding with the dry or wet seasons, and species decreasing or increasing in population density over the one-year sampling period, which were considered random population fluctuations. Even in Goa, reproductive periodicity is indicated for several species with varying degrees of eurytolerance. The mole crab, Emerita holthuisi and the surf clams, Donax incarnatus and D. spiculum, decrease in abundance or disappear completely during the monsoon period, but recover quickly (Ansell et al., 1972a, b). All three species undergo at least two main periods of recruitment, one during the prernonsoon months and the other in the monsoon period, during which time total community diversity and species richness decline markedly (Harkantra & Parulekar, 1985).
Dry tropics In regions where rainfall is sporadic, high temperatures and desiccation are the major factors influencing seasonality of intertidal benthos. The most comprehensive study of intertidal communities in the dry tropics has been conducted in north Queensland, Australia (Alongi, 1988a, b). The dynamics of microbial and meiofaunal communities were examined over one year at four intertidal mangrove and sandflat habitats. Densities of most microbial and meiofaunal groups fluctuated significantly over time at each habitat with no distinct seasonality. Figure 4 demonstrates the apparently random fluctuations in densities of surface bacteria, ciliates and total meiofauna on the sandflat as measured over weekly to tri-weekly intervals. Such long time intervals and analysis only at high taxon level invariably mask the real influence of physicochemical factors such as temperature. In fact, protozoan and meiofaunal abundances decrease significantly over a tidal cycle during summer at these sites when sediment temperatures increase from 27°C at daybreak to 40°C at noon. During winter when sediment temperatures vary only by a few degrees over a tidal cycle, densities do not vary significantly (Figs 6 and 7 in Alongi, 1988b). Nematode communities undergo marked seasonal changes in their feeding type composition (deposit-feeders, epigrowth-feeders and predatory-omnivorous forms) in temperate and some subtropical habitats (see review of Heip, Vincx & Vranken, 1985). These changes are attributed mainly to coincident seasonal changes in available food supply. In boreal autumn and winter, populations of deposit-feeders and omnivore-predators increase in response to increases in deposition of plant detritus. In spring and summer, epigrowth-feeding nematodes attain peak densities coincident with increases in benthic microalgae. Figure 5 (left column A, B) is a schematic representation of the seasonal trends in nematode feeding types (graph B) with coincident changes in potential food resources (graph A) frequently observed in various temperate shallow-water habitats. In contrast, Alongi (1990) found that seasonal changes in nematode trophic types (greater densities in autumnwinter; lowest densities in spring and summer) on the sandflats discussed above were related to changes in temperature. Figure 5 (right column, graphs C, D) depicts the variations in feeding types on a dry tropical sandflat. Changes were not related to available
TROPICAL BENTHIC ECOSYSTEMS
Fig 4. —Temporal changes in densities of bacteria, ciliates, and meiofauna in surface sediments of a tropical sandflat with (n) and without (o) deposited mangrove detritus, Chunda Bay, Queensland, Australia (modified from Alongi, 1988b).
405
406
DANIEL M.ALONGI
food as no seasonality was observed for particulate nutrients, and bacterial and microalgal standing stocks (Alongi, 1988b). The relationship between nematode abundances and temperature may be either positive or negative depending upon the annual temperature range. In temperate intertidal habitats, the relationship is usually positive with peak densities occurring in late spring through mid-summer (Heip et al., 1985). In the wet tropics, seasonal changes are inconsistent due to the confounding effects of monsoonal rains occurring in different seasons in different geographical regions. For instance, in areas of intense monsoonal activity in India, low meiofaunal densities are found in winter. In northeastern Australia, highest faunal densities have been observed when monsoonal activity is less frequent in summer (Alongi, 1987a). The relationship is nearly always negative in dry tropical and subtropical habitats because lowest faunal densities occur during the hottest months of the year (Natividad, 1979; Alongi, 1987a, 1988a, b, 1990). Other climatic disturbances Less known is the effect of other climatic disturbances such as upwelling and the El Niño phenomenon on tropical intertidal assemblages. Bally (1987) recently reviewed the ecology of sandy beaches along the west coast of South Africa as influenced by the Benguela upwelling. Macrofaunal abundances (see
Fig 5. —Idealised diagram of temporal changes in detritus food supply to shallowwater benthos (A, C) and responses of nematode feeding types (B, D). Left-hand column (A, B) depicts temperate situation; right-hand column depicts tropical conditions (C, D). Code for top figures, I=deposition of decaying vascular plant detritus; II=sedimentation of pelagic material; III=benthic microalgae.
TROPICAL BENTHIC ECOSYSTEMS
407
Table V) and biomass are extraordinarily high along the Benguela coastline indicating strong input from upwelling offshore. Mean biomass levels range from 69 to 1249 g·m -2 along beaches with significant kelp input in northern Benguela; other South African beaches are much lower in biomass (37–53 g·m 2 ). The highest values are generally on beaches that have some food subsidy, either from kelp debris deposited by upwelling currents or from surfzone blooms of phytoplankton. There is little comparable information on microfauna and meiofauna, but the study of sandy beaches of the Skeleton coast of southwest Africa (northern Benguela) by Tarr, Griffiths & Bally (1985) indicate very low (<100·10 cm -2 ) densities of meiofauna. The effect of El Niño on infaunal communities of sandy beaches in the Peruvian upwelling system has been more extensively described (see review of Arntz, Valdivia & Zeballos, 1988). On a sandy beach of Santa Maria del Mar (south of Lima), Arntz, Brey, Tarazona & Robles (1987) investigated a surf clam (Mesodesma donacium and Donax peruvianus) community prior to, during, and after the El Nino of 1982–1983. During the event, Mesodesma donacium became extinct locally and had not recolonised the area even three years after the return of normal conditions. Donax peruvianus dominated immediately after the event, but did not attain densities comparable with those reached by its predecessor prior to the arrival of El Niño. Spionid polychaetes increased in density after El Niño indicating a fundamental long-term shift in species composition to small opportunists. Similar shifts in community structure have occurred as a result of previous El Niño events. The extent to which these upwelling communities change appears to depend upon the strength and frequency of occurrence of El Niño showing either high resilience with a rapid recovery from minor, short-term El Niño events or major decade-long changes in response to major El Niño events, as occurred in 1982–1983. Zonation The zonation of intertidal sand fauna was first popularly conceived by Dahl (1953) who described the crustacean fauna inhabiting sandy beaches in Europe and South America. He divided sandy shores into three horizontal belts: (1) the sub terrestrial fringe (“Talitrid-Ocypodid belt”), which harbours mainly talitrid amphipods on temperate beaches and ocypodid crabs on beaches in lower latitudes; (2) the midlittoral fringe (“Cirolana belt”), of which cirolanid isopods are the most common inhabitants; and (3) the sublittoral fringe which is the most diverse belt, having a rich and varied fauna with members typical of other sandy shores as well as dominant subtidal dwellers. Many subsequent workers on tropical and subtropical sandy shores have followed Dahl’s (1953) classification, basing the zonation of beach fauna on species “belts” or “associations” (Table VII). MacNae & Kalk (1962) examined the intertidal sand and muddy sandflats around the island of Inhaca at the mouth of the Bay of Lourenco Marques in Mozambique. They recognised four zones which today roughly correspond to the low, mid- and high-intertidal zones (Table VII): (1) a supralittoral (high intertidal) fringe dominated by ocypodid crabs and talitrid amphipods; (2) an upper midlittoral (mid-intertidal) fringe, dominated by the surf clam, Donax faba, tubicolous polychaetes (e.g., Phyllochaetopterus), and eurydicid isopods; (3) the lower midlittoral; and (4) infralittoral (low intertidal)
408
DANIEL M.ALONGI
fringes, dominated by the crabs Dotilla fenestrata and Macrophthalmus grandidieri, and the echinoderm Astropecten granulatus. In later studies similar zones were recognised on tropical sandy shores, particularly the dominance of ocypodid crabs in high intertidal areas (Berry, 1964; Pichon, 1967; Vohra, 1971). Gauld & Buchanan (1956) noted earlier that some beaches with steep slopes were inhabited by a very sparse fauna, mainly by the ghost crab, Ocypode hippeus, on the Gold Coast in Africa. Steep tropical beaches of coarse sand, inhabited almost solely by ocypodid crabs, are commonly known as the “Denu type”, after the town near where Gauld & Buchanan (1956) first studied intertidal zonation. They found that beaches consisting of finer sand and being less steep were characterised by a richer and more varied fauna, although the Ocypode zone was still recognised as were zones dominated by the isopod, Excirolana latipes and the lamellibranch, Donax pulchellus. Berry (1964) observed a similar faunal zonation along the shores of North Penang in Malaysia. The habitat, however, was considerably more muddy in the lower shore reaches and consisted of a more diverse fauna dominated by gastropods, tubiculous polychaetes, the burrowing anemone Cerianthus, the bivalve Pinna and the razor clam, Solen. Nevertheless, the high intertidal zone was inhabited mainly by Ocypode spp. In perhaps the most comprehensive study of tropical sandy beaches, Pichon (1967) examined the sandy shore fauna in the region of Tulear in southeast Madagascar. She attempted to define the distribution and zonation of the beaches by quantitatively and qualitatively sampling a large number of transects bisecting the beaches between the extreme tide marks. Three littoral stages were recognised: (1) the supralittoral or high littoral region, dominated by the amphipod Talorchestia sp. and the isopod Excirolana natalensis; (2) a mediolittoral or midlittoral stage, inhabited by spionid polychaetes and Excirolana orientalis; and (3) several subdivisions of an infralittoral fringe (the high subdivision of which is now more commonly accepted as being within the mid-intertidal zone) dominated by Donax elegans and D. aemulus. The first two subdivisions constitute the low intertidal zone and were dominated by bivalves, polychaetes, and enteropneusts. Pichon (1967) argued that although the species on Madagascar beaches differ from those inhabiting other tropical sands, the general scheme of Dahl (1953) and Gauld & Buchanan (1956) was applicable to her study. It was not until the Scottish-Indian IBP programme that the most comprehensive studies of intertidal zonation on tropical sandy shores were, however, made. In one of the first studies published from the project, Trevallion et al. (1970) summarised the tropical intertidal literature to date and compared the faunal zonation on the Indian beaches at Shertallai and Cochin. They noted that many differences were attributable to minor variations in exposure and beach slope, with the most extreme example being the “Denu type” of highly exposed beach described originally by Gauld & Buchanan (1956). Trevallion et al. (1970) observed that even with these qualifications a close similarity was evident among all the tropical sands studied and they summarised them as follows. An upper zone (corresponding to the high intertidal) is characterised by talitrid amphipods and ocypodid crabs. Cirolanid isopods, both marine (e.g. Exciroland) and terrestrial species, were common as well as some Donax species. Both isopods and Donax frequently occurred from the high water mark to the mid-intertidal or the middle zone, which was also inhabited by
TROPICAL BENTHIC ECOSYSTEMS
409
spionid polychaetes. Non-migratory species of Donax, such as D. faba in Madagascar (Pichon, 1967) and Mozambique (MacNae & Kalk, 1962), were common inhabitants in the lower reaches of this zone. The lower or infralittoral zone (low intertidal) was less well defined by species residents. Echinoderms, gastropods, crabs, bivalves and a very varied and numerically rich fauna occurs in the low intertidal region, particularly surface deposit- and suspension-feeding detritivores. Finally, a mobile fauna was recognised consisting of those species which migrate across tidal zones over each tidal cycle. This group includes migrating species of Donax, crustaceans of the family Hippidae (crabs), and gastropod molluscs, including species from the genera Terebra, Bullia, Olivella, Umbonium, and Olivaricella. In later studies the general applicability of Dahl’s (1953) zonation scheme (as modified by Trevallion et al., 1970) to the macrofauna of other tropical sandy habitats (Edwards, 1973a; Gibbs, 1978; Jones, 1979; Tarr et al, 1985; Jaramillo, 1987) has been recognised despite latitudinal replacement of most of the characterising species. Dahl (1953) was among the first to recognise latitudinal differences in faunal zonation on sandy beaches. For instance, he observed that talitrid amphipods inhabit the upper beaches in temperate zones, whereas in warmer latitudes, ocypodid crabs dominate or co-dominate with amphipods. Decapods are well represented on the lower reaches of tropical and subtropical beaches; in temperate and boreal regions, amphipods are the dominant crustaceans. Dahl (1953) suggested that differences in latitudinal dominance reflect differences in reproductive behaviour between decapods and amphipods. In general, tropical sandy shores are usually dominated by decapod crustaceans, isopods, and bivalve molluscs, whereas temperate sandy habitats are inhabited mainly by gastropod molluscs and polychaetes (Alongi, 1989b). Broom (1982) and Swennen, Duiven & Spaans (1982) noted the virtual absence of polychaetes in intertidal mudflats in Malaysia and South America, respectively. In contrast, Vargas (1988) found that the mudflats of Costa Rica are dominated by polychaetes and also by a rich and highly diverse microcrustacean fauna (ostracods and cumaceans). Broom (1982) suggested that although different phyla dominate in different latitudes, the various trophic types (deposit-feeders, scavengers, suspension-feeders, algal grazers, predators) are well represented worldwide, with different but similar genera filling identical niches. For example, on Malaysian mudflats the gastropod Stenothyra glabrata occupies the role of hydrobiid snails (Hydrobia) in temperate mudflats. Jaramillo (1987) found that significant changes in species composition occur with latitude along the Chilean coast, particular on the mid- and highlevels of sandy beaches. There is a decrease in the number of species of cirolanid isopods (Excirolana spp.) on middle zones of beaches from south (temperate) to north (tropics), with their absence on some tropical sites. Oniscoid isopods are found only on high-level beaches in northern Chile, talitrid amphipods only on northern central and southern central (warm temperate) beaches, and ocypodid crabs (mainly Ocypode gaudichaudii) only in tropical areas. These geographic variations are attributed to an increase in rainfall and a decrease in temperatures from north to south. Nearly all differences in species composition occur in high intertidal zones with virtually no differences at low tidal levels, indicating that hydrographic and climatic barriers (or the lack of them) are major factors fostering latitudinal differences.
Intertidal zonation of dominant macrofauna on some tropical sandy shores. D=decapod; I=isopod; B=bivalve; C= cumacean; P=polychaete; E=echinoderm; G=gastropod; Br=brachiopod; A=anthozoan; AM=amphipod. *designation of zones by tidal height varies greatly among authors and among habitats and depends upon tidal amplitude and elevation of the shore. On average, high=EHWS-MHWS; mid=MHWS-MHWN; low=ELWS-MHWN (Alongi, 1989a).
Table VII
410 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
411
412
DANIEL M.ALONGI
The apparent success of crustaceans and bivalves in the tropics can be attributed to their motility and ability to escape or avoid high temperatures and salinity or desiccation. Their physiological and behavioural adaptations to life in the tropics are discussed in a later section. Some circumstantial evidence suggests that predation is more intense in tropical intertidal habitats, further accentuating differences in phyla, and at generic and specific levels, between tropical and temperate intertidal communities. Nearly all of the evidence is based on studies of predation on intertidal gastropods (Vermeij, 1978; Garrity, Levings & Caffey, 1986). Vermeij (1978) argued that thickened shells, low spires, narrow or occluded apertures, and more pointed sculpture are much more common on shells of tropical molluscs in comparison with temperate mollusc shells. Indeed, the experiments of Garrity et al. (1986) indicate that shell-crushing predation of intertidal gastropods is greater in the tropics. Successful gastropods curtail their foraging time as a behavioural modification to avoid predation. The dominance of ocypodid crabs in the high intertidal zones of tropical beaches may be the result of their scavenging and/or predatory ability. Wolcott (1978) found that ghost crabs have no major competitors or beach predators and that their success may be attributed to flexible feeding habits. Ghost crabs are able to endure a physically unstable environment as well as long periods of starvation. Empirical evidence from two intertidal studies indicates, however, that at least on some mudflats, the infauna are not greatly controlled by either epifauna or other macro-predators such as birds and fish (Black & Peterson, 1988; Vargas, 1988). In caging experiments, Vargas (1988) found no significant changes in infaunal abundances or species composition inside cages deployed for three months on a mudflat in the Gulf of Nicoya in Costa Rica. Similarly, in Western Australia, Black & Peterson (1988) noted an apparent absence of predation or competition for space between small infauna and larger, suspension-feeding bivalves. It is likely that biotic and abiotic factors governing species composition and community structure in intertidal habitats are generally similar with latitude, with many differences being only a matter of degree (e.g. competition, temperature, grain size, rainfall, beach slope, etc.). Differences between abiotic factors can be very great, however, especially those inducing stress in the intertidal (Moore, 1972a). The dominance and adaptation of crustaceans and bivalves on tropical beaches can be invoked as a prime example that latitudinal differences in common regulatory factors (rainfall, temperature, salinity) can lead to fundamental differences between habitats at different latitudes. Diversity and species richness Differences in species composition and trophic structure do not necessarily lead to significant differences in species diversity and species richness between temperate and tropical latitudes. The earlier studies of Sanders (1968, 1969), among others, predicted highest species richness per habitat in the tropics. They hypothesised that physically stable, benign environments such as coral reefs and tropical rain forests favour the development of more diverse, species-rich communities in comparison with young or stressed regions where physical factors dominate in regulating community diversity. Thorson (1957) even earlier
TROPICAL BENTHIC ECOSYSTEMS
413
suggested that species richness increases markedly towards the Equator for epifauna, although not for infauna. It is reasonably clear that species richness (as number of species; see Table V, p. 396) and diversity (as the Shannon-Wiener function H’) are not greater for benthos in the tropics. Many workers have found species diversity levels roughly equivalent to analogous habitats in temperate regions for the same phyla (Jackson, 1972, 1973; Shelton & Robertson, 1981; Harkantra & Parulekar, 1985; Alongi, 1987b; Shin, 1987). Marine benthic diversity varies greatly within the tropics, as other studies have found very high species diversity in coral reefs (see review of Alongi, 1989a), in seagrasses (Young & Young, 1982) and on mudflats (Srinivasa Rao & Rama Sarma, 1983). Wide variations in diversity occur more commonly within the same habitat over time (Vargas, 1988) or with tidal elevation. In many intertidal sandy shores, H’ increases from high to low water with highest diversity at the low water mark (Vohra, 1971; Dexter, 1979; Broom, 1982; Harkantra & Parulekar, 1985). It is most likely that latitudinal patterns of species diversity differ at the phyletic level. For instance, a review of the literature on seagrass epifauna indicates that diversity of amphipod and decapod crustaceans increases with decreasing latitude, whereas isopod and fish diversity show no significant trends with latitude (Virnstein, Nelson, Lewis & Howard, 1984). Virnstein et al. (1984) concluded that body size generally decreases towards the tropics but with no significant trend in predation pressure, further citing an astonishingly small volume of data supporting early hypotheses of latitudinal changes in diversity. Comparative studies of species diversity and community composition of sandy beach fauna indicate that within-latitude variations are frequently greater than differences among latitudes (Dexter, 1972, 1974, 1976, 1979; Shelton & Robertson, 1981). Dexter (1974) found that the faunas of the Pacific beaches of Costa Rica and Colombia were seven times more abundant, and contained significantly more species, than the Atlantic beaches of both countries. The beaches varied greatly in many physical factors, including sediment composition and mean grain size. She found similarly wide variations in species richness and diversity on sandy beaches of Mexico (Gulf of Mexico compared with the Pacific coasts, Dexter, 1976) and in Panama (Dexter, 1972, 1979). Shannon-Wiener diversity was generally low at all of these beaches, as is typical of the habitat worldwide. The old ideas of tropical compared with temperate diversity gradients may be irrelevant, as postulated by Huston (1979), who suggested that variations in within-habitat diversity are caused by varying levels of disturbance. Intertidal regions in the tropics, in my experience, are fairly inhospitable habitats where organisms are normally subjected to desiccation, low dissolved oxygen levels, very high (>30°C) temperatures, chemical defenses of plants (e.g. mangrove tannins), and monsoons. Such conditions are borne much less frequently by their temperate counterparts. Moore’s (1972a) contention that tropical intertidal communities are, on the average, subjected to greater environmental stress than temperate organisms appears to be true in light of present information.
ESTUARIES AND LAGOONS
It is ironic that arguments concerning species diversity of benthos have concentrated on their supposedly high diversity in tropical estuaries, yet the least
414
DANIEL M.ALONGI
amount of information is available from these areas. Tropical estuaries are heavily influenced by monsoonal rains and their effects on sedimentation, erosion, and the general distribution of oxygen and nutrients. High temperatures, high turbidity, high sulphide, and polyphenolic acid concentrations, low dissolved oxygen levels and wide variations in salinity are environmental factors common to many warmwater estuaries (Wade, 1972a,b; Boto & Bunt, 1981; Epifanio, Maurer & Dittel, 1982; Maurer & Vargas, 1984). Near the mouths of major tropical rivers, seasonal freshwater run-off and concomitant transport of high concentrations of suspended solids may lead to burial, erosion or organic enhancement of estuarine benthos. High rates of sediment run-off and deposition lead to the eventual formation of estuarine embayments and lagoonal habitats in many such coastal areas. Coastal lagoon complexes develop in many dry tropical regions, originating as wavecut terraces when sea levels were lower during the Pleistocene glaciations. For instance, in the Arabian Gulf, marine terraces or “sabkhas” surround these high saline lagoons. Aeolian dunes migrate across the terraces under the influence of northwesterly or “Shamal” winds (Jones, Price & Hughs [sic], 1978). Other high saline lagoonal pools are equally ancient, formed by similar sea level changes isolating areas behind raised coral reefs receiving a subterranean supply of sea water seeping through coral stone (e.g. Di Zahavhpool, Gulf of Flat, Por & Dor, 1975). Not all coastal lagoons are hypersaline. Large stretches of the Pacific coast of Mexico consist of lagoons frequently lying between rivers and connected by “esteros”, narrow and winding sea channels which permit ocean water to enter as a typical salt wedge and having all the characteristics of stratified estuaries. Salinities vary in relation to the wet and dry seasons (Edwards, 1978). Lagoons and estuaries in the wet tropics are frequently oligohaline for long periods of time. The lagoons along the north coast of the Gulf of Guinea (Ivory Coast) are situated in an equatorial climate where the annual rainfall is about 2000 mm. In Ebrie lagoon, the largest of three main systems, temperature varies little but salinity varies with season and in different parts of the lagoon, ranging from euryhaline to oligohaline conditions. The lagoon is frequently deoxygenated by pollution and by lack of circulation in the deeper areas (Durand & Skubich, 1982).
Distribution and abundances Nearly all of the benthic surveys of tropical estuaries have taken place along the east and west coasts of India (Tables VIII, IX). Lagoonal studies have been conducted mostly in the Middle East, Australia, and Florida, focusing almost solely on macroinfauna and epifauna. Mean densities of macrofauna (Table VIII) and meiobenthos (Table IX) in tropical estuaries are at the lower end of the range compared with densities in temperate estuarine regions (see Gray, 1981, for temperate references). The limited number of studies from one biogeographical province (not to mention various sieve sizes, sampling techniques) does not allow extrapolation to other tropical areas, as Indian estuaries may be especially stressed during the southwest and northeast monsoons.
TROPICAL BENTHIC ECOSYSTEMS
415
Many pre-1975 surveys were qualitative, providing species lists and amalgamating communities using Thorson’s “parallel-level bottom” community concept. McNulty, Work & Moore (1962a,b) examined macrobenthic communities in south Florida, generalising on the distribution of feeding types in relation to sediment type. They claimed that in subtropical south Florida, the occurrences of the bivalves Tellina and Macoma were shifted in terms of sediment preference compared with their northern counterparts. In agreement with Longhurst (1959) for West Africa, they found that whereas Tellina prefers sand and Macoma prefers mud in temperate waters, in Florida, Tellina is found in all sediment types equally and Macoma prefers muddy sand and sand habitats. Other community associations were less similar to Longhurst’s (1959) or Thorson’s (1957) level bottom community characteristics, suggesting simple regional variation and the failure of the parallel-bottom community concept to apply beyond the North Atlantic. The most extensive investigations of subtropical estuarine macrobenthos were conducted by Stephenson and his co-workers near Brisbane in Queensland, Australia (Stephenson, Williams & Cook, 1972; Stephenson, Cook & Raphael, 1977, and references within). Their studies were a breakthrough in benthic ecology, focusing on the subjectivity of Thorson’s community concept and advancing the use of multivariate statistics to define community patterns. Classification and ordination techniques revealed patterns (“site-groups”) different from those constructed on the basis of obvious dominants or major species associations. Stephenson et al. (1972) maintained that Thorson’s scheme was applicable in higher latitudes, but that workers in the subtropics and tropics had failed to find communities with a few dominant species. Analysing genera which occur with Amphioplus in other habitats, they noted that very few habitats had associated genera in common and that any similarity among Amphioplus communities reflects the distribution of a single dominant genus or that similar genera follow similar environmental patterns. Using these techniques, Stephenson et al. (1977) examined the effect of a severe flood caused by a cyclone on the macrobenthos of Bramble Bay in Queensland. Thirty-six of the 74 most abundant species showed no significant effects. The others showed varying effects and were categorised as transient decreases, permanent decreases, transient increases, and permanent increases. Most increases were accounted for by increases in species of the genus Spisula. Indian studies suggest that the effects of flooding by monsoons and cyclones are a function of the duration and intensity of the disturbance, river geomorphology, and faunal composition. Salinity patterns are irregular in most Indian estuaries, but generally low during the monsoon periods, with higher values prevailing during the summer as observed in the Godavari estuary and in the Vellar estuary (Sreeramamoorty & Rama Sarma, 1986). The distribution of dissolved oxygen varies greatly among and within estuaries, dependent not only on the magnitude of freshwater input, but also on the presence of benthic algae, mangroves, and seagrass beds. It is unlikely that dissolved oxygen levels are responsible for any decrease in faunal abundance during monsoons as dissolved oxygen concentrations usually attain maximum levels during this period. Minimum levels are usually associated with post-monsoon periods. Maurer & Vargas (1984) examined abundances and diversity of soft-bottom benthos in the Gulf of Nicoya (Costa Rica) and found that the infauna was depauperate. Lower benthic density and biomass in the tropics compared with
Macrobenthic community structure in some tropical estuaries and lagoons, a=wet wt; b=infauna only; c=wet wt. with hard parts; *=mean only
TABLE VIII
416 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
417
Densities of meiobenthos (no. individuals·10 cm-2) in some Indian estuaries
TABLE IX
418 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
419
higher latitudes was reported earlier by Thorson (1957) and Stephenson & Williams (1971). Maurer & Vargas (1984) updated the tropical benthic data and concluded that tropical communities are generally low in density and biomass; Tables VII and VIII support this finding. Several explanations have been put forward to explain this phenomenon: low benthic algal production, widely fluctuating salinities, erosion, very high temperatures, and low plankton production. Benthic communities are, however, more abundant in lagoons where salinities remain tolerable (<40‰) and plankton production is enhanced by continental inputs and higher nutrient levels. Edwards (1978) measured a net water-column production of 2.45 gC·m -2·day -1 in a coastal lagoon complex in Mexico, noting that macrophytic production (e.g. Ruppia) was high enough to account for epifaunal productivity. The main sources of plant input into a lagoon are plankton and benthic microalgae, seasonal decomposition of dead vegetation (e.g. Salicornia spp.), growth of macrophytes in the wet season (e.g. Ruppia) and dry season (e.g. Enteromorpha, Cladophora) and detritus transported from fringing mangroves. In lagoons of coastal Mexico, infaunal communities are dominated by polychaetes, amphipods, and bivalves (Edwards, 1978). Some lagoonal areas dry out and are subjected to large changes in salinity. These “marisma” or peripheral zones are dominated by opportunistic polychaetes, mainly spionids, with lower numbers of corophiid amphipods. Dominant epifauna include gastropods, especially of the genus Cerithidea, and may attain densities in excess of 500·m 2 . The distribution of epifaunal invertebrates appears to be closely related to food sources, particularly macrophytic debris. During the dry season, many species aestivate or migrate to deeper channels to survive the drought conditions. In other tropical regions of the Caribbean, nearshore key lagoons occupy the centre of small oceanic isles and are mainly marine in character, supporting an abundant flora and epifauna and fringed with mangroves or patches of seagrass. Lagoons on large islands or on coasts are more estuarine, but most studies which have examined these lagoons are descriptive (e.g. Rodriguez, 1959). A nearshore marine lagoon in the upper Florida Keys was examined by Holm (1978) who found that macrofaunal densities ranged from 275 to 10808·m -2. Spionid and amphinomid polychaetes were major components of the infauna. Poriferans, coelenterates, gastropods, and arthropods were the dominant epifauna, although ophiuroids were fairly common. Vegetation was dominated subtidally by marine algae such as Chondria and Anadyomene. Holm (1978) suggested that phytoplankton was the major food source for the subtidal communities instead of Thalassia detritus, as indicated by the dominance of epifaunal suspensionfeeders. Lagoons along the Indian coastline have been examined and similarly indicate fairly high densities of macrofauna (>3000 individuals·m -2). Ashtamudi Lake in southwest India is a brackish lagoon where salinity differences among lower, middle and upper reaches greatly influence faunal dominance at the taxa level (Divakaran, Murugan & Balakrishnan Nair, 198la). Polychaetes and amphipods dominate faunal numbers and biomass in the more marine, lower reaches, whereas oligochaetes are abundant in the upper reaches of the estuary. Seasonal fluctuations are wide with some groups such as amphipods attaining peak abundances during the monsoon period. An inverse correlation was observed between salinity and total population densities. In Chilka Lake in the Bay of Bengal, mean density was 3318 individuals·m -2 with minimum densities during the
420
DANIEL M.ALONGI
July to September monsoon period (Patnaik, 1971). Meiofaunal densities were very low, as in most Indian estuarine subtidal areas, but dominated by foraminiferans; species of Polystomella, Spirillina, and Rotalia were the most common. Molluscs comprised the bulk of macrobenthic biomass. The most comprehensive study of a tropical brackish water lagoon was made by Webb in Lagos lagoon on the Guinea coast of West Africa (Webb, 1958a, b, c; Hill & Webb, 1958). The marginal lagoons in this region vary greatly in their characteristics and two types are recognised, based on the presence or absence of large rivers. Most of the lagoons are subjected to wide changes in freshwater influence. In the wet season, Lagos lagoon receives rainwater draining from large expanses of tropical forest. In the dry season, the rivers dry up into a series of isolated pools and the lagoon becomes marine near its mouth and brackish up the smaller lagoons and creeks. The benthic biota of the lagoon are thus closely tied to seasonal variations in salinity (Webb, 1958a, b, c). Pauly (1975) provides a very thorough description of the ecology of a small lagoon near Ghana, West Africa, characterising the floral and faunal components, including fishes. The gastropod, Tympanotonus radula, and the cichlid fish, Tilapia melanotheron, comprise most of the faunal biomass. Both organisms are deposit-feeders and are tolerant of the rapid changes in salinity. The number of marine species increases after the rainy period, but infaunal groups including polychaetes and oligochaetes are sparse, represented by only a few species. Benthic communities in high salinity lagoons have received considerably less attention than marine and brackish water lagoons (Fishelson, 1971; Jones et al., 1978). Several investigations have been conducted on the Sinai peninsula. In the Red Sea, Fishelson (1971) observed that shallow subtidal assemblages were dominated by many organisms found intertidally in other tropical shores. A Hippa picta-Mactra olorina community was described associated with detritus from the algae Caulerpa, Cystoseira and Padina and included the molluscs Mesodesma, Polynices, Aglaja, Murex, Strombus, Atrina, and Oliva spp. The polychaetes Perinereis, Notomastus, Pectinaria, Dasybranchus, and Eunice are common as are the sea urchins, Lovenia and Echinodiscus. Halophila-Asymmetron meadows border shallow shores and shelter a rich variety of foraminiferans, hydrozoans, serpulid polychaetes, and bryozoans. Gravel and coarse sand deposits are dominated by the foraminiferan Operculina gaimardi and by gastropods such as Turritella terebia and Strombus spp. The high saline lagoons of Dawhat as Sayh in the Arabian Gulf are dominated by gastropods, nereid and spionid polychaetes, and ampeliscid amphipods (Jones et al., 1978). Faunal densities are high (see Table VIII) considering the wide fluctuations in salinity. The high salinity in the lagoon is thought to be responsible for the absence of halophytic vegetation, echinoderms and low numbers of species of molluscs, coelenterates, and crustaceans. At these high salinities (>40‰) migration of the marine fauna ceases and insufficient connection with the open sea limits larval recruitment of the few marine residents. Hyper saline pools are absent from the Dawhat as Sayh lagoon complex, but occur frequently in upper tidal areas and are characterised by generally high salinities (80–100+‰) and a continental fauna. Hyperhaline pools, in contrast, occur in this region and are more saline (30– 300‰) with an impoverished, highly restricted, marine fauna. These latter pools dry out occasionally, but do become flooded during high spring tides,
TROPICAL BENTHIC ECOSYSTEMS
421
and replenished by euryhaline species from the neighbouring lagoons and the open sea.
Demersal fisheries Numerous studies have documented the species composition, community structure, and feeding habits of demersal fish and crustaceans (and some molluscs) in tropical lagoons and estuaries, including mangroves and seagrass beds. Several recent papers, workshop reports and books have reviewed this information (UNESCO, 1981; Kapetsky, 1984, 1985; Chullasorn & Martosubroto, 1986; Longhurst & Pauly, 1987; Lowe-McConnell, 1987), some aspects of which will be only briefly summarised here. Longhurst & Pauly (1987) and Lowe-McConnell (1987) have pointed out that the great majority of fishes found in tropical estuaries are juveniles and adults of species which are also found on adjacent shelf grounds. The distinction between estuarine and shelf-fish faunas is somewhat blurred, particularly in the wet tropics due to the ‘estuarisation’ of some continental shelves. Indeed, Sharp (1988) noted that the characteristics of fish faunas are not greatly different between the true estuarine regions off southwest Africa and the wet shelf regions of the Indo-Pacific, for example, in the Bay of Bengal and the Indonesian archipelago. A list of fish families characteristic of tropical and subtropical estuaries is difficult to compile mainly due to the large numbers of families and species recorded in many areas. For instance, in brackish waters of the Gulf of Thailand more than 300 species (all commercially utilised) belonging to nearly 30 families of demersal fish are known with many other species poorly described or only recently known (Chullasorn & Martosubroto, 1986). Several families, namely the Clupeidae, Engraulidae, Atherinidae, Chanidae, Synodontidae, Belonidae, Mugilidae, Polynemidae, Sciaenidae, Cichlidae, Gobiidae, Haemulidae, and various families of catfishes and flounders, especially the Soleidae and Cynoglossidae are, however, important. In addition, shrimps particularly of the Penaeidae, are important constituents of many demersal or semi-nektonic estuarine assemblages in the tropics and subtropics. Seasonal variations in rainfall in the wet tropics tend to alter species composition and recruitment of fish communities in many brackish water areas. For example, in estuaries along the east coast of South Africa, recruitment of juvenile fishes shows marked seasonal variation (Wallace, 1975). Most recruitment takes place in the winter dry season when river output is at a minimum, and in spring until the start of the wet season. In summer, the high rainfall reduces the number of species present and larger size classes predominate. Seasonal abundance patterns in individual fish were also not evident in Laguna Joyuda in Puerto Rico (Stoner, 1986). Fishes associated with benthic habitats showed less variation than species associated with the water column, which varied with wet season activity. Maximum standing stocks of amphipods and polychaetes corresponded closely with the influx of juvenile demersal fishes. Subsequent decline of macrobenthos after a few weeks may have reflected the effects of fish predation. In the same lagoon, Buchanan & Stoner (1988) found that high abundances of blue crabs (Callinectes sp.) correlated with high infaunal densities.
422
DANIEL M.ALONGI
As noted earlier, the importance of benthos in the diets of most tropical demersal organisms, namely fish and penaeid prawns, has generally been well documented (Longhurst, 1957a,b; Pauly, 1975; Wallace, 1975; Chong & Sasekumar, 1981; Stoner, 1986; Wassenberg & Hill, 1987; Buchanan & Stoner, 1988). Longhurst (1957b) first investigated the relationship between demersal fish and soft-bottom benthos in a West African estuary and found that macroinvertebrates were the main diet for the fish. The demersal fishes were arranged into three groups based on their diet: (1) ichthyophagous, (2) active epifauna and fish-eaters, and (3) sedentary infauna and epifauna-eaters. The first group consisted of a few species which were specialised fish-eaters. The second group consisted of those fish which consumed mainly active epifauna. The last group included those species which feed on the infauna, especially polychaetes, bivalves, brachiopods and some crustaceans. Longhurst (1957b) observed that their diets were not affected by climatic changes, with very little or no seasonal variation, although on occasions some fishes ate usually rare foods almost exclusively. Only one species showed a marked decline in feeding intensity with the onset of the wet season. In coastal lagoons of Mexico, Warburton (1978) and Yanez-Arancibia, Amezcua Linares & Day (1980) similarly classified fish communities by feeding types as (1) first order consumers (plankton-feeders, omnivores, some detritus-feeders, (2) second order consumers (mainly carnivores, including those which consumed small amounts of detrital plant matter), and (3) third order consumers (carnivores which fed exclusively on macrofauna and smaller fishes). The trophic composition of demersal fish communities is very similar in other lagoonal and estuarine systems (e.g. Lagos lagoon, Fagade & Olaniyan, 1973). Most of these studies examined trophic interrelationships by analysing stomach contents and thus it is not possible to compute rates of energy flow. Studies which have attempted to deduce energetic requirements such as rates of food consumption have been rare for warm-water, demersal organisms (e.g., Odum, 1970; Pauly, 1976). The predominance of demersal fishes and crabs in tropical lagoons and estuaries suggest, however, a strong trophic link between the benthos and species of demersal fisheries, and indigenous fishermen. This link is probably stronger in the tropics than in higher latitudes because many species of fish regarded as ‘trash fish’ in developed nations are readily consumed by humans in poorer nations. Pollution It is very likely that estuaries, lagoons, and other tropical coastal habitats will become more polluted with higher population densities of humans in the future (Hatcher, Johannes & Robertson, 1989). These authors argue that pollution is likely to be more catastrophic in tropical marine environments because such warmwater habitats are intrinsically more fragile. That is, dissolved oxygen and nutrient levels are naturally low in the tropics suggesting that tropical habitats are closer to the brink of catastrophe if pollution is introduced. Many tropical habitats are polluted, but the number of studies which have documented such effects on softbottoms is low (McNulty, 1961; Rosenberg, 1974; Abdul Azis & Balakrishnan Nair, 1983; Govindan, Varshney & Desai, 1983; Raman & Ganapati, 1983;
TROPICAL BENTHIC ECOSYSTEMS
423
Thompson & Shin, 1983; Balakrishnan Nair et al., 1984; Varshney, Govindan & Desai, 1984; Ansari, Ingole & Parulekar, 1986b; Leong et al., 1987; Varshney, Govindan, Gaikwad & Desai, 1988) compared with the number of temperate studies (see review by Pearson & Rosenberg, 1978). As with temperate sea floors inundated with pollution, tropical benthic communities are negatively affected by environmental alteration. In Biscayne Bay, Florida, McNulty (1961) was among the first workers to examine sewage pollution in the subtropics. He observed an absence of benthic life at some stations closest to the point sources with a “peak of opportunists” (sensu Pearson & Rosenberg, 1978), namely tubiculous amphipods, some distance away. These areas were revisited by Rosenberg (1974) more than 15 years later. Rosenberg found higher densities (280–650 individuals·m -2 ) than McNulty (1961), who originally estimated densities of between 110 and 278 individuals·m -2 . Rosenberg, however, found lower biomass indicating that the benthic communities had evolved towards smaller individuals more densely packed together. An analysis of the species present indicated a major change in composition from an equilibrium assemblage to one dominated by opportunists as pollution had increased with time in the Bay. Most of the other tropical pollution studies similarly indicate a dominance of small opportunistic species and a lowering of species diversity in proximity to the point source(s) of pollution. For instance, on a transect grading away from a sewage inlet in Visakhapatnam Harbour in the Bay of Bengal, the macrobenthos exhibited peak densities of opportunists a moderate distance from the source (Ansari et al., 1986b). The sea floor closer to the sewage was smothered with organic matter and no benthic life was present. After the peak of opportunists, population densities decreased to normal levels and species diversity (H’) increased from 1.18 to 4.74 and Capitella capitata was the dominant opportunist as observed in polluted temperate areas. In some coastal areas of India, even ‘control’ sites may be polluted as indicated by the lack of major differences between sites receiving domestic sewage and sites that were supposedly controls (Ansari et al., 1986b; Varshney et al., 1988). Thompson & Shin (1983) similarly found a benthic gradient in response to sewage pollution in Victoria Harbour, Hong Kong. The infaunal communities responded by conforming to the pattern of an abiotic area successively replaced with distance from the pollution source by a peak of opportunists, an ecotone point, and an eventual transition to a normal fauna. The oligochaete, Thalassodrilides gurwitschi, and the polychaetes, Capitella capitata and Minuspio cirrifera, were the dominant opportunists present and more abundant than observed nearly seven years earlier (with presumably much less organic pollution as well). Thalassodrilides has not been described as an opportunist before this study, but it is a common genus in subtropical and tropical estuaries of the Americas and the results in Hong Kong suggest that it may be an important indicator species of pollution in tropical habitats. Meiobenthic communities in the tropics appear to respond similarly to organic pollution (Abdul Azis & Balakrishnan Nair, 1983; Govindan et al., 1983), at least in India where the only such studies have been conducted. Along estuaries and lagoons of the west coast of India in the vicinity of Bombay, large amounts of sewage are emitted into nearshore waters. Densities and biomass of meiofauna are reduced in close proximity to the pollution sources and densities are extremely low at all study sites (>100·10 cm -2 ), although many of the
424
DANIEL M.ALONGI
transects also exhibit gradients in water depth, temperature, salinity, and sediment composition. Some notable effects occur at the phyletic level such as the appearance of kinorhynchs and gastropods only at offshore (and presumably, less polluted) sites. Studies of organic pollution in these areas are rendered difficult by confounding factors such as monsoonal rains and the input of industrial wastes (Varshney et al., 1988). It is likely that much of the west coast of India is disturbed to varying degrees considering the high amounts of silt, low levels of dissolved oxygen, and very low densities of meiofauna observed in much of this region. Nevertheless, at the species level, the effects of organic pollution on meiofauna have been noted by Abdul Azis & Balakrishnan Nair (1983) in the backwaters of Kerala along the southwest coast of India. Pollution in these backwaters is caused by subtidal deposition of retted coconut husks, which leads to the development of a sulphide biome. The number of species is low (12) compared with nonretting zones (28). The nematodes, Sabatieria intermissa, Desmodora sp., and Dorylaimus sp., are disproportionately abundant in the retting area; species of the genus Sabatieria are usually abundant in sulphide-rich sediments and are frequently found to inhabit polluted sediments worldwide (Heip, Vincx & Vranken, 1985). Foraminiferans and most of the crustaceans found in the non-retting zone were not found in the sulphide biome. As in other Indian estuaries, however, meiofaunal densities are depauperate suggesting that pollution is widespread. Probably only the relative effects of pollution can be observed in this area. The effects of other types of pollution such as petroleum hydrocarbons on tropical benthos have rarely been observed. In Brunei, Leong et al. (1987) found that population densities of intertidal and subtidal macrobenthos were much lower in proximity to a crude oil terminal. The opportunists Capitella capitata, Pseudopolydora sp., and Mediomastus sp. were most abundant subtidally at the terminal discharge site. The polychaetes, Scolelepis sp. and Leiocapitellides sp., and the crustaceans, Canuella perplexa and Microprotopus sp., were more abundant intertidally near the discharge area. Although few in number, studies which have examined the effects of pollution on tropical benthic communities have shown that the responses are nearly always negative and not unlike those predicted by Pearson & Rosenberg (1978) for temperate assemblages. Species diversity and richness Many subtidal benthic communities in the tropics are less abundant in terms of numbers of individuals and species, and less diverse, compared with temperate benthic assemblages. Wide variations in abundances and species richness exist among faunal groups within all latitudes. Maurer & Vargas (1984) and Maurer, Vargas & Dean (1988) noted a mean Shannon-Wiener diversity of 1.91 (range=0 to 3.09) in a tropical estuary of Costa Rica. A listing of benthic invertebrates in the estuary suggests a habitat no more rich in species than most temperate estuaries. Wade (1972b) and later, Wu & Richards (1981) suggested that tropical communities in fluctuating environments will have low density and be dominated by a few species. Benthic communities in Indian estuaries are indeed characterised by low population densities and low species richness (see Tables VIII, IX, pp. 416 and 418 ), perhaps an indication of severe environmental stress. In the Indian
TROPICAL BENTHIC ECOSYSTEMS
425
estuaries, wide fluctuations in salinity and erosion caused by monsoons, low dissolved oxygen concentrations, and high temperatures are commonplace and are probably in many ways more stressful than environmental conditions to which temperate benthic organisms are subjected (low temperatures, erosion caused by ice movement, freezing). Polluted tropical environments are also characterised by low species richness and diversity (e.g., Rosenberg, 1974). Other stressed habitats include basins which periodically turn anoxic, for example, in the Golfo Dulce of Costa Rica (NicholsDriscoll, 1976), in the Fosa de Cariaco basin off Venezuela (Nichols, 1976), and some estuaries in India. Depending upon water circulation and dissolved oxygen levels, species diversity (H’) and richness varies greatly in some Indian estuaries as in the Kulti and Bidyadhari rivers (Datta & Sarangi, 1986). The influence of sewage, industrial wastes, high turbidity, and variations in organic input may also have a direct bearing on the inconstancy of community composition in many tropical estuaries. Low densities and biomass have also been recorded from a number of other stressed and non-stressed tropical habitats (Longhurst, 1959; Wade, 1972a,b; Rosenberg, 1974; Nichols, 1976; Nichols-Driscoll, 1976; Holm, 1978; Wu & Richards, 1981; Shin & Thompson, 1982; Maurer & Vargas; 1984). Low densities are probably the result of stress caused by frequent and wide variations in physicochemical factors, by greater predation and less food input. The Indian studies indicate conditions favourable for the development of opportunistic assemblages, which are usually species-poor. Shifts at the phyletic level appear to be common as a result of monsoons; foraminiferans and turbellarians have been observed to disappear entirely during monsoonal periods in some estuaries (Fernando, Khan & Kasinathan, 1983) with a decrease of total population densities. The study by Bhat & Neelakantan (1988) in the Kali estuary, central west coast of India, indicates that organic carbon in sediments, and salinity are the most highly significant factors governing macrobenthic densities in the estuary. Estuarine benthic invertebrates of all latitudes are controlled by the same fluctuating conditions (Wolff, 1983), but unfortunately there is not enough tropical data to assess properly the applicability of Remane’s classic species-salinity relationship to lower latitude communities. It is clear, however, that many estuarine subtidal assemblages in the tropics are less diverse and more depauperate of individuals and species compared with temperate communities.
CONTINENTAL SHELVES (INCLUDING MARINE COASTAL REGIONS)
The first exploration of tropical continental shelves began off the western edge of Africa in the 1950s (Sparck, 1951; Buchanan, 1957, 1958; Longhurst, 1957a, b, 1959). It was not until the mid-1970s, however, that there was a discernible increase in the study of tropical benthic communities on continental shelves (Tables X, XI). The majority of studies have been conducted off the east and west coasts of India and along the west coast of Africa where demersal fisheries first developed in the tropics (Pauly, 1979; Longhurst & Pauly, 1987). Comparatively little data exist for microbes on low latitude shelves, with nearly all of the available data obtained in the past few years (e.g. Alongi, 1989c; Lok Tan & Ruger, 1989; Alongi, Boto & Tirendi, 1989). These sparse
426
DANIEL M.ALONGI
data will be assessed within the context of ecosystem dynamics in a later section (p. 457). Meiofauna on tropical continental shelves have also only been sporadically investigated, with most of the information obtained from the Indian Ocean (Table XI). Nevertheless, the available data suggest low to moderate densities compared with communities of higher latitudes (see temperate references in Heip et al., 1985, and in McLusky & Mclntyre, 1988). The data for shelf macrobenthos are considerably greater, although also nearly exclusively quantitative, indicating low densities and biomass except in areas of upwelling where primary production is enhanced. Data for macrobenthic diversity and species richness on tropical shelves are rare (e.g. Damodaran, 1973; Lee, 1978), with most available information focusing on megafauna such as echinoderms, corals, some molluscs and fishes (Briggs, 1985; Birtles & Arnold, 1988; Steele, 1988). Several environmental factors appear to mitigate against the development of stable, high diversity benthic biocoenoses on some low latitude continental shelves. Many warm-water shelves are warm, wide and shallow, susceptible to stress from climatic disturbances such as monsoons, or by infringements of mass water movement and lack of seasonal water-column turnover, both of which facilitate the development of oxygen minimum zones. Upwelling The benthos of upwelling regions has been reviewed by Thiel (1978) and Rowe (1981). Not surprisingly, benthic standing stocks are high beneath the highly productive surface waters in these regions. The available studies listed in Table X support this concept, but in some areas oxygen becomes depleted in the nearbottom water because of high rates of detrital deposition and microbial decomposition. This leads to a build-up of hydrogen sulphide and organic matter in the sediment resulting in reduction or, in some cases, obliteration of the benthic fauna. Rates of sulphate reduction and denitrification are high in these oxygendepleted areas, and extensive mats of sulphur bacteria develop. Gallardo (1977) observed large contiguous microbial mats at depths of 50–280 m off the coast of Chile in sulphide-rich sediments underneath the deoxygenated waters of the Peru-Chile Subsurface Countercurrent. These mats are called “estopa” (meaning uncleansed wool or flax in Spanish) by local fisherman because of the dominance of filamentous bacteria. At 60-m depth off Concepcion, Chile, Gallardo (1977) found that microbial biomass (1060g WW·m-2) greatly outweighed infaunal biomass (115g WW·m -2 ). The dominant prokaryote is the gliding bacterium, Thioploca spp., and the other constituents are cyanobacteria, flexibacteria (Chlorophlexis) and other bacterial morphotypes. The sediments in this region are diatomaceous mud containing leftover remnants of obliterated benthic communities, including empty polychaete tubes, shell fragments, faecal pellets and fish scales. It is likely that highly productive sites within other upwelling regions have similar sulphureta communities. Rosenberg et al. (1983) conducted a more comprehensive investigation of the benthic ecosystem in this region, examining macrobenthic biomass and species composition, the microbial mats, dissolved oxygen, sedimentary organic matter, and demersal fish catches. Macrofaunal biomass correlated positively with oxygen concentrations and negatively with Thioploca biomass over most of the region;
TROPICAL BENTHIC ECOSYSTEMS
427
high infaunal biomass was found only nearshore (0– 2 m depth). Summarising previous work and their own data, Rosenberg et al. (1983) divided the sea floor off Peru into six zones: (1) exposed beach, where oxygen is at saturation levels, and animal biomass and individual body sizes are large, but where species diversity is low; (2) sheltered beach, where environmental conditions and faunal characteristics are very similar to exposed beaches; (3) coastal areas (3–20-m depth), where oxygen levels vary with season, but where biomass is still high to moderate as is species diversity; (4) deeper coastal areas (20–80 m) where oxygen levels begin to become stressful to benthic life as evidenced by a decrease in biomass and diversity; (5) the continental slope (80–700-m depth), which exhibits a permanent oxygen deficiency (0.1–1 ml·l -1) and low biomass and diversity (Thioploca, nematodes and cirratulid polychaetes dominate); and (6) the deep sea (>700-m depth) where organic deposition is lower than on the shelf proper and slope. This fauna is typical of other deep-sea communities (Frankenberg & Menzies, 1968; Rowe, 1971a). Upwelling also occurs in inner shelf embayments and gulfs which only intermittently receive intrusions of oxygen-rich waters, causing anoxia for long periods. For example, Golfo Dulce on the west coast of Costa Rica is usually anoxic. Nichols-Driscoll (1976) found very low abundances and biomass of macro-infauna within the gulf despite high concentrations of sedimentary organic nitrogen and carbon. Diversity (as H’) was also generally low, ranging from 1.3 to 1.8. Along an inner sill (60–70 m) within the Gulf, the fauna was rich (650 to 9240 individuals·m -2 ) but biomass was still low. The fauna was mainly composed of small opportunists which are most capable of repeated colonisation when intermittent intrusions of oxygenated water permit the flushing of stagnant waters. Other anoxic regions undoubtedly exist (e.g., off Chile and southwest Africa) near upwelling centres where primary production is very high and oxygen levels are reduced to about 5% of saturation (Nichols, 1976; Rowe, 1981; Thiel, 1982). In upwelling sites where conditions do not lead to the development of anoxic sediments, benthic standing stocks are high. Off northwest Africa, for instance, benthic biomass and densities are high, ranging from 2.4–94.4g WW·m -2 and 1635 to 35 200 individuals·m -2, respectively, over the entire continental shelf (Table X). Megafauna are most abundant along the shelf-slope boundary where shelf-break upwelling produces considerable amounts of organic matter. Rowe (1981) estimates that the secondary production of this group is approximately =0.2 gC·m -2·yr -1, an order of magnitude lower than that of the infauna. Microbial and meiofaunal communities in upwelling areas have been extensively surveyed only off northwest Africa (Thiel, 1978, 1982; Lok Tan & Ruger, 1989). Meiofaunal densities in this region range from 600–2800 individuals·10 cm -2 over a depth range of 50 to 500 m, generally higher than on non-upwelled, continental shelves (see Table XI). The relatively high densities are probably the result of high food availability from upwelling. In fact, sedimentary chlorophyll values off northwest Africa are equal to or higher than in many shallower sediments (Thiel, 1982). Latitudinal differences along the northwest African coast appear to be related to the intensity of upwelling. Further south, off Cape Blanc, the lower continental slope has a richer fauna and higher concentrations of organic matter than on the upper slope, deviating from the expected decrease in faunal abundances with depth and underscoring the importance of enhanced food supply from upwelling. Bacterial standing stocks and
-2
TABLE X
Densities (no.·m ) and biomass (g WW·m ) of macrofauna on some tropical and subtropical continental shelves, a=dry weight; *=range only; **=mean only
-2
428 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
429
2
TABLE XI
Densities (no.·10 cm ) and biomass (mg WW·10 cm ) of meiofauna on some tropical and subtropical shelves, a=dry weight; *=range only
-2
430 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
431
activity also relate to variations in upwelling intensity. Off northwest Africa, Lok Tan & Ruger (1989) observed that highest densities (2.2×10 8 cells·g -1 DW) and biomass (14.8 µgC·g -1) of sedimentary bacteria were recorded at 21°N, a site for year-round upwelling, with correspondingly lower densities and biomass at different latitudes. Direct counts of bacteria were higher in deep sediments at 2°C than in shallow sediments at 20°C indicating that all benthic components respond more to favourable food inputs than water depth or temperature. Sea-bed comparisons between upwelled and non-upwelled sites are rare (Smith, Rowe & Clifford, 1974; Lee, 1978). In the Gulf of Panama, upwelling occurs in the dry season when primary productivity nearly doubles compared to during the wet season (Lee, 1978). Recruitment of macrofauna occurs mainly during the latter half of the upwelling resulting in high seasonal densities. After the upwelling, total densities and species richness decrease rapidly. Most of the species are opportunistic, responding rapidly to seasonal changes in food availability. In the nearby Gulf of Chiriqui, there is no upwelling and the benthos fluctuates much less than in the upwelling region; opportunists are also less numerous. Lee (1978) hypothesised that recruitment occurs during upwelling phases because of increased food availability; more food increases the probability of larval survival. Species-rich, dense communities can be maintained in an unstable environment where competition and physical factors are not able to account for seasonal changes. Predation by epibenthic predators, mainly portunid crabs, appears to be the major factor regulating communities in the upwelling regime off Panama but the generally high densities of both infaunal prey and epibenthos must ultimately be regulated by food supplied from upwelling.
A special case: El Niño-Southern Oscillation (ENSO) ENSO events involve a massive alteration of oceanographic conditions (see p. 387 ) which affect both positive and negative changes on the sea floor off central Peru, and to a lesser degree, along most of the western coastline of South and Central America. Glynn (1988) has recently summarised the general ecological effects of the ENSO event of 1982–1983, probably the strongest of this century. The event had marked effects on the “mariscos” or commercially exploited invertebrates and other noncommercial benthos, from the rocky and sandy shores to the deeper sea floor. Many crabs, molluscs and sea-urchins suffered mass mortalities while others recorded post-event increases (scallops, octopus, purple snail) or extended their distribution (stalked barnacles, swimming crabs, shrimps, rock lobster). The result was generally beneficial for the fisherman, particularly those exploiting the enormous population increases of the local scallop (Argopecten purpuratus). The migration of several species of penaeid prawns which normally live in warmer waters produced a boom to the local fishery by giving rise to a new market. Less profitable was the harvesting of the stalked barnacle (Pollicipes elegans) which replaced many shellfish wiped out on the rocky shores. The proliferation of other commercially-exploited species such as Octopus fontaneanus, Thais chocolata, and Squilla paramensis helped to fill in gaps during closed seasons of the scallop fishery. After ENSO, the crab fishery recovered, but a large proportion of the fishermen switched to fishing for scallops and rock lobsters (Arntz, Valdivia & Zeballos, 1988).
432
DANIEL M.ALONGI
Soft-bottom macrobenthic communities also responded positively to the ENSO event of 1982–1983 (Tarazona, 1984; Arntz et al., 1987; Tarazona, Salzwedel & Arntz, 1988a,b). In the Bay of Ancon off Peru, the benthos normally suffers from hypoxia and, at times, anoxic conditions (Rosenberg et al., 1983). During and after ENSO, the warmer water temporarily converted this cold upwelling zone into a subtropical or tropical environment, and oxygen conditions of the near-bottom waters improve considerably. These changes allowed colonisation by species introduced by the inflow of subtropical or warmwater masses or by resident species held in check by the normally low oxygen conditions. Figure 6 delimits the effects of the 1982–1983 ENSO event on the soft-bottom benthos of the Bay of Ancon. In the first months of ENSO (OctoberDecember 1982) the number of species increased from 6 to 24 due mainly to recruitment of polychaetes. No crustaceans or molluscs were found before September 1982 and after May 1984. Population densities and biomass increased markedly with the onset of ENSO and oscillated greatly for the next twenty months, closely mirroring oxygen concentrations in the near bottom waters (Tarazona et al., 1988a, b). The ophiuroids, Ophiactis kroyeri, and the polychaetes, Leitoscoloplos chilensis, Magelona phyllisae, Paraprionospio pinnata, Sigambra bassi, Polydora aggregata and Chaetozone sp., dominated in numbers. Densities before the ENSO averaged <425·m -2 and increased to 13550·m -2 in the early ENSO months. Species diversity nearly tripled by the end of February 1983 (Fig 6). The species changes were distinguished as follows: (1) “tolerant residents” or those abundant under the normal hypoxic conditions, (2) “immigrants” or those which invaded during the ENSO event; and (3) “opportunists” or those which persist in low numbers normally, but proliferate rapidly when oxygen concentrations improve. The upwelling ecosystem off the Peruvian shelf is unusual within the tropics, having many of the characteristics of temperate biocoenses, and having evolved the ability to respond rapidly to environmental changes induced by ENSO. Benthic responses are, however, not greatly different to those expected by the stress recovery model of Pearson & Rosenberg (1978). Their model was developed from the responses of temperate communities to disturbance, signifying the universality and predictability of benthic recovery from stress, irrespective of latitude. Shelf benthos of the Indian Ocean Knowledge of the distribution and abundances of benthic communities on tropical shelves is most extensive for the Indian Ocean, due mainly to Indian and Soviet work conducted during the 1960s and 1970s (see Tables IX and X, and review of Neyman, Sokolova, Vinogradova & Pasternak, 1971). Figure 7 summarises the distribution of macrobenthic biomass (g WW·m-2 ) in the tropical and subtropical latitudes of the Indian Ocean. The highest benthic biomass is found in the northern half of the Ocean, on the shelves bordering India, Pakistan, and Iran and near oceanic islands. The Arabian Sea has the richest bottom fauna where biomass can exceed 500 g WW·m -2 and averages about 35 g WW·m-2 (Neyman, 1969; Neyman & Kondritskiy, 1974). Southward, it decreases gradually along the coasts of the Arabian peninsula and Africa from 15–20 to 3–5 g WW·m-2, and along the western coast of India from 25–30 to =5 g WW·m-2 (Savich, 1971; Harkantra, Nair, Ansari
TROPICAL BENTHIC ECOSYSTEMS
433
Fig 6. —Numbers of species (·0.12 m-2), density (·0.04 m-2), biomass (g AFDW·0.04 m-2), diversity (H’, log ) and evenness (log ) of soft-bottom macrobenthos at 342 m depth in Ancon Bay,2 Peru (September 1981 to September 1984). Shaded area corresponds to the El Niño period. From Tarazona et al. (1988a); reproduced with permission of Springer-Verlag.
& Parulekar, 1980). The rich bottom life in the Arabian Sea is attributed to the extreme richness of plankton in the region enhanced by intensive intrusions of subsurface water during the monsoons. Where ridges or sills have developed, low oxygen and high hydrogen sulphide conditions are common and the benthos is very impoverished (<0.01 g·m -2) or, in some areas, entirely absent. The benthos of the eastern half of the Indian Ocean is less abundant than in the more productive western half. Benthic biomass in the Bay of Bengal and in the Andaman Sea is generally within the range of 1 to 10 g WW·m -2 (Ansari,
434
DANIEL M.ALONGI
Fig 7. —Large-scale distribution of soft-bottom benthic biomass (g WW·m-2) in the Indian Ocean (modified and updated from Neyman et al., 1971).
Harkantra, Nair & Parulekar, 1977). The meiobenthic fauna is similarly poor, with densities of less than 250·10 cm -2 and biomass not more than 3.5 g·m -2 (Rodrigues, Harkantra & Parulekar, 1982; Table X). The depauperate fauna is probably the result of low plankton production in these sharply stratified, low salinity, surface waters (Qasim, 1979). Analogous biomass values are found in the central regions of the Andaman Sea, where microbial and meiofaunal densities are also very low (Rao, 1980; Ansari & Parulekar, 1981). Further east, in the southeast Asian region, benthic biomass and abundances are rich mainly near certain areas of the Malay Archipelago, along the western coasts of Sumatra and Java, where intensive upwelling periodically occurs. In the Malacca Strait connecting the Indian and Pacific Oceans, macrofaunal and meiofaunal densities are low (means of 258 m -2 and 149·10 cm -2 , respectively), but biomass of both components are generally high (Parulekar & Ansari, 1981b). Macrofaunal biomass varies from 0.2 to 70.9 g WW·m -2 , averaging 14.5 g·m -2 . Meiofaunal biomass is moderately high, averaging 9 g WW·m -2 and ranging from 1.0 to 26.9 g·m -2 . Many southeast Asian coasts are not influenced by upwelling. In these areas, benthic densities and biomass are low (Sek Harbour, Papua New Guinea, Stephenson & Williams, 1971; Bay of Nha Trang, Vietnam, Gallardo et al., 1977; Hong Kong harbour, Shin & Thompson, 1982; northern coast of central Java, Warwick & Ruswahyuni, 1987; Seribu Islands, Aswandy, Kastoro, Aziz & Al Hakim, in press; Kastoro, Aziz, Aswandy & Al Hakim, in press; Negros Oriental, Philippines, Estacion & Onate, in press; eastern Gulf of
TROPICAL BENTHIC ECOSYSTEMS
435
Thailand, Chareonruay, 1980). Shin & Thompson (1982) and Warwick & Ruswahyuni (1987) have suggested several reasons for the low biomass and densities: (1) low plankton production; (2) high temperatures; (3) wide range of salinities; (4) low dissolved oxygen levels; (5) a stratified water column; and (6) a moderate to high degree of climatic disturbance. Mudbanks Seshappa (1953) first described how populations of molluscs, ophiuroids, and polychaetes disappear when the famous mudbanks or “chakara” of the Malabar coast off southwest India are destroyed during the southwest monsoon in July to September. The benthic communities do not fully recolonise the mudbanks for at least six to eight months. Abundances of macrofauna are very variable, depending upon the migratory stage of particular mudbanks and the season of the year (Kurian, 1971; Damodaran, 1973). Seshappa (1953), Damodaran (1973), and Harkantra & Parulekar (1987) recorded very low abundances of macro-infauna, generally no more than several hundred animals per m 2 with some stations on some banks devoid of infauna. Off Cochin, the fauna is composed mainly of polychaetes (82.5%) dominated by Nephthys, Glycera, Nereis, Aphrodita, Owenia, Onuphis, Diopatra, and Pectinaria (Harkantra & Parulekar, 1987). The shelf was sampled during the pre-monsoon season, when densities would be expected to be low corresponding to the minimum period of primary production. In the mudbanks south of Cochin, benthic biomass is high (400 g WW·m -2) during June-July, but declines to <50 g WW·m -2 by SeptemberOctober after the monsoon season. Biomass of macrofauna is less further north of Cochin, ranging from 30–100 g WW·m -2 . On some mudbanks, dense populations of tube-dwelling polychaetes (e.g. Sabellaria cementarium) develop when the mudbanks first form, but quickly vanish when the mudbanks disappear (Damodaran, 1973). Less information is available for the meiobenthos of the mudbanks (Damodaran, 1973; Ansari, 1978). Densities are generally high (>1000·10 cm -2) during pre-monsoon months, but become rapidly depleted during the southwest monsoon period when bottom muds are resuspended and the banks are destroyed. Recolonisation by meiofauna is faster than for the macrobenthos, with complete recovery attained in a few months. Crustaceans appear to be most affected by destruction of the mudbanks, probably the result of sulphides released into the water column. On more stable muds closer to the coast, high population densities of meiofauna appear to be maintained thoughout the year (Ansari, 1978). Unlike most other muddy habitats, foraminiferans are comparatively abundant; factors causing these high densities are unknown. Effects of major rivers The distal effects of major river run-off of freshwater and suspended sediments on tropical nearshore habitats are well described compared with knowledge of proximal effects. A few studies have examined benthic communities in close proximity to major river mouths (Neyman, 1969; Harper, McKinney, Salzer & Case, 1981; Rhoads et al., 1985; Aller & Aller, 1986). In the immediate
436
DANIEL M.ALONGI
proximity of the mouths of the Ganges and Irrawaddy Rivers, Neyman (1969, and references therein) recorded biomass values in excess of 40 g WW·m -2. Some distance from both rivers, benthic biomass is generally low, seldom greater than 10 g WW·m -2 . In the Gulf of Mexico, large-scale hypoxia occurs off the Louisiana coast west of the Mississippi Delta during spring when the Mississippi and Atchafalaya Rivers discharge large volumes of fresh water and silt (Harper et al., 1981). Polychaetes are not greatly affected by hypoxia, but crustaceans and echinoderms are most affected, with a decline in total densities. In July, waves caused by summer storms relieve the hypoxia and population blooms occur as recolonisation takes place. Off many of the large rivers, sediment burial per se is the cause for benthic decline (Rhoads et al., 1985; Aller & Aller, 1986). Based on their work in the East China Sea off the Changjiang, Rhoads et al. (1985) modelled the response of benthos to river effluent. Closest to the river mouth episodic deposition and erosion events take place and benthic communities are routinely made extinct with little influence on sedimentary facies. With distance from the river mouth, rates of sediment deposition decrease and rates of primary production increase as a result of nutrients borne by the river effluent. In these mid-shelf regions away from the river, conditions allow for the development of abundant benthic populations with diverse feeding habits. Bioturbation, burrows, tubes and feeding activities modify the sedimentary record by obliterating physical laminations. Most fauna live at the sediment surface feeding on bioseston. Benthic standing stocks decline further from the river mouth because of oligotrophy on the outer shelf. This scenario applies to the benthos off the Amazon (Aller & Aller, 1986). Stations within the delta are nearly devoid of benthic life due to the very high rates of sediment turnover and the development of fluid mudbanks. Bacterial abundances are low within the inshore muds, but are higher several hundred kilometres northwest of the delta, with densities over the region ranging from 1.3 to 21×10 9·g -1 DW in the top 10 cm of sediment. Meiofaunal and macroinfaunal densities mirror the variations in bacterial abundance with fluid mudbanks generally devoid of benthic life. In firm muds some distance from the river mouth, maximum abundances are exhibited by the meiofauna (2045·10 cm -2) and infauna (3953·m -2 ). Nematodes and polychaetes are the dominant taxa, and the communities are characterised by small-size, low diversity, and high mobility. The responses of infaunal communities off the Changjiang and Amazon River Deltas are very similar. High rates of physical disturbance, an unstable sea bed, and generally low food inputs appear to be the major factors controlling the structure and function of benthos off major subtropical and tropical rivers. More comprehensive investigations are, however, necessary to determine the universality of the Rhoads’ et al. (1985) model for the effects of major river effluent in low latitudes. Carbonate-dominated shelves Several continental shelves in the subtropics and tropics are carpeted, to varying degrees, with carbonate deposits (see p. 390 ). The early studies of Buchanan (1957, 1958) and Longhurst (1957a, b, 1959) off west Africa were the first to indicate faunal differences between shallow tropical shelves and their quartz sand-
TROPICAL BENTHIC ECOSYSTEMS
437
dominated counterparts in higher latitudes. Off Ghana, Buchanan (1957, 1958) recognised four distinct animal communities. (1) A transition zone between the surf zone and shallow subtidal dominated by infauna. (2) An inshore fine sand community (13% CaCO ) dominated by the bivalve Cultellus tenuis and the tube3 dwelling polychaete Diopatra neapolitana. Other dominant forms are patchily distributed as “Owenia beds”, “Accra Bay silt patches or Macoma beds” and “Dentalium zones”. (3) A silty-sand community with varying amounts of carbonate (30 to 50%); two species of large foraminiferans dominate this transitional sea bed (Jullienella foetida and Schizammina sp.) —a single specimen can weigh up to 1.5 g. Epifaunal organisms are abundant, particularly ophuiroids and holothurians. (4) The final zone is an offshore coarse sand community (68–80% carbonate), composed mostly of carbonate deposits with outcrops of solid limestone and colonised by an abundant epifauna. The solitary coral, Caryophyllia clavus, is common as is other sessile epibenthos. Longhurst (1957a, 1959) recognised that the benthos of the west African shelf bears a close resemblance to that of the Mediterranean fauna. Working off the Gambia and Sulima Rivers at the Sierra Leone and Liberian borders, he found that this section of the shelf contains various proportions of muds: black reducing muds in the estuarine areas, grey or blue muds in the offshore oxidised areas, and olivebrown muds in other inshore areas. At depths exceeding 100 m offshore, calcareous sands predominate, composed of the remains of planktonic foraminiferans. Hard stony substrata occur across the shelf, generally in shallow depths; a zone of yellow coral (Dendrophyllia sp.) occurs on rocky bottom at depths of 80–100 m and is described variously as madreporic “sills”, “fonds coralligenes” or “massifs corallens”. The benthic communities across the shelf were partitioned on the basis of sediment type and dominant species. (1) Shallow soft-deposit communities, dominated by Venus on shelly sands on the Guinea and Senegal shelves and Amphioplus on muds and muddy sands in the same areas; (2) shallow hard substrata communities such as inshore reef, estuarine gravel and coastal rock communities; (3) deep soft-deposit communities, on muddy sands from 80 m to below the shelf break, dominated by ophiuroids, cnidarians and holothurians; and (4) deep hard substrata communities, occurring on rock ground (yellow corals), very soft rock or “marl” at the shelf edge off Guinea. These early studies supported the contention of Thorson (1957) that no increases in infaunal densities and species richness occur from the Arctic to the tropics, but an increase does occur in the richness and diversity of epifauna. Longhurst (1957a) found that many of the communities occurring on soft deposits of blue and grey muds did not fit into the available classification of benthic communities. Disturbingly, the tropical west African shelf fauna did not entirely fit into the temperate-boreal scheme of things. In the 1960s, workers on carbonate-bearing shelves in the Caribbean found similarly complex benthic communities (Lewis, 1965; Wade, 1972a). Lewis (1965) described three community zones off Barbados in the West Indies on the basis of water depth: (1) a sponge and coral community (50–150 m); (2) a diverse and abundant community of molluscs, echinoderms and coelenterates (100–300 m); and (3) a mollusc-dominated community between 300 and 400 m. These communities are similar in some respects to the west African assemblages, namely in the abundance of coelenterates and the sporadic occurrence of hard substrata composed mostly of limestone. Polychaetes dominate both shelves between depths of 40 to 250 m. Ophiuroids are common to depths of 250 m as are small bivalves such as Venus and Astarte.
438
DANIEL M.ALONGI
One characteristic of Thorson’s (1957) scheme which appears to hold true is the increase in abundance and diversity of large epibenthic invertebrates. Epifaunal assemblages are rich and diverse on the continental shelves of West Africa (Buchanan, 1957, 1958; Longhurst, 1957a, 1959), Madagascar (Picard, 1967), in the Gulf of Mexico (Hedgpeth, 1955), Brazil (Aller & Aller, 1986), and the Great Barrier Reef (Birtles & Arnold, 1988). The fauna of many carbonatedominated shelves is dominated by lancelets (e.g. Branchiostoma) and large foraminiferans such as Jullienella, Marginopora and Alveolinella (above references; see also Webb, 1956a; Gosselck & Kuehner, 1973; Gosselck, 1975; Basov, 1976; Flood, Braun & DeLeon, 1976; Alongi, 1989c). Several reasons have been put forward to explain their dominance on tropical carbonate shelves, including attraction to hard-bottom areas of limestone and the general lack of anoxic muddy conditions on the sandy, compacted bottoms of many of these shelves (Alongi, 1989b). The life cycles of many genera such as Branchiostoma are well adapted to tropical conditions (see p. 453 ). Several continental shelves are characterised by gradients in terrigenous to carbonate sedimentation resulting in various mixed terrigenous-carbonate sedimentary facies (e.g. off Belize, Wantland & Pusey, 1975; Grand Banks off the Bahamas, Newell et al., 1959; within the Great Barrier Reef lagoon, Alongi, 1989c). These variations occur across shelves which are lagoonal in character, rimmed by relict or living coral reefs. The shallow continental shelf of the central Great Barrier Reef (GBR) province is characterised by such an across-shelf sedimentary transition, and is commonly subjected to various physical disturbances such as cyclones, storms, and commercial prawn trawling (Alongi, 1989c). Standing stocks of bacteria, protozoans, and meiofauna generally do not vary across the central shelf, although macro-infaunal densities decrease significantly (Fig 8). Small, tube-building deposit- and suspension-feeding polychaetes and amphipods dominate the infauna; bivalve molluscs are notably absent. The studies of Aller & Aller (1986) and Alongi (1989c) provide comprehensive accounts of the two most disparate types of shelves in the tropics, those dominated by massive riverine inputs (the Amazon shelf), and those characterised by a lack of terrestrial input and dominated by pelagic (mainly reefal) sedimentation (the central Great Barrier Reef lagoon). Table XII depicts the effects of such different environments on the major infaunal components. Densities of the major groups are higher on the central GBR shelf (see Fig 8) where the sea bed is more stable, compacted, and where food input is probably of greater quality and quantity (from reef export of detritus?). In contrast, the sea bed off the Amazon is generally unstable and fluid. Away from the mouth, densities of bacteria, meiofauna and macroinfauna are considerably greater due to a more stable sea bed and greater food input from sedimenting phytoplankton blooms. Both shelves appear to have at least two features in common: high to moderate levels of physical disturbance (outwelling off the Amazon, cyclones and trawling in the GBR lagoon) and detrital food limitation (Table XII). Sedimentary organic nitrogen and carbon concentrations are much higher off the Amazon than on the central GBR shelf, but the amounts are low compared with levels on temperate shelves (Walsh, 1983) and on tropical shelves influenced by upwelling (Longhurst & Pauly, 1987). Many tropical shelves are characterised by infaunal assemblages composed mainly of pioneering, small opportunists that are surface deposit- and/or suspension-feeders, reflecting
TROPICAL BENTHIC ECOSYSTEMS
Fig. 8. —Across-shelf distribution of meiofauna (top) and macro-infaunal (bottom) abundances on the central Great Barrier Reef. S=summer; Sp=spring. (Modified from Alongi, 1989c).
439
440
DANIEL M.ALONGI
TABLE XII Comparison of major infaunal groups and sedimentary characteristics on the Amazon (Aller & Aller, 1986) and Central Great Barrier Reef (Alongi, 1989c) continental shelves. Values are means; ranges in parentheses
benthic adaptation to respond quickly to erratic, generally low, food inputs and to physical disturbances (Longhurst, 1957a; Harkantra et al., 1980; Yingst & Rhoads, 1985; Alongi, 1989b, c). In summary, tropical and subtropical continental shelves are generally shallow, driven by intermittent intrusions of nutrient-rich, upwelled water and/or by outwelling of estuarine detritus (in some cases, by some input of reef detritus). Benthic communities thrive in tropical up welling regions off Panama, Peru, Arabia, and northwest Africa, and in areas where there is massive, large-scale estuarine outwelling, such as off India. These shelves, however, are commonly subjected to anoxia with deleterious effects on the benthos if inputs of river effluent and upwelling episodes occur on a massive scale, too frequently or occur simultaneously with periods of stagnant water mass. These conditions probably account for the wider variations of benthic abundances and diversity on tropical shelves than on continental shelves of higher latitudes. Demersal fish communities Another common feature of subtropical and tropical shelves are abundant demersal fisheries as found off the coasts of Ghana (Buchanan, 1958), Sierra Leone
TROPICAL BENTHIC ECOSYSTEMS
441
(Longhurst, 1983), India (Harkantra et al., 1980), Australia (Robertson & Dredge, 1986), in the Gulf of Mexico (Yingst & Rhoads, 1985) and off Peru (Arntz, Valdivia & Zeballos, 1988). As in higher latitudes, tropical fisheries potential is generally related to both water-column production and benthic standing crop (see reviews: Kapetsky, 1984; Longhurst & Pauly, 1987; Sharp, 1988). Longhurst & Pauly (1987) have summarised some general principles of demersal fish communities on tropical shelves: (1) an increase in diversity towards the Equator, (2) an east-west gradient in diversity with more taxa in the western Atlantic than the eastern Atlantic, and (3) more families in the IndoWest Pacific region. Benthic communities and demersal fish assemblages appear to have been influenced by similar environmental and biogeographic barriers. Similar fish families occur throughout the tropics chiefly in response to the same factors, such as the presence of reefs and hard rocky bottoms, sediment type (i.e., preferences for muds, sands, carbonates) and the degree of brackish conditions in lagoons and rivers. Pelagic fishes are thought to be relatively more abundant and diverse than demersal assemblages in tropical seas, but many genera such as many clupeids and engraulids are bentho-pelagic, and the distinction between pelagic and demersal fish assemblages is somewhat blurred (Sharp, 1988). Some groups appear to be particularly abundant in the tropics. Several genera and species of sea catfish occur in estuarine waters despite belonging to a predominantly freshwater group (siluroid catfish). The Triglidae (e.g. Lepidotrigla, Prionotus) and Platycephalidae (e.g. Platycephalus) are Scorpaeniformes usually found on sandy bottoms. About a dozen families of the Perciformes dominate demersal fish assemblages in the tropics, and may be grouped on the basis of sediment type preferences. On rocky grounds, the Serranidae, Lutjanidae, and Lethrinidae (usually known as groupers and snappers) are common. On inshore muddy areas, Sciaenidae often dominate. Commonly known as croakers and drums, they frequently co-occur with threadfins (Polynemidae) and spadefishes (Ephippidae). Many attain large size and have specialised feeding habits. Breams (Sparidae), grunts (Pomadasyidae), threadfin breams (Nemipteridae), ponyfish (Leiognathidae), and other families (Mullidae, Gerreidae, and Priacanthidae) occur on sandy grounds, feeding mainly on the benthic epifauna, particularly decapod crustaceans and molluscs. Pleuronectiform flatfishes range throughout the tropics, particularly some genera of the Psettodidae, Soleidae, Pleuronectidae, Citharidae, and Bothidae. A few genera (e.g. of the Balistidae, Ostracrontidae, and Zeidae) commonly found on coral reefs occasionally wander into open neritic seas and may be caught in demersal trawl catches. Generally, there appear to be four types of communities: nearshore and estuarine softbottom areas dominated by sciaenids, sandy bottoms characterised by sparids, rocky bottoms dominated by lutjanids and reef areas dominated by no particular family (Longhurst & Pauly, 1987). The wealth of bentho-pelagic scombroids and clupeoids is one peculiar characteristic of tropical demersal assemblages compared with temperate fish faunas. Extensive surveys of demersal fish stocks have been conducted on several continental shelves, most notably in the eastern Atlantic (e.g. Gulf of Guinea) and western Atlantic (e.g. off Guiana) regions and in the Gulf of Thailand, off Indonesia and around India (see references in Lowe-McConnell, 1987, and Longhurst & Pauly, 1987). The continental shelf of the eastern Gulf of Guinea
442
DANIEL M.ALONGI
was comprehensively surveyed from 1950 to the mid-1960s. Based on recurrent group analysis, Fager & Longhurst (1968) identified several sets of demersal assemblages in this region: a coastal and estuarine sciaenid community (turbid, muddy water), a lutjanid community of the mixed layer and upper thermocline, a sparid community below the thermocline and hakes and related fish comprising deeper shelf and slope assemblages, all essentially determined by nature of sediment type and depth. In the western Atlantic, four demersal assemblages have been distinguished: (1) sparid communities (Ariidae, Clupeidae, Carangidae, Mullidae, Sciaenidae, Sparidae, Synodontidae) occurring in mainly subtropical regions (mostly sand and muddy sand bottoms), (2) lutjanid communities (Lagocephalidae, Balistidae, Lutjanidae, Serranidae, Pomadasyidae, Synodidae) occurring on rock and other hard substrata from Florida to Brazil, (3) subtropical, and (4) tropical sciaenid assemblages, the former associated with soft sediments near river mouths from Cape Hatteras into the Gulf of Mexico and the latter associated with soft coastal deposits from Brazil to the islands of the southern Caribbean (see summary in Longhurst & Pauly, 1987). These main species groups are also found in the IndoPacific (Lowe-McConnell, 1987). Trophically, nearly a quarter of tropical demersal fishes are benthic-feeders with a slightly higher proportion (about 38%) of mixed benthic- and fish-feeders (Pauly, 1979). Partitioning many of the most abundant families is somewhat subjective as differences in feeding types exist within a single genus (Tiews, Divino, Ronquillo & Marques, 1972). Nevertheless, the major benthic-feeders in the tropics are mullets (Mugil spp.), rays (Trygon, etc.), Sciaenidae, sheepshead, flatfish (Soleidae), ladyfish, snake-eels, some sharks (Mustelis, Leptocharias), scabbard fish (Trichurus), toadfish (Batrachoides), and some eels (e.g. Muraena). Benthic-feeders dominate in areas where detrital outwelling is common, such as along the coastlines of the northern Indian Ocean. In his study of foods eaten by demersal fish of west Africa, Longhurst (1960) found that most species were non-specific in their feeding habits. For instance, polychaetes were found in the stomachs of nearly 40 fish species, and cephalopods and other molluscs were found in over 30 species. More important, there were large year-to-year variations in the diets of most of the species as well as large differences in stomach contents between coastal and offshore fish. Among trawl-caught fishes off Guiana (northeast South America), LoweMcConnell (1962) found similar evidence of seasonal and spatial partitioning of food resources, with sciaenid species agglomerated into three trophic groups: (1) pelagic shrimp-feeders, (2) benthic-feeders, which includes a wide range of species, and (3) predators, which also include many species, particularly all of the large sciaenids. As off other tropical shelves, the fish faunas are zoned, with type of bottom rather than water depth or distance from shore appearing to be the main controlling factor. Information on the fishery potential of many tropical regions is still scanty, often composed of data obtained mainly from the early surveys (e.g. Salzen, 1957; Longhurst, 1965a,b). Pauly (1979) and Sharp (1988) have provided useful summaries of tropical demersal fishery types and characteristics, including main taxa exploited, resources base, stock density and catch quality characteristics, major disturbances and seasonal variations. It is clear from their tables (Table IV in Pauly, 1979; Table IX in Sharp, 1988) that tropical demersal fisheries possess characteristics different from fisheries of other latitudes and are at least as
TROPICAL BENTHIC ECOSYSTEMS
443
dependent upon the benthic environment as are temperate demersal fishes, if not more so.
PHYSIOLOGICAL AND BEHAVIOURAL ADAPTATIONS TO STRESS Many aspects of the tropical environment indicate that benthic assemblages in the low latitudes are subjected to greater stress than their temperate counterparts (Moore, 1972a). Tropical organisms are commonly subjected to long durations of very high (>30°C) temperatures, desiccation, low and variable dissolved oxygen levels and food supply, chemical defences of plants, wide variations in salinity induced by seasonal monsoons, smothering by massive riverine sedimentation or by erosion of estuarine mudbanks, and by anoxia caused when coastal water masses are impinged by heavy continental run-off and when subsequent diatom blooms occur. Benthic organisms in the tropics are thus exposed to a wide variety of stresses to which to adapt, migrate from, or die.
TEMPERATURE AND SALINITY TOLERANCES
Early physiological studies indicate that tropical organisms are generally as intolerant to temperature and salinity stress as are temperate and boreal organisms (Mayer, 1914; Scholander, Flagg, Walters & Irving, 1953; Bullock, 1955). Mayer (1914) maintained that tropical marine organisms normally live within 10 to 15°C of their upper temperature tolerance level and within 5°C of their maximal metabolic rate. In early experiments with Scyphomedusae, he found that whereas temperate or Arctic animals exhibit little differences in metabolic activity over a considerable temperature range, the activities of tropical invertebrates change markedly only a few degrees from their average habitat temperature. Mayer noted that tropical marine organisms can withstand cooling better than heating, indicating that lower temperatures constitute less stress than higher temperatures which can cause death by asphyxiation when oxygen levels become too low to support the increased metabolic rate. Benthic organisms normally attempt to avoid stress by a variety of physiological and behavioural mechanisms (see discussion below of Donax) including horizontal and vertical migration, aestivation, hibernation, and habitat modification (e.g. ventilation of tubes and burrows). Lewis (1963) points out, however, that body temperatures of intertidal poikilotherms are not necessarily the same as the ambient temperature or the micro-climate they inhabit but are, in many instances, higher. Working with the barnacle Tetraclita squamosa, the limpet Fissurella barbadensis, and the gastropod Nerita tesselata, Lewis found that intertidal animals do not simply absorb radiation as do inanimate objects but act to reduce solar heating by evaporation. The differences between body and ambient temperatures depend on degree of cloudiness, and to a lesser extent, on genetic adaptation, as the gastropod Nerita was most effective at evaporative cooling. Position in the intertidal is partially dependent upon the ability to regulate body temperature.
444
DANIEL M.ALONGI
Adaptation of tropical protozoans and meiofaunal organisms to high temperatures has been reported by Lee & Fenchel (1972), Wieser (1975), Hartwig, Gluth & Wieser (1977), and Wieser & Schiemer (1977). Survival and growth of three species of the marine ciliate Euplotes (temperate, tropical, and Antarctic sea-ice species) were examined at different temperatures in laboratory cultures (Lee & Fenchel, 1972). The Antarctic species survived and grew between -2°C and 10°C; the temperate and tropical species survived between -2°C to about 30°C and between 5 and 40°C, respectively (Fig 9). Not all protozoans thrive at high temperatures because the lethal limits for poikilotherms are very close to the maximum temperatures in which they live, as suggested earlier by Mayer (1914). For instance, the ciliate Geleia nigriceps dominates some sheltered carbonate sand beaches in Bermuda, migrating vertically to keep within a narrow temperature range (Hartwig et al., 1977). Experiments reveal that G. nigriceps tolerates high temperatures (> 35°C) for only short periods and migrates vertically in synchrony with the tides. This species is highly adaptable to tropical beach conditions, being tolerant to oxidised and reduced conditions which enable it to minimise exposure to stress. Tropical and subtropical meiofauna are similarly adapted to avoid or withstand stress in the intertidal with the vertical distribution of most species closely related to upper lethal temperature and pH conditions (Wieser, 1975). Temperature tolerances, and thus vertical and temporal distribution patterns, vary among species. At the same locality in Bermuda where the ciliate study was conducted, Wieser & Schiemer (1977) found that the most abundant nematode species, Steineria sterreri, Trefusia schiemeri, and Theristus floridanus exhibited distinct temperature tolerances. Steineria sterreri, which occurs in the upper beach, is more heat tolerant than Theristus floridanus which is the least heat tolerant and inhabits lower beach levels. Trefusia schiemeri is intermediate in its heat tolerance ability. Earlier studies with several species of nematodes, harpacticoid copepods, and foraminiferans indicate that temperatures within the 33 to 35°C range induce thermal stress, at least for meiofauna associated with decaying mangrove leaves (Hopper, Fell & Cefalu, 1973). A comparison of temperature and salinity tolerances between tropical and temperate meiofaunal species has not yet been made. Stress induced by one environmental variable tends to reduce the ability of an organism to tolerate other factors but relatively few studies have examined several variables simultaneously (Moore, 1972a; Wieser, 1975). In fact, few workers have examined the tolerances of warm-water benthic invertebrates to changes in salinity (e.g. Talikhedkar & Mane, 1976; Hammond, 1983). That the majority of intertidal organisms are sensitive to salinity changes can be inferred from the fact that most benthic communities exhibit maximum abundances and species richness closer to the sea. It can be fairly assumed that those species abundant in high intertidal habitats are eurytolerant to high salinities and temperatures, and to desiccation (e.g., the sand beach isopod Excirolana, Dexter, 1977). Adaptations may be either physiological or behavioural, or both. Crustaceans and molluscs are particularly well-known for their behavioural adaptations in the intertidal. Lasiak & Dye (1986) observed the movements of the whelk, Telescopium telescopium, in the upper intertidal zone of mangroves in tropical Queensland, Australia. They found that the snails exhibit active and inactive phases, the timing of which depends upon the state of the tide. The snails cluster
TROPICAL BENTHIC ECOSYSTEMS
445
Fig 9. —Generation times (h) of three Euplotes spp. from Antarctic, temperate (Denmark), and tropical (Florida) regions at different temperatures. From Lee & Fenchel (1972); reproduced with permission of Gustav Fischer Verlag.
under stunted mangrove trees in their inactive phase; when wetted by tide, the active phase is initiated. Animals exposed to open, unshaded areas under the canopy die of heat stress. On the sandflats on Phuket Island in southern Thailand, Huttel (1986) found that populations of the archeogastropod, Umbonium vestiarium, form conspicuous aggregations or banks which are generated by the snails cementing sand grains with mucus. These aggregations migrate subtidally during calm weather and serve to facilitate reproduction, protect from high temperatures and desiccation, and to provide optimal conditions for filter-feeding. Burrowing rates of the infaunal brachiopod, Lingula anatina, are greatly influenced by salinity changes and physical disturbances (Hammond, 1983). Salinity levels between 20 and 50‰ can be tolerated for several weeks, but avoidance behaviour is retarded and the animals suffer 30–50% mortality if buried below 20 cm sediment depth. These results indicate that this species is susceptible to mortality from salinity changes and erosion, which accompany disturbances such as cyclones. Most tropical organisms inhabiting the intertidal can tolerate wide variations in temperature and salinity, but reproductive and feeding behaviour are generally normal only within a very narrow range of environmental conditions.
TEMPERATURE COMPENSATION AND METABOLISM
446
DANIEL M.ALONGI
Scholander et al. (1953) and Bullock (1955) indicated by a series of laboratory experiments on fishes, crustaceans, and various insects that metabolic rates are several times lower for Arctic species than tropical species over their natural temperature range. This suggests that metabolic rates of Arctic species are displaced lower compared with warm-water organisms, although in both groups there was an increase in oxygen uptake with increasing temperatures. That is, the metabolic rate-temperature relationship of organisms from different latitudes are nearly identical but shifted (or temperature-compensated) with respect to one another. Scholander et al. (1953) found that Arctic aquatic species at 0°C had a three to ten times lower metabolic rate than the tropical aquatic organisms at 30°C. Extrapolating the tropical metabolism-temperature curves to 0°C would result in their being thirty and forty times lower than for the cold-water species. Clarke (1980) has cast doubt upon these earlier results, arguing that these experiments were conducted on excited Arctic and Antarctic animals, thus artificially raising their metabolic-temperature curves. More recent studies indicate temperature compensation in temperate and tropical fish with lower metabolic rates for the tropical species compared with the temperate species at similar temperature ranges (Edwards et al., 1970; Ursin, 1984). Edwards et al. (1970) measured respiration rates of the tropical fish Halophrye dussumieri (toadfish) and Cynoglossus brevis (Malabar sole) and two temperate demersal counterparts, Cottus scorpius (sea scorpion) and Pleuronectes platessa (plaice) within temperature tolerance ranges of 2.5 to 25.0°C and 15.0 to 37.5°C, respectively. The oxygen consumption rates of the tropical fish were from 1.2 to 1.45 times greater than the temperate fish at their respective temperatures on a per weight basis. At the same temperature (20°C) and at roughly similar weights, the temperate species Pleuronectes consumed, however, several times more oxygen per hour than its tropical counterpart Cynoglossus (Fig 10). It is probable that not all poikilotherms exhibit temperature compensation. Lee & Fenchel (1972) found that growth rates of Euplotes spp. from different latitudes were not temperature-compensated, that is, the Antarctic ciliate grew at a rate expected from extrapolating the growth-temperature relationship of the tropical and temperate ciliates to polar temperatures (see Fig 9). It is conceivable, however, that other physiological functions such as metabolism and locomotion may be temperature-compensated in protists. Oxygen consumption of tropical benthic invertebrates as a function of temperature, salinity and other environmental factors has been measured by several workers (Lewis, 1971; Edwards, 1973b; McLusky & Stirling, 1975; Dhamne & Mane, 1976; Mathew & Menon, 1983; see Moore, 1972a, for earlier references). In general, the rates of oxygen consumption of subtidal species correspond to extrapolations to higher temperatures of metabolismtemperature curves for temperate species as observed by Ansell et al. (1972c) and Edwards (1973b), indicating an absence of temperature compensation in some subtidal organisms. As with temperate intertidal organisms, the respiratory responses of their tropical counterparts are not exceptional, responding similarly to changes in the environment. For example, the respiration rates of three tropical nereid gastropods increased from 30 to 37°C and were greater in species taken from areas of higher mean temperatures; oxygen consumption decreased with an increase in exposure time (Lewis, 1971). Similar variations in respiratory activity are known for a variety of tropical bivalves (McLusky & Stirling, 1975; Dhamne & Mane, 1976).
TROPICAL BENTHIC ECOSYSTEMS
447
Fig 10. —The effect of temperature on respiration of the temperate plaice, Pleuronectes platessa and the tropical Malabar sole (Cynoglossus brevis). From Edwards et al. (1970); reproduced with permission of Pergamon Journals Ltd.
The effects of human-induced stress, such as pollutants, on the respiration of tropical invertebrates are almost wholly unknown. Mathew & Menon (1983) examined the effect of heavy metals (Ag, Cu, Zn, and Pb) on oxygen
448
DANIEL M.ALONGI
consumption in the bivalves, Perna viridis and Meretrix casta, taken from an Indian estuary. Respiration decreased in both species at sublethal concentrations (>0.01-0.02 mg·l -1 for Ag, 0.05-1.0 mg·l -1 for Cu and Zn, respectively). Lead at concentrations greater than 0.4 mg·l -1 accelerated rates of oxygen consumption. It appears that these tropical bivalves are more sensitive to pollutant stress than their temperature counterparts; respiratory stress was evident at concentrations well below the LC per 96 h values established for some temperate molluscs. 50 Considering the generally lower dissolved oxygen levels in the tropics and higher respiratory rates for most tropical invertebrates, it is conceivable that benthic communities in the tropics may indeed be functioning closer to the threshold of extinction than their temperate counterparts (Hatcher, Johannes & Robertson, 1989).
GROWTH
The general conclusion may be drawn from the literature that metabolic rates of most invertebrate species are about the same or slightly lower from higher latitudes compared with lower latitude species at their natural range of temperatures. At any given temperature, however, metabolic activity is greater in animals from colder oceans when compared with individuals of the same species in warmer seas. Marine poikilotherms thus compensate metabolically for changes in temperature with respect to latitude. But, as pointed out by Dehnel (1955), metabolism and growth are entirely different factors, and many studies indicate temperature-dependence of growth. Examining rates of growth of gastropods among different latitudes, Dehnel (1955) found that the growth rate of a boreal gastropod population was greater than in a population of the same species in the subtropics at comparable temperatures. Dehnel concluded that growth rates of these gastropods are temperature-compensated. It is more likely, however, that temperature dependence of metabolism and growth varies with physiological temperature. Edwards et al. (1971) found that metabolism of the tropical flatfish, Cynoglossus, was temperature-dependent between 15 and 30°C but was temperature-independent at higher temperatures as rates of oxygen uptake reached a plateau. In an earlier study, Edwards et al. (1970) found that the metabolism of Cynoglossus brevis and Halophryne dussumieri from southern India reached a plateau at a lower temperature (28°C). Parulekar (1984) compared the growth rates and size class structure of the tropical bivalves, Paphia malabarica and Meretrix casta, with populations of the temperate bivalves, Abra alba and Nuculana minuta. In general, the tropical species have a wider size range, fewer size classes and higher growth rates than their temperate counterparts (Table XIII). Growth rings were not demarcated in the tropical bivalves probably due to the lack of discernible seasonal variations in temperature at the Indian estuary. Higher growth rates in the tropical species were attributed to the generally warmer and less variable temperatures. Parulekar (1984) pointed out that with a higher growth rate, tropical bivalves can be commercially exploited faster, but are invariably less stable over time considering their continuous breeding behaviour and early sexual maturity.
TROPICAL BENTHIC ECOSYSTEMS
449
TABLE XIII Comparison of size classes and growth of tropical and temperate estuarine bivalves (modified from Parulekar, 1984). *Mandovi estuary, west India; water temperature (annual range) =23–33°C; **Clyde Sea Area, Scotland; water temperature (annual range) =7–14°C
REPRODUCTION
Breeding and reproductive activity are not continuous for most tropical benthic species. Several breeding habits have long been noted: (1) continuous breeding throughout the year at the same intensity, irrespective of season; (2) continuous breeding with higher activity periods occurring in a particular season; (3) breeding only at a definite time of the year, and (4) discontinuous breeding throughout the year, often occurring irregularly in response to cues such as wet or dry seasons, or lunar cycles (Vohra, 1971; Ansell et al., 1972a, b; Govindan Kutty & Nair, 1972; DeVries, Epifanio & Dittel, 1983a,b).
Invertebrates Most species are either discontinuous breeders or breed at low rates throughout the year with peaks occurring at certain times of the year (Govindan Kutty & Nair, 1972; Berry 1975; Kenchington & Hammond, 1978; Bertness, 1981a, b; Broom, 1982; DeVries el al., 1983a, b; Berry & bin Othman, 1983; Ong Che & Gomez, 1985; Subramoniam & Panneerselvam, 1985). Comparatively few studies have documented the occurrence of continuous breeding (e.g., Goodbody, 1965; Varadarajan & Subramoniam, 1982). The breeding patterns of most tropical benthic species appear to be cued to monsoonal activity and the resultant salinity patterns. Comparison of reproductive patterns of crustaceans along the east and west coasts of India indicates that on the west coast breeding is minimal during May to July (the southwest monsoon) when salinity is low; on the east coast, many crustaceans (mainly decapods) exhibit semi-annual or nearly continuous breeding with peaks in January and July. The higher breeding rates along the east coast probably reflect the lesser intensity of the southwest and northeast monsoons on that side of the subcontinent. In southwest India, the mole crab, Emerita holthuisi, undergoes recruitment in February and March (pre-monsoon months) and again during the monsoon (Ansell et al., 1972b; Achuthankutty & Wafar, 1976). There was some evidence of low-level recruitment throughout the year. A similar reproductive pattern is exhibited by several species of the wedge clam genus Donax (Ansell et al., 1972c). In India, Donax species spawn either once or twice a year with the major spawning period occurring between October and January and a small spawning
450
DANIEL M.ALONGI
interval around April to June, usually before or immediately after the onset of the monsoonal rains. Data on the reproductive habits of tropical meiofauna are meagre. Govindan Kutty & Nair (1972) observed meiofaunal breeding patterns similar to those of larger benthic organisms along the Kerala coast of India: (1) species which breed almost continuously with different species exhibiting reproductive peaks at various times of the year; (2) species which breed during the hottest time of the year, exhibiting breeding peaks when salinity is maximal during the pre-monsoon period; and (3) species which breed mainly during the monsoon and post-monsoon periods. The factors leading to breeding cycles in tropical benthic species in the dry tropics are poorly understood. Reproduction of three sympatric species of hermit crabs (Calcinus, Clibanarius, and Pagurus) in the Bay of Panama appears to be determined mainly by a limited supply of shells (Bertness, 1981a). Calcinus is the dominant species and exhibits reproductive peaks in December and January, coinciding with the onset of upwelling in the dry season. This phenomenon is common for other intertidal organisms in the Bay of Panama (Lee, 1978). Clibanarius shows four seasonal peaks evenly spaced, probably due to competition with Calcinus for shell habitats; Pagurus reproduces continuously at a high rate year-round because of its very poor supply of shells. The reproductive patterns of all three species are ultimately cued to dry season upwelling when increases in food supply result in increased growth rates of the hermit crabs which, in turn, lead to shortages in shell supply. Breeding patterns of macrobenthos in the dry tropics are determined either by changes in sea-water temperature and salinity, or are episodic and not easily related to environmental change. Most species breed semi-annually with reproductive pulses occurring when sea-water temperatures are either maximal or minimal or both. For populations of the sea cucumber, Holothuria scabra, at Calatagan in the Philippines, both temperature and salinity regulate reproductive patterns (Ong Che & Gomez, 1985). A reproductive pulse from May to June coincides with minimum salinity and maximum temperatures and another pulse in November to January coincides with falling temperatures and rising salinities. In north Queensland, Australia, recruitment of the brachiopod, Lingula anatina, is episodic, at times failing completely. The cause (or causes) is (are) not completely understood as the recruitment failures are not easily related to changes in environmental factors (Kenchington & Hammond, 1978). Adaptation to lunar rhythms is another method for many subtropical and tropical crustaceans (De Vries et al., 1983a,b). In the Gulf of Nicoya off Costa Rica, pulses in hatching of eggs of the subtidal portunid crab, Callinectes arcuatus, are induced by lunar cycles superimposed on a year-long background of continuous, low-level breeding with a distinct peak in the dry season (De Vries et al., 1983a, b). The adaptive significance of lunar rhythmicity is unclear. Latitudinal variations in reproduction and larval dispersal of benthic invertebrates were first recognised by Thorson (1950), who observed an increase in the proportion of pelagic to non-pelagic larvae from temperate to tropical oceans. This observation has generated disagreement from some workers (Jablonski & Lutz, 1983) who maintain that Thorson’s results are an artifact of the faunas studied (the Persian Gulf and some oceanic islands). Spight (1981) conducted a more extensive survey to test Thorson’s hypothesis and compiled data for over 110 species of gastropods. His results support Thorson’s original observations, but found a sharp decline in planktonic development only above
TROPICAL BENTHIC ECOSYSTEMS
451
40°S and N latitides with variable evidence for latitudinal gradients in larval development in the tropics. As indicated by Spight (1981), Jablonski & Lutz (1983), and Steele (1988), such latitudinal gradients probably vary at the phyletic level and perhaps even lower on the phylogenetic order. It is very likely that patterns of reproduction and larval dispersal vary widely within the tropical oceans on both sides of the Equator. For example, most invertebrates in the Indian Ocean have long-range dispersive larvae that are widespread throughout the Indo-West-Pacific region. Reproductive and larval dispersion patterns, however, vary among geographic areas (Pearse & Barksdale, 1986). In the northern subtropical areas of the Indian Ocean, benthic invertebrates spawn primarily in the boreal summer while their counterparts in the southern subtropical regions spawn in the austral summer. In between these extremes, temporal patterns vary widely, with some species spawning continuously on the southeastern coast of India and other species on the western coastline spawning mainly during the pre- and post-monsoon periods. These variations render generalisations more difficult with regard to latitudinal gradients in reproduction and larval dispersal, as similar variations probably occur in other tropical seas. Although low latitudinal conditions may theoretically favour pelagic larval dispersal over non-pelagic reproduction, conclusions regarding the relative success between the two methods is not possible owing to the present lack of data. Demersal fishes Tropical demersal fishes appear to be as plastic in their reproductive habits as their invertebrate counterparts (Johannes, 1978; Murphy, 1982; Longhurst & Pauly, 1987). Johannes (1978) reviewed the reproductive habits of coastal fishes in the marine tropics and concluded that models of reproduction formulated for temperate fishes are inappropriate to most tropical fishes. High predation pressure was invoked as the major factor determining reproductive behaviour of tropical fishes especially those species that live in mangroves, seagrass beds, and coral reefs. Reproductive behaviour is geared to minimise or to avoid predation at the larval and juvenile stages, with particular forms of behaviour being more common in the tropics, such as lunar periodicity. Johannes (1978) contends that synchrony with lunar cycles facilitates offshore transport of eggs and larvae on the lunar spring tides. At least three types of reproductive behaviour are recognised for coastal marine fishes in the tropics. Several are exhibited by demersal species: (1) demersal spawning with guarding of the eggs, (2) offshore spawning migration and, (3) spawning within or near sheltered objects (e.g. high rocks, coral heads). Other modes of reproductive behaviour are exhibited mainly by pelagic forms: parental guarding by larvae, live-bearing, and nearshore spawning by coastal pelagics. Murphy (1982) suggests, however, that case histories of recruitment in tropical pelagic and demersal fishes are limited and do not appear to be greatly different from temperate fish communities. He concluded that a wide spectrum of reproductive behaviour is exhibited by fish species of all latitudes and that interspecific interactions (predation, competition) do not need to be invoked to explain fish reproduction. Some aspects of fish behaviour in the tropics are unusual, such as territoriality of many reef species, but most fishes of all latitudes
452
DANIEL M.ALONGI
are characterised by spawning and recruitment periodicity, and most have reproductive curves which appear to be density-dependent. Evidently, more data are needed on recruitment of tropical fishes to ascertain whether or not real reproductive behavioural differences exist between temperate and tropical fishes.
SUPERB ADAPTATORS
Donax Species of the bivalve genus Donax are extremely successful inhabitants of most tropical and subtropical sandy beaches and shallow subtidal sandflats (see review by Ansell, 1983). Donax species are the dominant bivalves in high energy, warm-water habitats, but they are displaced by other species in colder climates, in more sheltered habitats, and on beaches with more carbonate than quartz sand. The ability of this bivalve to migrate in response to environmental change accounts greatly for its success (Ansell & Trevallion, 1969; Trueman, 1971; Ansell & Trueman, 1973). Wade (1967, 1968) observed the migratory ability of D. denticulatus on a sandy beach in the West Indies, noting that the clams, using their siphons and foot, migrate in synchrony with the tides to maintain their position in the intertidal. Trueman (1971) conducted a thorough analysis of the burrowing and migratory behaviour of D. denticulatus and observed that the bivalve reacts to tactile stimulation which initiates burrowing. Its burrowing speed is remarkable, penetrating from an erect position on the sand at a rate of 0.4 cm·s -1 with complete burial achieved in a few seconds. More remarkably, D. denticulatus is able to burrow quickly and repeatedly, and to return to the sand surface. These migratory responses are non-rhythmic, depending upon changes in physical conditions on the beach. Other tropical molluscs burrow at rapid rates on sandy beaches, but species of Donax are able to re-establish feeding activity immediately after disturbance (Ansell & Trevallion, 1969). The energetic cost of tidal migration to D. incarnatus and D. denticulatus is estimated to be relatively small (Ansell & Trueman, 1973). Migration may add an additional one-third to the daily maintenance requirement, but tidal migration is, in the long-term, a highly successful adaptation which prolongs the feeding time of Donax. The disturbed wash zone in which the species lives probably provides some protection from predation by Ocypode spp. and other decapods and wading birds. Most Donax are short-lived (1–2 yr) and grow rapidly to maximum size and sexual maturity (Ansell, 1983). Donax are resource exploiters rather than conservers, which enhances their ability to exploit periods of high beach production. This phenomenon is true for many tropical species which are generally smaller, more opportunistic and more productive (and shorter living) than their temperate counterparts. The physiology of the tropical species is poorly understood, but it is clear that Donax are superbly adapted to tropical intertidal conditions. Branchiostoma Populations of the amphioxus (or lancelet) genus Branchiostoma occur regularly throughout warm and temperate oceans, but are particularly abundant on hard sandy
TROPICAL BENTHIC ECOSYSTEMS
453
grounds on tropical and subtropical continental shelves (Webb, 1956a,b, 1958c; Makarov & Averin, 1968; Gosselck & Kuehner, 1973; Gosselck, 1975; Flood, Braun & DeLeon, 1976; Alongi, 1989b,c). Other lancelets such as Amphiopsis are dominant on some tropical shelves, such as in the Mozambique Channel where it constitutes nearly 56% of the entire epibenthic biomass in sandy regions (Makarov & Averin, 1968). Lancelets appear to be particularly diverse and abundant along the west African coastline (Webb, 1956a; Buchanan, 1957, 1958; Longhurst, 1957a, 1959) comprising mainly Branchiostoma senegalense, B. leonense, B. takoradii, B. nigeriense, and B. africae. Off the coasts of Spanish Sahara and Gambia, Gosselck (1975) found lancelet populations to depths of 40 m, attaining densities of up to 9000 animals·m -2. Populations of B. senegalense spawn from April to June off the west African coast. The larvae are mainly plankton-feeders. In Lagos Lagoon, Webb (1958c) traced the life cycle of B. nigeriense: larvae enter the lagoon in autumn when salinities are low, metamorphose at the end of the year, and then colonise sand deposits of the lagoon or migrate out to the shelf as adults the following March. Adults in the lagoon spawn at that time and die when salinity falls below threshold levels. The larvae reach maturity at the end of July, thus completing the life cycle. The food and environmental preferences of tropical lancelets are not completely known. Gosselck (1975) found that the guts of adult Branchiostoma were filled with detritus and a few diatoms and Alongi (pers. obs.) obtained similar results for lancelets on the central Great Barrier Reef shelf. Tropical species prefer sandy bottoms and salinites above 13‰ (Webb, 1956b). In laboratory choice experiments, Webb (1956b) found that lancelets prefer sands of mixed grain sizes and of low silt content. They prefer undisturbed sands, particularly sandy bottoms with a rich covering of microfauna and flora, but with little detrital matter. The frequent occurrence of lancelet populations in many continental shelf and lagoonal habitats suggest that they may be an overlooked, major predator of benthic populations in tropical subtidal sandy environments.
ECOSYSTEM DYNAMICS Many structural attributes of benthic communities in the tropics have been and are being explored, but relatively little information is available concerning functional aspects. Population interactions (predation, competition, etc.), rates and types of feeding, and various aspects of materials and energy flow have remained wholly unknown until very recently. Trophic processes in tropical benthic food webs have been examined mainly in rocky intertidal communities with lesser amounts of work done on coral reefs and in mangroves (see reviews by Alongi, 1988c, 1989a). It is unlikely, however, that models of food-chain patterns in these ecosystems should apply equally to soft-bottom communities in different biogeographical provinces. Trophic interactions invariably must exist and operate within tropical soft-bottom communities as they do in the higher latitudes but, on the whole, they remain rarely studied. It is conceivable that trophic interrelationships among the major functional groups (microbes, meiofauna, macrofauna, megafauna) may differ in magnitude rather than in
454
DANIEL M.ALONGI
basic structure. For instance, the recent trophic studies of Ansell & Morton (1987), Black & Peterson (1988) and Alongi (1988b) indicate that interrelationships among the benthic size groups may indeed be different from those in temperate food chains. For example, the works of Vermeij (1978) and Ansell & Morton (1987, and references therein) suggest higher rates of predation in the tropics. High predation pressure has led to the evolution of complex predation tactics and modes of avoidance behaviour not found in their temperate counterparts. Higher rates of secondary production and predation coupled with unusual environmental characteristics may operate in concert to regulate tropical communities differently from temperate assemblages. What little functional information there is pertains mainly to estimates of secondary productivity and patterns of benthic biomass in response to pelagic production. These elements are discussed below and form the basis for some temperate-tropical comparisons.
PRODUCTION
Microalgal productivity Table XIV summarises most of the available primary production data for tropical sediments. As in the other compilations, the results vary because of the different methods used, time of day, season, sediment type, and water depth. Only gross production values are presented as few studies have measured respiration (see Table XV, p. 459 ) to calculate net primary production. The rates of gross productivity are within the lower end of the range measured in similar temperate habitats (see Colijn & de Jonge, 1984, for temperate information). Rates above 1 gC·m -2 ·day -1 have been measured only in shallow coastal lagoons, in some coral reefs (Alongi, 1989a, for references) and in some seagrass meadows (see reviews by Hargraves, 1982; Duarte, 1989). Several reasons can be offered for these high production rates: the presence of more macroalgae, higher nutrient retention and more quiescent conditions which foster clear water and the development of algal mats. In the vicinity of Carrie Bow Cay in Belize, Hargraves (1982) measured primary production of the seagrass, Thalassia testudinum, mixed algae on coral rubble, and in coral sand using the bell jar method. Daily net production rates in the Thalassia beds ranged from 0.7 to 12.7 gC·m -2 with negligible phytoplankton input. These values are typical of values measured in other tropical seagrass meadows and are generally higher than in temperate latitudes (Duarte, 1989). Many unvegetated habitats in the tropics have low rates of net primary production or are heterotrophic with P/R values less than 1. Several reef habitats, such as mixed algal-coral rubble stands and highly exposed coral sands, harbour a rich and abundant fauna of microbes and larger fauna that contribute to high rates of community respiration. Heterotrophic pockets exist in many coastal lagoons (Edwards, 1973a, b, 1978) where high rates of gross primary production are offset by equal or greater rates of community metabolism. The muddy sands and muds of mangrove forests are also heterotrophic (Alongi, 1988a, 1989a) with low or no net primary production. In a mangrove forest in Thailand, Kristensen, Andersen & Kofoed (1988) measured low gross primary production rates ranging from 146 to 250 mgC·m -2 ·day -1 but respiration
-1
TABLE XIV
Rates of gross primary production (mg C·m ·day ) and chlorophyll a concentrations in some tropical and subtropical intertidal and subtidal sediments (excluding vegetated sediments)· a=converted to carbon assuming a respiratory quotient of 1 and a molar constant of 0.375; b=estimated from mg·m-2 using core diameter and sediment depth provided; *=range only; **=mean only; n.a.=not measured
-2
TROPICAL BENTHIC ECOSYSTEMS 455
456
DANIEL M.ALONGI
was high resulting in net oxygen uptake rates of 56 to 91 mgC·m -2 ·day -1 . Similarly, mangrove forest floors in northern Australia are heterotrophic and at several sites oxygen consumption rates were identical between light and dark bottles (Alongi, unpubl. data). Subtidal coastal habitats in the tropics are generally shallow, muddy, and turbid, with low or negligible rates of primary production (Bunt, Lee & Lee, 1972). Shallow (< 50 m) calcareous shelf areas may exhibit some net production, but it is thought to be minor compared with phytoplankton input (Qasim, 1979). Microalgal standing stocks (measured as chlorophyll a) are generally low in tropical sediments, usually <5 µg·g -1 sediment dry weight (Table XIV; Trevallion, Ansell, Sivadas & Narayanan, 1970; Achuthankutty et al., 1978; Broom, 1982, Alongi, 1988a, b) and much lower compared with temperate sediments (Colijn & de Jonge, 1984). Several factors probably account for the low benthic microalgal densities: low light intensity (especially under mangrove canopies), low dissolved inorganic nutrient concentrations in the porewaters (see p. 392 ), selection for smaller cell sizes due to high light intensity on unvegetated flats (as for tropical phytoplankton in surface waters), high temperatures, wide variations in salinity, erosion of surface sediments, and inhibition of growth by soluble phenolic compounds in the vicinity of mangroves (Alongi, 1989a, b). Faunal composition in tropical communities may also be responsible (i.e., high rates of predation) but this has not been examined. Seasonal variations of benthic chlorophyll have been examined in intertidal habitats of India (Ansell et al., 1972a; Achuthankutty et al., 1978), Malaysia (Broom, 1982), and Australia (Alongi, 1988b). Concentrations of benthic chlorophyll a showed no clear signs of seasonal variation on a Malaysian mudflat, but concentrations were low (Broom, 1982). Chlorophyll measurements probably reflect a variety of pigmented microorganisms, and thus seasonal fluctuations of individual species may be obscured by differences in pigment characteristics of dominant algae. On sandy beaches in India, decreases in chlorophyll a concentrations coincide with the monsoons when heavy rains and erosion cause the flora to wash into the water column (Ansell et al., 1972a; Achuthankutty et al., 1978). In the dry tropics, chlorophyll a levels drop sharply on intertidal sandflats with the onset of hot (>30°C) summer temperatures (Alongi, 1988b). This has important trophic implications, partially explaining coincident decreases in algal-feeding nematodes on some Australian sandflats in summer (Alongi, 1990). Variations in chlorophyll a levels do not necessarily result from changes in benthic primary production, owing to changes in growth state and species composition, and consumption by predators (Plante-Cuny, 1978). In the most comprehensive study to date of microphytobenthic production in the tropics, Plante-Cuny (1978) observed no significant correlation between standing stocks and productivity in marine sediment at Nosy-Be in Madagascar. Plante-Cuny (1978) found that seasonal variations of both factors coincided with seasonal fluctuations of bottom illumination, with maximal values at the end of winter and beginning of summer. Rapid decreases occurred during the wet season when river run-off increased water turbidity. The seasonal fluctuations were small compared with higher latitude systems but similarly declined sharply with water depth to negligible values beyond depths of 30m.
TROPICAL BENTHIC ECOSYSTEMS
457
Heterotrophic microbial activity and the fate of bacterial production Various methods exist to measure the activity of marine micro-heterotrophs, including the use of radiolabels to estimate cell production (DNA synthesis), protein and RNA syntheses, rates of carbon fixation and anaerobic mineralisation processes (sulphate reduction, methanogenesis and nitrate reduction), and oxygen consumption or carbon dioxide production to estimate (mainly) microbial respiration. These methods, and the processes they measure, deal mainly with heterotrophic bacteria. Nothing is known, (and no adequate methods exist) to estimate production of protozoans and fungi in marine sediments. Very little data are available on anaerobic processes (Alongi, 1989a), but information on respiration and bacterial productivity does exist to provide some meaningful interpretation of benthic microbial activity in the tropics. Rates of oxygen consumption (“total community aerobic respiration”) in some tropical benthic habitats are presented in Table XV (values measured in mangroves and coral reefs can be found in Alongi, 1989a). Oxygen uptake rates in tropical sediments are within the upper end of the range for temperate habitats, although the lack of seasonal studies precludes further comparison. Nevertheless, rates are moderate to high, and outpace net primary production in many habitats. Highest respiration rates are usually recorded in coral reefs or in coastal lagoons where detrital matter frequently accumulates. Rates are lower in mangroves, probably reflecting more anaerobic conditions in contrast to the generally more oxidised sands on coral reefs (Alongi, 1989a). Seasonal variations in benthic metabolism have been examined only in a eutrophic, subtropical lagoon in southern Brazil (Machado & Knoppers, 1988) and in mangroves in northern Australia (Alongi, 1989a, and unpubl. data). Machado & Knoppers (1988) found no significant seasonal fluctuations in benthic respiration (Table XV), probably reflecting the lack of seasonal change in watercolumn productivity. In northern Australia, temperatures vary seasonally, probably causing the observed maximum values in summer (250–600 mgC·m -2·day -1) and minimum readings in winter (160– 340mgC·m -2 ·day -1 ) in the mangroves on Hinchinbrook Island. Respiration on tropical continental shelves and in subtidal coastal habitats has rarely been measured. On the central Great Barrier Reef shelf at depths of 15 to 46 m, oxygen consumption rates varied from 161 to 483 mgC·m 2 ·day -1, averaging 273 mgC·m -2·day -1; in a subtropical upwelling region off Baja California at 23-m depth, respiration rates were moderate, averaging 430 mgC·m 2 ·day -1 and ranging from 271–504 mgC·m-2·day -1 (Table XV). Both shelves exhibit mean respiration rates at the upper end of values measured on most temperate shelves (Walsh, 1983). The results of most microbial measurements of activity and growth are relative and cannot be readily converted to estimates of cell carbon production, thus limiting their usefulness for estimating materials and energy flow within ecosystems. Recent methods to measure the synthesis of nucleic acids in bacteria has provided ecologists with meaningful estimates of cell carbon production as well as rates of daily specific growth of natural assemblages, even in sediments. Recent estimates of bacterial production in tropical marine sediments based on rates of DNA synthesis are listed in Table XVI. Nearly all of these studies were conducted within the Great Barrier Reef province of Australia. The magnitude of production seems to depend to some extent on population density. Densities within the range of 10 8 to 10 9 cells·g -1 sediment dry wt exhibit production rates ranging
458
DANIEL M.ALONGI
from 20–300 mgC·m -2. day -1. This is particularly true for coral reef sediments. In mangroves and on the shelf proper, the range of densities is higher, from 10 9 to 10 11 cells·g -1 sediment dry wt and production is correspondingly high, ranging from 0.2 to 4.5 gC·m -2 ·day -1 . These values are not absolute because of the uncertainty regarding the conversion factors used. Nevertheless, it is clear that bacterial productivity is high in this tropical region. Other workers have found generally high production and rapid microbial growth in other tropical and subtropical regions (Table XVI; in a Colombian lagoon, Hoppe, Gocke, Zamorano & Zimmerman, 1983; in subtidal Philippine sediments, Balzer, von Bodungen & Pollehne, 1985; in Florida Halodule meadows, Moriarty, Iverson & Pollard, 1986; in an Hawaiian bay, Karl & Novitsky, 1988; off northwest African upwelling region, Lok Tan & Ruger, 1989). Figure 11 depicts the temporal fluctuations in bacterial productivity and growth rates measured over weekly to tri-weekly intervals in two sandflat habitats in a dry tropical region of Queensland, Australia. Fluctuations were large and apparently random, not correlating with any environmental conditions measured or with predator abundances. Rates of production were high ranging from 45 to 1725 mgC·m -2·day -1; growth rate (µ) was also rapid varying from 0.21 to 4.1·day1 , averaging a turnover rate of half a day. These results must be considered with caution, however, because rates of productivity and growth vary with tidal cycles, correlating significantly with the daily temperature range (Alongi, 1988b). Estimates of bacterial densities, production and growth vary widely with sediment depth in mangroves (Stanley, Boto, Alongi & Gillan, 1987) and in shelf sediments of the central Great Barrier Reef (Fig 12, bottom). Across the central Great Barrier Reef (Fig 12, top), vertical depth profiles indicate no consistent trends, excluding the station closest to the shelf break (Stn. 0S4) where no thymidine uptake was observed below a depth of 6 cm. Nearly all of the subsurface growth rates did not differ noticeably from surface values indicating that most subsurface bacteria utilise thymidine in these moderately anaerobic, disturbed sands. Similarly, in mangroves on Hinchinbrook Island, significant incorporation rates were observed (also under a nitrogen atmosphere) to a sediment depth of 10 cm (Stanley et al., 1987). These sediments are nearly entirely anaerobic below 2 cm, so it is probable that some anaerobic bacteria utilise thymidine. Figure 13 summarises turnover rates of sedimentary bacteria measured in various habitats within the Great Barrier Reef province. Several facts are evident: (1) turnover time is rapid (<4 days) in most intertidal sediments, (2) turnover is slower (>4 days) in most subtidal areas, and (3) bacterial turnover is more temperaturecontrolled in the intertidal than in the subtidal habitats. This is reflected in the higher regression coefficient for the intertidal values (note the scatter of subtidal values due, in part, to different water depths). These turnover times are, on average, greater than those obtained for temperate bacterial assemblages (see Kemp, 1987, and references therein). High densities, productivity and growth rates of sedimentary bacteria in this tropical region raise some interesting questions concerning regulatory factors. Why do tropical bacteria grow so rapidly and what is the fate of the biomass produced? Early (pre-1980) studies suggested that the main function of sedimentary bacteria was as food for benthic invertebrates and protozoans—a hypothesis based as much on theory as on empirical evidence. For instance, Gerlach (1978, and references therein) is popularly cited for the idea that meiofaunal organisms and larger
-1
TABLE XV
Rate of total community aerobic respiration (mgC·m ·day ) in some tropical and subtropical benthic habitats (excluding vegetated sediments), a=converted to carbon assuming a respiratory quotient of 1 and molar constant of 0.375; *=mean only; **=range only -2
TROPICAL BENTHIC ECOSYSTEMS 459
Estimates of bacterial densities and rates of bacterial production in some tropical and subtropical sediments, a=all production values estimated as mgC·m-2·day-1 using DNA synthesis method (Moriarty, 1986); b=gC·m-2·day-1; *=mean only; **=range only; n.a.=not measured
TABLE XVI
460 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
Fig 11. —Temporal changes in bacterial production (top) and specific growth rate of bacteria (production÷standing crop) in tropical sandflat sediments with (n) and without (£) inputs of mangrove detritus. Chunda Bay, Queensland, Australia (modified from Alongi, 1988b).
461
462
DANIEL M.ALONGI
invertebrates stimulate bacterial productivity by feeding on mainly senescent bacteria, keeping densities below threshold limits, by secreting mucus, and by aerating the sediments by irrigating tubes and burrows. This idea is based on three premises which now appear doubtful: (1) that bacterial communities in sediments are largely dormant and not highly productive; (2) that benthic invertebrates feed mainly on bacteria (in reality, a varied diet is required for most species), and (3) that temperate conditions can be extrapolated to habitats in other latitudes. A rapidly expanding database of bacterial production from all latitudes indicates rates of productivity that were considered unreasonable only a few years ago. The fate of this biomass production has been questioned by several workers (Alongi & Hanson, 1985; Alongi, 1988a, b, c, 1989a, b, c; Boto, Alongi & Nott, 1989; Kemp,
Fig 12. —Vertical distribution of bacterial numbers, production, and growth rates (bottom, left to right) in sediments (0–20-cm depth) across the central Great Barrier Reef shelf. Isotope incubations were conducted under a N atmosphere. Station 2 numbers correspond to those in top map. Modified from Alongi (1989c).
TROPICAL BENTHIC ECOSYSTEMS
463
1987, 1988 and see references therein). For instance, Kemp (1987) found that bacterial production in temperate sediments exceeds production of macrofauna by one or several orders of magnitude, suggesting that macrofauna probably seldom consume more than a small proportion of the bacteria produced. In a further experiment, Kemp (1988) found that bacterivory by benthic ciliates accounts for less than 4% of bacterial abundances daily or of bacterial production per hour.
Fig 13. —Relationship between surface sediment temperature and turnover of bacterial populations in various benthic habitats within the Great Barrier Reef province. Both regressions are significant at P < 0.01 significance level. Coral reef and seagrass data are not included in regressions. Dashed horizontal line separates most of the intertidal and subtidal data. Compiled from Moriarty & Pollard (1982), Moriarty et al. (1985), Moriarty (1986), Hansen et al. (1987), Alongi (1988a,b, 1989c), and Alongi, Boto & Tirendi (1989).
464
DANIEL M.ALONGI
Alongi (1988c, 1989a) proposed the carbon sink hypothesis which states that only a small proportion of bacterial biomass is consumed in sediments (mainly on the surface where predators are most abundant and/or on tubes and in burrow linings) with the remaining bacterial carbon recycled efficiently within sedimentary microbial food chains. The hypothesis evolved from observations in tropical mangroves that (1) bacterial biomass is large (210 gC·m -3 ) and productivity exceeds the highest rates of primary production; (2) densities of protozoans, meiofauna, and macro-infauna are low compared with other benthic systems and extrapolation of laboratory ingestion rates indicates that only a small proportion of bacterial biomass is consumed; (3) microalgal biomass is low with no measurable benthic net primary production; (4) the particulate and dissolved sedimentary carbon pools are large; (5) tidal cycle studies indicate regulation of bacterial growth by temperature and not by predators; (6) bacterial densities and growth rates frequently correlate with temperature, organic carbon or nitrogen, but rarely with meiofauna, protozoans and macro-infauna; (7) dissolved free amino acids and dissolved organic carbon in the sediment porewater are rapidly and completely utilised by bacteria at the sediment-water interface. DOC and amino acid fluxes across the interface are negligible, but when poisons are applied to the sediment surface, the fluxes are large and significant; and (8) there is a close similarity between the spectrum of major amino acids found free in the interstitial waters and those found within the intracellular pools of some sulphate-reducing bacteria (see chromatograms in Alongi, 1988c). ßglutamic acid, for instance, is a non-protein amino acid found in some sulphate-reducing bacteria and is a major component of the porewater DFAA pool in mangroves (Stanley et al., 1987). The amino acid is not derived from other sources such as mangrove leachates or from bacteria damaged during pore-water extraction, suggesting that the acid is derived from the natural breakdown and recyling of bacterial intracellular pools. Bacteria have short lifespans, so if they are not significantly grazed by predators, are reproducing rapidly but their numbers are not increasing greatly, then what other possible fate is there but cell lysis and recycling? Recycling may not be as dominant in other benthic systems as in tropical mangrove sediments. In temperate sandy habitats, physical conditions may dominate (e.g. on exposed sandy beaches) and temperatures in winter will invariably slow down consumption and natural mortality. This is probably true in the deep-sea as well. The fate of bacterial production therefore depends upon many factors such as temperature, nutrient conditions and the abundances of predators relative to bacterial prey densities. Nevertheless, these tropical results are compelling and indicate that concepts formulated from temperate conditions may not necessarily be applicable to their tropical counterparts; the reverse may also be true.
Macrofauna Meiofaunal production in the tropics has been estimated indirectly using annual turnover rates (P/B) derived from temperate communities (see references in Alongi, 1989a, b). These estimates must be considered invalid and inaccurate because turnover rates for tropical meiofauna are unknown and annual P/B ratios
TROPICAL BENTHIC ECOSYSTEMS
465
for temperate communities vary widely. There are also no valid tropical production estimates for protozoans or fungi. The productivity of macrofauna is generally easier to estimate than for smaller benthos, but the work is tedious and time-consuming, with estimation of distinct size classes easier for some phyla than for others. Nevertheless, several workers have estimated productivity of some tropical macrofaunal species (Table XVII). Moore (1972b) first estimated production of calcium carbonate by tropical molluscs from upper Biscayne Bay in Florida. The values vary greatly among species, ranging from less than 1 g to nearly 400 g·m -2·yr -1. In one intertidal area, the estimate was as high as 1000 g·m -2.yr -1. Production: biomass (P/B) ratios were low ranging from 0.6 to 2.4. The most extensive analyses of macrobenthic production were made by Edwards (1973a, b) in Venezuela and by Ansell, McLusky, Stirling & Trevallion (1978) in India. Edwards (1973b) used biomass and respiration estimates to estimate production using the relationship between total annual population respiration and production. On a shallow sub tidal beach at San Luis, he calculated a total production of 54.4 kcal·m -2·yr -1 and estimated that over 70% was consumed by demersal fish and 13% by the blue crab Callinectes. On a similar beach at Los Maritas, a total macrofaunal production of 170 kcal·m -2 ·yr -1 was calculated of which approximately 13% was eaten by starfish and nearly 90% was consumed by demersal fish. Using production-elimination methods and the P/R relationship, Ansell, Sivadas, Narayanan & Trevallion (1972b, but see Ansell et al., 1978) estimated production of two species of the wedge clam, Donax incarnatus and D. spiculum from exposed sandy beaches at Shertallai and Cochin. They estimated production rates of 7.2 and 5.8 kcal·m -2·yr -1, respectively, which are at the lower end of the range estimated for other tropical molluscs (Table XVII). Production estimates, however, can vary greatly among populations of the same species both among locations and recruitment years. Ansell et al. (1978) noted that on Goa beaches in India, both Donax species are much more abundant, suggesting much higher rates of production than found at Cochin or Shertallai. The productivity of other macro-invertebrates on the Indian beaches was estimated mainly using the production-respiration relationship because the data were too incomplete to provide growth and mortality estimates to measure production more directly (Table XVII). At Shertallai, total macrobenthic (mainly detritivores, carnivores, and herbivores) production was approximately 2445 kcal·m -1 transect (a mean P/B of 26.1). At Cochin, total production was lower, nearly 1455 kcal·m -1 transect (mean P/B of 39.5) and dominated by carnivores such as the mole crab Emerita holthuisi. Ansell et al. (1978) proposed that a large proportion of the production was passed on via predation to demersal fishes and crabs, although a proportion of the gametes and larvae were also lost by passage into the water column. Man is the main predator on the molluscs, particularly Donax. Production of some species is low on both beaches due to high mortality and disruption caused by the monsoons. Production is probably higher on more sheltered, lower-energy sandflats. In Malaysia, Berry & bin Othman (1983) observed the life cycle of the trochacean gastropod, Umbonium vestiarium on sandy shores in north Penang. Heavy recruitment was observed in June-July with the cohort growing to full size by January-March of the following year. Death occurred in May-June after spawning in March-May. This weakly seasonal, annual cycle is probably keyed
Annual production estimates (kcal·m-2) and production : biomass ratios for some tropical macro-invertebrates (modified and updated from Ansell et al., 1978). a=converted to kcal from gDW by multiplying by 4 (Crisp, 1975)
TABLE XVII
466 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
467
468
DANIEL M.ALONGI
to changes in wind direction, wave action and salinity caused by the northeast monsoon. Production was estimated at more than 300 kcal·m -2·yr -1, representing almost the entire secondary production on the sandflat. Upwelling areas are also sites of high benthic secondary production (Lee, 1978; Arntz et al., 1987; Bally, 1987; Arntz, Valdivia & Zeballos, 1988). Along the west coast of southern Africa, the Benguela upwelling enhances primary production, some of which (mainly kelp) impinges on some sandy beaches along the coast (see review by Bally, 1987, and references therein). As shown in Table XVIII, benthic secondary production is higher on southern Benguela beaches with significant kelp input. No data are available for production of subtidal macrofauna in proximity to the kelp-influenced beaches, but production estimates for subtidal populations without kelp input are high, indicating some, less obvious, food input such as phytoplankton. The estimates for microbes and meiofauna must be considered with caution but it is evident that these beach communities are positively influenced by upwelling. The responses of benthos to upwelling along the Peruvian coastline are more complex, with the upwelling and El Niño-Southern Oscillation events causing both positive and negative effects. On a sandy beach south of Lima, some species such as the bivalve Mesodesma donacium suffered heavy mortality but survived the events of 1982–1983 by high rates of production (see Table XVII). Mortality was largely a function of the above-average water temperatures. Production among commercially exploited invertebrates was similarly variable with some species suffering mass mortalities and others exhibiting enormous population increases, such as the scallop Argopecten purpuratus (Arntz et al., 1988). Ansell et al. (1978) compared macrofauna production of tropical and temperate beaches, and concluded that an equivalent biomass in the tropics produces a rate of biomass turnover ten times faster than in the temperate habitats. This is expressed in higher growth rates and mortality, and in the production to biomass (P/B) ratio. There is considerable overlap, but their analysis of P/B ratios in relation to the major zoogeographic divisions indicates a clear trend of increasing ratios towards warmer latitudes (Fig. 14). Latitudinal comparisons based on the P/B ratio must be considered with caution and must be based on populations with the same or similar age structures. The latitudinal trend is clearest for the bivalves probably because more production estimates are available for this group. As pointed out by Ansell and his co-workers, temperature is not the sole determinant (the Mediterranean values are generally higher than those for the warmer Caribbean); the results undoubtedly reflect better representation of some species in some areas than in others. The higher turnover rates for tropical benthos have been ascribed to a lack of temperature-compensation compared with their temperate counterparts (Ansell & Trevallion, 1969; Steele, 1976) but tropical demersal fishes appear to temperature-compensate. In comparison, tropical species exhibit greater mobility, faster growth rates, higher rates of mortality, shorter life spans, and greater rates of production per unit biomass than temperate macrobenthos. More production information is needed from all latitudes to determine the universality of this preliminary comparison but the differences appear to be real.
FOOD CHAIN DYNAMICS
TROPICAL BENTHIC ECOSYSTEMS
469
TABLE XVIII Annual secondary production (gDW·m -2) of benthos along the southern Benguela coastline (modified from Bally, 1987). To convert to kcal multiply by 4 (Crisp, 1975)
Benthic-pelagic coupling Benthic biomass and activity in all latitudes is closely related to food supply originating mainly from the overlying water column, and decreasing from shallow coastal and shelf regions to the deep sea (Rowe, 1971b; Cushing, 1988). The relationship between benthic biomass and depth was described statistically by Rowe (1971b) to estimate the effect of the magnitude of surface primary production on benthos. The results indicate that average benthic biomass is significantly higher in regions of high water-column production (e.g., New England and Peru) than in areas of low production (e.g., Bermuda, the Gulf of Mexico, and Brazil). The slope is dependent on the rate of decline in surface production away from the continents. As noted earlier, however, some regions experiencing high productivity and unique hydrographic conditions may be depleted of oxygen in both the water column and sediments inhibiting benthic production. Tseythin (1987) has recently analysed the relationship between benthic biomass and detrital flux to the sea bed using Soviet data obtained using dredges. Figure 15 summarises Tseythin’s results showing the significant dependence of benthic biomass on detrital flux to the bottom. The wide variability is due to the variations in depth, sediment type, geographical location, salinity, and temperature to name the most obvious covariates, but there is a clear trend. More interestingly, Tseythin (1987) analysed the data from cold-water regions (defined as mean annual water temperatures <20°C) and warm-water regions (>20°C), separately. He found that the benthic biomass of warm-water regions was less than the benthic biomass of cold-water regions by a factor of 20. The separation between cold- and warm-water regions was arbitrary, but the Soviet results are significant and indicate real biomass differences between climate regions, at least for megafauna obtained by dredging. It is interesting to note that the slopes were very similar suggesting that the community responses of large benthic organisms to increased food supply are generally positive at all latitudes. A comparison of available shallow-water (<100-m depth) benthic biomass data with phytoplankton production in various tropical regions is depicted in Figure 16 and similarly agrees with Rowe’s (1971b) earlier conclusions. The relationship in
470
DANIEL M.ALONGI
Fig 14. —Range of production: biomass (P/B) ratios for benthic macrofauna from different biogeographical areas; A=Indian tropical; B=Mediterranean, C=Caribbean, D=northern temperate and boreal. From Ansell et al. (1978); reproduced with permission of the Royal Society of Edinburgh.
shallow waters is naturally more variable compared with Rowe’s analysis because shallow-water communities are more influenced by changes in climate and are dependent upon a more diverse food supply from in situ plant production and estuarine outwelling. The pattern is, however, similar with highest faunal biomass occurring in upwelling regions. As in the Peruvian situation, high rates of primary production do not always preclude a high benthic standing crop. In the mudbank region off southwest India where primary production is high, the mudbanks are unstable and benthic biomass is low; more stable mudbanks are inhabited by a rich and highly abundant benthos attaining biomass values in some areas, as high as 500 g WW·m -2. The benthos of the west coast of India is more productive than on the east coast because the shelf is narrower and receives more continental run-off (Neyman, 1969). The relationship between benthic biomass or production and demersal fish catch in the tropics appears to be less rigorous than the benthic connection to primary production. Several workers in the tropics, mainly off the coasts of Peru and India, have suggested a close link between annual benthic production (or average benthic biomass) and potential fish yield (Savich, 1971; Harkantra
TROPICAL BENTHIC ECOSYSTEMS
471
et al., 1980; Parulekar, Harkantra & Ansari, 1982; Nair & Pillai, 1983; Rosenberg et al., 1983; Prabhu & Reddy, 1987; Cushing, 1988). Regression analyses of data available in these studies indicate a range of low correlations (r 2 =-0.19 to 0.31) and statistically non-significant relationships. It is undeniable that many, if not most, species of demersal fishes and crustaceans feed on benthic organisms but several factors may account for the lack of significant results: (1) there are not enough data from regions in which demersal fishes and benthic organisms have been sampled concurrently; (2) analyses at the total benthic biomass and total potential yield levels obfuscate interactions at the family or species level by grouping organisms of different trophic levels, age groups and phyla; (3) temporal and spatial scales are very different for both groups masking possible small-scale interactions. But much of this is true for plankton as well, suggesting that the dynamics of both fishes and benthos are more closely related to total water-column production than to each other. On a larger scale, rich demersal fisheries and abundant benthic communities tend to coincide in regions where primary production is high, such as in upwelling areas (Cushing, 1988). Comparisons between benthic and demersal fish and crustacean communities in the tropics are also limited by the various ways in which fisheries data are expressed (kg·ha -1; tonnes trawl·h -1; kg·20 min -1, etc.). It is probable, however, that the nature of fisheries and their ecosystem potential differs with latitude and different kinds of aquatic ecosystems (Jones, 1982; Marten & Polovina, 1982; Ursin, 1984). Marten & Polovina (1982) concluded that the best indicators of fishery yield in the tropics are water depth and primary production, with no single indicator predicting fish yields very precisely. Tropical fisheries comprise more species than in temperate areas, increasing the uncertainty regarding yield prediction (Jones, 1982). The relationship between benthos and fishery potential, and more generally, among all the trophic levels in the tropics may best be understood by examining the transfer of energy at the systems level and by comparing food chains of different latitudes.
Energy transfer within tropical benthic food chains and some latitudinal comparisons The principal pathways of energy flow through benthic food chains are unlikely to differ greatly with latitude but the actual amounts of material fluxing through certain pathways may be different. Earlier latitudinal comparisons of soft intertidal habitats and continental shelves are re-examined, expanded and updated in this section.
Intertidal habitats The first comparisons between tropical and temperate intertidal habitats were attempted as a result of the Scottish-Indian IBP programme (Stirling, 1975; Steele, 1976; Ansell et al., 1978; Munro, Wells & McIntyre, 1978). It was concluded that in comparison with the west Scottish beaches, the Indian sandy beaches have a much greater rate of energy flow, higher rates of oxygen consumption, lower population biomass and faunal diversity, higher levels of organic carbon and phosphate, lower levels of chlorophyll a, higher temperatures, and higher rates of invertebrate growth and mortality.
472
DANIEL M.ALONGI
Fig 15. —Relationship between flux of pelagic detritus to the sea bed and benthic biomass in cold-water (n) and warm water (o) regions at depths ≤200 m in various oceans; 1=regression for cold-water data, y=0.06341.1 (r=0.6), 2=regression for warm-water data, y=0.003640.96 (r=0.7). From Tseythin (1987); reproduced with permission of the American Geophysical Union.
TROPICAL BENTHIC ECOSYSTEMS
473
Fig 16. —Relationship between pelagic primary production and benthic biomass in some tropical oceans. Regression is significant at P<0.01 level. Compiled from Neyman (1969), Kurian (1971), Savich (1971), Desai (1973), Nichols & Rowe (1977), Harkantra et al. (1980), Parulekar, Dhargalkar & Singbal (1980), Rodrigues et al. (1982), Nair & Pillai (1983), Rosenberg et al. (1983), Yingst & Rhoads (1985), Aller & Aller (1986), Bally (1987), Furnas & Mitchell (1987), Prabhu & Reddy (1987), Cushing (1988), and Alongi (1989c).
These differences are undoubtedly real, but the major problem of such a comparison is that the variations within a latitudinal zone have not been considered. That is, variations among similar intertidal habitats within a given biogeographical region (e.g., a north temperate area) may be as wide as variations between latitudinal regions. To demonstrate, in Table XIX, the biotic components of a tropical sandy beach and a tropical mudflat are compared with a temperate sandflat and a temperate mudflat. In some respects the sandy habitats of both latitudes are more similar to each other than to their counterparts within the same climatic zone. Both the Indian sandy beach and sandflat on the Isle of Sylt are characterised by higher macrofaunal biomass than both mudflats. Conversely, the mudflats of different latitudes have similar bacterial biomass and levels of primary production. Other components such as respiration, bacterial turnover, and meiofaunal biomass are similar among the four intertidal habitats. These latitudinal similarities do not preclude differences in the magnitude of energy transfer along their respective food chains or differences in trophic and/or species composition. Nevertheless, it is clear that several habitat locations within a given latitudinal province must first be considered before rigorous conclusions regarding latitudinal similarities and differences can be made.
Continental shelves Energy transfer, benthic biomass and species richness, and fish yields within shelf ecosystems of different climatic zones have been compared
474
DANIEL M.ALONGI
previously by Golikov & Scarlato (1973), Hopner Petersen & Curtis (1980), Jones (1982), Marten & Polovina (1982), Hopner Petersen (1984), and Ursin (1984). The detailed comparisons of Hopner Petersen & Curtis (1980), Hopner Petersen (1984) and, to a lesser extent, of Golikov & Scarlato (1973) indicated fundamental differences in energy flow through boreal, temperate and tropical marine shelves. Comparing shelf ecosystems in Greenland, the North Sea, and in Thailand, Hopner Petersen & Curtis (1980) and Hopner Petersen (1984) reached several conclusions: (1) pelagic primary production increases from the subarctic to the tropics, but efficiency of energy transfer decreases to warmer latitudes; (2) zooplankton comprise a dominant link within tropical ecosystems; (3) partitioning of energy flow between zooplankton and the benthos is more equal in the subarctic; and (4) fisheries in the tropics are dominated by pelagic organisms, whereas demersal forms are of greater importance in higher latitudes. They further concluded that a relatively greater proportion of assimilated energy is lost via higher rates of respiration in the tropics and that all of these factors help to explain lower densities of benthos, greater symbiotic associations, and a higher incidence of toxins in the tropics. It is evident that such latitudinal comparisons are fraught with identical problems as with the intertidal comparisons. Undoubtedly, some structural and functional aspects are peculiar to tropical ecosystems but many of the above-mentioned characteristics such as lower densities and the greater prevalence of toxins in tropical systems may have alternative explanations, such as greater rates of physical disturbance and higher rates of predation. Table XX expands and updates the latitudinal comparisons of shelf ecosystems as originally attempted by Hopner Petersen & Curtis (1980). In this exercise, estimates of energy flow through more than one shelf ecosystem within the boreal, temperate, and tropical climatic zones are presented. As with the comparisons of intertidal habitats, variations in energy flow are as great within a climatic zone as they are among them. Primary and secondary production of plankton and benthos vary widely within climatic zones and even within a given ecosystem. In fact, the widest variations occur within tropical latitudes, probably reflecting the generally greater range of environmental conditions (e.g., up welling compared with non-upwelling areas, reefs, mangroves, fluid mudbanks, monsoons, mixed terrigenous-carbonate facies). Latitudinal comparisons of fishery potential are not conclusive mainly because information on tropical fisheries lags behind data on higher latitude fisheries which have been worked more extensively (and have been more affected by man). At this stage, there are no clear latitudinal differences in pelagic compared with demersal fish yields to man (Table XX). In fact, nominal fish catch data from a variety of tropical nations indicate that pelagic yields are roughly equal to or even less than yields of demersal organisms (Pauly, 1979) casting some doubt on the conclusions of Hopner Petersen & Curtis (1980) and Ursin (1984). In his analysis of benthicpelagic coupling on the continental shelf of Sierra Leone, Longhurst (1983) similarly suggested a lack of clear latitudinal trends in production and fish yield within marine shelf ecosystems. The attenuation of energy up the food chain to man is similar in all ecosystems, emphasising the fact that the basic laws of thermodynamics must apply to the transfer of energy within all ecosystems, irrespective of climate and latitude.
Biotic comparisons of tropical and temperate mud- and sandflats. References: 1 Steele, 1976; Munro et al., 1978 and references therein; 2 Alongi, 1988a & unpubl. data; 3 Reise, 1985 and references therein; 4 Schwinghamer, Hargrave, Peer & Hawkins, 1986.
TABLE XIX TROPICAL BENTHIC ECOSYSTEMS 475
TABLE XX
Comparison estimates of production and fish yield to man (kcal·m ·yr-1) for some boreal, temperate and tropical continental shelf ecosystems (modified from Hopner Petersen & Curtis, 1980). References: 1 Hopner Petersen & Curtis, 1980; 2 Cushing, 1988; 3 Sharp, 1988; 4 Walsh, 1983; 5 Jones, 1984; 6 Probert, 1986; 7 Menasveta & Hongskul, 1988; 8 Longhurst, 1983; 9 Alongi, 1989c; 10 Furnas & Mitchell, 1987; 11 Williams, Dixon & English, 1988 and unpubl. data, a=estimated using P/B ratios in Ref. 8 -2
476 DANIEL M.ALONGI
TROPICAL BENTHIC ECOSYSTEMS
477
SUMMARY AND CONCLUSIONS
(1) The diversity of benthic habitats peaks in the tropics. Wide variations in monsoonal rainfall are responsible for the formation and maintenance of many sedimentary facies and habitats: fluid mudbanks, carbonate shelves, green and blue anoxic mud regions, mixed terrigenous-carbonate bedforms, stromatolites, hypersaline lagoons, mangroves, and coral reefs. (2) Seasonality of shallow-water benthos depends upon distance from the Equator and wet compared with dry locations. Run-off of continental water and sediment occurs mainly in the wet tropics, causing sediment erosion and displacement and/or mortality of most benthic fauna. In seasons or in areas where evaporation exceeds precipitation, high temperatures and salinity and desiccation, control most intertidal and shallow coastal assemblages. (3) Faunal densities in intertidal habitats are similar to their temperate counterparts but are dominated mainly by ocypodid crabs, isopods, and bivalves of the genus Donax. (4) Faunal densities in lagoons and estuaries are lower than in similar temperate habitats, probably due to greater stress associated with high continental run-off and subsequent sediment disturbance and low dissolved oxygen levels. (5) Infaunal diversity is not higher in the tropics but there is some evidence for higher abundances and diversity of warm-water epifauna. Variations in species richness are wide, reflecting the greater range of habitat types and climate in the tropics. (6) Low-latitude shelves are either open or are protected lagoons rimmed by coral reefs, differing from colder shelves by the more frequent occurrence of carbonate deposits and migrating mudbanks. They are generally shallow, driven by intermittant intrusions of nutrient-rich, upwelled water and/or by estuarine outwelling. Benthic communities generally thrive in these regions but are commonly subjected to anoxia when river inputs and upwelling events occur too frequently, on a massive scale or simultaneously with periods of stagnant and/or stratified water masses. (7) As in all latitudes, benthic biomass in the tropics relates to patterns of primary production. Areas of low biomass are prevalent in the tropics reflecting not only low plankton production but stress induced by high temperatures, wide variations in salinity, compacted sediments, low oxygen conditions, and moderate to high levels of climatic disturbance. Tropical species are as negatively affected by stressful conditions as are temperate species. (8) Breeding and reproduction are not continuous in most benthic species. Spawning, in many cases, coincides with the onset of monsoons. (9) Few data exist about trophic interrelationships among tropical benthic organisms. Energetically, production by microalgae is within temperate levels, but standing stocks are lower. There is some evidence for higher rates of total community metabolism, bacterial growth, and secondary production but pelagic and demersal fish yields to man are latitudinally equivalent. (10) Real differences and discontinuities exist among benthic assemblages at different latitudes but earlier comparisons of differences in energy transfer and foodchain yields among boreal, temperate, and tropical latitudes are doubtful because differences within latitudinal regions were not considered. The lack of clear latitudinal trends at the ecosystem level reflects thermodynamic constraints which must apply to benthic food webs of all latitudes.
478
DANIEL M.ALONGI
ACKNOWLEDGEMENTS I thank the librarians at the Australian Institute of Marine Institute, especially Bronwyn Betts, for patiently finding many references. Kim Truscott is thanked for typing another long manuscript. Several publishers and authors are thanked for allowing me to modify and reproduce published figures. Mr Murray Eagle of OK Tedi Mining Ltd supplied unpublished data on river run-off in Papua New Guinea. Alistar Robertson and Tom Pearson reviewed the manuscript, and Alan Dartnall parsed my sentences. The financial and logistical support of the Australian Institute of Marine Science is gratefully acknowledged.
REFERENCES Abdul Azis, P.K. & Balakrishnan Nair, N., 1983. Meiofauna of the EdavaNadayara Paravur backwater system—southwest coast of India. Mah. Bull. Natl. Inst. Oceanogr., 16, 55–65. Achuthankutty, C.T., 1976. Ecology of sandy beach at Sancoale, Goa: Part I— Physical factors influencing production of macrofauna. Indian J. Mar. Sci., 5, 91–97. Achuthankutty, C.T., Stirling, A., Nair, S., Loka Bharathi, P.A. & Menezes, M.R., 1978. Sandy beach at Baina, Goa: its ecology and production. Indian J. Mar. Sci., 7, 23–29. Achuthankutty, C.T. & Wafar, M.V.M., 1976. Ecology of sandy beach at Sancoale, Goa. Part II. Population model and production of Emerita holthuisi Sankolli. Indian J. Mar. Sci., 5, 98–102. Aladro Lubel, M.A., 1984. Algunos ciliados intersticiales de Isla de Enmedia, Veracruz, Mexico. An. Inst. Biol. Univ. Nac. Auton, Mex. Ser. Zool., 55, 1– 59. Aller, J.Y. & Aller, R.C., 1986. General characteristics of benthic faunas on the Amazon inner continental shelf with comparison to the shelf off the Changjiang River, East China Sea. Cont. Shelf. Res., 6, 291–310. Alongi, D.M., 1986. Quantitative estimates of benthic protozoa in tropical marine systems using silica gel: a comparison of methods. Estuarine Coastal Shelf Sci., 23, 443–450. Alongi, D.M., 1987a. Intertidal zonation and seasonality of meiobenthos in tropical mangrove estuaries. Mar. Biol., 95, 447–458. Alongi, D.M., 1987b. Inter-estuary variation and intertidal zonation of freeliving nematode communities in tropical mangrove systems. Mar. Ecol. Prog. Ser., 40, 103–114. Alongi, D.M., 1988a. Bacterial productivity and microbial biomass in tropical mangrove sediments. Micro. Ecol., 15, 59–79. Alongi, D.M., 1988b. Microbial-meiofaunal interrelationships in some tropical intertidal sediments. J. Mar. Res., 46, 349–365. Alongi, D.M., 1988c. Detritus in coral reef ecosystems: fluxes and fates. Proc. Sixth Int. Coral Reef Symp., 6, 29–36. Alongi, D.M., 1989a. The role of soft-bottom benthic communities in tropical mangrove and coral reef ecosystems. Rev. Aquat. Sci., 1, 234–280. Alongi, D.M., 1989b. Ecology of tropical soft-bottom benthos: a review with emphasis on emerging concepts. Rev. Biol. Trop., 37, 73–88.
TROPICAL BENTHIC ECOSYSTEMS
479
Alongi, D.M., 1989c. Benthic processes across mixed terrigenous-carbonate sedimentary facies on the central Great Barrier Reef continental shelf. Cont. Shelf Res., 9, 629–663. Alongi, D.M., 1990. Community dynamics of free-living nematodes in some tropical mangrove and sandflat habitats. Bull. Mar. Sci., 46, in press . Alongi, D.M., Boto, K.G. & Tirendi, F., 1989. Effect of exported mangrove litter on bacterial productivity and dissolved organic carbon fluxes in adjacent tropical nearshore sediments. Mar. Ecol. Prog. Ser., 56, 133–144. Alongi, D.M. & Hanson, R.B., 1985. Effect of detritus supply on trophic relationships within experimental benthic food webs. II. Microbial responses, fate and composition of decomposing detritus. J. Exp. Mar. Biol. Ecol., 88, 167–182. Ansari, Z.A., 1978. Meiobenthos from the Karwar region (central west coast of India). Mah. Bull Natl. Inst. Oceanogr., 11, 163–167. Ansari, Z.A., 1984. Benthic macro and meiofauna of seagrass (Thalassia hemprichii) bed at Minicoy, Lakshadweep. Indian J. Mar. Sci., 13, 126–127. Ansari, Z.A., Chatterji, A. & Parulekar, A.H., 1984a. Effect of domestic sewage on sand beach meiofauna at Goa, India. Hydrobiologia, 111, 229–233. Ansari, Z.A., Chatterji, A. & Parulekar, A.H., 1986a. Growth and production of benthic-bivalve, Gafrarium pectinatum (Linn.) from west coast of India. Indian J. Mar. Sci., 15, 262–263. Ansari, Z.A., Harkantra, S.N., Nair, S.A. & Parulekar, A.H., 1977. Benthos of the Bay of Bengal: a preliminary account. Mah. Bull. Natl. Inst. Oceanogr., 10, 55–60. Ansari, Z.A. & Ingole, B.S., 1983. Meiofauna of some sandy beaches of Andaman Islands. Indian J. Mar. Sci., 12, 245–246. Ansari, Z.A., Ingole, B.S. & Parulekar, A.H., 1984b. Macrofauna and meiofauna of two sandy beaches at Mombasa, Kenya. Indian J. Mar. Sci., 13, 187–189. Ansari, Z.A., Ingole, B.S. & Parulekar, A.H., 1986b. Effect of high organic enrichment of benthic polychaete populations in an estuary. Mar. Pollut. Bull., 17, 361–365. Ansari, Z.A. & Parulekar, A.H., 1981. Meiofauna of the Andaman Sea. Indian J. Mar. Sci., 10, 285–288. Ansari, Z.A., Parulekar, A.H. & Jagtap, T.G., 1980. Distribution of sublittoral meiobenthos off Goa Coast, India. Hydrobiologia, 74, 209–214. Ansari, Z.A., Rodrigues, C.L., Chatterji, A. & Parulekar, A.H., 1982. Distribution of meiobenthos and macrobenthos at the mouth of some rivers of the east coast of India. Indian J. Mar. Sci., 11, 342–343. Ansell, A.D., 1983. The biology of the genus Donax. In , Sandy Beaches as Ecosystems, edited by A. McLachlan & T. Erasmus, Dr W. Junk Publ., The Hague, pp. 607– 636. Ansell, A.D., McLusky, D.S., Stirling, A. & Trevallion, A., 1978. Production and energy flow in the macrobenthos of two sandy beaches in South West India. Proc. R. Soc. Edinburgh, Sect. B, 76, 269–296. Ansell, A.D. & Morton, B., 1987. Alternative predation tactics of a tropical naticid gastropod. J. Exp. Mar. Biol. Ecol., 111, 109–119. Ansell, A.D., Sivadas, P. & Narayanan, B., 1973. The ecology of two sandy beaches in southwest India. IV. The biochemical composition of four common invertebrates. Spec. Publ. Mar. Biol. Assoc. India, 333–348. Ansell, A.D., Sivadas, P., Narayanan, B., Sankaranarayanan, V.N. & Trevallion, A., 1972a. The ecology of two sandy beaches in South West India. I. Seasonal changes in physical and chemical factors, and in the macro fauna. Mar. Biol., 17, 38–62.
480
DANIEL M.ALONGI
Ansell, A.D., Sivadas, P., Narayanan, B. & Trevallion, A., 1972b. The ecology of two sandy beaches in south west India. II. Notes on Emerita holthuisi. Mar. Biol., 17, 311–317. Ansell, A.D., Sivadas, P., Narayanan, B. & Trevallion, A., 1972c. The ecology of two sandy beaches in South West India. III. Observations on the population of Donax incarnatus and D. spiculum . Mar. Biol., 17, 318–332. Ansell, A.D. & Trevallion, A., 1969. Behavioural adaptations of intertidal molluscs from a tropical sandy beach. J. Exp. Mar. Biol. Ecol., 4, 9–35. Ansell, A.D. & Trueman, E.R., 1973. The energy cost of migration of the bivalve Donax on tropical sandy beaches. Mar. Behav. Physiol., 2, 21–32. Arntz, W.E., Brey, T., Tarazona, J. & Robles, A., 1987. Changes in the structure of a shallow sandy beach community in Peru during an El Nino event. S. Afr. J. Mar. Sci., 5, 645–658. Arntz, W.E., Valdivia, E. & Zeballos, J., 1988. Impact of El Nino 1982–1983 on the commercially exploited invertebrates (mariscos) of the Peruvian shore. Meeresforsch., 32, 3–22. Aswandy, I., Kastoro, W.W., Aziz, A. & Al Hakim, I., in press. Distribution, abundance and species composition of macro benthos in Seribu Islands. In, Living Resources in Coastal Areas, edited by A.C.Alcala et al., University of Philippines Press, Manila, in press. Balakrishnan Nair, N., Abdul Azis, P.K., Arunachalam, M., Dharmaraj, K. & Krishnakumar, K., 1984. Ecology of Indian estuaries: ecology and distribution of benthic macrofauna in the Ashtamudi estuary, Kerala. Mah. Bull Natl. Inst. Oceanogr., 17, 89–101. Bally, R., 1987. The ecology of sandy beaches of the Benguela ecosystem. S. Afr. J. Mar. Sci., 5, 759–770. Balzer, W., von Bodungen, B. & Pollehne, F., 1985. Benthic degradation of organic matter and regeneration of nutrients in shallow water sediments off Mactan, Philippines. Philipp. Sci., 22, 30–41. Banse, K., 1968. Hydrography of the Arabian Sea shelf of India and Pakistan and effects on demersal fishes. Deep-Sea Res., 15, 45–79. Basov, I.A., 1976. Quantiative distribution of benthic formanifers on the Northwest African shelf. Oceanology, 15, 223–225. Berry, A.J., 1964. The natural history of the shore fauna of North Penang. Malay. Nat. J., 18, 81–103. Berry, A.J., 1975. Patterns of breeding activity in West Malaysian gastropod molluscs. Malays. J. Sci., 3, 49–59. Berry, A.J. & bin Othman, Z., 1983. An annual cycle of recruitment, growth and production in a Malaysian population of the trochacean gastropod Umbonium vestiarium (L.). Estuarine Coastal Shelf Sci., 17, 375–363. Bertness, M.D., 1981a. Seasonality in tropical hermit crab reproduction in the Bay of Panama. Biotropica, 13, 292–300. Bertness, M.D., 1981b. Pattern and plasticity in tropical hermit crab growth and reproduction. Am. Nat., 117, 754–772. Bhat, U.G. & Neelakantan, B., 1988. Environmental impact on the macrobenthos distribution of Kali estuary, Karwar, central west coast of India. Indian J. Mar. Sci., 17, 134–142. Birtles, R.A. & Arnold, P.W., 1988. Distribution of trophic groups of epifaunal echinoderms and molluscs in the soft sediment areas of the central Great Barrier Reef shelf. Proc. Sixth Int. Coral Reef Symp., 6, 325–332. Black, R. & Peterson, C.H., 1988. Absence of preemption and interference competition for space between large suspension-feeding bivalves and smaller infaunal macro-invertebrates. J. Exp. Mar. Biol. Ecol., 120, 183–198. Bolin, B., Degins, E.T., Kempe, S. & Ketner, P., 1979. The Global Carbon Cycle. John Wiley & Sons, Chichester, 491 pp.
TROPICAL BENTHIC ECOSYSTEMS
481
Boto, K.G., Alongi, D.M. & Nott, A.L.J., 1989. Dissolved organic carbonbacteria interactions at sediment-water interface in a tropical mangrove system. Mar. Ecol. Prog. Ser., 51, 243–251. Boto, K.G. & Bunt, J.S., 1981. Dissolved oxygen and pH relationships in northern Australian mangrove waterways. Limnol. Oceanogr., 26, 1176– 1178. Briggs, J.C., 1985. Species richness among the tropical shelf regions. Soviet J. Mar. Biol., 11, 295–302. Broom, M.J., 1982. Structure and seasonality in a Malaysia mudflat community. Estuarine Coastal Shelf Sci., 15, 135–150. Buchanan, B.A. & Stoner, A.W., 1988. Distributional patterns of blue crabs (Callinectes sp.) in a tropical estuarine lagoon. Estuaries, 11, 231–239. Buchanan, J.B., 1957. Benthic fauna of the continental edge off Accra, Ghana. Nature (London), 179, 63–635. Buchanan, J.B., 1958. The bottom fauna across the continental shelf off Accra, Gold Coast. Proc. Zool. Soc. London, 130, 1–56. Bullock, T.H., 1955. Compensation for temperature in the metabolism and activity of poikilotherms. Biol Rev., 30, 311–342. Bunt, J.S., Lee, C.C. & Lee, E., 1972. Primary productivity and related data from tropical and subtropical marine sediments. Mar. Biol., 16, 28–36. Bush, L.F., 1966. Distribution of sand fauna in beaches at Miami, Florida. Bull. Mar. Sci., 16, 58–75. Camacho-Ibar, V.F. & Alvarez-Borrego, S., 1988. Nutrient concentrations in pore waters of intertidal sediments in a coastal lagoon: patchiness and temporal variations. Sci. Total Environ., 75, 325–339. Cane, M.A. & Sarachik, E.S., 1983. Equatorial oceanography. Rev. Geophys. Space Phys., 21, 1137–1148. Chardy, P. & Clavier, J., 1988. Biomass and trophic structure of the macrobenthos in the southwest lagoon of New Caledonia. Mar. Biol., 99, 195–202. Chareonruay, M., 1980. Bottom productivity in the Gulf of Thailand. Mar. Fish. Lab., Bangkok, Circ. Pap., No. 14, 17 pp. Chong, V.C. & Sasekumar, A., 1981. Food and feeding habits of the white prawn Penaeus merguiensis. Mar. Ecol. Prog. Ser., 5, 185–191. Chullasorn, S. & Martosubroto, P., 1986. Distribution and important biological features of coastal fish resources in Southeast Asia. FAO Fish. Tech. Paper, No. 278, 84 pp. Clarke, A., 1980. A reappraisal of the concept of metabolic cold adaption in polar marine invertebrates. Biol. J. Linn. Soc., 14, 77–92. Colijn, F. & de Jonge, V.N., 1984. Primary production of microphytobenthos in the Ems-Dollard Estuary. Mar. Ecol. Prog. Ser., 14, 185–196. Corredor, J.E. & Capone, D.G., 1985. Studies on nitrogen diagenesis in coral reef sands. Proc. Fifth Int. Coral Reef Symp., 3, 395–00. Corredor, J.E. & Morell, J.M., 1989. Assessment of inorganic nitrogen fluxes across the sediment-water interface in a tropical lagoon. Estuarine Coastal Shelf Sci., 28, 339–345. Crisp, D.J., 1975. Secondary productivity in the sea. In, Productivity of World Ecosystems, edited by D.E. Richle, et al., Natl. Acad. Sci., Washington, D.C., pp. 71–89. Cushing, D.H., 1988. The flow of energy in marine ecosystems, with special reference to the continental shelf. In, Continental Shelves. Ecosystems of the World 27, edited by H.Postma & J.J.Zijlstra, Elsevier, Amsterdam, pp. 203– 226. Dahl, E., 1953. Some aspects of the ecology and zonation of the fauna of sandy beaches. Oikos, 4, 1–27.
482
DANIEL M.ALONGI
Damodaran, R., 1973. Studies on the benthos of the mudbanks of the Kerala coast. Bull. Dept. Mar. Sci. Univ. Cochin, 6, 1–126. Datta, N.C. & Sarangi, N., 1986. Benthic macroinvertebrate community of estuarine waters of West Bengal, India. In, Indian Ocean. Biology of Benthic Marine Organisms, edited by M.-F.Thompson et al., A.A.Balkema, Rotterdam, pp. 247–256. Dehnel, P.A., 1955. Rates of growth of gastropods as a function of latitude. Physiol. Zool., 28, 115–144. De la Cruz, A.A., 1986. Tropical wetlands as a carbon source. Aquat. Bot., 25, 109–115. De la Cruz, E. & Vargas, J.A., 1986. Estudio preliminar de la meiofauna de la playa fangosa de Punta Morales, Golfo de Nicoya, Costa Rica, Brenesia, 25–26, 89–97. Desai, B.N., 1973. Benthic productivity in the Indian Ocean. Mah. Bull. Natl. Inst. Oceanogr., 6, 128–132. Deshmukh, I., 1986. Ecology and Tropical Biology. Blackwell Scientific Publishers, Palo Alto, 387 pp. DeVries, M.C., Epifanio, C.E. & Dittel, A.I., 1983a. Reproductive periodicity of the tropical crab Callinectes arcuatus Ordway in Central America. Estuarine Coastal Shelf Sci., 17, 709–716. DeVries, M.C., Epifanio, C.E. & Dittel, A.I., 1983b. Lunar rhythms in the egg hatching of the subtidal crustacean Callinectes arcuatus Ordway (Decapoda: Brachyura). Estuarine Coastal Shelf Sci., 17, 717–724. Dexter, D.M., 1972. Comparison of the community structures in a Pacific and an Atlantic Panamanian sandy beach. Bull. Mar. Sci., 22, 449–462. Dexter, D.M., 1974. Sandy beach fauna of the Pacific and Atlantic coasts of Costa Rica and Colombia. Rev. Biol Trop., 22, 51–66. Dexter, D.M., 1976. The sandy beach fauna of Mexico. Southwest. Nat., 20, 479–485. Dexter, D.M., 1977. Natural history of the Pan-American sand beach isopod Excirolana braziliensis (Crustacea: Malacostraca). J. Zool., 183, 103– 109. Dexter, D.M., 1979. Community structure and seasonal variation in intertidal Panamanian sandy beaches. Estuarine Coastal Mar. Set., 9, 543–558. Dhamne, K.P. & Mane, U.H., 1976. Respiration in the clam, Paphia laterisulca. J. Mar. Biol. Assoc. India, 18, 499–508. Divakaran, O., Murugan, T. & Balakrishnan Nair, N., 1981a. Distribution and seasonal variation of the benthic fauna of the Ashtamudi Lake, southwest coast of India. Mah. Bull. Natl. Inst. Oceanogr., 14, 167–172. Divakaran, O., Murugan, T. & Balakrishnan Nair, N., 1981b. Distribution and seasonal variation of the benthic fauna of Vizhinjam inshore water, southwest coast of India. Mah. Bull. Natl. Inst. Oceanogr., 14, 193–198. Duarte, C.M., 1989. Temporal biomass variability and production/biomass relationships of seagrass communities. Mar. Ecol. Prog. Ser., 51, 269– 276. Durand, J.R. & Skubich, M., 1982. The lagoons of the Ivory Coast. Aquaculture, 27, 211–250. Dwivedi, S.N., Ayyappan Nair, S. & Rahim, A., 1973. Ecology and production of intertidal macrofauna during monsoon in a sandy beach at Calangute, Goa. J. Mar. Biol. Assoc. India, 15, 274–284. Edwards, R.R.C., 1973a. Production ecology of two Caribbean marine ecosystems. I. Physical environment and fauna. Estuarine Coastal Mar. Sci., 1, 303–318.
TROPICAL BENTHIC ECOSYSTEMS
483
Edwards, R.R.C., 1973b. Production ecology of two Caribbean marine ecosystems. II. Metabolism and energy flow. Estuarine Coastal Mar. Sci., 1, 319–333. Edwards, R.R.C., 1978. Ecology of a coastal lagoon complex in Mexico. Estuarine Coastal Mar. Sci., 6, 75–92. Edwards, R.R.C., Blaxter, J.H.S., Gopalan, U.K. & Mathew, C.V., 1970. A comparison of standard oxygen consumption of temperate and tropical bottom-living marine fish. Comp. Biochem. Physiol., 34, 491–495. Edwards, R.R.C., Blaxter, J.H.S., Gopalan, U.K., Mathew, C.V. & Finlayson, D.M., 1971. Feeding, metabolism, and growth of tropical flatfish. J. Exp. Mar. Biol. Ecol., 6, 279–300. Ekman, S., 1953. Zoogeography of the Sea. Sidgwick & Jackson Ltd, London, 417pp. Epifanio, C.E., Maurer, D. & Dittel, A., 1982. Seasonal changes in nutrients and dissolved oxygen in the Gulf of Nicoya, a tropical estuary on the Pacific coast of central America. Hydrobiologia, 101, 231–238. Estacion, J.S. & Onate, J.A., in press. Soft-bottom invertebrates of Bais Bays, Negros Oriental, Philippines. In, Living Resources in Coastal Areas, edited by A.C. Alcala et al., University of Philippines Press, Manila, in press. Fagade, S.O. & Olaniyan, C.I.O., 1973. The food and feeding relationships of the fishes in Lagos lagoon. J. Fish Biol., 5, 205–225. Fager, E.W. & Longhurst, A.R., 1968. Recurrent group analysis of species assemblages of demersal fish in the Gulf of Guinea. J. Fish. Res. Board Can., 25, 1405–1421. Fernando, S.A., Khan, S.A. & Kasinathan, R., 1983. Observations on the distribution of benthic fauna in Vellar estuary, Porto Novo. Mah. Bull. Natl. Inst. Oceanogr., 16, 341–348. Fishelson, L., 1971. Ecology and distribution of the benthic fauna in the shallow waters of the Red Sea. Mar. Biol., 10, 113–133. Flood, P.R., Braun, J.G. & DeLeon, A.R., 1976. On the annual production of Amphioxus larvae (Brachiostoma senegalense Webb) off Cap Blanc, North West Africa. Sarsia, 61, 63–70. Frankenberg, D. & Menzies, R.J., 1968. Some quantitative analyses of deep-sea benthos off Peru. Deep-Sea Res., 15, 623–626. Froidefond, J.M., Pujos, M. & Andre, X., 1988. Migration of mud banks and changing coastline in French Guiana. Mar. Geol., 84, 19–30. Furnas, M.J. & Mitchell, A.W., 1987. Phytoplankton dynamics in the central Great Barrier Reef. II. Primary production. Cont. Shelf Res., 7, 1049–1062. Gallardo, A., 1963. Notos sobre la densidad de la fauna bentonica en el sublitoral del norte de Chile. Gayana Zool., 10, 3–15. Gallardo, V.A., 1977. Large benthic microbial communities in sulphide biota under Peru-Chile subsurface countercurrent. Nature (London), 268, 331–332. Gallardo, V.A., Castillo, J.G., Retamal, M.A., Yanez, A., Moyano, H.I. & Hermosilla, J.G., 1977. Quantitative studies on the soft-bottom macro benthic animal communities of shallow Antarctic bays. In, Adaptations within Antarctic Ecosystems: Proceedings of the Third SCAR Symposium on Antarctic Biology, edited by G.A.Llano, Smithsonian Inst, Houston, Texas, pp. 361–387. Ganapati, P.N. & Rao, G. C, 1962. Ecology of the interstitial fauna inhabiting the sandy beaches of Waltair coast. J. Mar. Biol. Assoc. India, 4, 44–57. Ganapati, P.N. & Rao, M.V.N., 1958. Systematic survey of marine ciliates from Visakhapatnam. Andhra Univ. Mem. Oceanogr., 2, 75–90. Garrity, S.D., Levings, S.C. & Caffey, H.M., 1986. Spatial and temporal variation in shell crushing by fishes on rocky shores of Pacific Panama. J. Exp. Mar. Biol. Ecol., 103, 131–142.
484
DANIEL M.ALONGI
Gauld, D.T. & Buchanan, J.B., 1956. The fauna of sandy beaches in the Gold Coast. Oikos, 7, 293–301. Gerlach, S.A., 1978. Food-chain relationships in subtidal silty sandy marine sediments and the role of meiofauna in stimulating bacterial productivity. Oecologia (Berlin), 33, 55–69. Gibbs, P.E., 1978. Macro fauna of the intertidal sand flats on low wooded islands, northern Great Barrier Reef. Phil. Trans. R. Soc. London, Ser. B, 284, 81–97. Glynn, P.W., 1988. El Nino-Southern Oscillation 1982–1983: nearshore population, community and ecosystem responses. Annu. Rev. Ecol. Syst., 19, 309–345. Gocke, K., Vitola, M. & Rojas, G., 1981. Oxygen consumption patterns in a mangrove swamp on the Pacific coast of Costa Rica. Rev. Biol. Trop., 29, 143– 154. Golikov, A.N. & Scarlato, O.A., 1973. Comparative characteristics of some ecosystems of the upper regions of the shelf in tropical, temperate and Arctic waters. Helgol. Wiss. Meeresunters., 24, 219–234. Goodbody, I., 1965. Continuous breeding in populations of two tropical crustaceans, Mysidium colombiae (Zimmer) and Emerita portoricensis (Schmidt). Ecology, 46, 195–197. Gopinathan, C.K. & Qasim, S.Z., 1974. Mud banks of Kerala—their formation and characteristics. Indian J. Mar. Sci., 3, 105–114. Gosselck, F., 1975. The distribution of Brachiostoma senegalense (Acrania, Branchiostomidae) in the offshore shelf region off North Africa. Int. Rev. Gesamten Hydrobiol., 60, 199–207. Gosselck, F. & Kuehner, E., 1973. Investigations on the biology of Branchiostoma senegalense larvae off the Northwest African coast. Mar. Biol., 22, 67–73. Gourbault, N. & Renaud-Mornant, J., 1989. Distribution, assemblages et strategies trophiques des micro-meiofaunes d’un atoll semi-ferme (Tuamotu Est). C.R. Acad. Sci., Ser. III, 309, 69–75. Govindan, K., Varshney, P.K. & Desai, B.N., 1983. Benthic studies in South Gujarat estuaries. Mah. Bull. Natl Inst. Oceanogr., 16, 349–356. Govindan Kutty, A.G. & Nair, N.B., 1966. Preliminary observations on the interstitial fauna of the southwest coast of India. Hydrobiologia, 28, 101–122. Govindan Kutty, A.G. & Nair, N.B., 1972. Observations on the breeding periods of certain interstitial nematodes, gastrotrichs, and copepods of the southwest coast of India. J. Mar. Biol. Assoc. India, 14, 402–406. Gray, J.S., 1981. The Ecology of Marine Sediments. Cambridge University Press, Cambridge, 185 pp. Green, R.H., 1968. Mortality and stability in a low diversity subtropical intertidal community. Ecology, 49, 848–854. Grelet, Y., Falconetti, C., Thomassin, B.A., Vitiello, P. & Abu Hilal, A.H., 1987. Distribution of the macro- and meiobenthic assemblages in the littoral soft bottoms of the Gulf of Aquaba (Jordan). Atoll Res. Bull. No. 308, 27 pp. Hammond, L.S., 1983. Experimental studies of salinity tolerance, burrowing behavior and pedicle regeneration in Lingula anatina (Brachipoda, Inarticulata). J. Paleontol., 57, 1311–1316. Hansen, J.A., Alongi, D.M., Moriarty, D.J.W. & Pollard, P.C., 1987. The dynamics of benthic microbial communities at Davies Reef, central Great Barrier Reef. Coral Reefs, 6, 63–70. Hargraves, P.E., 1982. Production of some benthic communities at Carrie Bow Cay, Belize. In, The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize, I, Structure and Communities, edited by K.Rutzler & I.G.Macintyre, Smithsonian Institution Press, Washington, D.C., pp. 109–114.
TROPICAL BENTHIC ECOSYSTEMS
485
Harkantra, S.N., Nair, A., Ansari, Z.A. & Parulekar, A.H., 1980. Benthos of the shelf region along the west coast of India. Indian J. Mar. Sci., 9, 106– 110. Harkantra, S.N. & Parulekar, A.H., 1981. Ecology of benthic production in the coastal zone of Goa. Mah. Bull. Natl. Inst. Oceanogr., 14, 135–139. Harkantra, S.N. & Parulekar, A.H., 1985. Community structure of sanddwelling macrofauna of an estuarine beach in Goa, India. Mar. Ecol. Prog. Ser., 30, 291–294. Harkantra, S.N. & Parulekar, A.H., 1987. Benthos off Cochin, southwest coast of India. Indian J. Mar. Sci., 16, 57–59. Harper, D.E., McKinney, L.D., Salzer, R.R. & Case, R.J., 1981. The occurrence of hypoxic bottom water off the upper Texas coast and its effects on the benthic biota. Contrib. Mar. Sci., 23, 53–79. Hartwig, E.O., 1976. The impact of nitrogen and phosphorus release from a siliceous sediment on the overlying water. In, Estuarine Processes, Vol. 1, edited by M. Wiley, Academic Press, New York, pp. 103–117. Hartwig, E.O., Gluth, G. & Wieser, W., 1977. Investigations on the ecophysiology of Geleia nigriceps Kahl (Ciliophora, Gymnostomata) inhabiting a sandy beach in Bermuda. Oecologia (Berlin), 31, 159–175. Hatcher, B.G., Johannes, R.E. & Robertson, A.I., 1989. Review of research relevant to the conservation of shallow tropical marine ecosystems. Oceanogr. Mar. Biol. Annu. Rev., 27, 337–414. Hayes, M.O., 1967. Relationships between coastal climate and bottom sediment type of the inner continental shelf. Mar. Geol., 5, 111–132. Hedgpeth, J.W., 1955. Bottom communities of the Gulf of Mexico. U.S. Fish Wildl. Serv. Fish. Bull., 55, 203–214. Heip, C., Vincx, M. & Vranken, G., 1985. The ecology of marine nematodes. Oceanogr. Mar. Biol Annu. Rev., 23, 399–89. Hill, M.B. & Webb, J.E., 1958. The ecology of Lagos Lagoon. II. The topography and physical features of Lagos Harbour and Lagos Lagoon. Phil. Trans. R. Soc. London, Ser. B, 241, 319–333. Hines, M.E., 1985. Microbial biogeochemistry in shallow water sediments of Bermuda. Proc. Fifth Int. Coral Reef Congr., Tahiti, 3, 427–32. Holm, R.F., 1978. The community structure of a tropical marine lagoon. Estuarine Coastal Mar. Sci., 7, 329–345. Hopner Petersen, G., 1984. Energy flow in comparable aquatic ecosystems from different climatic zones. Rapp. P.-V. Réun. Cons. Int. Explor. Mer, 183, 119–125. Hopner Petersen, G. & Curtis, M.A., 1980. Differences in energy flow through major components of subarctic, temperate and tropical marine shelf ecosystems. Dana, 1, 53–64. Hoppe, H.-G., Gocke, K., Zamorano, D. & Zimmerman, R., 1983. Degradation of macromolecular organic compounds in a tropical lagoon (Cienaga Grande, Colombia) and its ecological significance. Int. Rev. Gesamten Hydrobiol., 68, 811–824. Hopper, B.E., Fell, J.W. & Cefalu, R.C., 1973. Effect of temperature on life cycles of nematodes associated with the mangrove (Rhizophora mangle) detrital system. Mar. Biol., 23, 293–296. Hulings, N.C., 1971. A comparative study of the sand beach meiofauna of Lebanon, Tunisia, and Morocco. Thalassia Jugosl., 7, 117–122. Huston, M., 1979. A general hypothesis of species diversity. Am. Nat., 113, 81–101. Huttel, M., 1986. Active aggregation and downshore migration in the trochid snail Umbonium vestiarium (L.) on a tropical sand flat. Ophelia, 26, 221– 232.
486
DANIEL M.ALONGI
Ingole, B.S., Ansari, Z.A. & Parulekar, A.H., 1987. Meiobenthos of Saphala salt marsh, west coast of India. Indian J. Mar. Sci., 16, 110–113. Ittekkot, V., 1988. Global trends in the nature of organic matter in river suspensions. Nature (London), 332, 436–438. Jablonski, D. & Lutz, R.A., 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev., 58, 21–89. Jackson, J.B.C., 1972. The ecology of molluscs of Thalassia communities, Jamaica, West Indies. II. Molluscan population variability along an environmental stress gradient. Mar. Biol., 14, 304–337. Jackson, J.B.C., 1973. The ecology of molluscs of Thalassia communities, Jamaica, West Indies. I. Distribution, environmental physiology, and ecology of common shallow-water species. Bull. Mar. Sci., 23, 313–345. Jacob, P.G. & Qasim, S.Z., 1974. Mud of a mud bank in Kerala, southwest coast of India. Indian J. Mar. Sci., 3, 115–119. Jaramillo, E., 1987. Sandy beach macroinfauna from the Chilean coast: zonation patterns and zoogeography. Vie Milieu, 37, 165–174. Johannes, R.E., 1978. Reproductive strategies of coastal marine fishes in the tropics. Environ. Biol. Fishes, 3, 65–84. Jones, D.A., 1979. The ecology of sandy beaches in Penang, Malaysia, with special reference to Excirolana orientalis (Dana). Estuarine Coastal Mar. Sci., 9, 677–682. Jones, D.A., Price, A.R.G. & Hughs [sic], R.N., 1978. Ecology of the high saline lagoons Dawhat as Sayh, Arabian Gulf, Saudi Arabia. Estuarine Coastal Mar. Sci., 6, 253–262. Jones, R., 1982. Ecosystems, food chains and fish yields. In, Theory and Management of Tropical Fisheries, edited by D.Pauly & G.I.Murphy, ICLARM and CSIRO, Manila, pp. 195–239. Jones, R., 1984. Some observations on energy transfer through the North Sea and Georges Bank food webs. Rapp. P.-V. Réun. Cons. Int. Explor. Mer, 183, 204–217. Kapetsky, J.M., 1984. Coastal lagoon fisheries around the world: some perspectives on fishery yields, and other comparative fishery characteristics. In , Management of Coastal Lagoon Fisheries, edited by J.M.Kapetsky & G.Lasserre. Stud. Rev. GFCM/Etud. Rev. CGPM No, 61, pp. 97–139. Kapetsky, J.M., 1985. Mangroves, fisheries and aquaculture. FAO Fisheries Rep., No. 338 (Suppl.), 17–36. Karl, D.M. & Novitsky, J.A., 1988. Dynamics of microbial growth in surface layers of a coastal marine sediment ecosystem. Mar. Ecol. Prog. Ser., 50, 169–176. Kastoro, W.W., Aziz, A., Aswandy, I. & Al Hakim, I., in press. The macrobenthic community of Seribu Islands, Jakarta. In, Living Resources in Coastal Areas, edited by A.C.Alcala et al., University of Philippines Press, Manila, in press. Kemp, P.F., 1987. Potential impact on bacteria of grazing by a macrofaunal deposit-feeder, and the fate of bacterial production. Mar. Ecol. Prog. Ser., 36, 151–161. Kemp, P.F., 1988. Bacterivory by benthic ciliates: significance as a carbon source and impact on sediment bacteria. Mar. Ecol. Prog. Ser., 49, 163–169. Kenchington, R.A. & Hammond, L.S., 1978. Population structure, growth and distribution of Lingula anatina (Branchiopoda) in Queensland, Australia. J. Zool, 184, 63–81. Knox, R.A. & Anderson, D.L.T., 1985. Recent advances in the study of lowlatitude ocean circulation. Prog. Oceanogr., 14, 259–317. Kondalarao, B., 1983. Distribution of meiofauna in the Gautami-Godavari estuarine system. Mah. Bull. Natl. Inst. Oceanogr., 16, 453–457.
TROPICAL BENTHIC ECOSYSTEMS
487
Kondalarao, B. & Ramana Murty, K.V., 1988. Ecology of intertidal meiofauna of the Kakinada Bay (Gautami-Godavari estuarine system), east coast of India. Indian J. Mar. Sci., 17, 40–47. Kristensen, E., Andersen, F.O. & Kofoed, L.H., 1988. Preliminary assessment of benthic community metabolism in a southeast Asian mangrove swamp. Mar. Ecol. Prog. Ser., 48, 137–145. Kurian, C.V., 1971. Distribution of benthos on the southwest coast of India. In, Fertility of the Sea, edited by J.Costlow, Gordon & Breach, New York, pp. 225–239. Lasiak, T. & Dye, A.H., 1986. Behavioral adaptations of the mangrove whelk, Telescopium telescopium (L.) to life in a semi-terrestrial environment. J.Moll. Stud., 52, 17–179. Lee, C.C. & Fenchel, T., 1972. Studies on ciliates associated with sea ice from Antarctica. II. Temperature responses and tolerances in ciliates from Antarctic, temperate and tropical habitats. Arch. Protistenkd., 114, 237–244. Lee, II, H., 1978. Seasonality, predation and opportunism in high diversity softbottom communities in the Gulf of Panama. Ph.D. dissertation, University of North Carolina, Chapel Hill, NC., 180 pp. Leong, T.S., Leong, Y.K., Ho, S.C., Khoo, K.H., Kam, S.P., Sulaiman, H., Wong, T.M., Legore, R.S., De Ligny, W. & Tan, G.T., 1987. Effects of a crude oil terminal on tropical benthic communities in Brunei. Mar. Pollut. Bull., 18, 31–35. Lewis, J.B., 1963. Environmental and tissue temperatures of some tropical intertidal marine animals. Biol. Bull. (Woods Hole, Mass.), 124, 277–284. Lewis, J.B., 1965. A preliminary description of some marine benthic communities from Barbados, West Indies. Can. J. Zool, 43, 1049–1074. Lewis, J.B., 1971. Comparative respiration of some tropical intertidal gastropods. J. Exp. Mar. Biol. Ecol, 6, 101–108. Lok Tan, T. & Ruger, H.-J., 1989. Benthic studies of the Northwest African upwelling region—bacterial standing stock and ETS-activity, ATP biomass and adenylate energy charge. Mar. Ecol. Prog. Ser., 51, 167–176. Longhurst, A.R., 1957a. An Ecological Survey of the West African Marine Benthos. No. 11, Colonial Office, Fishery Publ., London, 102 pp. Longhurst, A.R., 1957b. The food of the demersal fish of a West African estuary. J. Anim. Ecol., 26, 369–387. Longhurst, A.R., 1959. Benthos densities off tropical West Africa. J. Cons., Cons. Int. Explor. Mer, 25, 21–28. Longhurst, A.R., 1960. A summary of the food of West African demersal fish. Bull. Inst. Fr. Afr. Noire, Ser. A, 22, 276–282. Longhurst, A.R., 1965a. The fish resources of the eastern Gulf of Guinea. J. Cons., Cons. Int. Explor. Mer, 29, 302–334. Longhurst, A.R., 1965b. The biology of west African polynemid fishes. J. Cons., Cons. Int. Explor. Mer, 30, 58–74. Longhurst, A.R., 1983. Benthic-pelagic coupling and export of organic carbon from a tropical Atlantic continental shelf—Sierra Leone. Estuarine Coastal Shelf Sci., 17, 261–285. Longhurst, A.R. & Pauly, D., 1987. Ecology of Tropical Oceans. Academic Press, New York, 407 pp. Lowe-McConnell, R.H., 1962. The fishes of the British Guiana continental shelf, Atlantic coast of South America, with notes on their natural history. J. Linn. Soc. London Zool, 44, 669–700. Lowe-McConnell, R.H., 1987. Ecological Studies in Tropical Fish Communities. Cambridge University Press, Cambridge, 382 pp. Machado, E.C. & Knoppers, B.A., 1988. Sediment oxygen consumption in an organic-rich, subtropical lagoon, Brazil. Sci. Total Environ., 75, 341–349.
488
DANIEL M.ALONGI
MacNae, W. & Kalk, M., 1962. The fauna and flora of sandflats at Inhaca Island, Mozambique. J. Anim. Ecol., 31, 93–128. Makarov, Y.N. & Averin, B.S., 1968. Quantitative distribution of zoobenthos in the shelf waters of the Mozambique Channel. Oceanology, 8, 845–848. Marten, G.G. & Polovina, J.J., 1982. A comparative study of fish yields from various tropical ecosystems. In, Theory and Management of Tropical Fisheries, edited by D.Pauly & G.I.Murphy, ICLARM and CSIRO, Manila, pp. 255–289. Mathew, R. & Menon, N.R., 1983. Oxygen consumption in tropical bivalves Perna viridis (Linn.) and Meretrix costa (Chem.) exposed to heavy metals. Indian J. Mar. Sci., 12, 57–59. Maurer, D. & Vargas, J.A., 1984. Diversity of soft-bottom benthos in a tropical estuary: Gulf of Nicoya, Costa Rica. Mar. Biol., 81, 97–106. Maurer, D., Vargas, J.A. & Dean, H., 1988. Polychaetous annelids from the Gulf of Nicoya, Costa Rica. Int. Rev. Gesamten Hydrobiol., 73, 43–59. Mayer, A.G., 1914. The effect of temperature upon tropical marine animals. Pap. Tortugas Lab., Carnegie Inst. Washington, 6, 1–24. Mclntyre, A.D., 1968. The meiofauna and macrofauna of some tropical beaches. J. Zool, 156, 377–392. McLachlan, A., 1985. The ecology of two sandy beaches near Walvis Bay. Madoqua, 14, 155–163. McLusky, D.S. & McIntyre, A.D., 1988. Characteristics of the benthic fauna. In, Continental Shelves. Ecosystems of the World 27, edited by H.Postma & J.J. Zijlstra, Elsevier, Amsterdam, pp. 131–154. McLusky, D.S., Nair, S.A., Stirling, A. & Bhargava, R., 1975. The ecology of a central west Indian beach, with particular reference to Donax incarnatus. Mar. Biol., 30, 267–276. McLusky, D. & Stirling, A., 1975. The oxygen consumption and feeding of Donax incarnatus and Donax spiculum from tropical beaches. Comp. Biochem. Physiol., 51A, 943–947. McNulty, J.K., 1961. Ecological effects of sewage pollution in Biscayne Bay, Florida: sediments and the distribution of benthic and fouling macroorganisms. Bull. Mar. Sci., 11, 395–47. McNulty, J.K., Work, R.C. & Moore, H.B., 1962a. Level sea bottom communities in Biscayne Bay and neighbouring areas. Bull. Mar. Sci., 12, 204–233. McNulty, J.K., Work, R.C. & Moore, H.B., 1962b. Some relationships between the infauna of the level bottom and the sediment in South Florida. Bull. Mar. Sci., 12, 322–332. Menasveta, D. & Hongskul, V., 1988. The Gulf of Thailand. In, Ecosystems of the World 27, Continental Shelves, edited by H.Postma & J.J.Zijlstra, Elsevier, Amsterdam, pp. 363–383. Menzies, R.J., George, R.Y. & Rowe, G.T., 1973. Abyssal Environment and Ecology of the World Oceans. Wiley-Interscience, New York, 488 pp. Milliman, J.D. & Meade, R.H., 1983. World-wide delivery of river sediment to the oceans. J. Geol, 91, 1–21. Moore, H.B., 1972a. Aspects of stress in the tropical marine environment. Adv. Mar. Biol., 10, 217–269. Moore, H.B., 1972b. An estimate of carbonate production by macrobenthos in some tropical soft-bottom communities. Mar. Biol., 17, 145–148. Moore, H.B., Davies, L.T., Eraser, T.H., Gore, R.H. & Lopez, N.R., 1968. Some biomass figures from a tidal flat in Biscayne Bay, Florida. Bull. Mar. Sci., 18, 261–279. Moriarty, D.J.W., 1983. Bacterial biomass and productivity in sediments, stromatolites and waters of Hamelin Pool, Shark Bay, Western Australia. Geomicrobiol. J., 3, 121–133.
TROPICAL BENTHIC ECOSYSTEMS
489
Moriarty, D.J.W., 1986. Bacterial productivity in ponds used for culture of penaeid prawns. Microb. Ecol, 12, 259–269. Moriarty, D.J.W., Boon, P.I., Hansen, J.A., Hunt, W.G., Poiner, I.R., Pollard, P.C., Skyring, G.W. & White, D.C., 1985. Microbial biomass and productivity in seagrass beds. Geomicrobiol. J., 4, 21–51. Moriarty, D.J.W., Iverson, R.L. & Pollard, P.C., 1986. Exudation of organic carbon by the seagrass Halodule wrightii (Aschers) and its effect on bacterial growth in the sediment. J. Exp. Mar. Biol Ecol., 96, 115–126. Moriarty, D.J.W. & Pollard, P.C., 1982. Diel variation of bacterial productivity in seagrass (Zostera capricorni) beds measured by rate of thymidine incorporation into DNA. Mar. Biol, 72, 165–173. Munro, A.L.S., Wells, J.B.J. & McIntyre, A.D., 1978. Energy flow in the flora and meiofauna of sandy beaches. Proc. R. Soc. Edinburgh Sect. B, 76, 297– 315. Murphy, G.I., 1982. Recruitment of tropical fishes. In, Theory and Management of Tropical Fisheries, edited by D.Pauly & G.I.Murphy, ICLARM and CSIRO, Manila, pp. 141–148. Nair, P.V.R, & Pillai, V.K., 1983. Productivity of the Indian Seas. J. Mar. Biol. Assoc. India, 25, 41–50. Nair, S. & Loka Bharathi, P.A., 1980. Heterotrophic bacterial populations in tropical sandy beaches. Mah. Bull. Natl. Inst. Oceanogr., 13, 261–267. Nandi, S. & Choudhury, A., 1983. Quantitative studies on the benthic macrofauna of Sagan Island, intertidal zones, Sunderbans, India. Mah. Bull. Natl. Inst. Oceanogr., 16, 409–14. Natividad, M.R., 1979. Fluctuations in the population density of a meiofauna community on a tropical sandy beach. Philipp. Sci., 16, 119–123. Newell, N.D., Imbrie, J., Purdy, E.G. & Thurber, D.L., 1959. Organism communities and bottom facies, Great Bahama Bank. Bull. Am. Mus. Nat. Hist., 117, 183–228. Neyman, A.A., 1969. Some data on the benthos of the shelves in the northern part of the Indian Ocean. Oceanology, 9, 861–866. Neyman, A.A. & Kondritskiy, A.V., 1974. Quantitative distribution of benthos in the Persian Gulf and in the shallow coastal waters of the southern part of the Red Sea. Oceanology, 14, 291–293. Neyma, A.A., Sokolova, M.N., Vinogradova, N.G. & Pasternak, F.A., 1971. Some patterns of the distribution of bottom fauna in the Indian Ocean. In, The Biology of the Indian Ocean, edited by B.Zeitzschel, Springer-Verlag, Berlin, pp. 467–544. Nichols, J.A., 1976. The effect of stable dissolved oxygen stress on marine benthic invertebrate community diversity. Int. Rev. Gesamten Hydrobiol., 61, 747–760. Nichols, J.A. & Rowe, G.T., 1977. Infaunal macrobenthos off Cap Blanc, Spanish Sahara. J. Mar. Res., 35, 525–536. Nichols-Driscoll, J.A., 1976. Benthic invertebrate communities in Golfo Dulce, Costa Rica, an anoxic basin. Rev. Biol. Trop., 24, 281–297. Nieuwolt, S., 1977. Tropical Climatology. J.Wiley & Sons, London, 207 pp. Odum, W.E., 1970. Utilization of the direct grazing and plant detritus food chains by the striped mullet Mugil cephalus. In, Marine Food Chains, edited by J.H. Steele, Oliver & Boyd, Edinburgh, pp. 222–240. Ong Che, R.G. & Gomez, E.D., 1985. Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Mar. Biol., 2, 21– 30. Parulekar, A.H., 1984. Studies on growth and age of bivalves from temperate and tropical estuarine ecosystems. Indian J. Mar. Sci., 13, 193–195.
490
DANIEL M.ALONGI
Parulekar, A.H. & Ansari, Z.A., 1981a. Benthic macrofauna of the Andaman Sea. Indian J. Mar. Sci., 10, 280–284. Parulekar, A.H. & Ansari, Z.A., 1981b. Bottom fauna of the Malacca Strait. Mah. Bull. Natl. Inst. Oceanogr., 14, 155–158. Parulekar, A.H., Dhargalkar, V.K. & Singbal, S.Y.S., 1980. Benthic studies in Goa estuaries. Part III. Annual cycle of macrofaunal distribution, production and trophic relations. Indian J. Mar. Sci., 9, 189–200. Parulekar, A.H. & Dwivedi, S.N., 1974. Benthic studies in Goa estuaries. Part I. Standing crop and faunal composition in relation to bottom salinity distribution and substratum characteristics in the estuary of Mandovi River. Indian J. Mar. Sci., 3, 41–45. Parulekar, A.H., Harkantra, S.N. & Ansari, Z.A., 1982. Benthic production and assessment of demersal fishery resources of the Indian Seas. Indian J. Mar. Sci., 11, 107–114. Parulekar, A.H. & Wagh, A.B., 1975. Quantitative studies on benthic macrofauna of Northeastern Arabian Sea shelf. Indian J. Mar. Sci., 4, 174– 176. Patnaik, S., 1971. Seasonal abundance and distribution of bottom fauna of the Chilka Lake. J. Mar. Biol. Assoc. India, 13, 106–125. Pauly, D., 1975. On the ecology of a small west African lagoon. Ber. Dtsch. Wiss. Komm. Meeresforsch., 24, 46–62. Pauly, D., 1976. The biology, fishery and potential for aquaculture of Tilapia melanotheron in a small west African lagoon. Aquaculture, 7, 33–49. Pauly, D., 1979. Theory and management of tropical multispecies stocks: A review, with emphasis on the southeast Asian demersal fisheries. ICLARM Stud. Rev., 1, 1–35. Pearse, J.S. & Barksdale, M.J., 1986. Temporal patterns of reproduction by shallow-water invertebrates in the Indian Ocean. In, Indian Ocean. Biology of Benthic Marine Organisms, edited by M.-F.Thompson et al., A.A.Balkema, Rotterdam, pp. 13–18. Pearson, T.H. & Rosenberg, R., 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Annu. Rev., 16, 229–311. Philander, S.G., 1985. Tropical oceanography. Adv. Geophys., 28A, 461–77. Picard, J., 1967. Essai de classement des grands types de peuplements marins benthiques tropicaux d’après les observations effectivées dans les parages de Tulear (S.W.Madagascar). Recl. Trav. Stn. Mar. Endoume, Fasc. Hors. Ser. Suppl., 6, 3–24. Pichon, M., 1967. Contribution à l’étude des peuplements de la zone intertidale sur sables fins et sables vaseux non fixés dans la region de Tuléar. Recl. Trav. Stn. Mar. Endoume, Fasc. Hors. Ser., Suppl, 7, 57–100. Plante-Cuny, M.-R., 1977. Pigments photosynthétiques et production primaire du microphytobenthoc d’une lagune tropicale, La Lagune Ébrié (Abidjan, Côte d’Ivoire). Cah. ORSTOM, Sér. Océanogr., 15, 3–25. Plante-Cuny, M.-R., 1978. Pigments photosynthetiques et production primaire des fonds meubles neritiques d’une region tropicale (Nosy-Be, Madagascar). Trav. Doc. ORSTOM No. 96, 359 pp. Pomeroy, L.R., 1960. Primary productivity of Boca Ciega Bay, Florida. Bull. Mar. Sci. Gulf Caribb., 10, 1–10. Por, F.D. & Dor, I, 1975. Ecology of the metahaline pool of Di Zahav, Gulf of Elat, with notes on the Siphocladacea and typology of the nearshore marine pools. Mar. Biol., 29, 37–44. Prabhu, V. & Reddy, M.P.M., 1987. Macrobenthos and sediment distribution in relation to demersal fish catches off Baikampady-Suratkal, South Kanara coast. Indian J. Mar. Sci., 16, 60–64.
TROPICAL BENTHIC ECOSYSTEMS
491
Premuzic, E.T., Benkovitz, C.M., Gaffney, J.S. & Walsh, J.J., 1982. The nature and distribution of organic matter in the surface sediments of world oceans and seas. Org. Geochem., 4, 63–77. Probert, P.K., 1986. Energy transfer through the shelf benthos off the west coast of South Island, New Zealand. N.Z.J. Mar. Freshwater Res., 20, 407–417. Qasim, S.Z., 1979. Primary production in some tropical environments. In, Marine Production Mechanisms, edited by M.J.Dunbar, Cambridge University Press, Cambridge, pp. 31–69. Ramachandra, U., Gupta, T.R.C. & Katti, R.J., 1984. Macrobenthos and sediment characteristics of Mulki estuary, west coast of India. Indian J. Mar. Sci., 13, 109–112. Raman, A.V. & Ganapati, P.N., 1983. Pollution effects on ecobiology of benthic polychaetes in Visakhapatnam Harbour (Bay of Bengal). Mar. Pollut. Bull., 14, 46–52. Rao, G. & Ganapati, P., 1968. The interstitial fauna inhabiting the beach sands of Waltair coast. Proc. Natl. Inst. Sci. India, Part B, 34, 82–125. Rao, G.C., 1980. On the zoogeography of the interstitial meiofauna of the Andaman and Nicobar Islands, Indian Ocean. Rec. Zool. Surv. India, 77, 153– 178. Reeburg, W.S., 1983. Rates of biogeochemical processes in anoxic sediments. Annu. Rev. Earth Planet. Sci., 11, 269–298. Reise, K., 1985. Tidal Flat Ecology. Springer-Verlag, Berlin, 191 pp. Rhoads, D.C., Boesch, D.F., Zhican, T., Fengshan, X., Liqiang, H. & Nilsen, K.J., 1985. Macrobenthos and sedimentary facies on the Changjiang delta platform and adjacent continental shelf, East China Sea. Cont. Shelf Res., 4, 189–213. Ridd, P., Sandstrom, M.W. & Wolanski, E., 1988. Outwelling from tropical tidal salt flats. Estuarine Coastal Shelf Sci., 26, 243–253. Riddle, M.J., 1988. Patterns in the distribution of macrofaunal communities in coral reef sediments on the central Great Barrier Reef. Mar. Ecol. Prog. Ser., 47, 281–292. Robertson, J. & Dredge, M., 1986. Redspot king prawn research off central Queensland. Aust. Fish., 45, 18–20. Rodrigues, C.L., Harkantra, S.N. & Parulekar, A.H., 1982. Sublittoral meiobenthos of the northeastern Bay of Bengal. Indian J. Mar. Sci., 11, 239– 242. Rodriguez, G., 1959. The marine communities of Margarita Island, Venezuela. Bull. Mar. Sci. Gulf Caribb., 9, 237–280. Romankevich, E.A., 1984. Geochemistry of Organic Matter in the Ocean. Springer-Verlag, Berlin, 334 pp. Rosenberg, R., 1974. Stressed tropical benthic faunal communities of Miami, Florida. Ophelia, 14, 93–112. Rosenberg, R., Arntz, W.E., Chuman de Flores, E., Flores, L.A., Carbajal, G., Finger, I. & Tarazona, J., 1983. Benthos biomass and oxygen deficiency in the upwelling system off Peru. J. Mar. Res., 41, 263–279. Rowe, G.T., 1971a. Benthic biomass in the Pisco, Peru upwelling. Invest. Pesq., 35, 127–135. Rowe, G.T., 1971b. Benthic biomass and surface productivity. In, Fertility of the Sea, edited by J.Costlow, Gordon & Breach, New York, pp. 441–54. Rowe, G.T., 1981. The benthic processes of coastal upwelling ecosystems. In, Coastal Upwelling, edited by F.A.Richards, Am. Geophys. Union, Washington, D.C., pp. 464–471. Salzen, E.A., 1957. A trawling survey off the Gold coast. J. Cons., Cons. Int. Explor. Mer, 23, 72–82. Sanders, H.L., 1968. Marine benthic diversity: a comparative study. Am. Nat., 102, 243–282.
492
DANIEL M.ALONGI
Sanders, H.L., 1969. Benthic marine diversity and the stability-time hypothesis. Brookhaven Symp. Biol., 22, 71–81. Sankaranarayanan, V.N. & Panampunnayil, S.U., 1979. Studies on organic carbon, nitrogen and phosphorus in sediments of the Cochin backwater. Indian J. Mar. Sci., 8, 27–30. Savich, M.S., 1971. Quantitative distribution and food value of benthos from the West Pakistan shelf. Oceanology, 10, 113–119. Scholander, P.F., Flagg, W., Walters, V. & Irving, L., 1953. Climatic adaptation in Arctic and tropical poikilotherms. Physiol. Zool., 26, 67–92. Schwinghamer, P., Hargrave, B., Peer, D. & Hawkins, C.M., 1986. Partitioning of production and respiration among size groups of organisms in an intertidal benthic community. Mar. Ecol. Prog. Ser., 31, 131–142. Sellwood, B.W., 1986. Shallow-marine carbonate environments. In, Sedimentary Environments and Fades, edited by H.G.Reading, Blackwell Scientific Publishers, Oxford, pp. 283–342. Seshappa, G., 1953. Observations on the physical and biological features of an inshore sea bottom along the Malabar coast. Proc. Natl. Inst. Sci. India, 19, 257–279. Sharp, G.D., 1988. Fish populations and fisheries, their perturbations, natural and man-induced. In, Ecosystems of the World 27, Continental Shelves, edited by H. Postma & J.J.Zijlstra, Elsevier, Amsterdam, pp. 155–202. Shelton, C.R. & Robertson, P.B., 1981. Community structure of intertidal macrofauna on two surf-exposed Texas sandy beaches. Bull. Mar. Sci., 31, 833–842. Shin, P.K.S., 1987. Infaunal macrobenthos of beach sediments in Hong Kong. Asian Mar. Biol., 4, 141–146. Shin, P.K.S. & Thompson, G.B., 1982. Spatial distribution of the infaunal benthos of Hong Kong. Mar. Ecol. Prog. Ser., 10, 37–47. Sivakumar, V., Thangaraj, G.S., Chandran, R. & Ramamoorthi, K., 1983. Seasonal variations in carbon, nitrogen and phosphorus in sediment off the Vellar estuary. Porto Novo. Mah. Bull. Natl. Inst. Oceanogr., 16, 175–181. Siva Rama Sarma, N. & Chandra Mohan, P., 1981. On the ecology of the interstitial fauna inhabiting the Bhimilipatnam coast (Bay of Bengal). Mah. Bull. Natl. Inst. Oceanogr., 14, 257–263. Smith, K.L., Rowe, G.T. & Clifford, H., 1974. Sediment oxygen demand in an outwelling and upwelling area. Téthys, 6, 223–229. Sparck, R., 1951. Density of bottom animals in the ocean floor. Nature (London), 168, 112–113. Spight, T.M., 1977. Diversity of shallow-water gastropod communities on temperate and tropical beaches. Am. Nat., 111, 1077–1097. Spight, T.M., 1981. Latitude and prosobranch larvae: whose veligers are found in tropical waters? Ecosynthesis, 1, 29–52. Sreeramamoorty, R. & Rama Sarma, D.V., 1986. Distribution and abundance of benthic macrofauna in the Gosthani and Champavathi River estuaries of AndhraPradesh, India. In, Indian Ocean. Biology of Benthic Marine Organisms, edited by M.-F.Thompson et al., A.A.Balkema, Rotterdam, pp. 257–272. Srinivasa Rao, D. & Rama Sarma, D.V., 1983. Abundance and distribution of intertidal polychaetes in the Vasishta-Godavari estuary. Mah. Bull. Natl. Inst. Oceanogr., 16, 327–340. Stanley, S.O., Boto, K.G., Alongi, D.M. & Gillan, F.T., 1987. Composition and bacterial utilization of free amino acids in tropical mangrove sediments. Mar. Chem., 22, 13–30. Steele, D.H., 1988. Latitudinal variations in body size and species diversity in marine decapod crustaceans of the continental shelf. Int. Rev. Gesamten Hydrobiol., 73, 235–246.
TROPICAL BENTHIC ECOSYSTEMS
493
Steele, J.H., 1976. Comparative studies of beaches. Phil Trans. R. Soc. London, Ser. B, 274, 401–415. Stephenson, W., Cook, S.D. & Raphael, Y.I., 1977. The effect of a major flood on the macrobenthos of Bramble Bay, Queensland. Mem. Queensl. Mus., 18, 95– 119. Stephenson, W. & Williams, W.T., 1971. A study of the benthos of soft bottoms, Sek Harbour, New Guinea, using numerical analysis. Aust. J. Mar. Freshwater Res., 22, 11–34. Stephenson, W., Williams, W.T. & Cook, S.D., 1972. Computer analyses of Petersen’s original data on bottom communities. Ecol. Monogr., 42, 387–409. Stirling, A., 1975. A comparison of some problems related to tropical and temperate sandy beaches. Bull. Dept. Mar. Sci. Univ. Cochin, 7, 845–849. Stoner, A.W., 1986. Community structure of the demersal fish species of Laguna Joyuda, Puerto Rico, Estuaries, 9, 142–152. Subramoniam, T. & Panneerselvam, M., 1985. Semi-annual breeding pattern in the burrowing sand crab Albunea symmysta (L.) (=symnista) of Madras coast. Indian J. Mar. Sci., 14, 226–227. Swennen, C, Duiven, P. & Spaans, A.L., 1982. Numerical density and biomass of macrobenthic animals living in the intertidal zone of Surinam, South America. Neth. J. Sea. Res., 15, 406–418. Talikhedkar, P.M. & Mane, U.H., 1976. Salinity tolerance survival, behavior and weight changes of the wedge clam, Donax cuneatus. J. Mar. Biol. Assoc. India, 18, 476–487. Tarazona, J., 1984. Modificaciones de la infauna bentonica de una bahia con deficiencia de oxygeno durante “El Niño” 1982–1983. Rev. Comm. Perm. Pacifico Surv., 15, 223–238. Tarazona, J., Salzwedel, H. & Arntz, W., 1988a. Positive effects of “El Niño” on macrozoobenthos inhabiting hypoxic areas of the Peruvian upwelling system. Oecologia (Berlin), 76, 184–190. Tarazona, J., Salzwedel, H. & Arntz, W., 1988b. Oscillations of macrobenthos in shallow waters of the Peruvian central coast induced by El Niño 1982–83. J. Mar. Res., 46, 593–611. Tarr, J.G., Griffiths, C.L. & Bally, R., 1985. The ecology of three sandy beaches on the Skeleton coast of South West Africa. Madoqua, 14, 295–304. Taylor, J.D., 1968. Coral reefs and associated invertebrate communities (mainly molluscs) around Mahe, Seychelles. Phil. Trans. R. Soc., London, Ser. B, 254, 129–206. Tenore, K.R. & Coull, B.C., 1980. Editors, Marine Benthic Dynamics. University of South Carolina, Columbia, SC. 451 pp. Thiel, H., 1978. Benthos in upwelling regions. In, Upwelling Ecosystems, edited by R. Boje & M.Tomczak, Springer-Verlag, Berlin, pp. 124–138. Thiel, H., 1982. Zoobenthos of the CINECA area and other upwelling regions. Rapp. P.-V. Réun. Cons. Int. Explor. Mer, 180, 323–334. Thompson, G.B. & Shin, P.K.S., 1983. Sewage pollution and the infaunal benthos of Victoria Harbour, Hong Kong. J. Exp. Mar. Biol. Ecol., 67, 279–299. Thorson, G., 1950. Reproductive and larval ecology of marine bottom invertebrates. Biol. Rev., 25, 1–45. Thorson, G., 1957. Bottom communities (sublittoral or shallow shelf). In, Treatise on Marine Ecology and Paleoecology, Vol. 1, Ecology, edited by J.W.Hedgpeth, Geol. Soc. Am. Mem. 67, pp. 461–535. Tiews, K., Divino, P., Ronquillo, I.A. & Marques, J., 1972. On the food and feeding of eight species of Leiognathus found in Manila Bay and San Miguel Bay. Proc. Indo-Pac. Fish Counc., 13, 93–99. Trevallion, A., Ansell, A.D., Sivadas, P. & Narayanan, B., 1970. A preliminary account of two sandy beaches in South West India. Mar. Biol., 6, 268–279.
494
DANIEL M.ALONGI
Trueman, E.R., 1971. The control of burrowing and the migratory behaviour of Donax denticulatus (Bivalvia: Tellinacea). J. Zool., 165, 453–69. Tseythin, V.B., 1987. Detritus flux to the ocean bed and benthic biomass. Oceanology, 27, 98–101. Ullman, W.J. & Sandstrom, M.W., 1987. Dissolved nutrient fluxes from the nearshore sediments of Bowling Green Bay, central Great Barrier Reef Lagoon (Australia). Estuarine Coastal Shelf Sci., 24, 289–303. UNESCO, 1979. Discharge of selected rivers of the world, mean monthly and extreme discharges (1972–1975). Stud. Rep. Hydrol., 5, 3, 104 pp. UNESCO, 1981. The coastal ecosystems of West Africa: coastal lagoons, estuaries and mangroves. UNESCO Rep. Mar. Sci., No. 17, 60 pp. Ursin, E., 1984. The tropical, the temperate and the Arctic seas as media for fish production. Dana, 3, 43–60. Valentine, J.W., 1971. Plate tectonics and shallow marine diversity and endemism, an actualistic model. Syst. Zool., 20, 253–264. Varadarajan, S. & Subramoniam, T., 1982. Reproduction of the continuously breeding tropical hermit crab, Clibanarus clibanaris. Mar. Ecol. Prog. Ser., 8, 197–201. Vargas, J.A., 1988. Community structure of macrobenthos and the results of macropredator exclusion on a tropical mud flat. Rev. Biol. Trop., 36, 287–308. Varshney, P.K., Govindan, K. & Desai, B.N., 1984. Benthos of the Naramda estuary. Mah. Bull. Natl. Inst. Oceanogr., 14, 141–148. Varshney, P.K., Govindan, K., Gaikwad, U.D. & Desai, B.N., 1988. Macrobenthos off Versova (Bombay), west coast of India, in relation to environmental conditions. Indian J. Mar. Sci., 17, 222–227. Vermeij, G.J., 1978. Biogeography and Adaptation. Patterns of Marine Life. Harvard University Press, Cambridge, MA, 337 pp. Vicente, H.J., 1979. Monthly fluctuations in the population density and vertical distribution of an intertidal meiofauna community in a tropical muddy substrate. Philipp. Sci., 16, 118–119. Virnstein, R.W., Nelson, W.G., Lewis, F.G. & Howard, R.K., 1984. Latitudinal patterns in seagrass epifauna: do patterns exist, and can they be explained? Estuaries, 7, 310–330. Vohra, F.C., 1971. Zonation of a tropical sandy shore. J. Anim. Ecol., 40, 679– 705. Vohra, F.C., 1972. Preliminary observations on population fluctuations and breeding on a tropical sandy shore. Malays. J. Sci., 1A, 71–92. Wade, B.A., 1967. Studies on the biology of the west Indian beach clam, Donax denticulatus Linne. 1. Ecology. Bull. Mar. Sci., 17, 149–174. Wade, B.A., 1968. Studies on the biology of the west Indian beach clam, Donax denticulatus (Linne). 2. Life history. Bull. Mar. Sci., 18, 877–899. Wade, B.A., 1972a. A description of a highly diverse soft-bottom community in Kingston Harbour, Jamaica. Mar. Biol., 13, 57–69. Wade, B.A., 1972b. Benthic diversity in a tropical estuary. Mem. Geol. Soc. Am., No. 133, 499–515. Wallace, J.H., 1975. The estuarine fishes of the east coast of South Africa. IV. Occurrence of juveniles in estuaries. S. Afr. Assoc. Mar. Biol. Res. Ocean. Res. Inst. Invest. Rep., 42, 3–18. Walsh, J.J., 1983. Death in the sea: enigmatic phytoplankton losses. Prog. Oceanogr., 12, 1–86. Walter, H., 1979. Vegetation of the Earth in Relation to Climate and Ecophysiology. Springer-Verlag, New York, 240 pp. Wantland, K.F. & Pusey III, W. C, 1975. Editors, Belize Shelf-Carbonate Sediments, Clastic Sediment, and Ecology. Am. Assoc. Petrol. Geol., Tulsa, OK, 599 pp.
TROPICAL BENTHIC ECOSYSTEMS
495
Warburton, K., 1978. Community structure, abundance and diversity of fish in a Mexican coastal lagoon system. Estuarine Coastal Mar. Sci., 7, 497–519. Warwick, R.M. & Ruswahyuni, 1987. Comparative study of the structure of some tropical and temperate marine soft-bottom macrobenthic communities. Mar. Biol, 95, 641–649. Wassenberg, T.J. & Hill, B.J., 1987. Natural diet of the tiger prawns Penaeus esculentus and P. semisulcatus. Aust. J. Mar. Freshwater Res., 38, 169–182. Webb, J.E., 1956a. On the populations of Branchiostoma lanceolatum and their relations with the West African lancelets. Proc. Zool. Soc. Lond., 127, 125– 140. Webb, J.E., 1956b. The effects of salinity and different sands on the distribution of a tropical Amphioxus. Proc. Zool. Soc. London, 126, 160–161. Webb, J.E., 1958a. The ecology of Lagos Lagoon I. The lagoons of the Guinea coast. Phil. Trans. R. Soc. London, Ser. B, 241, 307–318. Webb, J.E., 1958b. Ecology of Lagos Lagoon. V. Some properties of lagoon deposits. Phil. Trans. R. Soc. London, Ser. B, 241, 393–419. Webb, J.E., 1958c. The ecology of Lagos Lagoon III. The life history of Branchiostoma nigeriense (Webb). Phil. Trans. R. Soc. London, Ser. B, 241, 335–353. Wells, J.T. & Coleman, J.M., 1981. Physical processes and fine-grained sediment dynamics, coast of Surinam, South America. J. Sediment. Petrol., 51, 1053– 1068. Wieser, W., 1975. The meiofauna as a tool in the study of habitat heterogeneity— ecophysiological aspects. A review. Cah. Biol. Mar., 16, 647–670. Wieser, W. & Schiemer, F., 1977. The ecophysiology of some marine nematodes from Bermuda: seasonal aspects. J. Exp. Mar. Biol. Ecol., 26, 97–106. Williams, D. McB., Dixon, P. & English, S., 1988. Cross-shelf distribution of copepods and fish larvae across the central Great Barrier Reef. Mar. Biol., 99, 577–589. Williams, S.L., Gill, I.P. & Yarish, S.M., 1985. Nitrogen cycling in backreef sediments (St. Croix, U.S. Virgin Islands). Proc. Fifth Int. Coral Reef Congr., 3, 389–394. Wolanski, E., 1986. An evaporation-driven salinity maximum zone in Australian tropical estuaries. Estuarine Coastal Shelf Sci., 22, 415–424. Wolanski, E., Chappell, J., Ridd, P. & Vertessy, R., 1988. Fluidization of mud in estuaries. J. Geophys. Res., 93, 2351–2361. Wolanski, E. & Ridd, P., 1986. Tidal mixing and trapping in mangrove swamps. Estuarine Coastal Shelf Sci., 23, 759–771. Wolcott, T.G., 1978. Ecological role of ghost crabs, Ocypode quadrata (Fabricius) on an ocean beach: scavengers or predators? J. Exp. Mar. Biol. Ecol., 31, 67– 82. Wolff, W.J., 1983. Estuarine benthos. In, Ecosystems of the World 26, Estuaries and Enclosed Seas, edited by B.H. Ketchum, Elsevier Science Publishers, Amsterdam, pp. 151–182. Wu, R.S. S. & Richards, J., 1981. Variations in benthic community structure in a subtropical estuary. Mar. Biol., 64, 191–198. Wyrtki, K., 1964. Upwelling in the Costa Rica Dome. U.S. Fish Wildl. Serv. Fish. Bull, 63, 355–372. Yanez-Arancibia, A., Amezcua Linares, F. & Day, J.W., 1980. Fish community structure and function in Terminos Lagoon, a tropical estuary in the southern Gulf of Mexico. In, Estuarine Perspectives, edited by V.S. Kennedy, Academic Press, New York, pp. 465–82. Yingst, J.Y. & Rhoads, D. C, 1985. The structure of soft-bottom benthic communities in the vicinity of the Texas Flower Garden Banks, Gulf of Mexico. Estuarine Coastal Shelf Sci., 20, 569–592.
496
DANIEL M.ALONGI
Young, D.K. & Young, M.W., 1982. Macrobenthic invertebrates in bare sand and seagrass (Thalassia testudinium) at Carrie Bow Cay, Belize. In, The Atlantic Barrier Reef Ecosystem at Carrie Bow Bay, Belize, I. Structure and Communities, edited K.Rutzler & I.G.Macintyre, Smithsonian Institution Press, Washington, D.C., pp. 115–126.
AUTHOR INDEX References to complete articles are given in heavy type; references to pages are given in normal type; references to bibliographical lists are given in italics.
Aardema, B.W. 116; 132 Aaronson, W. See Silver, R.P., 96; 150 Abdul Azis, P.K., 423, 424; 479 See Balakrishnan Nair, N., 481 Abe, M., 90; 132 Abston, A. See Timoney, J.F., 300, 301, 302; 350 Abu Hilal, A.H. See Grelet, Y., 485 Achuthankutty, C.T., 395, 396, 402, 403, 450, 456, 457; 479 Acres, S.D. See Chan, R., 106; 135 Acton, R.T. 324; 330 Adams, W.N. See Andrews, W.H., 331 Adelberg, E.A. See Stanier, R.Y., 87; 150 Adey, W.H. See Brawley, S.H., 250; 256 Agegian, C.R. See Cowen, R., 250; 259 Aguilar, C. See Richardson, L.L., 114; 148 Aida, K. See Tago, Y., 89, 102, 111; 151 Akin, D.E., 114; 132 Akioka, H. See Masaki, T., 251; 267 See Noro, T., 246; 269 Al Hakim, I. See Aswandy, I., 435; 481 See Kastoro, W.W., 435; 487 Aladro Lubel, M.A., 395; 479 Alamo, R.M. See Perkins, F.O., 347 Alayse, A.M. See Fiala-Médioni, A., 292; 337 Albright, L.J., 121; 133 See Sibbald, M.J., 87; 150 Al Jebouri, M.M., 300, 302, 310, 315, 317; 330, 331 Allan, G.G., 99, 105; 133 Alldredge, A.L., 76, 111, 114; 133 See Silver, M.W., 110; 150 Allen, E.C. See ZoBell, C.E., 113; 153 Allen, W.W. See Trytek, R.E., 291; 351 Aller, J.Y., 392, 429, 430, 436, 438, 440, 473; 479 Aller, R.C. See Aller, J.Y., 392, 429, 430, 436, 438, 440, 473; 479 Allison, D.G. See Gilbert, P., 139 Allsopp, A., 208; 256 Alongi, D.M., 381–496; 381, 390, 391, 392, 393, 395, 399, 401, 402, 403, 404, 405, 406, 407, 409, 413, 426, 429, 430, 438, 439, 440, 441, 453, 454, 456, 457, 458, 459, 460, 461, 462, 463, 464, 465, 473, 474, 476; 479, 480 See Boto, K.G., 464; 481 See Hansen, J.A., 399; 485 See Stanley, S.O., 462; 493
Al Salihi, S.B.S. See Trollope, D.R., 299, 303, 317; 350 Alvarez, M., 325, 326; 331 See Friedl, F., 323; 338 Alvarez-Borrego, S. See Camacho-Ibar, V.F., 392; 482 Amezcua Linares, F. See Yanez-Arancibia, A., 422; 496 Ammerman, J.W. See Fuhrman, J.A., 285; 338 Amos, H.E. See Akin, D.E., 114; 132 Amouroux, J.M., 282, 283; 331 Amsler, C.D., 215, 226, 228; 256 Andersen, F.O. See Kristensen, E., 456; 487 Anderson, A.E. See Childress, J.J., 335 Anderson, D.L.T. See Knox, R.A., 382, 383; 487 Anderson, E.K., 195, 226, 241; 256 Anderson, J.M., 315; 331 Anderson, L.W. J., 110; 133 Anderson, R.J., 238; 256 Anderson, R.S., 324; 331 Andre, X. See Froidefond, J.M., 387; 484 Andrews, J.F. See Kornegay, B.H., 114; 142 Andrews, W.H., 308, 314, 315, 316; 331 Ang, P.O., 252; 256 Annandale, N., 360; 375 Annison, G., 89; 133 Anonymous, 12, 23, 24, 25, 26, 45, 49, 62, 301, 314, 318; 65, 331 Ansari, Z.A., 392, 393, 397, 400, 401, 403, 417, 418, 423, 429, 430, 434, 435, 436, 466; 480 See Harkantra, S.N., 434; 485 Stelngole, B.S., 401; 486 See Parulekar, A.H., 429, 430, 435, 471; 490 Ansell, A.D., 396, 399, 402, 403, 404, 448, 449, 450, 452, 453, 454, 456, 457, 465, 466, 467, 468, 469, 470, 474; 480 See Trevallion, A., 399, 456; 494 Anton, J., 89, 90; 133 Arad, S. See Kaplan, D., 76, 82; 141 Arasaki, S. See Ohno, M., 213, 214; 270 Arciz, W. See Kelly, C.B., 301; 341 Arimoto, R., 324, 326; 331 Armbruster, B. See Corpe, W.A., 91, 106; 136 Arnold, P.W. See Birtles, R.A., 426, 438; 481
498
OCEANOGRAPHY AND MARINE BIOLOGY
Arnott, S. See Moorehouse, R., 92; 144 Arntz, W.E., 407, 432, 441, 466, 468, 469; 480, 481 See Rosenberg, R., 492 See Tarazona, J., 432; 493 Arp, A.J., 292; 331 Arunachalam, M. See Balakrishnan Nair, N., 481 Arunpairojana, V. See Sly, L.I., 82; 150 Asakawa, M. See Yokote, M., 74, 99; 153 Asanuma, I. See Muneyama, K., 67 Aspinall, G.O., 79, 91, 92, 96, 102, 103, 122; 133 Aswandy, I., 435; 481 See Kastoro, W.W., 435; 487 Atkinson, L.P., 36; 65 See Lee, T.N., 39; 67 See Oey, L.Y., 36; 68 Atwell, R.W. See Grimes, D.J., 339 Auffret, M., 324; 331 Auld, K. See Renwrantz, L., 348 Austin, A.P., 218, 220; 256 Austin, H. See Griffen, M.R., 339 Austin, N.E. H., 158; 171 Averin, B.S. See Makarov, Y.N., 428, 453; 488 Avery, O.T., 96; 133 Aveyard, R., 81; 133 Avila, M. See Correa, J., 238, 239; 259 See Hoffman, A.J., 238, 240, 253; 263 See Santelices, B., 206; 272 Ayling, A.M., 246; 256 Ayres, P.A., 304, 309, 313, 317; 331 Ayyappan Nair, S. See Dwivedi, S.N., 402; 483 Azam, F. See Fuhrman, J.A., 285 Azevedo, C, 371; 375 Azis Abdul, P.K. See Balakrishnan Nair, N., 481 Aziz, A. See Aswandy, I., 435; 481 See Kastoro, W.W., 435; 487 Babb, M.S. See Jones, W.E., 213, 226; 264 Bachere, E., 323, 324; 332 Bacon, J.S. D., 122, 123, 124; 133 See Morris, E.J., 124; 145 Baggaley, A. See Srna, R.F., 326; 349 Baier, R.E., 235; 256 See Zambon, J.S., 153 Bailey, R.W. See Pickmere, E.S., 183; 270 Bailiff, M.D. See Karl, D.M., 116; 141 Baird, B.H., 105, 119; 133 Baird-Parker, A.C. See Anderson, J.M., 315; 331 Baker, C.J., 94; 133 Baker, E.T. See Cowen, J.P., 82, 117; 136 Baker, J., 210, 211; 256 Balakrishnan Nair, N. 423; 481 See Abdul Azis, P.K., 423, 424; 479 See Divakaran, O., 420; 483 Baldo, B.A., 324; 332
Balistrieri, L., 83, 128; 133 Ballard, J. See Nolan, C.M., 346 Bally, R., 170, 398, 407, 468, 469, 473; 171, 481 See Tarr, J.G., 407; 493 Balzer, W., 395, 458, 459; 481 Bandera Costa, J. See Blake, P. 332 Bane Jr, J.M., 51; 65 Banse, K., 386; 481 Banta, W.C. See Mihm, J.W., 113; 144 Barbosa, T. See Minet, J., 345 Barbosa, T.C., 288, 305, 317; 332 Bard, F. See Zaidi, R., 107; 153 Barilotti, D.C., 183, 240; 256 Barja, J.L. See Bolinches, J., 333 See Ledo, A., 342 Barksdale, M.J. See Pearse, J.S., 451; 490 Barnes, H., 353, 355, 356, 364, 366, 368, 370, 371, 372, 373; 375, 376 See Klepal, W., 353, 365, 367, 368, 369, 372, 373; 377, 378 See Munn, E.A., 355, 370; 378 Barnes, M. See Barnes, H., 355, 356; 375 See Klepal, W., 353, 367, 372, 373; 377 Barnes, W.D. See Zaneveld, J.S., 197; 276 Baron, D., 307, 311, 316; 332 Baross, J., 309; 332 Barret, T. See Wilson, R., 352 Barross, J.A. See Plante, C.J., 88; 147 Barrow, G.C. See Ayres, P.A., 309; 331 Bartell, P.F., See Orr, T., 91; 146 Bartlett, D.H., 96; 133 Bartley, C.H. See Metcalf, T.G., 303; 344 See Slanetz, L.W., 349 Basov, I.A., 438; 481 Bassindale, R. See Lilly, J.S., 266 Bate,G.C, 161, 171; 172 See Campbell, E.E., 156, 161, 166, 168, 170; 172 See Du Preez, D.R., 161; 172 See Sloff, D.S., 156; 174 See Talbot, M.M.B., 155–175; 156, 157, 159, 160, 161, 162, 164, 165, 166, 167, 169, 170; 174, 175 Batham, E.J., 373; 376 Bathmann, U.V. See Grant J., 101, 108, 109; 139 Bayer, M.A. See Moorehouse, R., 92; 144 Bayer, M.E., 95, 106; 133 Bayne, B.L., 281, 326; 332 Bayne, C.J., 326; 332 Bazin, M.J. See McFeters, G.A., 144 See Saunders, P.T., 114; 149 Bazzaz, F.A., 193; 256 See Reekie, E.G., 193; 271 Beber, R. See Sobsey, M.D., 349 BeBout, B.M. See Paerl, H.W., 114; 146 Becking, L.B., 156, 161, 167; 172 Bekheet, I.A. See Nasr, A.H., 198; 268 Belkin, S., 292; 332 Benedetti, E.L. See Boulègue, J., 333
AUTHOR INDEX
Benkovitz, C.M. See Premuzic, E.T., 391; 491 Bennett, C. See Acton, R.T., 330 Bensoussan, M.G. See Bianchi, A.J. 332 Berland, B.R., 283; 332 Berlin, E. See Scherrer, R., 124; 149 Bernard, F.R., 289, 290, 327; 332 Berner, R., 328; 332 Berner, R.A., 125; 134 Bernheimer, H.P. See Smith, E.E. B., 94; 150 Berry, A.J., 395, 408, 410, 450, 466, 468; 481 Berry, F., 286; 332 Bertness, M.D., 450; 481 Betzer, P.R. See Eppley, R.W., 110; 138 Beucher, M. See Plusquellec, A., 300; 347 Beveridge, T.J., 82; 134 See Ferris, F.G., 138 Bhargava, R. See McLusky, D.S., 399; 488 Bhat, U.G., 425; 481 Bhattacharya, D., 183; 256 Bianchi, A.J., 287; 332 Bianchi, M. See Bianchi, A.J., 332 Bianchi, T.S. See Rice, D.L., 125; 148 Biddanda, B.A., 87, 111, 279; 134, 332 Bidigare, R. See Childress, J.J., 335 Bidigare, R.R. See Brooks, J.M., 333 See Fisher, C.R., 337 See Kennicutt II, M.C., 341 Bidwell, R.G. S., 214; 256 See McLachlan, J., 213; 268 Bienfang, P.K., 110; 134 bin Othman, Z. See Berry, A.J., 450, 466, 468; 481 Birkbeck, T.H., 282; 332 See McHenery, J.G., 280, 281, 282, 283, 322; 344 See Nottage, A.S., 320, 322; 346 Birtles, R.A., 426, 438; 481 Bishop, C.T., 107; 134 Bishop, J.L. See Murchelano, R.A., 286; 345 Bitter-Suermann, D. See Roberts, I., 148 Bitton, G., 82; 134 See Marshall, K.C., 83; 144 Bjornsson, A. See Danielson, A., 84; 137 Black, R., 248, 412, 454; 256, 481 See Levine, M.M., 307; 343 Blackburn, T.H., 279; 332 See Fenchel, T., 329; 337 Blake, N.J. See Hood, M.A., 315; 340 See Rodrick, G.E., 348 Blake, P., 311; 332 Blake, P.A. See Wilson, R., 352 Blanton, J.O. See Atkinson, L.P., 36; 65 See Oey, L.Y., 36; 68 Blaschko, H., 289; 333 Blaxter, J.H.S. See Edwards, R.R.C., 483 Blecka, J. See DiSalvo, L.H., 321; 336 Bligh, E.G., 104; 134
499
Bluementhal, R. See Sutcliffe, J., 99; 151 Bocquet-Védrine, J., 354, 360, 371; 376 See Pochon-Masson, J., 370; 378 Bodungen, B. von, 110; 134 See Balzer, W., 458; 481 Bodvarsson, G.M., 21; 65 Boesch, D.F. See Rhoads, D.C., 491 Bogdan, G.F., See Gerba, C.P., 338 Bold, B.C., 181; 256 Bolin, B., 382; 481 Bolinches, J., 320, 322; 333 See Lodeiros, C., 343 Bolton, J.J. See Anderson, R.J., 238; 256 Bonar, D.B., 113; 134 See Coon, S.L., 298; 335 See Weiner, R.M., 152 Boney, A.D., 180, 208, 209, 212, 221, 223, 236, 239; 257, 258 See Huang, R., 236, 249, 252; 264 See Khfaji, A.J., 236; 265 Bonin, D.J. See Berland, B.R., 332 Boon, P.I. See Moriarty, D.J.W., 489 Booth, B.C., 279; 333 Borde, J. See Bouvy, M., 302, 303, 314, 317; 333 Boring, J.R. See Schwarzmann, S., 86; 149 Borowitzka, M., 210, 212; 257 Bos, S. See Breeman, A.M., 187; 257 Boss, K.J., 291; 333 Bostock, A.D., 317; 332 Boto, K.G., 386, 414, 464; 481 See Alongi, D.M., 426, 460, 463; 479 See Stanley, S.O., 462; 493 Boulnois, G. See Roberts, I., 148 Boulègue, J., 294; 333 Boulo, V. See Mialhe, E., 344 Bourdon, R. See Bocquet-Védrine, J., 354; 376 Boury, M., 302, 303, 314, 317; 333 Bouvy, M., 296; 333 See Soyer, J., 349 Bowen, S.H., 128; 134 Boyd, C.E., 329; 333 Boyer, I.C. See Kaspar, H.F., 341 Boyer, L.F. See Grant, W.D., 108; 139 See Tenore, K.R., 350 Boyle, C.D., 76, 78, 94, 102; 134 Boyle, W.C. See Mueller, J.A., 87, 114; 145 Boyles, W.A., 162; 172 Boynton, W.R. See Kemp, W.N., 330; 341 Bradford, H.B., 311; 333 Bradford, M., 104; 134 Brancato, M.S., 113, 298; 134, 333 Brand, D.G. See Reid, R.G.B., 297; 348 Brander, K.M. See Walley, L.J., 353, 372; 379 Bratbak, G., 79, 121; 134 Bråten, T., 210, 211, 215, 235; 257 Braun, J.G. See Flood, P.R., 438, 453; 484 Brautigam, E., 95; 134
500
OCEANOGRAPHY AND MARINE BIOLOGY
Brawley, S.H., 250; 257 Brayton, P.R. See Grimes, D.J., 339 Breeman, A.M., 187, 206; 257 See De Ruyter van Steveninck, E.D., 194; 260 Breeman, A.M. See Rietema, H., 199; 271 Breen, P.A., 247; 257 Breitburg, D.L., 251; 257 Bremer, P.J., 120; 134 Bresciani, J., 373; 376 Brewer, P.G. See Balistrieri, L., 83, 128; 133 Brey, T. See Arntz, W.E., 407; 480 Briggs, J.C, 426; 481 Brinkhurst, R.O. See Chua, K.E., 87; 135 Brisou, J., 286, 307, 308, 310; 333 Brockel, K.V. See Bodungen, B. von, 110; 134 Brooks, J.M., 293; 333 See Childress, J.J., 335 See Kennicutt II, M.C., 341 Broom, M.J., 397, 402, 404, 409, 413, 450, 456, 457; 481 Brown, A.C., 155; 172 Brown, C., 320, 321, 322, 323; 333, 334 See Murchelano, R.A., 286; 345 Brown, CM., 118; 134 See Wardell, J.N., 84, 115; 152 Brown, D.F. See Spite, G.T., 311; 349 Brown, K.N. See Mackie, E.B., 106; 143 Brown, L.D., 306, 307; 334 Brown, M.J., 79, 80, 81, 93, 101, 102, 126; 134 Brown, M.R.W. See Gilbert, P., 139 Brown, S. See Gaines, S., 231; 262 Bruland, K.W. See Cowen, J.P., 81, 126; 136 Bryan, F.L., 306, 307, 308, 309, 310, 311, 312, 315; 334 Bryers, J.D. See McFeters, G.A., 144 Bubucis, P.M. See Buck, J.D., 310; 334 Buchanan, B.A., 422; 481 Buchanan, J.B., 426, 428, 437, 438, 441, 453; 482 See Gauld, D.T., 396, 408, 409; 484 Buck, J.D., 310; 334 Buckle, K.A. See Quadri, R.B., 314; 347 Buckmire, F.L.A., 89; 135 Buestel, D., 323; 334 Buggeln, R.G., 203; 257 Bui, M.N. See Cheng, T.C., 334 Buller, H. See Madden, R.H., 312; 343 Bullock, T.H., 443, 446; 482 Bünning, E., 205; 257 Bunt, J.S., 455, 456; 482 See Boto, K.G., 386, 414; 481 Burney, C.M., 76; 135 Burns, R.L., 191, 239; 257 See Mathieson, A.C., 183; 267 Burrows, E.M., 230, 240, 241, 247; 257 See Chapman, A.R.O., 198, 241; 258 Burt, W.V. See Trump, C. 1., 36; 69 Busch, P.L., 74, 109, 111; 135
Burton, H.W. See Ayres, P.A., 331 Buschmann, A., 202, 206, 219, 229; 257 Bush, L.F., 400, 402; 482 Butler, J.H.S. See Ladd, J.N., 78; 142 Butman,C.A., 112; 135 Buttiaux, R., 307; 334 Cabelli, V.J., 299, 300, 301, 302, 303, 304, 317; 334 See Heffernan, W.P., 303, 304, 305, 339 Cabot, E.L. See Smith, B.D., 103; 150 Caffey, H.M., 229; 257 See Garrity, S.D., 412; 484 Cahet, C. See Soyer, J., 349 Cahet, G. See Bouvy, M., 333 See FialaMédioni, A., 292; 337 Cal, R.M. See Tenore, K.R., 350 Caldwell, E. See McFeters, G.A., 144 Callan, H.G., 353; 376 Callow, M.E., 210, 211; 257 See Evans, L.R., 105; 138 Calloway, C.B. See Waterbury, J.B., 290; 351 Calvert, S.E. See Jumper, S.K., 117; 141 Camacho-Ibar, V.F., 392; 482 Cammen, L., 108, 118, 120, 125; 135 Cammen, L.M., 280, 329; 334 Campbell, E.E., 156, 161, 166, 167, 168, 170; 172 See Du Preez, D.R., 161; 172 See Talbot, M.M. B., 155–175 Campello, C. See Marjori, L., 315; 343 Cancino, J. See Santelices, B., 188, 248; 271 Cane, M.A., 382, 383, 385; 482 Capon, B. See Lofthouse, P.F., 210; 266 Capone, D.G. See Corredor, J.E., 392; 482 Caraway, C.T. See Mackowiack, P.A., 311; 343 Carbajal, G. See Rosenberg, R., 492 Carefoot, T.H., 332 Carlson, C.A. See Stewart, G.S., 116; 151 Carlson, D.J., 326; 334 Carlsson, J., 74; 135 Carlton, J.F., 219; 257 Caron, D.A., 87, 111; 133 See Alldredge, A.L., 76; 133 Carpenter, E.J., 290; 334 Carrick, R.J. See Sobsey, M.D., 349 Carson, B. See Kulm, L.D., 342 Carson, J. See Osborn, M.J., 98; 146 Carter, A.R., 185; 257 Carval, J.P. See Prieur, D., 347 Case, R.J. See Harper, D.E., 436; 485 Cassie, R.M., 156; 172 Cassie, V. See Cassie, R.M., 156; 172 Castenholz, R.W. See Decho, A.W., 87; 137 Castilla, J.C. See Santelices, B., 188, 248; 271 Castillo, J.G. See Gallardo, V.A., 484 Casu, B. See Perlin, A.S., 107; 147
AUTHOR INDEX
Cavanaugh, C.M., 292, 293, 294; 334 Cawthon, C.D. See LeChevallier, M.W., 115; 142 Cech, I. See Gerba, C.P. 338 Cefalu, R.C. See Hopper, B.E., 445; 486 Certes, A., 289; 334 Chagot, D. See Bachere, E., 323; 332 See LeGall, G., 342 See Mialhe, E., 344 Chakrabarty, A.M. See Deretic, V., 137 Chakraborty, A.K. See Nath, R.K., 107; 145 Chakroun, F., 286; 334 Chamberlain, A.H.L., 85, 99, 107, 210, 235; 135, 258 See Daniel, G.F., 76, 82, 99; 137 Chambers, J.E., 122; 135 Chan, K. See Kueh, C.S.W., 288, 302; 341 Chan, R., 106, 135 Chandra Mohan, P. See Siva Rama Sarma, N., 400, 402, 403; 492 Chandran, R. See Sivakumar, V., 391; 492 Chang, H.T., 106; 135 Chang, P.W. See Gulka, G., 319; 339 Chanley, P.E. See Tubiash, H.S., 320; 351 Chaperon, J. See Pinot, M., 311; 347 Chapman, A.R.O., 177, 193, 194, 195, 198, 222, 236, 238, 241, 243, 247, 248, 249, 251; 258 Chapman, D.J. See Kieras, J.H., 104; 142 Chappell, J. See Wolanski, E., 387; 495 Characklis, W.G., 53, 74, 99; 135 See Matson, J.V., 81, 114; 144 See McFeters, G.A., 144 See Turakhia, M.H., 95; 152 Chardy, P., 399; 482 Chareonruay, M., 435; 482 Charlton, S.E. See Lock, M.A., 143 Charnov, E.L., 372, 374; 376 Charters, A.C., 214, 235; 258 See Coon, D., 194, 221, 223; 259 See Neushul, M., 235; 268 Chatterji, A. See Ansari, Z.A., 402; 480 Chemin, M.E., 238, 239; 258 Chen, C. See Lewin, J., 157; 173 Chen, L.C.-M., 183, 210; 258 See McLachlan, J., 197; 268 Cheng, K.G., 78, 102; 135 Cheng, K.J. See Costerton, J.W., 76, 84, 87, 88, 94, 106, 114, 118; 136 See Kudo, H., 114; 142 Cheng, M.H., 80; 135 Cheng, T. See Renwrantz, L., 348 Cheng, T.C., 323, 324, 325, 326; 334, 335 See Foley, D.A., 325; 338 See Howland, K.H., 325; 340 See Mohandas, A., 324, 325, 326; 345 See Vasta, G.R., 324; 351 Chern, C.S., 14, 28; 65 See Wang, J., 22; 70
501
Chester, I.R., 95; 135 Chevelot, L. See Samain, J.F., 348 Chew, K.K. See Lipovsky, V.P., 320; 343 Chi, E.Y., 210; 258 Chia, F.S., 297; 335 Childress, J.J., 293; 335 See Arp, A.J., 292; 331 See Brooks, J.M., 333 See Felbeck, H., 292; 337 See Fisher, C.R., 295, 337 Choat, J.H., 247; 258 See Schield, D.R., 249, 250; 272 Chong, V.C., 422; 482 Choudhury, A. See Nandi, S., 397, 402, 403; 489 Christensen, B.E., 82, 88, 89, 90, 92, 94; 135 Christiaen, D. See Kaplan, D., 76, 82; 141 Christie, A.O., 203, 210, 211, 215, 235; 258 See Evans, L.V., 210, 211; 261 Chu, T.Y., 18, 20, 22, 27, 29; 65 Chua, K.E., 87; 135 Chuang, W.S., 24, 26; 65 See Shim, T., 41; 69 Chugh, T.D., 308; 335 Chullasorn, S., 421; 482 Chuman de Flores, E. See Rosenberg, R., 492 Churchill, A.C., 219; 258 Cipriano, F. See Knauer, G.A., 112; 142 Clark, M.E. See Pearse, J.S., 270 Clarke, A., 446; 482 Clarke, W.D. See Rosenthal, R.J., 248, 250; 271 Clauss, H. See Müller, S., 198; 268 Clavier, J. See Chardy, P., 399; 482 Clayton, M.N., 178, 180, 184, 185, 200; 258 Clegg, F.L., 315; 335 Clement, M.L. See Levine, M.M., 307; 343 Clendenning, K.A., 241; 258 Clifford, H. See Smith, K.L., 431; 492 Cochard, J.C. See Buestel, D., 334 See Jeanthon, C., 285; 340 See Nicolas, J.L., 320, 321; 346 See Samain, J.F., 348 Cochran, G.R. See Kulm, L.D., 342 Cockcroft, A.C., 170; 172 Cody, M.L., 190; 259 Coffin, R.B., 81; 135 See Wright, R.T., 352 Cohen, D. See Levin, S.A., 216; 266 Cohen, R.D.H., 326; 335 Cohen, Y. See Alldredge, A.L., 114; 133 Cole, J.J., 130, 279; 135, 335 See Alldredge, A.L., 76; 133 Cole, K. See Brooks, J.M., 333 See McBride, D.L., 208, 209, 210, 211, 212, 214, 235; 267
502
OCEANOGRAPHY AND MARINE BIOLOGY
Cole, K.M. See Pueschel, C.M., 210, 211, 212; 271 Cole,M.T., 313, 315, 316; 335 Coleman, J.M. See Wells, J.T., 389, 390; 495 Coles, S.L., 93, 117, 127; 136 Colijn, F., 456; 482 Collier, A., 355; 376 Collos,Y., 162; 172 Colvin, J.R. See Lewin, J., 157; 173 Colwell, R.R., 286, 319; 335 See Bonar, D. B., 113; 134 See Kaneko, T., 320 See Costerton, J.W., 118; 136 See Elston, R.A., 320; 337 See Grimes, D.J., 339 See Hada, H.S., 339 See Hussong, D., 304; 340 See Joseph, S.N., 341 See Kaneko, T., 341 See Kaper, J., 341 See Lovelace, T.E., 286; 343 See Tubiash, H.S., 321; 351 See Weiner, R.M., 113, 298; 152, 351, 352 Comar, P.G., 315; 335 Combs, T.J. See Buck, J.D., 310; 334 Commeau, R. See Paull, C.K., 346 Comps, M., 319; 335 See Mialhe, E., 344 Connell, J.H., 187, 225, 227, 231, 237; 259 Connor, V.M., 234; 259 Conover, J.T., 197, 232, 236; 259 Conway, P.L. See Wrangstadh, M., 85; 153 Cook, S.D. See Stephenson, W., 415; 493 Cooke, M.D., 300, 301, 308; 335 Cooksey, B., 95; 136 See Cooksey, K.E., 95, 99; 136 Cooksey, K.E., 94, 95, 99; 136 See Characklis, W.G., 83, 99; 135 See Cooksey, B., 95; 136 See Turakhia, M.H., 95; 152 See Webster, D.R., 85, 100, 109; 152 Coon, D., 194, 221, 223; 259 Coon, D.A. See Charters, A.C., 214, 235; 259 See Neushul, M., 235; 268, 269 Coon, S.L., 298; 335 Cooper-Willis, C.A., 324; 336 Corall, J. See Tenore, K.R., 350 Cormaci, M., 197; 259 Cormier, M. See Minet, J., 345 Corner, E.D.S. See Boney, A.D., 239; 257 Cornet, C. See Henry, M., 296; 339 Cornette, J.E. See Rodrick, G.E., 348 Cornford, N.E. See Rosen, M.W., 74, 87; 149 Corpe, W.A., 79, 84, 89, 91, 92, 102, 106, 126, 298; 136, 336 See Tosteson, T.R., 113; 151 Corral, L. See Azevedo, C., 371; 375 Correa, J., 200, 238, 239; 259 See Santelices, B., 206; 272 Corredor, J.E., 392, 395; 482 Corso, W.P. See Paull, C.K., 346 Cory, R.L. See Cohen, R.D.H., 335
Costerton, J.D. See Chan, R., 106; 135 Costerton, J.M. See Cheng, K.G., 78, 102; 135 Costerton, J.W., 74, 76, 77, 84, 85, 87, 88, 93, 94, 95, 106, 108, 114, 115, 116, 118; 136 See Geesey, G.G., 82; 139 See Kudo, H., 114; 142 See Ladd, T.I., 116; 142 See Lock, M.A., 143 See Mackie, E.B., 106; 143 Costlow, J.D. See Maki, J.S., 113; 143 Coughlan, J. See Fleming, J.M., 106; 138 Coull, B.C. See Hicks, G.R. F., 126; 140 See Tenore, K.R., 383; 493 Couperwhite, I. See Annison, G., 89; 133 Cousens, R., 192, 249, 250; 259 Cowen, J.P., 81, 82, 111, 117, 126; 136, 137 Cowen, R., 250; 259 Craigie, J.S., 183; 259 See McCandless, E.L. 183; 267 See McLachlan, J., 236; 268 Crayton, M.A., 99; 137 Creese, R.G., 248; 259 Crevatin, E. See Marjori, L., 315; 343 Crisp, D.J., 298, 353, 355, 356, 358, 368, 373, 374, 466, 469; 336, 376, 482 See Barnes, H., 353, 373; 375 See Manahan, D.T., 283, 284; 343 Cross, G., 309, 311; 336 Crowe, G.E. See Shannon, R.K., 237; 273 Cruickshank, R.H. See Marshall, K.C. 84, 144 Crump, E. See West, J.A., 202; 275 Crumpton, W.G., 93; 137 Csanady, G.T., 39; 65 Cuba, T. See Roderick, G.E., 348 Cubit, J. See Lubchenco, J., 178, 184, 239; 267 Cubit, J.D., 248; 259 Cucci, T.L. See Shumway, S.D., 349 Culler, J.J. See Li, W.K. W., 343 Culliney, J.L. See Carpenter, E.J., 290; 334 Cullum, M.L. See Ayres, P.A., 331 Cundell, A.M., 287; 336 Cunningham, E.M. See Guiry, M.D., 186, 199; 262 Curray, J. See Paull, C.K., 346 Currie, V. See Dayton, P.K., 260 Curtis, M.A. See Hopner Petersen, G., 474, 476, 477; 486 Cushing, D.H., 387, 388, 470, 471, 473, 476; 482 Cutlip, R.C. See Page, A., 319; 346 Cutter, J.M., 290; 336 Cutter, J.M. See Rosenberg, F.A., 290; 348 Dahl, A.L. See Neushul, M., 240; 269 Dahl, E., 407, 408, 409, 410; 482 Dahlbäck, B., 327, 328; 336
AUTHOR INDEX
Dalley, E. See Griffen, M.R., 339 Dalton, H. See Whittenburry, R., 294; 352 Dame, R.F., 326, 329; 336 Damgaard, H.N. See Costerton, J.W., 88, 94, 106; 136 Damodaran, R., 426, 430, 435; 482 Dando, P.R., 295, 296, 374; 336, 376 See Spiro, B., 349 Daniel, G.F., 76, 82, 99, 100; 137 Daniel, J.Y. See Maginot, M, 343 See Samain, J.F., 348 Daniels, J. See Renwrantz, L., 324; 348 Daniels, W.G. See DiSlavo, L.H., 106; 137 Danielson, A., 84; 137 Dankers, N. See Dame, R.F., 329; 336 D’Antonio, C, 181, 183; 259 Dao, J.C. See Buestel, D., 334 Darbyshire, B., 76, 78; 137 Darley, W.M., 214, 222; 259 Darwin, C., 353, 356, 360, 361, 373; 376 Dasgupta, M. See Costerton, J.W., 136 Datta, N.C., 417, 425; 482 Daumas, R., 117; 137 Davies, L.T. See Moore, H.B., 489 Davis, B. See Wilson, R., 352 Davis, C.H. See Loosanoff, V.L., 284; 343 Davis, C.L. See Seiderer, L.J., 125; 149, 349 Davis, D. See DeFlaun, M.F., 116; 137 Davis, J.A. See Luoma, S.N., 80, 81, 101; 143 Davis, J.D. See Platt, R.M., 93; 147 Dawes, C.J. See Friedlander, M. 202; 262 See Lawrence, J.M., 219; 266 Dawson, R. See Meyer-Reil, L.A., 344 Day, J.W. See Yanez-Arancibia, A., 422; 496 Dayton, P.K., 188, 221, 226, 229, 231, 244, 247, 248, 250, 253; 259, 260 See Rosenthal, R.J., 248, 250; 271 Dazzo, F.B. See Abe, M., 90; 132 See Sherwood, J.E., 86; 150 See Vasse, J.M., 74, 81, 86; 152 Dea, L C.M., 94; 137 Dean, H. See Maurer, D., 425; 488 Dean, J.M. See Holland, A.F., 108; 140 Dean, R.C., 290; 336 Dean, T.A., See Deysher, L., 244, 253; 260 Deavin, L. See Jarman, T.R., 89; 141 De Billy, F. See Bouvy, M., 333 De Boer, J.A., 199; 260 De Boer, P.L. See Vos, P.C., 99, 108; 152 De Burgh, M.E., 292; 336 Decho, A.W., 73–153; 87, 94, 103, 105, 119, 125; 137 Defant, A., 23; 65 DeFlaun, M.F., 108, 116; 137 See Paul J.H., 116; 147 Degins, E.T. See Bolin, B., 382; 481
503
Degushi, Y. See Sugita, H., 350 Dehnel, P.A., 448; 482 De Jonge, V.N. See Colijn, F., 456; 482 De la Campa, S. See Guzmán del Pró, S.A., 195; 262 De la Cruz, A.A., 381, 401; 482 Delattre, J.M., 300, 301, 318; 336 See Hernandez, J.F., 308; 339 DeLeon, A.R. See Flood, P.R., 438, 453; 484 Delesmont, R. See Delattre, J.M., 300, 301, 318; 336 De Ligny, W. See Leong, T.S., 487 Delivopoulos, S.G. See Kugrens, P., 210; 266 Dempsey, M.J., 82; 137 Denis, F.A., 310; 336 Denley, E.J. See Underwood, A.J., 229, 231; 274 Denny, M., 232; 260 Deretic, V., 96; 137 De Ruyter van Steveninck, E.D., 194; 260 Desai, B.N., 473, 482 See Govindan, K., 423; 485 See Varshney, P.K., 423; 494 De Santiago, G. See Tenore, K.R., 350 Deshmukh, I., 382, 483 Deslandes, E. See Floc’h, J.Y., 220; 261 Dethier, M., 188; 260 Deutsch, A., 122; 137 De Vinny, J.S., 233; 260 De Vries, M.C., 449, 450, 451; 483 Dewar,W. K. See Bane Jr, J.M., 51; 65 DeWitt, P.W., 42, 66 DeWreede, R., 179, 182, 185, 190, 192, 193, 198, 228, 237; 260 See Dyck, L., 183; 261 DeWreede, R.E. See Vandermeulen, H., 226; 275 Dexter, D.M., 396, 397, 411, 413, 445; 483 Deysher, L., 215, 221, 244, 253; 260 Dhamne, K.P., 448; 483 Dhargalkar, V.K. See Parulekar, A.H., 473; 490 Dharmaraj, K. See Balakrishnan, Nair, N., 481 DiSalvo, L.H., 106, 321, 323; 137, 336 Dickson, M.R. See Humphrey, B.A., 85, 91, 104; 140 See Popham, J.D., 291; 347 Diggs, C.D. See Andrews, W.H., 331 Dikshit, R. See Deretic, V., 137 Dillon, P.S., 113; 137 Diouris, M. See Le Pennec, M., 342 Dittel, A. See Epifanio, C.E., 414; 483 Dittel, A.I. See De Vries, M.C., 449; 483 Divakaran, O., 417, 420; 483 Divino, P. See Tiews, K., 442; 494 Dixon, P. See Williams, D. McB., 476; 495 Dixon, P.S., 182, 185, 186, 187, 238; 260
504
OCEANOGRAPHY AND MARINE BIOLOGY
Doboszewski, B. See Vreeland, V., 107; 152 Doering, P.H., 328; 336 Doherty, P., 178, 237; 260 Dong, L.X. See Wang, K.S., 36; 70 Donn Jr, T.E., 170; 172 Donta, S.T. See Joseph, S.N., 341 Donval, A. See Le Pennec, M., 342 Dopazo, C.P. See Lodeiros, C., 343 Dor, I. See Por, F.D., 414; 491 Dorn, C.R. See Brown, L.D., 306; 334 Doty, M.S., 218,. 232, 243; 260 See Fahey, E.M., 228; 261 See Santelices, B., 179; 272 Doudoroff, M. See Stanier, R.Y., 87; 150 Downes, B.J. See Keough, M.J., 237; 265 Downes, J.C.U. See Cheng, T.C., 324; 335 Doyle, A.P. See Henrichs, S.M., 100, 121, 125; 140 Doyle, W.T. See Hansen, J.E., 185; 262 Drebes, G., 157, 158; 172 Dredge, M. See Robertson, J., 441; 491 Dresler, P.V. See Cohen, R.D. H., 335 Drew, K.M., 182, 240; 260 Dring, M. See Lüning, K., 198; 267 Dring, M.J., 198, 199, 200, 203, 204, 236; 261 Driscoll, E.G., 327; 336 Dron, D. See Boulègue, J., 333 Druehl, L.D., 184; 261 See Hsiao, S.I.C., 184; 264 Du Preez, D.R., 161; 172 Duarte, C.M., 456; 483 Dubois, M., 101; 137 Duboise, M. See Greenberg, E.P., 303; 338 Ducklow, H., 74, 117; 137 Dudman, W.F., 78, 81, 89; 138 Dugan, P.R., 79, 80, 93, 126; 138 See Friedman, B.A., 111; 139 See Joyce, G.H., 81, 93, 126, 128; 141 See Parsons, A.B., 97, 102; 147 Duggins, D.O., 247; 261 See Paine, R.T., 189; 270 Duguid, J.P., 106; 138 Duiven, P. See Swennen, C., 409; 493 Duncan, M.J. See Lobban, C.S., 204, 207, 215, 221, 236; 266 Dunlap, T. See Ruddel, C.L., 348 Dunstan, W.M. See Tenore, K.R., 327; 350 Duran, A.P. See Twedt, R.M., 351 Durand, R.J., 414; 483 Duro, A. See Cormaci, M., 197; 259 Dwivedi, S.N., 402; 483 See Parulekar, A.H., 416; 490 Dyck, L., 183; 261 Dye, A.H. See Lasiak, T., 445; 487 See McLachlan, A., 174
Dyer, W.J. See Bligh, E.G., 104; 134 Eagle, G.A., 156, 159, 166, 169; 172 Earampamoorthy, S., 306, 308; 336 Eaton, J.F. See Carlson, D.J., 334 Ebeling, A.W. See Reed, D.C., 213, 216, 237; 271 Ebeling, F.J. See Lilly, J.S., 266 Eccles, C.R. See Horan, N.J., 111; 140 Echelberger, W.F. See Pavoni, J.L. 91, 102, 116; 147 Eckman, J.E. See Lewin, J., 170; 173 Edelstein, T. See Chen, L.C.-M., 183; 258 See McLachlan, J., 197; 268 Edgar, G.J., 219; 261 Edgar, L.A., 85, 99, 109; 138 Edwards, P., 183, 243; 261 Edwards, R.A. See Quadri, R.B., 314; 347 Edwards, R.R.C., 396, 399, 409, 414, 416, 419, 446, 447, 448, 449, 455, 456, 459, 465, 466, 467; 483 Edyvean, R.G. J., 192, 202; 261 See Ford, H., 192; 262 Eggenkan, A.E. See Van den Broek, M.J. M., 309; 351 Eguchi, H. See Kamihara, E., 67 See Fujiwara, I., 31; 66 See Shibata, A., 36; 69 Einav, P. See Sheintuch, M., 111; 150 Ekman, S., 383; 483 Eliot, C., 286; 336 Elliot, E.L. See Elston, R.A., 320; 327 Ellwood, D.C. See Brown, C.M., 118; 134 Elston, R., 284, 320, 321, 322; 336, 337 See Leibovitz, L., 322; 342 Elston, R.A., 319, 320, 321, 322, 323; 337 Eltringham, S.K., 155; 172 Embley, R.W. See Kulm, L.D., 342 Emerson, S.E., 228; 261 Emery, K.O. See Niino, H., 26, 42; 68 Endoh, M. See Yuan, Y.C., 48, 49; 71 Enfors, S. See Norberg, A.B., 76, 102; 146 English, S. See Williams, D. McB., 476; 495 Enomoto, R. See Kobayashi, T., 341 Enomoto, S. See Hori, T., 208, 210, 212; 263 Epifanio, C.E., 414; 483 See De Vries, M.C., 449; 483 Epp, R., W., 88; 138 Eppley, R.W., 110; 138 Erasmus, T. See McLachlan, A., 174 Espinasse, S. See Brisou, J., 333 Estacion, J.S., 435; 483 Evans, D.J. See Gilbert, P., 139 Evans, E.E. See Acton, R.T., 330 Evans, L.R., 102, 103, 105; 138
AUTHOR INDEX
Evans, L.V., 210, 211; 261 See Baker, J., 210, 211; 256 See Callow, M.E., 210; 211; 257 See Chamberlain, A.H.L., 210, 235; 258 See Christie, A.O., 203, 210, 211, 215; 258 Evans, S. See Kautsky, N., 328; 341 Fagade, S.O., 422; 483 Fager, E.W., 442; 484 Fahey, E.M., 228; 261 Falconetti, C. See Grelet, Y., 485 Fallen, R.D., 121; 138 Fan, K.L., 25, 26; 65 Farced, V. See Evans, L.R., 105; 138 Farmer, W. See Martin, J., 121; 144 Farnham, W.F., 219; 261 Farr, A.L. See Lowry, O.H., 104, 143 Fattom, A., 85; 138 Fay, R.R. See Kennicutt II, M.C., 341 Fazio, S.A., 100, 108; 138 Feeney, F.L. See Johnstone, G.R., 185; 264 Felbeck, H., 292, 293, 294, 297; 337 See Schweimanns, M., 295; 349 Feldman, J., 182; 261 Fell, J.W. See Hopper, B.E., 445; 486 Feltham, C.B. See ZoBell, C.E., 278, 285; 352 Fenchel, T., 87, 279, 285, 327, 329; 138, 337 See Lee, C.C., 444, 445, 447; 487 Fengshan, X. See Rhoads, D.C., 491 Fenner, M., 180, 187, 190, 194, 227; 261 Ferguson, R.L., 279; 337 Fergusson, J.C., 337 Fernando, S.A., 417, 418, 425; 484 Ferris, F.G., 80; 138 Fetter, R., 182; 261 Fiala, M. See Berland, B.R., 332 Fiala-Médioni, A., 291, 292, 294; 337 See Hily, A., 340 Fiedler, F. See Brautigam, E., 134 Fieger, E.A. See Lartigue, D., 286; 342 See Novak, A.F., 286; 346 Field, J. See Becking, L.B., 172 Field, J.G. See Newell, R.C., 120, 125, 126, 280, 281, 327; 145, 345 Filic, Z. See Fuks, D., 304; 338 Findlay, R.H. See White, D.C., 120; 152 Findlay, S., 120; 138 See Cole, J.J., 130; 135 Finenko, Z.Z. See Khaylov, K.M., 81; 141 Finger, I. See Rosenberg, R., 492 Finlayson, D.M. See Barnes, H., 356; 375 See Edwards, R.R.C., 483 Finne, G. See Peixotto, S.S., 347 Fishelson, L., 386, 420; 484 Fisher, C.R., 294, 295; 337 See Arp, A.J., 292; 331 See Brooks, J.M., 333 See Childress, J.J., 335 Fisher, M.R., 295; 337 Fitzpatrick, M. See Griffen, M.R., 339
505
Flagg, W. See Scholander, P.F., 443; 492 Flammann, H.T. See Brautigam, E., 134 Flannigan, B. See Wardell, J.N., 84, 115; 152 Fleet, G.H., 301, 306, 307, 313; 338 See N’Guyen Thi Son, 303, 307, 308, 309, 310, 311; 346 See Rowse, A.J., 303, 304, 305; 348 See Yoovidhya, T., 314, 315; 352 Fleming, J.M., 106; 138 Fleming, R.H. See Sverdrup, H.U., 14, 41; 69 Fletcher, M., 83, 84, 89, 91, 92, 93, 94, 95, 106, 111; 138, 139 Fletcher, R.L., 192; 261 See Farnham, W.F., 219; 261 Fletcher, S.M. See Fletcher, R.L., 192; 261 Floc’h, J.Y., 220; 261 Flood, P.R., 438, 453; 484 Floodgate, G.D., 114; 139 See Fletcher, M., 84, 89, 92, 93, 94, 106, 111; 139 Flores, L.A. See Rosenberg, R., 492 Foley, D.A., 325; 338 See Cheng, T.C., 335 Fonck, E. See See Santelices, B., 250; 272 Foote, C.J., 285; 338 Forbes, M.A., 235; 262 Ford, H., 192; 262 See Edyvean, R.G. J., 192, 202; 261 Foreman, R.E. See Smith, B.D., 103; 150 Fornalik, M.S. See Zambon, J.S., 153 Forsberg, L.S. See Pazur, J.H., 102; 147 Forsyth, J. See Cross, G., 336 Foster, B.A., 353, 355, 358, 373; 376 Foster, M.S., 188, 231, 237, 245, 246, 250; 262 See Cowen, R., 250; 259 See Neushul, M., 269 See Reed, D.C., 228, 248, 250; 271 Foster, R.C., 106; 139 Foster-Smith, R.L., 327; 338 Foulds, J. See Sutcliffe, J., 99; 151 Fraiser, M.B., 308, 310, 316; 338 Franca, S.M. C., 309; 338 Francis, D.W. See Twedt, R.M., 351 Frankel, L., 108; 139 Frankenberg, D., 329, 427, 428; 338, 484 Fraser, B.A. See Gotschlich, E.C., 139 Fraser, T.H. See Moore, H.B., 489 Fredericq, S. See Hommersand, M.H., 196; 263 Freeman-Lynde, R.P. See Paull, C.K., 346 Frerman, F.A. See Troy, F.A., 98; 151 Fretter, R. See Norton, T.A., 233; 269 Friedlander, M., 202; 262 Friedl, F., 323; 338 See Alvarez, M.R., 325, 326; 331 Friedman, B.A., 111; 139 Friehofer, V. See Bitton, G., 82; 134 Froidefond, J.M., 387; 484
506
OCEANOGRAPHY AND MARINE BIOLOGY
Fry, B. See Van Dover, C.L., 152 Fuhrman, J.A., 285; 338 See Riemann, B., 148 Fujimaki, N. See Yanagimachi, R., 353; 379 Fujita, D. See Masaki, T., 251; 267 Fujiwara, I., 31, 32; 66 Fukasawa, M., 47; 66 Fukase, S., 36; 66 Fuks, D., 304; 338 Fukui, T. See Ikeda, F., 140 Furfari, S.A., See Andrews, W.H., 331 Furnari, G. See Cormaci, M., 197; 259 Furnas, M.J., 473, 476; 484 Fustec-Mathon, E. See Martin, J., 121; 144 Fyfe, W.S. See Ferris, F.G., 138 Gabrielson, P.W., 238; 262 Gaffney, J.S. See Premuzic, E.T., 391; 491 Gaikwad, U.D. See Varshney, P.K., 423; 494 Gaines, S., 231; 262 Gaines, S.D., 178, 206, 229, 231; 262 Gallardo, V.A., 426, 428, 429, 435; 484 Galtsoff, P.S., 326; 338 Ganapati, P. See Rao, G., 395; 491 Ganapati, P.N., 395, 400, 402; 484 See Raman, A.V., 423; 491 Gander, J.E. See Osborn, M.J., 98; 146 See Tonn, S.J., 76, 78; 151 Gangarosa, E.J. See Blake, P., 332 Garbary, D., 183; 262 See Dyck, L., 183; 261 See Gabrielson, P.W., 238; 262 Garber, J. See Nixon, S.W., 346 Garcia-Fernandez, C. See Tenore, K.R., 350 Garland, C.D., 289, 321; 338 Garrity, S.D., 412; 484 Garver, J.L., 158, 160, 165, 166, 167; 172 Gauld, D.T., 396, 408, 409; 484 Gebelein, C.D. See Neumann, A.C., 108; 145 Gee, J.M. See Moore, M.N., 122; 144 Geesey, G.G., 73, 77, 82, 90, 111, 118; 139 See Costerton, J.W., 87, 118; 136 See Ladd, T. L, 116; 142 See Mittelman, M.W., 81; 144 See Platt, R.M., 93; 147 See Smith, J.J., 79, 92, 101; 150 Geiger, J.C., 286; 338 Gelder, S.R., 122; 139 See Jennings, J.B., 122; 141 Geldreich,E. E., 315; 338 Gelli, D.S., 309; 338 George, R.Y. See Menzies, R.J., 383; 489 Gérard, A. See Buestel, D., 334 Gerba, C.P., 316; 338 Gerhardt, P. See Scherrer, R., 124; 149
Gerlach, S.A., 464; 484 Gerrodette, V. See Dayton, P.K., 260 Gerson, T. See Patel, J.J., 88; 147 Ghiselin, M.T., 373, 374; 376 Ghuysen, J.M., 122; 139 Gianuca, N.M., 156, 159, 161, 166, 167; 172 Gibbs, D.L. See Franca, S.M. C., 338 Gibbs, P.E., 393, 409; 484 Gibor, A. See Pome-Fuller, M., 206; 271 Giere, O., 295; 338 Gieskes, W.W., 279; 338 Gilbert, P., 86; 139 Gilg, J.G., 14; 66 Gill, I.P. See Williams, S.L., 392; 495 Gillan, F.T. See Stanley, S.O., 462; 493 Gilles, K.A. See Dubois, M., 137 Gillespie, P.A. See Kaspar, H.F., 341 Glenn, A.R., 329; 338 Glocke, K. See Hoppe, H.-G., 458; 486 Gluth, G. See Hartwig, E.O., 444; 485 Glynn, P.W., 388, 431; 484 Gocke, K., 459; 484 Goldberg, E.G., 311; 338 Goldman, C.P. See Paerl, H.W., 111; 147 Goldman, J.C., 100; 139 Goldstein, I.J., 85; 139 Golikov, A.N., 474; 484 Golubic, S. See Paull, C.K., 346 Gomez, E.D. See Ong Che, R.G., 450, 451; 490 Gonzalez, E. See Ledo, A., 342 Gonzalez, N. See Tenore, K.R., 350 Gonzalez-Gurriaran, E. See Tenore, K.R., 350 Goodbody, I., 450; 484 Goodwin, C.P. See Andrews, W.H., 331 Goodyear, C.P. See Boyd, C.E., 329; 333 Gopalan, U.K. See Edwards, R.R. C., 483 Gopinathan, C.K., 389; 484 Gordon, M.E., See Liu, X.-W., 203; 266 Gore, R.H. See Moore, H.B., 489 Gosselck, F., 438, 453; 484, 485 Gotschlich, E.C., 95; 139 Gottfried, M., 106, 117; 139 Gottlieb, A. See Rosenberg, E., 85; 149 Gottlieb, M.S. See Shear, C.L., 313; 349 Goudey, C.L. See Chapman, A.R. O., 222, 248; 258 Gouleau, D. See Robert, J.M., 108; 148 Gourbault, N., 399; 485 Govan, J.R.W. See Hacking, A.J., 96; 140 Govindan Kutty, A.G., 402, 403, 449, 450; 485 Govindan, K., 417, 423, 424; 485 See Varshney, P.K., 423; 494 Goyal, S.M. See Gerba, C.P., 338 Graham, S. See Kirchman, D., 113; 142, 341 Grant, J., 101, 108, 109; 139 Grant, W.D., 108; 139
AUTHOR INDEX
Grassle, J.F., 291, 292; 338 See Van Dover, C.L., 152 Gray, G.W., 102, 103; 139 Gray, J. S., 383, 415; 485 Green, R.B. See Geesey, G.G., 82; 139 Green, R.H., 402; 485 Greenberg, E.P., 303, 315; 338 Greenberg, H. See Cross, G., 336 Greenwood, P.R. See Spiro, B., 349 Grelet, Y., 393, 398, 399, 401; 485 Griffin, M.R., 311; 339 Griffiths, C.L. See Newell, R.C., 327; 345 See Tarr, J.G., 407; 493 See Velimirov, B., 248; 275 Griffiths, P.R., 107; 140 Grimes, D.J., 307; 339 Grindley, J.R., 156; 172 Grischkowsky, R.S., 320, 323; 339 Grizel, H. See Bachere, E., 323; 332 See LeGall, G., 319; 342 See Mialhe, E., 344 Gross, J., 289; 339 Grund, D.W. See Garbary, D., 183; 262 Gruvel, A., 360; 376 Grygier, M.J., 353, 374, 375; 376, 377 Gschwend, P.M. See Morel, F.M. M., 112; 144 Guan, B. See He, C.B., 22; 66 Guan, B.X., 18, 24, 26, 29, 30, 31, 32, 36, 37, 63, 64; 66 See Liu, J.P., 64; 67 See Su, J.L., 11–71 Guckert, J.D. See Nichols, P.D., 145 Guillard, R.R.L., 284, 320; 339 Guiry, M.D., 186, 199; 262 Gulka,G., 319; 339 Gunn, R. See Wilson, R., 352 Gunnarsson, L.A.H. See Dahlbäck, B., 327, 328; 336 Gunnill, F.C., 178, 206, 229; 262 Gunter, G., 156, 167, 168; 172, 173 Guo, B.H., 36, 39, 41; 66 See Song, W.X., 41; 66 Gupta, T.R.C. See Ramachandra, U., 417; 491 Gutnick, D.L. See Rubinovitz, C., 91, 103; 149 Guzewich, J.J., 307, 312; 339 Guzmán del Pró, S.A., 195; 262 Hacking, A.J., 96; 140 Hackney, C.A. See Sobsey, M.D., 349 Hackney, C.R. See Cole, M.T., 335 Hada, H.S., 321; 339 Hage, E. See Rasmussen, L.P. D., 323; 347 Haider, K. See Martin, J., 121; 144 Hallam, N.D. See Forbes, M.A., 235; 262 Hamilton, J.K. See Dubois, M., 137 Hamilton, W.A., 74; 140 Hammond, L.S., 445, 446; 485 See Kenchington, R.A., 450, 451; 487
507
Hamons, F. See Kaneko, T., 320; 347 Hand, S.C. See Fisher, M.R., 295; 337 Handa, N., 99; 140 Handley, P.S. See Gilbert, P., 139 Hanna, M.O. See Peixotto, S.S., 347 Hannach, G., 183, 185; 262 Hansen, J.A., 392, 395, 399, 455, 459, 460, 463; 485 See Moriarty, D.J.W., 489 Hansen, J.E., 181, 183, 185; 262 Hansen, P.D. See Renwrantz, L., 324; 348 Hanson, R.B., See Alongi, D.M., 464; 480 See Rice, D.L., 121; 148 See Tenore, K.R., 151, 350 Hanzawa, Y. See Fujiwara, I., 31; 66 See Sawara, T., 36, 39, 41; 68 See Konaga, S., 48; 67 Hardy, F.G. See Ford, H., 192; 262 Harger, B.W. See Neushul, M., 269 Hargrave, B. See Schwinghamer, P., 475; 492 Hargrave, B.T., 329; 339 Hargraves, P.E., 455, 456, 459; 485 Harkantra, S.N., 392, 403, 404, 413, 417, 429, 434, 435, 441, 471, 473; 485 See Ansari, Z.A., 434; 480 See Parulekar, A.H., 471; 490 See Rodrigues, C.L., 434; 491 Harlin, M.M., 245; 262 Harper, D.E., 429, 436; 485 Harper, J.L., 190, 193, 216, 227, 237, 238, 240, 250; 262 See Vernet, P., 193; 275 Harris, R.H., 83; 140 Harrison, J. See Cross, G., 336 Harrison, P.J. See Lobban, C.S., 204, 207, 215, 221, 236; 266 Harrison, W.G. See Li, W.K.W., 343 Harrold, C., 236, 246, 247; 262, 263 Hartnoll, R.G. See Hawkins, S.J., 236, 246; 263 Hartog, C. den, 219; 263 Hartwig, E.O., 392, 395, 444; 485 Harvey, R.W., 80, 89, 105, 118, 127, 283; 140, 339 Hasegawa, Y., 200; 263 See Sanbonsuga, Y., 201; 271 Hasevlat, R.C. See Mathieson, A.C., 193; 267 Hashem, M.A. See Mohsen, A.F., 198; 268 Hashimoto, T. See Becking, L.B., 172 Haskin, E. See Dame, R.F., 326; 336 Hasting, A. See Levin, S.A., 216; 266 Hastings, J.W., 87; 140 Hasunuma, K., 14, 15; 66 See Uda, M., 14; 70 See White, W.B., 14; 70 Hatcher, B.G., 381, 383, 384, 423, 448; 485 Hatton, H., 251; 263
508
OCEANOGRAPHY AND MARINE BIOLOGY
Haug, A. See Myklestad, S., 99, 110; 145 See Paulsen, B.S., 99; 147 Haugan, B. See Novak, J.T., 102, 146 Haugen, E.M. See Murphy, L.S., 279; 345 Haven, D.S., 304, 327, 329; 339 See Perkins, F.O., 347 Hawkes, M.W., 209, 210; 263 Hawkins, C.M. See Schwinghamer, P., 475; 492 Hawkins, S.J., 228, 236, 247, 248; 263 Hay, C.H., 248; 263 Hay, M., 252; 263 Hay, M.E., 198, 240; 263 Haydon, D.A. See Aveyard, R., 81; 133 Hayes, C.E. See Goldstein, I.J., 85; 139 Hayes, M.O., 388, 389; 485 Hayward, A.C. See Moriarty, D.J. W., 106, 108; 145 He, C.B., 22; 66 Heath, E.C. See Troy, F.A., 98; 151 Hebel, D. See Knauer, G.A., 112; 142 Hebert, W.O. See Twedt, R.M., 351 Hecker, B. See Paull, C.K., 346 Hedges, J.I. See Rau, G.H., 292; 347 Hedgpeth, J.W., 155, 438; 173, 485 Heffernan, W.P., 303, 304, 305; 339 See Cabelli, V.J., 299, 300, 301, 302, 303, 304, 317; 334 Heip, C., 404, 406, 424, 426; 486 Heitz, J.R. See Chambers, J.E., 122; 135 Hellebust, J.A., 203; 263 Hennig, H.F.-K.O. See Eagle, G.A., 156, 159, 166, 169; 172 Henrichs, S.M., 100, 121, 125; 140 Henricksen, K., 328; 339 Henry, D.P., 353, 356; 377 See McLaughlin, P.A., 353, 356, 357; 378 Henry, M., 296; 339 See Hily, A., 292; 339 Hensey, M.P. See Rodhouse, P.G., 348 Henson, J.M. See Nichols, P.D., 145 Hermansson, M., 85; 140 See Kjelleberg, S., 85; 142 Hermosilla, J.G. See Gallardo, V.A., 484 Hernandez, J.F., 308, 316, 317; 339 Herry, A., 296; 339 See Le Pennec, M., 342 Hesp, P.A. See McLachlan, A., 156, 166, 170; 174 Hessler, R.R. See Sanders, H.L., 291; 348 Hicks, G.R.F., 109, 126; 140 Hidaka, T., 290; 339 Hidu, H., 284; 339 High, N. See Roberts, I., 148 Hill, B.J. See Wassenberg, T.J., 422; 495 Hill, G.C.J. See Stebbins, G.L., 180, 182, 184; 273 Hill, M.B., 420; 486 Hill, S., 87; 140
Hill, W.F. See Presnell, M.W., 310; 347 Hily, A., 292; 339, 340 See Le Pennec, M., 292; 342 Hilyard, A.L. See Carlson, D.J., 334 Hines, A.H. See Pearse, J.S., 248, 250; 270 Hines, M.E., 395; 486 Hinsch, G.W., 326; 340 Hirano, K. See Fujiwara, I., 31; 66 Ho, S.C. See Leong, T.S., 487 Hobbie, J., 118; 140 Hobbie, J.E., 329; 340 Hobson, L.A., 156; 173 Hodgkinson, M.C. See Sly, L.I., 82; 150 Hodson, R.E., 111; 140 See Tenore, K.R., 151 Høeg, J.T., 353, 356, 362, 363, 366, 372; 377 Hoek, C. van den, 178, 186, 218, 227; 263 Hoek, P.P.C., 360; 377 Hoeksema, B.W. See Breeman, A.M., 206; 257 Hoffman, A.J., 178, 189, 196, 197, 199, 200, 225, 226, 227, 228, 229, 238, 240, 253; 263 Holland, A.F., 108; 140 Hollingsworth, R.I. See Abe, M., 90; 132 Holm, R.F., 416, 419, 425; 486 Holmes, R.W., 157; 173 Holm-Hansen, O., 116; 140 Hommersand, M.H., 196; 263 See West, J.A., 178, 240; 275 Hongskul, V. See Menasveta, D., 476; 489 Honjo, T. See Yokote, M., 74, 99; 153 Hood, M.A., 309, 315, 316; 340 See Rodrick, G.E., 348 Hook, J.E. See Paull, C.K., 346 Hope, D.B. See Blaschko, H., 289; 333 Hopkinson, C.S. See Fallen, R.D., 121; 138 Hopner Petersen, G., 474, 476, 477; 486 Hoppe, H.-G., 458; 486 Hopper, B.E., 445; 486 Horan, N.J., 111; 140 Hori, T., 208, 210, 212; 263 Horsley, R.W., 85; 140 Horstman, G.A. See Hutchings, L., 170; 173 Howard, R.K. See Virnstein, R.W., 413; 494 Howland, K.H., 325; 340 See Cheng, T.C., 325; 334, 335 Hoyle, M.D., 185; 263 Hoyt, W.D., 202, 205; 264 Hruby, T., 228, 234, 237, 243, 249, 251, 252; 264 See Lewin, J., 157, 159, 160, 161, 162; 173 Hsiao, S.I.C., 183, 198; 264 Hsueh, Y., 42; 66
AUTHOR INDEX
Huang, J.W. See Cheng, T.C., 335 Huang, R., 236, 249, 252; 264 Huber, P.S. See Zambon, J.S., 153 Huchon, A., 308; 340 Hugh, R. See Tubiash, H.S., 319; 357 Hughs [sic], R.N. See Jones, D.A., 386, 391, 414; 486 Huh, O.K., 36, 41; 66 See Shim, T., 41; 69 Hui, E., 358; 377 Hulings, N.C., 400; 486 Humm, J.H. See Pearse, A.S., 155; 174 Humphrey, B.A., 85, 91, 92, 104; 140 See Kjelleberg, S., 85; 142 Humphris, S. See Van Dover, C.L., 152 Hung, T.C., 21, 22; 66 Hunt, D.A., 314; 340 Hunt, J. See Twedt, R.M., 357 Hunt, J.R. See Logan, B.E., 78, 79, 111; 143 Hunt, W.G. See Moriarty, D.J. W., 489 Hunte, M. See Hinsch, G.W., 326; 340 Hunter, A.C., 286 Hunter, J.R. See Brown, C.M., 118; 134 Huntsman, S.A., 99, 105; 140 Hurlburt, H.E., 22; 66 Hussong, D., 304, 305; 340 Huston, M., 413; 486 Hutchings, L., 170; 173 Hutchings, M.J. See Cousens, R., 249, 250; 259 Huttel, M., 446; 486 Ichikawa, A., 353, 373; 377 Ichiye, T., 41; 66 See Muneyama, K., 67 Ichson, W.D. See Franca, S.M. C., 335 Iglesias, J. See Tenore, K.R., 350 Ikeda, F., 122; 140 Illenberger, W.K. See McLachlan, A., 167; 174 Imbrie, J. See Newell, N.D., 390; 489 Ingole, B.S., 401; 486 See Ansari, Z.A., 400, 423; 480 Ingram, J.M. See Cheng, K.G., 78, 102; 135 Inoh, S., 238; 264 Inooka, S. See Nakamura, M., 345 Irvin, R.T. See Costerton, J.W., 76, 84, 94; 136 Irvine, L.M. See Farnham, W.F., 219; 261 Irving, L. See Cross, G., 336 See Scholander, P.F., 443; 492 Irwin, B. See Li, W.K. W., 343 Ishii, H., 60, 62; 66 See Guo, B.H., 36; 66 See Sekine, Y., 60; 68 Ishino, M., 64; 67 Ishizaki, H. See Kamihara, E., 67 See Konaga, S., 48, 63; 67 See Yuan, Y. C, 48, 49; 71 Istock, C.A., 184; 264 Ittekkot, V., 386, 388; 486
509
Iverson, R.L. See Moriarty, D.J.W., 458; 489 Jablonski, D., 451; 486 Jackson, J. B.C., 413; 486 Jacob, P.G., 389, 390; 486 Jacobson, M.A. See Geiger, J.C., 286; 338 Jacq, E., 280; 340 Jagtap, T.G. See Ansari, Z.A., 392, 393; 480 Jann, B. See Jann, K., 74, 86; 141 Jann, K., 74, 86, 95; 141 See Roberts, I., 148 See Schmidt, M.A., 95; 149 Jannasch, H.W., 82, 117; 141 See Belkin, S., 292; 332 Janowski, H. See Wilson, R., 352 Janssen, W.A., 303; 340 Jaramillo, E., 398, 409, 411; 486 Jarman, R.N. See Weiner, R.M., 152 Jarman, T.R., 76, 89, 98, 130; 141 See Hacking, A.J., 96; 140 See Mian, F.A., 102; 144 Jeanthon, C., 285, 323; 340 See Prieur, D., 293, 297; 347 See Samain, J.F., 348 Jefferey, W.H. See Paul, J.H., 116; 147 Jeffries,V.E., 320, 321; 340 Jeffreys, D.B. See Comar, P.G., 315; 335 Jennings, H.J., 107; 141 See Bishop, C.T., 107; 134 Jennings, J.B., 122; 141 Jensen, A. See Henriksen, K., 328; 339 Jensen, K.T., 120; 141 Jeppesen, M. See Riemann, B., 148 Jernakoff, P., 206, 229, 231, 236, 246, 247, 248; 264 See Underwood, A.J., 229, 236, 247; 274 Jiang, J.Z. See Su, J.L., 11–71 Johannes, R.E., 452; 486 See Hatcher, B.G., 381, 383, 423, 448; 485 John, D.M., 218; 264 Johnson, C.R., 246; 264 Johnson, H.M., 324; 340 Johnson, M.W. See Sverdrup, H.U., 14, 41; 69 Johnson, P.G. See Allan, G.G., 99, 105; 133 Johnson, P.W., 279; 340 Johnson, R.G., 327; 340 Johnstone, G.R., 185; 264 Johnstone, J., 312; 340 Joint, I.R., 279, 280; 340 Jollès, P., 283; 340 Jones, A.M. See Thomas, K.C., 308; 350 Jones, D.A., 386, 391, 409, 414, 420; 486 Jones, E.B.G. See Daniel, G.F., 99; 137 Jones, G.W. See Kjelleberg, S., 85; 142 Jones, H.C., 106; 141 Jones, L.G. See North, W.J., 217; 269
510
OCEANOGRAPHY AND MARINE BIOLOGY
Jones, R., 381, 473, 474, 476, 477; 486 Jones, R.S. See Linker, A., 122, 123; 143 Jones, W.E., 213, 222, 226, 239, 249; 264 Jones, W.E. See Moorjani, S., 239; 268 Jordan, T.E., 326; 340 Jørgensen, B.B., 87; 141 See Fenchel, T., 87; 138 See Revsbech, N.P., 114; 148 Jørgensen, C.B., 280; 341 Joseph, S.N., 307; 341 Joseph, S.W. See Kaper, J., 341 Joyce, G.H., 81, 93, 126, 128; 141 Jumars, P.A. See Plante, C.J., 88; 147 Juniper, S.K., 117, 120, 293; 141, 341 Jurgen, L. See Sieburth, J. McN., 285; 349 Kadko, D.C. See Kulm, L.D., 342 Kai, A. See Kokubo, Y., 341 Kain, J.M., 185, 195, 197, 200, 201, 213, 214, 228, 238, 241; 264 Kaliaperumal, N., 195; 264 See Umamaheswara Rao, M., 202; 274 Kalk, M. See MacNae, W., 395, 408, 409, 410; 488 Kam, S.P. See Leong, T.S., 487 Kamihara, E., 58, 59; 67 Kane, B.E. See Comar, P.G., 315; 335 Kaneko, T., 320; 341 Kaper, J., 309, 315; 341 Kaper, J.B. See Joseph, S.N., 341 Kapetsky, J.M., 421, 441; 487 Kaplan, D., 76, 79, 80, 82; 141 Kapraun, D.F., 185; 264 Karadogan, H. See Cheng, T.C., 335 Karl, D.M., 116, 458; 141, 487 Karlog, O. See Rasmussen, L.P.D., 323; 347 Kasinathan, R. See Fernando, S.A., 425; 484 Kasper, D.L. See Baker, C.J., 94; 133 Kaspar, H.F., 327, 328, 330; 341 Kastoro, W.W., 429, 435; 487 See Aswandy, I., 435; 481 Katada, M., 203; 265 Katti, R.J. See Ramachandra, U., 417; 491 Kauri, T., 114; 141 Kautsky, N., 328; 341 Kawabe, M., 54, 55, 56, 63; 67 Kawai, H., 16; 67 See Worthington, L.V., 47; 70 Kawashima, S., 200; 265 Kawatate, K. See Takematsu, M., 69 Kaysner, C.A. See Nolan, C.M., 346 See Weagant, S.D., 309, 310; 351 Keddy, P.A., 184; 265 Kefford, B., 83, 85; 141 Kellar, P.E. See Paerl, H.W., 87; 146, 147 Keller, B.D. See Dayton, P.K., 260 Kelly, C.B., 301, 341
Kelly, D.P. See Wood, A.P., 297; 352 Kelly, C.B., 301; 341 See Doering, P.H., 336 Kemp, P.F., 126, 464; 141, 487 Kemp, W.N., 330; 341 Kempe, S. See Bolin, B., 382; 481 Kenchington, R.A., 450, 451; 487 Kenk, V.C., 292; 341 Kenne, L., 89; 141 Kennedy, A.F.D., 79, 91, 92, 102, 107, 123, 127; 141 Kennelly, S.J., 181, 233, 235, 237, 246, 249, 251; 265 Kennikut II, M.C., 293; 341 See Brooks, J.M., 333 See Childress, J.J., 335 Keough, M.J., 229, 237; 265 Kessler, J.O., 225; 265 Ketner, P. See Bolin, B., 382; 481 Khaleafa, A.F. See Mohsen, A.F., 198; 268 Khan, S.A. See Fernando, S.A., 425; 484 Khaylov, K.M., 81; 141 Khfaji, A.J., 236; 265 Khoo, K.H. See Leong, T.S., 487 Kieras, J.H., 104; 142 Kilar, J.A. See Norall, T.T., 183; 269 Kilgen, M.G. See Cole, M.T., 335 Killian, C., 238; 265 Kim, D.H., 202, 203; 265 Kindley, M.J., 156, 159, 162, 164, 165, 166, 167, 169; 173 Kiørboe, T., 281; 341 Kirchman, D., 111, 113, 298; 142, 341 See Mitchell, R., 113; 142 Kirk, P.W. See Odum, W.E., 329; 346 Kirkman, H., 248; 265 Kitching, J.A. See Lilly, J.S., 266 Kjelleberg, S., 85; 142 See Kefford, B., 85; 141 See Wrangstadh, M., 85; 153 Kjosbakken, J. See Christensen, B.E., 82, 88, 94; 135 Klepal, W., 353–379; 353, 355, 356, 358, 359, 361, 362, 365, 367, 368, 369, 372, 373; 377, 378 See Barnes, H., 355, 356, 364, 370, 371; 375 See Munn, E.A., 355; 378 Klinger, R. See DeWreede, R., 179, 182, 185, 190, 192, 193; 260 Klumpp, D.W. See Stuart, V., 281; 350 Knaggs, F.W., 179; 265 Knauer, G.A., 112; 142 Knight, M., 233; 265 Knoppers, B.A. See Machado, E.C., 458, 459; 488 Knox, R.A., 382, 383; 487 Kobashi, T. See Sugita, H., 350 Kobayashi, T., 288; 341 Koburger, J.A., 314; 341 See Fraiser, M.B., 308, 311, 316; 338 Koehler, S.A. See Cheng, T.C., 335 Koepp, L.H. See Orr, T., 91; 146
AUTHOR INDEX
Koff, R.S. See Earampamoorthy, S., 306, 308; 336 Kofoed, L.H. See Kristensen, E., 456; 487 Kokubo, 309; 341 Konaga, S., 48, 63; 67 Kondalarao, B., 401, 402, 403, 418; 487 Kondritsky, A.V. See Neyman, A.A., 428, 434; 489 Konuma, H. See Kokubo, Y., 341 Konyecsni, W.M. See Deretic, V., 137 Kornberg, H.L., 97; 142 Kornegay, B.H., 114; 142 Koterayama, W. See Takematsu, M., 69 Kraay, G.W. See Gieskes, W.W., 279; 338 Kraeuter, I.N., 327, 329; 341 Kranck, K., 110; 142 Kremer, B.P., 214; 265 Krishnakumar, K. See Balakrishnan Nair, N., 481 Krishnamurthy, V., 195; 265 See Oza, R.M., 195; 270 Kristensen, E., 455, 456, 459; 487 Kristiansen, A., 200; 266 Kroen, W.K., 99, 110; 142 Krom, M. See Tenore, K.R., 350 Kruger, I., 157, 158; 173 Krüger, P., 359, 360; 378 Krumbein, W.E. See Aardema, B.W., 116; 132 Kuehner, E. See Gosselck, F., 438, 453; 485 Kudo, H., 114; 142 Kueh, C.S. W., 288, 302; 341 Kuenzler, E.J., 329; 341 Kugrens, P., 210; 266 Kulm, L.D., 293; 342 Kuramoto, S. See Nishida, H., 57, 61; 68 Kurata, A., 284; 342 Kurelec, B. See Muller, W.E.G., 145 Kurian, C.V., 435, 473; 487 Kuriyama, M. See Nishikawa, S., 91, 116; 146 Kushner, D.J. See Kauri, T., 114; 141 Kusuki, Y., 327; 342 Kutsuwada, K., 63; 67 Kuwahara, S. See Kobayashi, T., 341 Laborde, P. See Pérès, J.-M., 156, 174 Lackman, D.B. See Sevag, M.G., 103, 149 Ladd, J.N., 78; 142 Ladd, T.I., 116; 142 See Costerton, J.W., 136 Laetsch, W.M. See Larson, B., 107; 142 See Vreeland, V., 107; 142 Lahaye, M., 107; 142 Laloy, L., 353; 378 Lam, J. See Mackie, E.B., 106; 143 La Motta, E.J., 81, 114; 142 Lane, D.J. See Stahl, D.A., 349 Lang, C., 246; 266 Langdon, C.J., 284; 342
511
Langseth, M.G. See Kulm, L.D., 342 Larkum, A.W.D. See Kenelly, S.J., 181, 237; 265 Larsen, B. See Myklestad, S., 99; 145 See Paulsen, B.S., 99; 147 Larson, B., 107; 142 Larson, H.K. See Tsuda, R.T., 219; 274 Lartigue, D., 286; 342 Lasiak, T., 445; 487 Lasiak, T.A. See McLachlan, A., 174 Laubier, L., 293; 342 Laur, D.R. See Reed, D.C., 213, 216, 237; 271 Lawrence, J.M., 219, 236, 246; 266 Laws, E. See Bienfang, P.K., 110; 134 Lawson, C.J. See Williams, A.G., 94; 153 Lawson, G. See Townsend, C., 243; 274 Lean, D.R.S. See Leppard, G.G., 111; 142 See Murphy, T.P., 82; 145 LeChevallier, M.W., 115; 142 Le Coz, J.-R. See Maginot, M., 343 Le Coz, J.R. See Samain, J.F., 348 Le Cross Clark, W.E., 367; 378 Ledo, A., 302, 303; 342 Lee, C., 109; 142 See Hobbie, J., 118, 329; 140, 340 Lee, C.C., 444, 445, 447; 487 See Bunt, J.S., 456; 482 Lee, E. See Bunt, J.S., 456; 482 Lee II, H., 426, 429, 431, 450, 468; 487 Lee, J.J. See Tietjen, J.H., 87, 122; 151 Lee, J.V. See Hada, H.S., 339 Lee, J.S. See Vasconcelos, G.J., 300, 303; 351 Lee, R.G. See LeChevallier, M.W., 115; 142 Lee, T.N., 39; 67 See Atkinson, L.P., 36; 65 Lee, V. See Nixon, S.W., 346 LeGall, G., 319; 342 Le Gall, Y. See Floc’h, J.Y., 220; 261 See Plusquellec, A., 300; 347 Legeckis, R. See Lee, T.N., 39; 67 Legore, R.S. See Leong, T.S., 487 Leibovitz, L., 322; 342 See Elston, R., 320, 321; 336, 337 Leifson, E. See Tubiash, H.S., 320; 351 Leighton, D.L. See Pearse, J.S., 270 Leippe, M., 324; 342, 343 Leonard, R.L. See Paerl, H.W., 111; 147 Leong, T.S., 423, 424; 487 Leong, Y.K. See Leong, T.S., 487 Le Pennec, M., 292, 293, 296, 322; 342 See Fiala-Médioni, A., 294; 337 See Herry, A., 296; 339 See Hily, A., 292; 339, 340 Leppard, G.G., 111; 142 Lessie, T.G., 103; 142 Lester, J.N. See Brown, M.J., 79, 80, 81, 93, 101, 102, 126; 134 See Rudd, T., 80, 102, 126; 149
512
OCEANOGRAPHY AND MARINE BIOLOGY
Letolle, R. See Boulègue, J., 333 Leung, C., 302, 304; 343 Lev, O. See Sheintuch, M., 111; 150 Levering, P.R. See Cavanaugh, C.M., 334 Levin, S.A., 216; 266 Levine, M.M., 307; 343 Levings, S.C. See Garrity, S.D., 412; 484 Levinton, J.S., 329; 343 See Lopez, G.R., 122, 123, 125, 126; 143 Levy Guimaraes, C. See Blake, P., 332 Lewin, J., 156, 157, 159, 160, 161, 162, 164, 165, 166, 168, 170; 173 See Allan, G.G., 99, 105; 133 See Collos, Y., 162; 172 See Garver, J.L., 158, 160, 165, 166, 167; 172 See McLachlan, A., 156, 159, 161, 166, 167, 168, 170; 174 Lewin, J.C., 94, 99, 105, 110, 122; 143 Lewin, R.A., 99, 105; 143 See Lewin, J.C., 105; 143 See Woolery, M.L., 198; 276 Lewis, B.T. See Kulm, L.D., 342 Lewis, F.G. See Virnstein, R.W., 413; 494 Lewis, I.F., 205; 266 Lewis, J.B., 428, 438, 444, 448; 487 Lewis, S.M., 241; 266 Lewis, W.M. See Epp, R.W., 88; 138 Li, W.K.W., 279; 343 Liddle, L.B., 183; 266 Lidstrom, M. See Cavanaugh, C.M., 334 Lieb, S. See Wilson, R., 352 Liebezeit, G. See Meyer-Reil, L.A., 344 Lightfoot, E.N. See Mueller, J.A., 87, 114; 145 Lilly, J.S., 233; 266 Lim, D.B., 41; 67 Lin, K. See Guo, B.H., 36; 66 See Song, W.X., 41; 69 Lincoln, R.E. See Boyles, W.A., 162; 172 Lindberg, B. See Kenne, L., 89; 141 Lindberg, J.M. See Harlin, M.M., 245; 262 Linden, B.R. See Hunter, A. C, 286; 340 Lindén, O. See Mattsson, J., 330; 344 Linker, A., 122, 123; 143 See Evans, L.R., 102, 103; 138 Linley, E.A.S. See Newell, R.C., 111, 279; 145, 345 Lipovsky, V.P., 320; 343 Liqiang, H. See Rhoads, D.C., 491 Lis, H. See Sharon, N., 113, 150 Listen, J., 309; 343 See Baross, J., 309; 332 See Colwell, R.R., 286; 335 See Grischkowsky, R.S., 320, 323; 339 Litja, J.L. See Nolan, C.M., 346 Littler, D.S. See Littler, M.M., 184, 188, 189, 233, 250, 252; 266 Littler, M.M., 184, 187, 188, 189, 232, 250, 252; 266 Liu, C.T., 22; 67 Liu, J.P., 64; 67
Liu, R.J. See Liu, C.T., 22; 67 Liu, T.Y., See Gotschlich, E.C., 139 Liu, X.-W., 203; 266 Lobban, C.S., 204, 207, 215, 221, 236; 266 Lock, M.A., 78, 82, 118; 143 Lockman, H. See Kaper, J., 341 Lodeiros, C., 321; 343 Lodge, S.M. See Burrows, E.M., 247; 257 Loeb, G.I. See Mihm, J.W., 113; 144 See Wallace, G.T., 162; 175 Lofthouse, P.F., 210; 266 Logan, B.E., 78, 79, 111; 143 Lok Tan, T., 426, 431, 458; 487 Loka Bharathi, P.A. See Achuthankutty, C.T., 479 See Nair, S., 395, 402; 489 Longhurst, A.R., 381, 382, 385, 390, 415, 421, 422, 425, 426, 428, 437, 438, 440, 441, 442, 443, 452, 453, 476, 477; 487, 488 See Eager, E.W., 442; 484 Lonsdale, P., 291, 343 Loosanoff, V.L., 284; 343 Lopez, G.R., 122, 123, 125, 126, 283; 143, 343 See Levinton, J.S., 329; 343 Lopez, N.R. See Moore, H.B., 489 Lopez-Jamar, E. See Tenore, K.R., 350 Lorenz, M.G. See Aardema, B.W., 116; 132 Losee, E. See Brown, C., 320, 321, 323; 333 Loutit, M.W. See Bremer, P.J., 120; 134 See Patrick, F.M., 119; 147 Lovelace, T.E., 286; 343 Lowe, D.M. See Moore, M.N., 122, 323, 324, 326; 144, 345 Lowe-McConnell, R.H., 421, 442, 443; 488 Lowry, O.H., 104; 143 Loya, Y. See Richman, S., 117; 148 Lubchenco, J., 178, 184, 239, 244, 247; 266, 267 Lucas, A. See Le Pennec, M., 293; 342 Lucas, M.I. See Newell, R.C., 111, 279; 145 See Stuart, V., 279; 350 Lucu, C. See Muller, W.E. G., 145 Lujan, R.J. See Tsuda, R.T., 219; 274 Luke, R. See Cross, G., 336 Lund, D.B. See McFeters, G.A., 144 Lüning, K., 186, 198, 199, 200, 203, 238; 267 Luoma, S.N., 80, 81, 101; 143 See Harvey, R.W., 80, 89, 105, 118, 127, 283; 140, 339 Lupton, F.S., 86; 143 Lutz, R.A. See Jablonski, D., 451; 486 Lützen, J., 354; 378 See Bresciani, J., 373; 376 Luxoro, C., 183, 184; 267
AUTHOR INDEX
Lyles, C.H. See Gunter, G., 156, 167, 168; 173 Maccubin, A.E. See Hodson, R.E., 111; 140 See Tenore, K.R., 151 MacDonald, B.A., 282; 343 Machado, E.C., 458, 459; 488 Mackas, D. See Lewin, J., 157, 168; 173 MacKenzie, A.L. See Kaspar, H.F., 341 Mackie, E.B., 106; 143 Macko, S.A. See Brooks, J.M., 333 MacKowiack, P.A., 311, 316; 343 MacLeod, C.M. See Avery, O.T., 96; 133 MacMillan, C.B. See Dugan, P.R., 93, 126; 138 MacNae, W., 395, 408, 409, 410; 488 Madden, J.K. See Rees, D.A., 123; 148 Madden, J.M. See Twedt, R.M., 351 Madden, R.H., 312; 343 Madsen, B.L., 118; 143 Maginot, M., 283; 343 Maestrini, S.Y., See Berland, B.R., 332 Mahood, A. See Holmes, R.W., 157; 173 Mailloux, M. See Brisou, J., 333 Makarov, Y.N., 428, 453; 488 Maki, J.S., 113; 143 See Dillon, P.S., 113; 137 Maki, S.S. See Cavanaugh, C.M., 334 Manahan, D.T., 283, 284; 343 Mane, U.H. See Dhamne, K.P., 448; 483 See Talikhedkar, P.M., 445; 493 Maneval, D.R. See Joseph, S.N., 341 Mann, K.H., 112, 329; 143, 343 See Breen, P.A., 247; 257 See Johnson, C.R., 246; 264 See Lang, C., 246; 266 Mantyla, A.W., 16; 67 See Reid Jr, J.L., 14; 68 Marchalonis, J.J. See Vasta, G.R., 324; 351 Marcussen, B. See Riemann, B., 148 Marden, P. See Kjelleberg, S., 85; 142 Marjori, L., 317; 343 Markey, D.R., 210; 267 Markham, J.W., 253; 267 Markovitz, A., 96; 143 Marques, J. See Tiews, K., 442; 494 Marrie, T.J. See Costerton, J.W., 114; 136 Marsh, D.H., 121; 143 Marshall, K. C, 76, 83, 84, 93, 94, 106; 143, 144 See Fletcher, M., 83, 84; 139 See Hermansson, M., 85; 140 See Humphrey, B.A., 85, 91, 104; 140 See Kefford, B., 83, 85; 141 See Kjelleberg, S., 85; 142 See Lupton, F.S., 86; 143 Marten, G.G., 473, 474; 488 Martin, J., 121; 144 Martin, Y., 284, 287, 322; 343, 344 Martin-Bouyer, G., 311; 344 Martinez, E. See Santelices, B., 229, 231; 272
513
Martinez, J.C., 290; 344 Martosubroto, P. See Chullasorn, S., 421; 482 Marty, Y. See Samain, J.F., 348 Masaki, T., 251; 267 See Noro, T., 246; 269 Massalski, A. See Leppard, G.G., 111; 142 Massoth, G.J. See Cowen, J.P., 82, 117; 136 See Kulm, L.D., 342 Masuda, M. See Nakahara, H., 184; 268 Masuzawa, J., 14, 16, 35, 49; 67 Mathew, C.V. See Edwards, R.R.C., 483 Mathew, R., 448; 488 Mathieson, A.C., 183, 193, 267 See Burns, R.L., 191, 239; 257 See Niemeck, R.A., 193; 269 See Norall, T.T., 183; 269 See Norton, T.A., 220, 240; 269 See Shannon, R.K., 237; 273 See Sideman, E.J., 193; 273 See Tveter, E., 222, 249; 274 See Zechman, F.W., 226, 228; 276 Matson, J.V., 81, 114; 144 Matsushita, S. See Kokubo, Y., 341 Matsuuchi, L. See Corpe, W.A., 91, 106; 136 Mattsson, J., 330; 344 Maurer, D., 414, 417, 419, 425; 488 See Epifanio, C.E., 414; 483 May, G., 181, 183; 267 Mayasich, S.A., 290; 344 Mayer, A.G., 443, 444; 488 Mayer, L.M. See DeFlaun, M.F., 108; 137 Maynard-Smith, J., 374; 378 Mazières, J., 301; 344 Mazières, S. See Mazières, J., 344 McBride, D.L., 208, 209, 210, 211, 212, 214, 235; 267 McCandless, E.L., 183; 267 McCarty, M., 96; 144 See Avery, O.T., 96; 133 McCay, S.G. See Twedt, R.M., 351 McClain, J. See Tenore, K.R., 151, 350 McCorkle, F.M. See Chambers, J.E., 122; 135 McCourt, R.M., 194; 267 McCrae, J.M. See Owen, G., 280; 346 McCrae, S.K. See Albright, L.J., 121; 133 McDermid, K.J., 228; 267 McDonald, K.L. See Lewin, J., 157; 173 McDonald, T.J. See Kennicutt II, M.C., 341 McDonell, D.N. See Madden, R.H., 312; 343 McEldowney, S. See Fletcher, M., 83; 139 McFeters, G.A., 93, 107; 144 McGwynne, L. See McLachlan, A., 174 McHenery, J.G., 280, 281, 282, 283, 322; 344 See Birkbeck, T.H., 282, 322; 332 McIntyre, A.D., 396, 400; 488 See McLusky, D.S., 426; 488 See Munro, A.L. S., 474; 489
514
OCEANOGRAPHY AND MARINE BIOLOGY
McKinney, L.D. See Harper, D.E., 436; 485 McKinnon, A.A. See Dea, I.C. M., 94; 137 McLachlan, A., 155, 156, 159, 161, 166, 167, 168, 169, 170, 398, 401; 173, 174, 488 See Bate, G.C., 161, 171; 172 See Sloff, D.S., 156; 174 McLachlan, J., 197, 213, 236, 238, 239; 267, 268 See Bidwell, R.G.S., 214; 256 See Chen, L.C.-M., 183, 258 See Correa, J., 200; 259 See Garbary, D., 183; 262 See Smith, A.H., 250; 273 McLaughlin, P.A., 353, 356, 357; 378 See Henry, D.P., 353, 356; 377 McLusky, D.S., 399, 426, 448; 488 See Ansell, A.D., 465; 480 McManus, G.B., 279; 344 McMeekin, T.A. See Garland, C.D., 289; 338 McMillin, H.C. See Becking, L.B., 172 McNulty, J.K., 415, 423; 488, 489 Mead, D.J. See Frankel, L., 108; 139 Meade, R.H. See Milliman, J.D., 386, 388; 489 Means, E.G. See Ridgeway, H.F., 82; 148 Means, J.C, 112, 128; 144 Menasveta, D., 476; 489 Mencer, S. See Moss, B., 233; 268 Menezes, M.R. See Achuthankutty, C.T., 479 Mengus, B. See Martin, Y., 284; 344 Menon, N.R. See Mathew, R., 448; 488 Menzies, R.J., 383; 489 See Frankenberg, D., 427, 428; 484 Meseguer, I. See Anton, J., 89; 133 Metcalf, T.G., 303, 315, 316, 317; 344 See Vaughn, J.M., 313; 351 Métivier, B. See Okutani, T., 294; 346 Métivier, C. See Fiala-Médioni, A., 291, 292; 337 Metwalli, A. See Mohsen, A.F., 198; 268 Mével, G. See Prieur, D., 277–352 Meyer, J.L. See Findlay, S., 120; 138 Meyer-Reil, L.A., 279; 344 Meyers, T.R., 319; 344 Mialhe, E., 319; 344 See Le Gall, G., 319; 342 Mian, F.A., 102; 144 Miao, Y.T., 39; 67 Michael, L.P. See Cole, F.F., 279; 335 Miescier, J.J. See Andrews, W.H., 331 See Presnell, M.W., 310; 347 Mihm, J.W., 113; 144 Miita, T., 41, 42; 67 Millar, R.H., 284; 345 Millard, R.C. See Toole, J.M., 20; 69 Miller, M.A., 113; 144 Miller, M.L. See Koburger, J.A., 314; 341 Milligan, T.G. See Kranck, K., 110; 142 Milliman, J.D., 386, 388; 489
Mills, A.L. See Robertson, M.L., 131; 148 Mills, E.L. See Grant, J., 101, 108; 139 Mills, G.T. See Smith, E.E.B., 94; 150 Minami, H. See Kamihira, E., 67 Minear, R.A. See Cheng, K.G., 80; 135 Minet, J., 288, 302; 345 Mirelman, D. See McFeters, G.A., 144 Misdrop, R. See Vos, P.C., 99, 108; 152 Misra, T.K. See Deretic, V., 137 Mitchell, A.W. See Furnas, M.J., 473, 476; 484 Mitchell, C.T. See North, W.J., 217; 269 See Pearse, J.S., 270 Mitchell, R., 89, 113, 298; 144, 345 See Cavanaugh, C.M., 334 See Dillon, P.S., 113; 137 See Ducklow, H., 74, 117; 137 See Harris, R., 83; 140 See Kirchman, D., 111, 113, 298; 142, 341 See Maki, J.S., 113; 143 See Marshall, K.C., 83, 93, 106; 144 See McFeters, G.A., 144 Mitsuyasu, H. See Takematsu, M., 69 Mittelman, M.W., 81; 144 Miyazaki, K. See Nishio, T., 346 Moal, J. See Maginot, M., 343 See Samain, J.F., 348 Moeller, H.W. See Churchill, A.C., 219; 258 Mogi, A., 13; 67 Mohandas, A., 324, 326; 345 Møhlenberg, F., 280; 345 See Kiørboe, T., 281; 341 Mohsen, A.F., 198; 268 Mol, I. See Stegenga, H., 218; 273 Moldan, A.G.S. See Shannon, L.V., 167; 174 Montalva, S. See Santelices, B., 250; 271 Mooney, P.A., 198; 268 Moore, B., 307; 345 See Cross, G., 336 Moore, H.B., 228, 395, 412, 414, 443, 445, 448, 465, 466, 467; 268, 489 See McNulty, J.K., 415; 489 Moore, J.C. See Kulm, L.D., 342 Moore, M.N., 122, 323, 324, 326; 144, 345 See Bayne, C.J., 332 Moore, P.G., 178, 206; 268 Moorehouse, R., 92; 144 Moorjani, S., 239; 268 Moraga, D. See Le Pennec, M., 342 Morales-Alamo, D.S. See Haven, D.S., 327, 329; 339 Morel, F.M.M., 112; 144 Morell, J.M. See Corredor, J.E., 392, 395; 482 Mori, K., 326; 345 See Nakamura, M., 345 Moriarty, D.J.W., 106, 108, 109, 111, 118, 120, 391, 458, 460, 463; 144, 145, 489 See Decho, A.W., 94, 103, 105, 119, 125; 137 See Hansen, J.A., 399; 485
AUTHOR INDEX
Morita, R.Y., 125, 280; 145, 345 See Novitsky, J.A., 121; 146 Moriyasu, S., 41, 54; 67 Morris, E.J., 124; 145 Morris, E.R. See Rees, D.A., 123; 148 Morris, J.G. See Wilson, R., 352 Morrison, C., 319; 345 Morse, D.L. See Guzewich, J.J., 307, 312; 339 Morton, B., 280, 283, 290, 291; 345 See Ansell, A.D., 454; 480 See Leung, C., 343 Moss, B., 233; 268 See Sheader, A., 241; 273 Mossel, D.A.A. See Van den Broek, M.J. M., 309; 351 Mountford, R. See Roberts, I., 148 Moyano, H.I. See Gallardo, V.A., 484 Moyse, J., 375; 378 See Hui, E., 358; 377 Mshigeni, K., 185, 208; 268 Mueller, J.A., 87, 114; 145 Müller, D. See Bünning, E., 205; 257 Müller, D.G., 207; 268 Müller, I. See Müller, W.E.G., 145 Müller, S., 198; 268 Müller, W.E.G., 74, 86, 113; 145 Muneyama, K., 41; 67 Munn, E.A., 355, 370; 378 See Barnes, H., 356, 370, 371; 375 See Klepal, W., 365; 378 Munn, R. See Ruddel, C.L., 348 Munro, A.L. S., 474, 475; 489 Murchelano, R.A., 286; 345 Murphy, G.I., 452; 489 Murphy, L.S., 279; 345 Murphy, T.P., 82; 145 Murray, J.W. See Balistrieri, L., 83, 128; 133 Murray, R.G.E. See Beveridge, T.J., 82; 134 See Chester, I.R., 95; 135 Murray, S.N. See Littler, M.M., 187; 266 Murugan, T. See Divakaran, O., 420; 483 Musselman, J.F. See Andrews, W.H., 331 Mutch, R. See Geesey, G.G., 82; 139 Myer, A.E. See Zambon, J.S., 153 Myklestad, S., 99, 110; 145 Nagata, Y., 29, 30; 68 Nair, A. See Harkantra, S.N., 434; 485 Nair, N.B., 290; 345 See Govindan Kutty, A.G., 402, 403, 449, 450; 485 Nair, P.V.R., 471, 473; 489 Nair, S., 395, 402; 489 See Achuthankutty, C.T., 479 Nair, S.A. See Ansari, Z.A., 434; 480 See McLusky, D.S., 399; 488 Nakahara, H., 184; 268 Nakajima,T., 114; 145
515
Nakamori, J. See Nishio, T., 346 Nakamura, M., 325; 345 See Mori, K., 326; 345 Nakamura, Y., 183; 268 See Guo, B.H., 36; 66 Nalewajko, C. See Murphy, T.P., 82; 145 Nandi, S., 397, 402, 403; 489 Narain, A.S., 323; 345 Narayanan, B. See Ansell, A.D., 468; 480 See Trevallion, A., 399, 456; 494 Nascimento, O.R. See Vieira, A.A.H., 80, 107; 152 Nash, G.V. See Garland, C.D., 289; 338 Nasr, A.H., 198; 268 Nath, R.K., 107; 145 Natividad, M.R., 407; 489 Nealson, K.H. See Hastings, J.W., 87; 140 See Richardson, L.L., 114; 148 Nealson, N.H., 81; 145 Neelakantan, B. See Bhat, U.G., 425; 481 Nelson, D. See Dame, R.F., 326; 336 Nelson, D.C. See Belkin, S., 292; 332 Nelson, G. See Hutchings, L., 170; 173 Nelson, W.G. See Virnstein, R.W., 413; 494 Ness, G.E. See Hood, M.A., 309, 315; 340 Neu, T.R., 94; 145 Neumann, A.C., 108; 145 Neumann, C. See Paull, C.K., 346 Neushul, M., 217, 221, 222, 228, 232, 233, 235, 240; 268, 269 See Charters, A.C., 214, 235; 258 See Chi, E. Y., 210; 258 See Coon, D., 194, 221, 223; 259 See Norton, T.A., 240; 269 See Okuda,T., 194; 270 Nevo, Z. See Mitchell, R., 89; 144 Newell, N.D., 390, 438; 489 Newell, R., 327, 328, 329; 345 Newell, R.C., 111, 120, 125, 126, 279, 280, 281, 327, 328; 145, 345 See Seiderer, L.J., 125, 231, 279, 280, 281; 145, 272, 349 See Shumway, S.D., 349 See Stuart, V., 279; 350 Newell, S.Y. See Fallon, R.D., 121; 138 See Sherr, B.F., 285; 349 Newman, W.A., 353, 354, 372, 374, 375; 378 See Tomlinson, J.T., 354, 362; 379 Neyman, A.A., 428, 433, 434, 436, 471, 473; 489, 490 Ngan, Y., 183, 185, 194, 196, 203, 204, 212, 223, 230; 269 N’Guyen Thi Son, 303, 307, 308, 309, 310, 311; 346 Nichols, F.H., 326; 346 Nichols, J.A., 392, 425, 427, 429, 473; 490 Nichols, K. See Smith, A.H., 250; 273 Nichols, P.D., 107; 145
516
OCEANOGRAPHY AND MARINE BIOLOGY
Nichols-Driscoll, J.A., 392, 425, 427, 429; 490 Nicholson, J.A. M., 109; 145 Nickel, J.C. See Costerton, J.W., 136 Nicolos, J.-L., 320, 321; 346 See Prieur, D., 277–352 Nielsen, P. See Riemann, B., 148 Niemeck, R.A., 193; 269 Nienhuis, P.H., 279; 346 Niesenbaum, R.A., 192; 269 Nieuwolt, S., 382, 385; 490 Niino, H., 26, 42; 68 Nilsen, G., 203; 269 Nilsen, K.J. See Rhoads, D.C., 491 Nilsson-Cantell, C.A., 358, 359, 360; 378 Nimmons, M.J. See Characklis, W.G., 74; 135 Nishida, H., 55, 57, 59, 60, 61; 68 Nishikawa, S., 91, 116; 146 Nishimoto, K. See Okada, M., 52, 54; 68 Nishimura, O. See Gotschlich, E.C., 139 Nishio, T., 304; 346 Nishiyama, K. See Konaga, S., 48, 63; 67 Nishizawa, J. See Kamihara, E., 67 Nitani, H., 14, 17, 18, 19, 20, 21, 22, 23, 32, 44, 49; 68 Nivens, D.E. See Nichols, P.D., 145 Nixon, S.W., 326; 346 See Kelly, J.R., 330; 341 Nohr, O. See Kiørboe, T., 281; 341 Nolan, C.M., 311; 346 Nomura, T. See Mori, K., 326; 345 See Nakamura, M., 345 Norall, T.T., 183; 269 Norambuena, R. See Santelices, B., 192, 252; 272 Norberg, A.B., 76, 102; 146 Nordby, O. See Nielsen, G., 203; 269 Norkans, B. See Danielson, A., 84; 137 Noro, T., 246; 269 Norris, J.N. See Hay, M.E., 198, 241; 263 See Lewis, S.M., 241; 266 Norris, R.E. See Lewin, J., 157; 173 North, W.J., 180, 188, 215, 217; 269 See Anderson, E.K., 195, 226, 241; 256 See Pearse, J.S., 270 Northcraft, R.D., 228; 269 Norton, T.A., 192, 220, 233, 240; 269 See Deysher, L., 215, 221; 260 See Hruby, T., 228, 234, 237, 243, 249, 251, 252; 264 See Schonbeck, M.W., 241, 244; 272 See Watson, D.S., 206, 228; 275 Norval, M., 98; 146 Nott, A.L.J. See Boto, K.G., 464; 481 Nott, J.A. See Foster, B.A., 355; 376 Nottage, A.S., 320, 322; 346 See Birkbeck, T.H., 322; 332 Novaczek, I., 192, 194, 200, 241; 269 See Correa, J., 200; 259
Novak, A.F., 286; 346 See Lartigue, D., 286; 342 Novak, J.T., 102; 146 Novitsky, J.A., 116, 121; 146 See Karl, D.M., 458; 487 Oceanographic Atlas, 33, 34, 43; 68 Oceanographic Atlas of Ker, 46, 49, 50, 51, 52; 68 O’Colla, P., 122; 146 Odham, G., 86; 146 Odum, W.E., 329, 422; 346, 490 See Marsh, D.H., 121; 143 Oey, L.Y., 36; 68 Ogata, E., 244, 245; 270 Ogawa, Y. See Miao, Y.T., 41, 42; 67 Oger, C. See Hernandez, J.F., 308; 339 Ohno, M., 202, 205, 213, 214; 270 Ohta, S. See Laubier, L., 293; 342 Ojeda, P., 251, 253; 270 See Santelices, B., 238, 244, 248, 249, 250, 253; 272 Okada, M., 52, 54; 68 Okasaki, R.K. See Ruddel, C.L., 348 Okuda, T., 194; 270 Okutani, T., 294; 346 Olaniyan, C.I.O. See Fagade, S.O., 422; 483 Oliger, P. See Santelices, B., 250; 272 Olsen, G.J. See Stahl, D.A., 349 Olson, B.H. See Ridgeway, H.F., 82, 148 Oltmanns, F., 238; 270 Onate, J.A. See Estacion, J.S., 435; 483 Ong Che, R.G. 450, 451; 490 Oppenheimer, C.H., 288; 346 Oremland, R.S. See Fisher, C.R., 337 Oren, A., 114; 146 Orr, T., 91; 146 Orskov, F. See Jann, K., 141 Orskov, I. See Jann, K., 141 Osborn, M.J., 95, 98; 146 O’Shea, A.C. See Mathieson, A.C., 193; 267 Otsuka, K. See Ishino, M., 64; 67 Otto, S.V. See Tubiash, H.S., 319; 351 Oviatt, C.A. See Doering, P.H., 336 See Nixon, S.W., 346 Owen, G., 280; 346 Oza, R.M., 195, 198, 221; 270 Pace, G.W. See Jarman, T.R., 76, 98, 130; 141 Pace, M.L. See Cole, J.J., 130; 135 Pace, N.R. See Stahl, D.A., 349 Padilla, D., 251; 270 Paerl, H.W., 74, 76, 79, 83, 86, 87, 93, 101, 106, 109, 111, 114, 115, 118, 130, 131; 146, 147 Paffenhöfer, G.A. See Atkinson, L.P., 36; 65 Page, A., 319; 346
AUTHOR INDEX
Paine, R.T., 188, 189, 221, 226; 270 Painter, R.J., 99; 147 Palhof, B. See Greenberg, E.P., 303; 338 Palmer, L.M. See Grimes, D.J., 339 Palmer, S.J. See Scott, J.A., 80; 149 Pamatmat, M.M. See Tenore, K.R., 350 Pan, Y.Q. See Su, J.L., 36, 37, 38, 39, 40; 69 Pan, Z.Q., 47; 68 Panampunnayil, S.U. See Sankaranarayanan,V.N., 391, 392; 492 Panneerselvam, M. See Subramonian, T., 450; 493 Paoletti, A., 299, 304; 346 Parisi, E. See Osborn, M.J., 98; 145 Park, Y.H., 43; 68 Parke, M. See Knight, M., 233; 265 Parker, J.H. See Fazio, S.A., 100; 138 Parsons, A.B., 97, 102; 147 Parsons, M. See Pickmere, E.S., 183; 270 Parulekar, A.H., 416, 429, 430, 435, 471, 473; 490 See Ansari, Z.A., 392, 393, 402, 423, 429, 430, 434; 480 See Harkantra, S.N., 403, 404, 413, 417, 434, 435; 485 See Ingole, B.S., 40l; 486 See Rodrigues, C.L., 434; 491 Pasternak, F.A. See Neyman, A.A., 433; 490 Patel, B.S. See Crisp, D.J., 355, 368; 376 Patel, J.J., 88; 147 Paterson, D.M., 85, 99, 106, 108, 109; 147 Patnaik, S., 416, 418, 420; 490 Patrick, F.M., 119; 147 Patterson, J.W. See Cheng, K.G., 80; 135 Paul, J.H., 116; 147 See DeFlaun, M.F., 116; 137 Paull, C.K., 293; 346 Paulsen, B.S., 99; 147 Pauly, D., 420, 422, 426, 442, 443, 477; 490 See Longhurst, A.R., 381, 382, 385, 421, 426, 440, 441, 442, 452; 488 Pavoni, J.L., 91, 102, 116; 147 Paya, I., 206; 270 See Santelices, B., 206, 234; 272 Pazur, J.H., 102; 147 Peacock, M.G. See Elston, R.A., 319; 337 Pearlman-Kothencz, M. See Rothfield, L., 95; 149 Pearlmutter, N.L., 179, 220; 270 Pearse, A.S., 155; 174 Pearse, J. See Harrold, C., 236, 246, 247; 262 Pearse, J.S., 246, 248, 250, 451; 270, 490 Pearson, D. See Wright, R.T., 352 Pearson, T.H., 423, 424, 432; 490 Pedersen, P.M., 178, 239, 240; 270 See Kristiansen, A., 200; 265 Peeler, J.T. See Twedt, R.M., 351 Peer, D. See Schwinghamer, P., 475; 492
517
Peixotto, S.S., 310; 347 Percival, E. See Evans, L.R., 105; 138 Pérès, J.-M., 156; 174 Pérès, J.M., 234; 270 Perez, A. See Tenore, K.R., 350 Perez, R., 238; 270 Perissinotto, R. See Webb, P., 170; 175 Perkins, F.O., 300, 301, 302, 304, 305; 347 See Haven, D.S., 339 Perlin, A.S., 107; 147 Persing, C. See Wright, R.T., 352 Peterson, C.H. See Black, R., 412, 454; 481 Peterson, W.T. See McManus, G.B., 279; 344 Peyriere, M., 210, 235; 270 Pfister, R.M. See Dugan, P.R., 93, 126; 138 See Friedman, B.A., 111; 139 Philander, S.G., 382, 383, 385, 387; 490 Phillips, E.J.P. See Cohen, R.D.H., 335 Phillips, N.W., 125, 126; 147 Philpott, D.E. See Lewin, J.C., 105; 143 Pianka, E.R., 187; 270 Picard, J., 438; 490 Pichon, M., 408, 409, 410; 490 Pickett-Heaps, J.D. See Edgar, L.A., 85, 99, 109; 138 Pickmere, E.S., 183; 270 Pickrum, H.M. See Dugan, P.R., 79, 80, 93; 138 Picologlou, B.F. See Characklis, W.G., 74; 135 Pierson, B.F. See Nicholson, J.A.M., 109; 145 Pillai, V.K. See Nair, P.V.R., 471, 473; 489 Pilsbry, H.A., 358, 359, 360; 378 Pineda-Barrera, J. See Guzmán del Pró, S. A., 195; 262 Pinot, M., 310, 311, 312, 313, 314; 347 Plante, C.J., 88; 147 Plante-Cuny, M.-R., 455, 457; 491 Platt, R.M., 93, 102, 103, 104; 147 Platt, T. See Li, W.K.W., 343 Plusquellec, A., 299, 300, 301, 303, 304, 317, 318; 347 See Prieur, D., 277– 352 Pochon-Masson, J., 370; 378 See Bocquet-Védrine, J., 371; 376 See Turquier, Y., 370, 372; 379 Poiner, I.R. See Moriarty, D.J.W., 489 Polanshek, A. See West, J.A., 181; 275 Polanshek, A.R., 181; 271 Pollard, P.C. See Hansen, J.A., 399; 485 See Moriarty, D.J.W., 458, 460, 463; 489 Pollehne, F. See Balzer, W., 458; 481 See Smetacek, V., 76, 100; 150 Polne-Fuller, M., 206; 271 Polovina, J.J. See Marten, G.G., 473, 474; 488
518
OCEANOGRAPHY AND MARINE BIOLOGY
Pomeroy, L.R., 73, 109, 455, 459; 147, 491 See Biddanda, B.A., 87, 111, 279; 134, 332 See Hodson, R.E., 111; 140 Pomroy, A.J., See Joint, I.R., 279, 280; 340 Poole, N.J., 126; 147 Popham, J.D., 291; 347 Por, F.D., 414; 491 Poralla, K. See Neu, T.R., 94; 145 Porter, K.G., 87, 88; 147 Portnoy, B.C., 306, 316; 347 Portnoy, B.J. See MacKowiack, P.A., 311; 343 Powell, D.A., 88, 90, 92; 147 Prabhu, V., 471, 473; 491 Premuzic, E.T., 391, 392; 491 Presnell, M.W., 310; 347 See Andrews, W.H., 314; 331 Preston, E., 117; 148 Price, A.R.G. See Jones, D.A., 386, 391, 414; 486 Price, I.R. See Ngan, Y., 183, 185, 194, 196, 203, 204, 212, 223, 230; 269 Prieur, D., 277–352; 282, 283, 287, 288, 289, 293, 297, 327; 347 See Hily, A., 340 See Jacq, E., 280; 340 See Jeanthon, C., 285; 340 See Le Pennec, M., 292, 293, 322; 342 See Minet, J., 345 See Plusquellec, A., 347 See Samain, J.F., 348 Pringle, J.D., 204; 271 See Craigie, J.S., 183; 259 Probert, P.K., 476; 491 Provasoli, L., 240; 271 Prufert, L.E. See Paerl, H.W., 114; 146 Pu, Y.X. See Su, J.L., 11, 25; 69 Pueschel, C.M., 210, 211, 212; 271 Pujos, M. See Froidefond, J.M., 387; 484 Purcell, E.M., 110; 148 Purdy, E.G. See Newell, N.D., 390; 489 Pusey III, W.C. See Wantland, K.F., 390, 438; 495 Qasim, S.Z., 434, 456; 491 See Gopinathan, C.K., 389; 484 See Jacob, P.G., 389, 390; 486 Quadri, R.B., 314; 347 Rahim, A. See Dwivedi, S.N., 402; 483 Rajagopalan, K., 287; 347 Raju, P.V., 252; 271 Ramachandra, U., 417; 491 Ramamoorthi, K. See Sivakumar, V., 391; 492 Raman, A.V., 423; 491 Ramana Murty, K.V. See Kondalarao, B., 401, 402, 403; 487 Rama Sarma, D.V. See Sreeramamoorty, R., 415; 492 See Srinivasa Rao, D., 413; 493
Ramus, J., 198, 202, 219; 271 See Wassman, R., 219; 275 Randall, R.J. See Lowry, O.H., 104; 143 Rao, C.S.P., 240; 271 Rao, G., 395; 491 Rao, G.C., 434; 491 See Ganapati, P.N., 400, 402; 484 Rao, M.V.N. See Ganapati, P.N., 395; 484 Rao, P.S., 195; 271 Rao, V.N.R. See Lewin, J., 159, 160; 173 Rapean, J.C. See Miller, M.A., 113; 144 Raphael, Y.I. See Stephenson, W., 415; 493 Rapson, A.M., 156, 166, 170; 174 Rasmussen, L.P.D., 323, 324; 347 Rasmussen, M.B. See Henriksen, K., 328; 339 Rau,G. H., 291, 292; 347 Ray, S. See Collier, J., 355; 376 Rayburn, W.R. See Kroen, W.K., 99, 110; 142 Reade, A.E. See Boyle, C.D., 76, 78, 94, 102; 134 Rebers, P.A. See Dubois, M., 137 Reddy, M.P.M. See Prabhu, V., 471, 473; 491 Reeburg, W.S., 392; 491 Reed, D.C., 192, 213, 216, 228, 237, 248, 250; 271 See Harrold, C., 247; 263 Reekie, E.G., 193; 271 See Bazzaz, F.A., 193; 256 Rees, D.A., 74, 79, 80, 92, 94, 123, 126; 148 See Dea, I.C.M., 94; 137 Reid Jr, J.L., 14, 15; 68 See Mantyla, A.W., 16; 67 Reid, R.G.B., 289, 297; 347, 348 Reily, L.A. See Cole, J.J., 335 Reise, K., 475; 491 Reish, D. See Kirchman, D., 113; 142, 341 Relyea, D. See Elston, R., 337 Remsen, C.C. See Friedman, B.A., 111; 139 Renaud-Mornant, J. See Gourbault, N., 399; 485 Rendelman, J.A., 79; 148 Renger, E.H. See Eppley, R.W., 110; 138 Renwrantz, L., 323, 324, 325, 326; 348 See Leippe, M., 324; 342, 343 See Wittke, M., 324; 352 Renwrantz, L.R. See Cheng, T.C., 335 Retamal, M.A. See Gallardo, V.A., 484 Revsbech, N.P., 114; 148 See Jørgensen, B.B., 87; 141 Reynolds, C.S. See Walsby, A.E., 222, 223, 224; 275 Rheinheimer, G. See Wiese, W., 108; 153
AUTHOR INDEX
Rhoads, D.C., 108, 327, 329, 429, 436, 437; 148, 348, 491 See Tenore, K.R., 350 See Yingst, J.Y., 429, 430, 441, 473; 496 Rhodes, M.W. See Haven, D.S. 339 See Perkins, F.O., 347 Rice, C.E., 286; 348 Rice, D. L., 121, 125; 148 Rice, M.A., 283, 284; 348 Rice, M.E. See Chia, F.S., 297; 335 Richard, B. See Mazieres, J., 344 Richards, J. See Wu, R.S. S., 425; 495 Richards, R.C. See Paerl, H.W., 111; 147 Richardson, K. See Manahan, D.T., 283; 343 Richardson, L.L., 114; 148 Richman, S., 117; 148 Ridd, P., 387; 491 See Wolanski, E., 387; 495 Riddle, C.F. See Wilson, R., 352 Riddle, M.J., 392, 399; 491 Ridgeway, H.F., 82; 148 Riemann, B., 120; 148 Riemann, F., 76, 110; 148 Rietema, H., 199; 271 Righelato, R.C. See Jarman, T.R., 89; 141 See Mian, F.A., 102; 144 Riisgård, H.U., 280; 348 See Møhlenberg, F., 280; 345 Riou, F. See Pinot, M., 310; 347 Risk, M.J. See Tunnicliffe, V., 120; 151 Ritger, S.D. See Kulm, L.D., 342 Rittman, B.E. See Chang, H.T., 106; 135 Rittschof, D. See Maki, J.S., 113; 143 Robb, F.T. See Seiderer, L.J., 125; 149, 349 Robbins, J.B. See Gotschlich, E.C., 139 Robert, J.M., 108; 148 Roberts, A. See Wilson, R., 352 Roberts, I., 96; 148 Robertson, A.I. See Hatcher, B.G., 381, 383, 423, 448; 485 Robertson, J., 441; 491 Robertson, M.L., 131; 148 Robertson, P.B. See Shelton, C.R., 397, 413; 492 Robles, A. See Arntz, W.E., 407; 480 Rochas, C. See Lahaye, M., 107; 142 Roden, C.M. See Rodhouse, P.G., 348 Roden, L. See Kieras, J.H., 104; 142 Roderick, C.N. See Twedt, R.M., 351 Rodhouse, P.G., 328; 348 Rodrick, G.E., 315, 325, 326; 348 See Cheng, T.C., 335 See Hood, M.A., 309; 340 Rodrigues, C.L., 429, 430, 434, 473; 491 See Ansari, Z.A., 480 Rodriguez, G., 395, 410, 419; 491 Rodriguez-Valera, F. See Anton, J., 89; 133 Rojas, G. See Gocke, K., 459; 484
519
Roland, G. See Brown, C., 322; 334 Rollins, D.M. See Grimes, D.J., 339 Roman, M.R. See Gottfried, M., 106, 117; 139 Romankevich, E.A., 391; 491 Romano, J.-C. See Peres, J.-M., 156; 174 Romea, R.D. See Hsueh, Y., 42; 66 Romer, G.S., 166, 170; 174 Rona, P.A. See Van Dover, C.L., 152 Ronquillo, I.A. See Tiews, K., 442; 494 Roper, E.H. See Rice, D.L., 125; 148 Rosebrough, N.J. See Lowry, O.H., 104; 143 Rosen, M.W., 74, 87; 149 Rosenberg, E., 85; 149 See Rubinovitz, C., 91, 103; 149 See Sar, N., 74, 87, 103; 149 See Shoham, Y., 123; 150 Rosenberg, F.A., 290; 348 See Cutter, J.M., 290; 336 Rosenberg, M. See Rosenberg, E., 85; 149 Rosenberg, M.L. See Blake, P., 332 Rosenberg, R., 392, 423, 425, 427, 429, 432, 471, 473; 491, 492 See Pearson, T.H., 423, 424, 432; 490 Rosenthal, R. See Dayton, P.K., 260 Rosenthal, R.J., 248, 250; 271 Roszak, D.B. See Grimes, D.J., 339 Roth, I.L., 74, 106, 107; 149 See Jones, H.C., 106; 141 Rothfield, L., 95; 149 Roughgarden, J. See Gaines, S., 231; 262 See Gaines, S.D., 231; 262 Round, F.E., 99; 149 Rounick, J.S., 118; 149 Rowe, G.T., 426, 427, 428, 470, 471; 492 See Menzies, R.J., 383; 489 See Nichols, J.A., 392, 429, 473; 490 See Smith, K.L., 431; 492 Rowe, J.J. See Ventullo, A.D., 114; 152 Rowse, A.J., 303, 304, 305; 348 Ruano, F. See Mialhe, E., 344 Rubin, E. See Sheintuch, M., 111; 150 Rubin, R.W. See Webster, D.R., 85, 100, 109; 152 Rubinovitz, C., 91, 103, 104; 149 Rublee, P. See Ferguson, R.L., 279; 337 Rudd, T., 80, 102, 126; 149 Ruddel, C.L., 323; 348 Ruger, H.-J. See Lok Tan, T., 426, 431, 458; 487 Rugh, W.D. See Kulm, L.D., 342 Russell, G., 220; 271 Russell-Hunter, W.D., 329; 348 Russo, D.J. See Brown, C., 322; 334 Ruswahyuni See Warwick, R.M., 429, 435; 495 Ryan, J.H. See Rodhouse, P.G., 348 Ryland, J.S. See Crisp, D.J., 298; 336 Saiki, M., 31, 63, 64; 68 Saito, K. See Hidaka, T., 290
520
OCEANOGRAPHY AND MARINE BIOLOGY
Saitoh, S. See Muneyama, K., 67 Sakasaki, R. See Kobayashi, T., 341 See Tubiash, H.S., 321; 351 Sakuma, H. See Gelli, D.S., 309; 338 Salaun, M. See Samain, J.F., 348 Salton, M.R. J., 283; 348 Salzen, E.A., 443; 492 Salzer, R.R. See Harper, D.E., 436; 485 Salzwedel, H. See Tarazona, J., 432; 493 Samain, J.F., 285; 348 See Maginot, M., 343 Samuels, P. See Franca, S.M.C., 338 San Clemente, C.L. See Usui, Y., 91; 152 Sanbonsuga, Y., 201; 271 Sanders, H.L., 291, 413; 348, 492 Sanders, W.M., 87, 114; 149 See Jones, H.C., 106; 141 Sand-Jensen, K. See Vermaat, J.E., 190; 275 Sandstrom, M.W. See Ridd, P., 387; 491 See Ullman, W.J., 392, 393, 395; 494 Sanford, L.P. See Grant, W.D., 108; 139 Sankaranarayanan, V.N., 391, 392; 492 See Ansell, A.D., 480 Santelices, B., 177–276; 179, 188, 192, 197, 198, 206, 229, 231, 234, 236, 238, 244, 248, 249, 251, 252, 253; 271, 272 See Buschmann, A., 202, 205, 206, 219, 229; 257 See Correa, J., 238, 239; 259 See Hannach, G., 183, 185; 262 See Hoffman, A.J., 238, 240, 253; 263 See Luxoro, C., 183, 184; 267 See Ojeda, P., 251, 252; 270 See Paya, L, 206; 270 Sar, N., 74, 87, 103; 149 Sarachik, E.S. See Cane, M.A., 382, 383, 385; 482 Sarangi, N. See Datta, N.C., 417, 425; 482 Saraswathy, M. See Nair, N.B., 290; 345 Sasaki, Y. See Muneyama, K., 67 Sasekumar, A. See Chong, V.C., 422; 482 Sato, T. See Ikeda, F., 140 Saunders, P.T., 114; 149 Savage, D.C., 74, 85; 149 Savich, M.S., 428, 434, 471, 473; 492 Sawada, T., 202; 272 Sawara,T., 36, 39, 41; 68 Sawyer, W.H. See Baldo, B.A., 332 Scammen, R.L. See Kulm, L.D., 342 Scantlon, J.A. See Carlton, J.F., 219; 257 Scarlato, O.A. See Golikov, A.N., 474; 484 Schaefer, C.T. See Lewin, J., 156, 161, 165, 166; 173 Scheltema, R.S., 298; 348 Scherrer, R., 124; 149 Schiel, D.R., 192, 193, 194, 249, 250; 272 See Foster, M.S., 188, 250; 262 Schiemer, F. See Wieser, W., 444; 495 Schmidt, M.A., 95; 149
Schmiede, P. See Santelices, B., 189, 248; 271 Schnal, R. See Cross, G., 336 Schneider, K.F. See Jann, K., 141 Schoenberg, D.A. See Cheng, T.C., 334 Scholander, P.F., 443, 446; 492 Schonbeck, M.W., 241, 244, 247; 272 Schrohenloher, R.A. See Acton, R.T., 330 Schubert, H., 279; 348 Schubert, R.H.W. See McFeters, G.A., 144 Schultze, S. See Ferris, F.G., 138 Schulz, D. See Drebes, G., 157, 158; 172 Schwarzmann, S., 86; 149 Schweimanns, M., 295; 349 Schwinghamer, P., 475; 492 Scoditti, P.M. See Bianchi, A.J., 332 Scoffin, G.P. See Neumann, A.C., 108; 145 Scott, J.A., 80; 149 Scott, J.M. See Millar, R.H., 284; 345 Scott, W.E. See Rees, D.A., 92; 148 Scullard, C. See Bayne, B.L., 326; 332 Searles, R.B., 182; 272 See Amsler, C.D., 226, 229; 256 See Lewis, S.M., 241; 266 Segall, A.M. See Weiner, R.M., 298; 352 Seiderer, L.J., 125, 231, 279, 280, 281, 282; 149, 272, 349 Seidler, R.J. See Tison, D.L., 321; 350 Seki, H., 131; 149 Sekine, Y., 52, 53, 54, 60; 68, 69 See Ishii, H., 60; 66 Sellwood, B.W., 390, 393; 492 Seoane-Camba, J., 220; 272, 273 Seshappa, G., 251, 386, 387, 389, 428, 435; 273, 492 Sevag, M.G., 103; 149 Shanks, A.L. See Silver, M.W., 112; 150 Shannon, L.V., 167; 174 Shannon, R.K., 237; 273 Sharon, N., 86, 113; 149 Sharp, G.D., 388, 421, 441, 443, 476; 492 Sharp, J. See Holm-Hansen, O., 116; 140 Sharp, J.H., 112; 150 Shaw, M. See Christie, A.O., 210, 211, 215, 235; 258 Sheader,A., 241; 273 See Moss, B., 233; 268 Shear, C L., 313; 349 Sheintuch, M., 111; 150 Shelton, C.R., 397, 413; 492 Sherr, B.F., 285; 349 Sherr, E.B., 106, 112, 119; 150 See Sherr, B.F., 285; 349 Sherwood, H.P. See Clegg, F.L., 315; 335 Sherwood, J.E., 86, 90; 150 See Abe, M., 90; 132 Shibao, Y. See Yamagata, T., 64; 70 Shibata, A., 36; 69 Shiewer, U. See Schubert, H., 279; 348
AUTHOR INDEX
Shilo, M. See Fattom, A., 85; 138 Shim, T., 41; 69 Shin, P.K. S., 398, 413, 425, 429, 435; 492 See Thompson, G.B., 423; 494 Shipman, J.W. See Mathieson, A.C., 193; 267 Shoham, Y., 123; 150 Shoji, D., 52, 53; 69 Short, A.D., 168; 174 Shortridge, K.F. See Leung, C., 343 Shum, G. See Morrison, C., 319; 345 Shumway, S.D., 281; 349 Shuto, H. See Ikeda, F., 140 Sibbald, M.J., 87; 150 Sibuet, M. See Juniper, S.K., 293; 341 See Laubier, L., 293; 342 Sideman, E.J., 193; 273 Siebers, D., 125; 150 Sieburth, J. McN., 74, 108, 285; 150, 349 See Conover, J.T., 236; 259 See Johnson, P.W., 279; 340 Siegismund, H.R. See Jensen, K.T., 120; 141 Sigerfoos, C.P., 290; 349 Sikes, E. See Paull, C.K., 346 Silva, A. See Bolinches, J., 333 Silver, M.W., 110, 112; 150 See Cowen, J.P., 82, 111, 117, 126; 137 Silver, R.P., 96; 150 Silver, S. See Summers, A.O., 82; 151 Silverman, M. See Bartlett, D.H., 96; 133 Silverthorne, W. See Barilotti, D.C., 240; 256 Singbal, S.Y.S. See Parulekar, A.H., 473; 490 Singla, C.L. See De Burgh, M.E., 292; 336 Singleton, F.L. See Grimes, D.J., 339 Sivadas, P. See Ansell, A.D., 468; 480 See Trevallion, A., 399, 456; 494 Sivakumar, V., 391; 492 Sivalingam, P.M. See Rajagopalan, K., 287; 347 Siva Rama Sarma, N., 400, 402, 403; 492 Skubich, M. See Durand, R.J., 414; 483 Skyring, G.W. See Moriarty, D.J. W., 489 Slanetz, L.W., 301, 315, 316, 317; 344 See Metcalf, T.G., 303; 349 Sloane, J.F. See Lilly, J.S., 266 Slobodkin, L.B. See Richman, S., 117; 148 Slocombe, S. See Jarman, T.R., 89; 141 Slocum, C.J., 178, 188, 239; 273 See Paine, R.T., 189; 270 Sloff, D.S., 156, 159, 162, 164, 165, 166; 174 Sloneker, J.H. See Huntsman, S.A., 99, 105; 140 Slots, J. See Zambon, J.S., 153 Sly, L.I., 82; 150 Smayda, T.J., 222, 224, 225; 273
521
Smetacek, V., 76, 100; 150 See Bodungen, B. von, 110; 134 See Sieburth, J. McN., 285, 349 Smetacek, V.S., 110, 130; 150 Smidsrod, O., 91, 94; 150 See Christensen, B.E., 82, 88, 94; 135 Smith, A.H., 250; 273 Smith, B.D., 103, 249, 253; 150, 273 Smith, E.E.B., 94; 150 Smith, F. See Dubois, M., 137 Smith, G., 353, 378 Smith, G.M., 202; 273 Smith, I.C.P. See Jennings, H.J., 107; 141 Smith, J.C. See Li, W.K., 343 Smith, J.J., 79, 92, 101; 150 Smith, K.L., 428, 431, 459; 492 See Frankenberg, D., 329; 338 Smith, P.J. See Findlay, S., 120; 138 Smith, R., 241; 273 Smolens, J. See Sevag, M.G., 103; 149 Smucker, R.A. See Mayasich, S.A., 290; 344 Scares, Ferreira, P. See Blake, P., 332 Sobsey, M.D., 315, 349 Sokolova, M.M. See Neyman, A.A., 433; 490 Solomon, H., 53, 57; 69 Somero, G.N. See Felbeck, H., 292; 337 Somerville, C.C. See Weiner, R.M., 152 Sonea,S., 117; 150 Song, W.X., 41; 69 See Guo, B.H., 36; 66 Sorokin, Y. I, 278, 280; 349 Sournia, A., 222; 273 Sousa, W.P., 226, 242; 273 South, E.R. See Hay, C.H., 248; 263 Southward, A.J., 355; 378 See Crisp, D.J., 355; 376 See Dando, P.R., 295, 296; 336 See Spiro, B., 349 Southward, E.C., 296; 349 See Dando, P.R., 295; 336 Souza-Lima, Y. See Peres, J.-M., 156; 174 Sowers, T. See Doering, P.H., 336 Soyer, J., 296, 297; 349 Soyer, L. See Bouvy, M., 333 Soyer-Gobillard, M.O. See Bouvy, M., 333 See Soyer, J., 349 Spaans, A.L. See Swennen, C., 409; 493 Sparck, R., 426, 428; 492 Sparks, A.K. See Colwell, R.R., 319; 335 Speck, M.L. See Sobsey, M.D., 349 Spight, T.M., 451; 492 Spira, W.N. See Joseph, S.N., 341 Spiro, B., 296; 349 Spiro, R.G., 101, 103; 150 Spite, G.T., 311; 349 Springer, S. See Hunt, D.A., 314; 340 Sreenivasa Rao, P., 198; 273 Sreeramamoorty, R., 415; 492 Srinivasa Rao, D., 413; 493 Srna, R.F., 326; 349
522
OCEANOGRAPHY AND MARINE BIOLOGY
Stahl, D.A., 297; 349 Stahmer, A. See Renwrantz, L., 323, 324, 325, 326; 348 Stanier, R.Y., 87; 150 Stanley, K.W. See Slanetz, L.W., 349 Stanley, S.O., 462, 463, 465; 493 Stebbins, G.L., 180, 182, 184; 273 Steele, D.H., 426, 451; 493 Steele, J.H., 399, 469, 474, 475; 493 Stegenga, H., 218; 273 Stein, D.C. See Weiner, R.M., 152 Stein, J.L., 120; 150 Stemmler, J. See Hada, H.S., 339 Steneck, R.S., 188, 202, 229, 236; 273 Stephens, G.C., 284; 349 See Rice, M.A., 283; 348 Stephenson, W., 415, 419, 435; 493 Sterritt, R.M. See Rudd, T., 80, 102, 126; 149 Stevens, S.A., 326; 350 Steward, M.G., 283; 350 Stewart, F.H., 360, 361; 378 Stewart,G. S., 116; 151 Stick, R.V. See Baldo, B.A., 332 Stirling, A., 399, 474; 493 See Achuthankutty, C.T., 479 See Ansell, A.D., 465; 480 See McLusky, D.S., 399, 448; 488 Stolz, J.F. See Nicholson, J.A. M., 109; 145 Stolzle, K.A. See Novak, A.F., 286; 346 Stommel, H., 12; 69 Stone, R.L. See Barnes, H., 366, 368; 376 Stoner, A.W., 422; 493 See Buchanan, B.A., 422; 481 Stout, R. See Marshall, K.C., 83, 93, 106; 144 Strathmann, R. See Coles, S.L., 93, 117, 127; 136 Strominger, J.L. See Ghuysen, J.M., 122; 139 Stryker, S. See Wilson, R., 352 Stuart, D.G. See McFeters, G.A., 93; 144 Stuart, F. See Cole, F.F., 279; 335 Stuart, V., 279, 281, 327, 328, 329; 350 Stumm, W. See Busch, P.L., 74, 109, 111; 135 Su, J.L., 11–71; 11, 24, 25, 26, 36, 37, 38, 39, 40; 69 See Miao, Y.T., 39; 67 See Wang, K.S., 36; 70 See Wang,W., 37, 41; 70 See Yuan, Y.C., 25, 39, 42, 43; 71 Subbarangaiah, G. See Umamaheswara Rao, M., 202, 203, 204; 274 Subba Rao, D.V. See Li, W.K. W., 343 Subramoniam, T., 450; 493 See Varadarajan, S., 450; 494 Suess, E. See Kulm, L.D., 342 Suginohara, N. See Yasuda, I., 62; 70 Sugita, H., 287, 300; 350 Suhara, T. See Takematsu, M., 69
Sulaiman, H. See Leong, T.S., 487 Sullivan, J.T. See Cheng, T. C, 334 Summer, C.E. See Garland, C.D., 338 Summers, A.O., 82; 151 Sundene, O., 226; 273 Sundin, P. See Odham, G., 146 Sutcliffe, J., 99; 151 Sutcliffe, W.H. See Holm-Hansen, O., 116; 140 Sutherland, I.W., 76, 78, 79, 84, 85, 88, 89, 90, 91, 92, 93, 94, 95, 97, 98, 99, 102, 104, 122. 123; 151 See Kennedy, A.F. D., 79, 91, 92, 102, 107, 123. 127; 141 See Norval, M., 98; 146 Suto, S., 195, 202, 203, 204, 213, 214, 215; 273 Svane, L, 353; 378 Svedelius, N., 181; 273 Sverdrup, H.U., 14, 41; 69 Swart, D.H., 167; 174 Sweeney, B.M., 204; 273 See Anderson, L.W. J., 110; 133 Swennen, C., 397, 409; 493 Symons, J.L., 286; 350 Szöllösi,A., 371; 379 Szyper, J. See Bienfang, P.K., 110; 134 Tachibana, T. See Gelli, D.S., 309; 338 Taft, B.A., 47, 48, 49; 69 Tago,Y., 89, 102, 111; 151 Taira, K. See Fukasawa, M., 47; 66 Takematsu, M., 48; 69 Takeoka, H., 64, 65; 69 Takeshita, K. See Nagata, Y., 29; 68 Talbot, M.M. B., 155–175; 156, 157, 159, 160, 161, 162, 164, 165, 166, 167, 169, 170; 174, 175 Talikhedkar, P.M., 445; 493 Tamplin, M. See Rodrick, G.E., 348 Tamplin, M.L. See Grimes, D.J., 339 Tan, G.T. See Leong, T.S., 487 Tanaami, H. See Sugita, H., 350 Tanaka, T., 107; 151 See McFeters, G.A., 144 Tanikawa, E., 286; 350 Tanner, C.E., 240; 274 Tarazona, J., 432, 433; 493 See Arntz, W.E., 407; 480 See Rosenberg, R., 492 Tarr, J.G., 398, 401, 407, 409, 411; 493 Tarr, R. See Hutchings, L., 170; 173 Taylor, A.R. A. See Chen, L.C.-M., 210; 258 Taylor, F.J. R., 158; 175 See Grindley, J.R., 156; 172 Taylor, I.W. F. See Hacking, A.J., 96; 140 Taylor, J.D., 393; 493 Taylor, J.E., 219; 274 Taylor, P.R. See Littler, M.M., 184, 252; 266 Tchernia, P., 14; 69
AUTHOR INDEX
Tenney, M.W. See Pavoni, J.L., 91, 102, 116; 147 Tenore, K.R., 126, 279, 281, 285, 327, 330, 383; 151, 550, 493 Tenover, F.C. See Nolan, C.M., 346 Teramoto, T., 11, 52; 69 See Fukasawa, M., 47; 66 Terwilliger, N.B. See Dando, P.R., 336 Terwilliger, R.C. See Dando, P.R., 336 Tettelbach, L.P. See Brown, C., 321, 322, 323; 334 Thangaraj, G.S. See Sivakumar, V., 391; 492 Thayer, L.A., 156, 161; 175 Theede, H., 329; 350 Thiel, H., 426, 427, 430, 431; 493 Thiriot-Quiévreux, C. See Bouvy, M., 333 See Soyer, J., 349 Thistle, D. See Baird, B.H., 105, 119; 133 Thorn, D. See Rees, D.A., 123; 148 Thomas, K.C., 308; 350 Thomassin, B.A. See Daumas, R., 117; 137 See Grelet, Y., 485 Thompson, G.B., 423; 494 See Shin, P.K. S., 425, 429, 435; 492 Thompson, J.A. J. See Juniper, S.K., 117; 141 Thompson, J.D. See Hurlburt, H.E., 22; 66 Thompson, R.J. See Bayne, C.J., 332 Thompson, W.K., 309; 350 Thornburg, T.M. See Kulm, L.D., 342 Thorson, G., 383, 413, 415, 419, 438, 451; 494 Thurber, D.L. See Newell, N.D., 390; 489 Thurow, H. See Bayer, M.E., 95, 106; 133 Tiedge, H. See Meyer-Reil, L.A., 344 Tietjen, J. See Tenore, K.R., 350 Tietjen, J.H., 87, 122; 151 Tiews, K., 442; 494 Tilzer, M.M. See Bodungen, B. von, 110; 134 Timmis, K. See Roberts, L, 148 Timoney, J.F., 300, 301, 302; 350 Tinley, K.L., 159; 175 Tirendi, F. See Alongi, D.M., 426, 460, 463; 479 Tison, D.L., 321; 350 Toba, Y. See Ishii, H., 60; 66 See Sekine, Y., 53, 54, 60; 68, 69 Tokida, J., 240; 274 Tolman, C.F. See Becking, L.B., 172 Tominaga, M., 21; 69 Tomita, K. See Ikeda, F., 140 Tomlinson, J., 353, 374; 379 Tomlinson, J.T., 354, 362, 363, 366, 372; 379 Tonn, S.J., 76, 78; 151 Toole, J.M., 20; 69
523
Toranzo, A.E. See Bolinches, J., 333 See Ledo, A., 342 See Lodeiros, C., 343 Tosteson, T.R., 84, 102, 107, 113; 151 See Zaidi, R., 107; 153 Toth, R., 208, 210, 211; 274 Townsend, C, 243; 274 Townsend, D.W. See Carlson, D.J., 334 Tozawa, Y. See Muneyama, K., 67 Trenholm, D.A. See Thompson, W.K., 309; 350 Trent, J.D. See Silver, M.W., 112; 150 Trevallion, A., 399, 408, 409, 411, 456; 494 See Ansell, A.D., 399, 452, 453, 465, 468, 469; 480 Tripodi, G., 210; 274 Tripp, M.R., 326; 350 See Arimoto, R., 324, 326; 331 Tripper, D.J. See Ghuysen, J.M., 122; 139 Trique, B. See Martinez, J.C., 290; 344 Tritar, S., 298; 350 Trollope, D.R., 299, 300, 303, 304, 310, 314, 317, 318; 350 See Al Jebouri, M.M., 300, 302, 310, 315, 317; 330, 331 Troy, F.A., 98, 103; 151 Truchet, G.L. See Sherwood, J.E., 86; 150 See Vasse, J.M., 74, 81, 86; 152 Trueman, E.R., 452; 494 See Ansell, A.D., 452, 453; 480 Trump, C.L., 36; 69 Trytek, R.E., 291; 351 Tschirner, E. See Schubert, H., 279; 348 Tseng, W.Y., 26; 69, 70 Tseythin, V.B., 470, 471, 472; 494 Tsuchiya, M., 327; 351 Tsuda, R.T., 219; 274 Tuan, T.L. See Yoshino, T.P., 324; 352 Tubiash, H.S., 319, 320, 321; 351 See Hidu, H., 284; 339 See Lovelace, T.E., 286; 343 Tunlid, A. See Odham, G., 146 Tunnicliffe, V., 120; 151 Turakhia, M.H., 95; 152 Turner, R.D. See Boss, K.J., 291; 333 See Waterbury, J.B., 290; 351 Turner, T., 252; 274 Turquier, Y., 362, 363, 370, 372; 379 See Pochon-Masson, J., 370; 378 Tveter, E., 222, 249; 274 Twedt, R.M., 309; 351 See Spite, G.T., 311; 349 Tyson, P.D., 168; 175 Tysset, C. See Brisou, J., 333 Uda, M., 14, 42, 52, 59; 70 Ugarte, R. See Hoffman, A.J., 189, 226, 228; 263 See Santelices, B., 198, 206; 272 Uhlenbruck, G. See Baldo, B.A., 332 See Müller, W.E.G., 145
524
OCEANOGRAPHY AND MARINE BIOLOGY
Uhlinger, D.J., 76, 89, 91, 100, 108, 121, 130; 152 See Fazio, S.A., 100; 138 Ullman, W.J., 392, 393, 395; 494 See Rhoads, D.C., 108; 148 Ulrich, S.A. See Rodrick, G.E., 325, 326; 348 Umamaheswara Rao, M., 202, 203, 204; 274 See Kaliaperumal, N., 195; 264 Umatani, S.I. See Yamagata, T., 64; 70 Underwood, A.J., 229, 231, 236, 247, 248; 274 See Kenelly, S.J., 235; 265 UNESCO, 386, 421; 494 Ursin, E., 446, 473, 474, 477; 494 Usui,Y., 91; 152 Utinomi, H., 362; 379 Vadas, R.L., 184, 187, 189, 247; 274 See Pearlmutter, N.L., 179, 220; 270 Vaghin, V.L., 373; 379 Valdivia, E. See Arntz, W.E., 407, 432, 441, 468; 481 Valentine, J.W., 383; 494 Valeur, A. See Odham, G., 146 Valiela, L, 328; 351 See Jordan, T.E., 326; 340 Van den Broek, M.J. M., 309; 351 Van der Horst, G. See McLachlan, A., 174 Van der Meer, J.P., 194; 275 Vandermeulen, H., 226; 275 Vander Wyk, J.C. See Lessie, T.G., 103; 142 Vanderzant, C. See Piexotto, S.S., 347 Van Dover, C.L., 117; 152 Van Essen, S. See Breeman, A.M., 187; 257 Van Mulekom, L.L. See Breeman, A.M., 187; 257 Vann, W.F. See Silver, R.P., 96; 150 Van Staden, J. See Mooney, P.A., 198; 268 Varadarajan, S., 450; 494 Vargas, J.A., 398, 404, 409, 412, 413; 494 See De la Cruz, E., 401; 482 See Maurer, D., 414, 417, 419, 425; 488 Varma, R.P., 228; 275 Varshney, P.K., 417, 418, 423, 424; 494 See Govindan, K., 423; 485 Vasconcelos, G.J., 300, 303; 351 Vasse, J.M., 74, 81, 86, 88; 152 See Sherwood, J.E., 86; 150 Vasta, G.R., 324, 325; 351 Vaughn,J. M, 313; 351 Velimirov, B., 234, 248; 275 Venosa, A.D., 88; 152 Ventresca, D. See Dayton, P.K., 260 Ventullo, R.M., 114; 152 See Lock, M.A., 143 Venugopal, R. See Raju, P.V., 252; 271 Vera, M.E. See Santelices, B., 197; 272 Vermaat, J.E., 190; 275 Vermeij, G.J., 383, 412, 454; 494
Vernet, P., 193; 275 Vertessy, R. See Wolanski, E., 387; 495 Verwey, J., 326; 351 Vetter, R.D., 295; 351 See Brookes, J.M., 333 Vicente, H.J., 400; 494 Vicente, N. See Henry, M., 296; 339 See Martin, Y., 322; 344 Vidaver, W., 206; 275 Vieira, A.A.H., 80, 107; 152 Vielhaben, V., 205; 275 Vigneulle, M. See Prieur, D., 277–252 Vincx, M. See Help, C, 404, 424; 486 Vinogradova, N.G. See Neyman, A.A., 433; 490 Virnstein, R.W., 413; 494 Vitiello, P. See Grelet, Y., 485 Vitola, M. See Gocke, K., 459; 484 Vohra, F.C., 396, 408, 411, 413, 449; 494 Volse, L.A. See De Vinny, J.S., 233; 260 Vos, P.C., 99, 108; 152 Vranken, G. See Help, C., 404, 424; 486 Vreeland, V., 107; 152 See Larson, B., 107; 142 Waaland, J.R., 183; 275 See Hannach, G., 185; 262 Wade, B.A., 414, 425, 428, 438, 452; 494, 495 Wade, T.L. See Kennicutt II, M.C., 341 Wafar, M.V.M. See Achuthankutty, C.T., 450; 479 Wagh, A.B. See Parulekar, A.H., 429; 490 Wakeham, S.G. See Lee, C., 109; 142 Walker, G., 353, 354, 372; 379 Walker, S.A. See Cammen, L.M., 280; 334 Wallace, G.T., 162; 175 Wallace, J.H., 421, 422; 495 Wallace, R.R. See Lock, M.A., 143 Walley, L.J., 353, 355, 372; 379 Walne, P.R., 284; 351 Walsby, A.E., 222, 223, 224; 275 Walsh, J.J., 440, 458, 476; 495 See Premuzic, E.T., 391; 491 Walter, A. See Sutcliffe, J., 99; 151 Walter, H., 382; 495 Walters, N.M. See Shannon, L.V., 167; 174 Walters, V. See Scholander, P.F., 443; 492 Wang, C.M. See Weng, X.C., 36; 70 Wang, J., 22; 70 Wang, K.S., 36; 70 Wang, W., 37, 41; 70 See Su, J.L., 24, 25, 26; 69 Wangersky, P.J.,. 280; 351 Wantland, K.F., 390, 438; 495 Warburton, K., 422; 495 Ward, W.E., See Geiger, J.C., 286; 338 Wardell, J.N., 84, 115; 152 Ware, G.N. See Lewin, J., 170; 173
AUTHOR INDEX
Warwick, R.M., 429, 435; 495 Wassenberg, T.J., 422; 495 Wassman, R., 219; 275 Watanabe, J.M., 229, 231; 275 Waterbury, J.B., 290, 291; 351 Watling, L., 108, 109; 152 See Steneck, R.S., 188, 229, 236; 273 Watson, D.S., 207, 229; 275 Watts, J.D., 21; 70 Weagant, S.D., 309, 310; 351 Webb, J.E., 390, 420, 438, 453, 454; 495 See Hill, M.B., 420; 486 Webb, P., 170; 175 Webster, D.R., 85, 100, 109; 152 Weckesser, J. See Brautigam, E., 134 Weiner, R.M., 97, 113, 298; 152, 351, 352 See Bonar, D.B., 113; 134 See Coon, S.L., 298; 335 See Hussong, D., 304; 340 Weldon, W.F.R. See Smith, G., 353; 378 Wells, J.B.J. See Munro, A.L.S., 474; 489 Wells, J.T., 389, 390; 495 Weng, X.C., 36; 70 West, J.A., 178, 181, 183, 189, 203, 240; 275 See Dring, M.J., 200; 260 See Krugens, P., 210; 266 See Polanshek, A.R., 181; 271 See Wetherbee, R., 210; 275 West, P.A. See Hada, H.S., 339 Westrich, J. See Tenore, K.R., 350 Wetherbee, R., 210; 275 Wetzel, R.G. See Crumpton, W.G., 93; 137 Wetzel, R.L., 120; 152 Wharton, G.W. See Pearse, A.S., 155; 174 Whedon, W.F. See Miller, M.A., 113; 144 White, D.C., 74, 101, 110, 114, 120; 152 See Fazio, S.A., 100; 138 See McFeters, G.A., 144 See Moriarty, D.J.W., 489 See Nichols, P.D., 145 See Odham, G., 146 See Platt, R.M., 93; 147 See Uhlinger, D.J., 76, 89, 91, 100, 108, 121, 130; 152 White, F. See Walley, L.J., 353, 372; 379 White, W.B., 14; 70 Whitfield, C., 96, 97; 152 Whittenburry, R., 294; 352 Wicken, A.J., 90; 153 Wiese, W., 108; 153 Wieser, W., 444, 445; 495 See Hartwig, E.O., 444; 485 Wijayaratne, R.D. See Means, J.C., 112, 128; 144 Wilce, R.T. See Markey, D.R., 210; 267 Wildish, D.J. See Poole, N.J., 126; 147 Wilkinson, C.R., 297; 352 Wilkinson, J.F. See Sutherland, I.W., 102; 151 Wilkinson, S.G. See Gray, G.W., 102, 103; 139 Williams, A., 90; 153 Williams, A.G., 89, 94, 97, 102; 153
525
Williams, D. McB., 476; 495 See Doherty, P., 178, 237; 260 Williams, J.L., 205; 275 Williams, L.P. See Nolan, C.M., 346 Williams, P.J. leB., 130; 153 Williams, S.L., 392; 495 Williams, W.T. See Stephenson, W., 415, 419, 435; 493 Wilson, B.R. See Kenk, V.C., 292; 341 Wilson, D.F. See Wallace, G.T., 162; 174 Wilson, E.G. See Kruger, I., 157; 173 Wilson, J.H., 281; 352 Wilson, J.J. See Andrews, W.H., 331 Wilson, R., 311; 352 Wilson, W.B. See Collier, J., 355; 376 Wimpenny, J.W.T., 115, 116, 117; 153 See Williams, A.G., 89, 94, 97, 102; 153 Windom, H.L. See Tenore, K.R., 350 Winter, D.F., 169; 175 Winter, W.T. See Moorehouse, R., 92; 144 Winterbourn, M.J. See Rounick, J.S., 118; 149 Wirsey, C.O. See Jannasch, H.W., 82, 117; 141 Wiseman Jr, W.J. See Shim, T., 41; 69 Withers, T.H. See Newman, W.A., 354; 378 Witschi, E., 353; 379 Witten, T.C. See Ferris, F.G., 138 Wittke, M., 324; 352 Woelkerling, W.J., 218; 276 Woessner, J.W. See Neushul, M., 269 Woitzik, D. See Brautigam, E., 134 Wojtowicz, M.B., 283; 352 Wolanski, E., 386, 387; 495 See Ridd, P., 387; 491 Wolcott, T.G., 412; 495 Wolff, W.J., 425; 495 Wong, P.S. See Leung, C., 343 Wong, T.M. See Leong, T.S., 487 Wood, A.P., 297; 352 Wood, P.C., 301, 304, 306, 317; 352 Wooldridge, T. See McLachlan, A., 174 Wooldridge, T.H. See Webb, P., 170; 175 Woolery, M.L., 198; 276 Woollacott, R.M., 113; 153 See Brancato, M.S., 113, 298; 134, 333 See Zimmer, R.L., 113; 153 Work, R.C. See McNulty, J.K., 415; 489 Worthington, L.V., 47; 70 Wrangstadh, M., 85; 153 Wright, L.D. See Short, A.D., 168; 174 Wright, M.E. See Bartlett, D.H., 96; 133 Wright, R.T., 280, 326; 352 Wu, R.S.S., 425; 495 Wullis, M. See Rice, M.A., 283; 348 Wynne, M.J. See Bold, H.C., 181; 256 Wyrtki, K., 22, 385; 70, 495 Xia, S.Y. See Yuan, Y.C., 25, 39, 43; 71
526
OCEANOGRAPHY AND MARINE BIOLOGY
Xiong, Q.C. See Zhao, B.R., 43; 71 Xiu, S.M. See Guo, B.H., 36; 66 Yamada, M. See Kokubo, Y., 341 Yamada, N., 179; 276 Yamagata, T., 64; 70 Yamamoto, H. See Tokida, J., 240; 274 Yanagimachi, R., 353; 379 See Ichikawa, A., 353, 373; 377 Yanez, A. See Gallardo, V.A., 484 Yanez-Arancibia, A., 422; 496 Yang, T.H., 34; 70 Yaphe, W. See Lahaye, M., 107; 142 Yarbrough, J.D. See Chambers, J.E., 122; 135 Yarish, S.M. See Williams, S.L., 392; 495 Yasuda, I., 62; 70 See Yoon, J.H., 45, 62, 63; 70 Yentsch, C.M. See Shumway, S.D., 349 Yi, S.U., 41; 70 Yingst, J.L. See Rhoads, D.C., 108; 148 Yingst, J.Y., 429, 430, 441, 473; 496 Yokote, M., 74, 99; 153 Yoon, J.H., 45, 62, 63; 70 See Yasuda, I., 62; 70 Yoovidhya, T., 314, 315; 352 Yoshida, K., 62; 70 See Hasunuma, K., 14, 15; 66 See Stommel, H., 12; 69 See Usui, Y., 91; 152 Yoshida, S., 53; 70 Yoshida, T., 218; 276 Yoshimura, T. See Takeoka, H., 64, 65; 69 Yoshino, T. See Renwrantz, L., 348 Yoshino, T.P., 324; 352 See Cheng, T.C., 335 Yoshioka, H., 64; 71 Young, D.K., 397, 413; 496 See Rhoads, D.C., 329; 348 Young, L. See Mitchell, R., 298; 345
Young, M.W. See Young, D.K., 397, 413; 496 Young, R.R. See Cundell, A.M., 287; 336 Yu, C.Y. See Fan, K.L., 25, 26; 65 Yu, H.H. See Miao, Y.T., 39; 67 Yuan, Y.C., 25, 39, 42, 43, 48, 49; 71 See Zhou, W.D., 18; 71 Zablackis, E. See Vreeland, V., 107; 152 Zahn, R.K. See Muller, W.E.G., 145 Zaidi, R., 107; 153 Zambon, J.S., 107; 153 Zamorano, D. See Hoppe, H.-G., 458; 486 Zaneveld, J.S., 197, 247; 276 Zatila, J. See Elston, R., 337 Zebal, R. See DiSalvo, L.H., 321; 336 Zeballos, J. See Arntz, W.E., 407, 432, 441, 468; 481 Zechman, F.W., 226, 228; 276 Zedler, J.B. See Emerson, S.E., 228; 261 Zeitzschel, B. See Bodungen, B. von, 110; 134 Zhang, F.G. See Zhao, B.R., 43; 71 Zhao, B.R., 42, 43; 71 Zhao, J.S. See Yuan, Y.C., 42; 71 Zhican, T. See Rhoads, D.C., 491 Zhou, W.D., 18; 71 Zieman, J.C. See Odum, W.E., 329; 346 See Robertson, M.L., 131; 148 Zimmer, R.L., 113; 153 Zimmerman, R. See Hoppe, H.-G., 458; 486 Zingmark, R.G. See Dame, R.F., 326; 336 See Holland, A.F., 108; 140 ZoBell, C.E., 83, 113, 278, 285, 298; 153, 352 See Oppenheimer, C.H., 288; 346 Zou, E. See Toole, J.M., 20; 69 Zullo, V.A. See Newman, W.A., 354; 378
SYSTEMATIC INDEX References to complete articles are given in heavy type; references to pages are given in normal type.
Abra alba, 449 Acanthohaustorius, 397 Acanthophora spicifera, 218 Achromobacter, 286, 287 Acinetobacter, 288 Acrochaetium, 240 pectinatum, 183 Acroscalpellum, 354 Acrothoracica, 353, 354, 362, 363, 366, 369, 374 Aerobacter, 90 Aeromonas, 287, 288 Agardhiella, 214 Aglaja, 420 Aglaophamus, 398 Agrobacterium, 90 Agropecten purpuratus, 432, 469 Alaria esculenta, 226 Alcaligenes, 286 Alcippe (=Trypetesa), 362 Alteromonas colwelliensis, 298 Alveolinella, 438 Amphibola, 119 Amphioplus, 415, 437 coniatodes, 467 Amphiopsis, 453 Amphipoda, 397, 417 Anadara granosa, 397, 404 Anadyomene, 419 Anaulus, 156 australis, 155–175; 155, 156, 157, 158, 159, 160, 161, 162, 164, 166, 167, 168, 169, 170, 171 australis (=birostratus), 156 Ancinus, 396, 411 Annelida, 467 Anodontia alba, 466 philippiana, 295 Anoplostoma viviparum, 403 Antithamnion, 240 Aphrodita, 435 Arctica islandica, 280 Ariidae, 442 Arthrobacter, 287 viscosus, 121 Arthromobacter, 287 Ascophyllum, 208, 218 nodosum, 192, 193, 218, 247
Ascothoracida, 353, 373, 374, 375 Astarte, 438 Asterionella, 156, 159 glacialis, 156, 157, 159, 161, 164 glacialis (=japonica), 156 socialis, 156, 157, 159, 160, 161, 168, 171 Astropecten granulatus, 408, 410 Asymmetron, 420 Atherinidae, 421 Atrina, 420 Audouinella purpureum, 200 Aulacodiscus, 156 johnsonii, 156 kittonii, 156, 157, 159, 161, 164 Aulacomya ater, 281 Aurivillialepas, 354 Australophialus, 362 turbonis, 363 Azotobacter, 89, 90
Bacillariophyta, 156 Bacillus, 90 cereus, 307, 310, 311 megaterium, 325 Bacteroides, 287 Balanomorpha, 355, 357, 371 Balanomorphoidea, 364 Balanus, 247, 356 amphitrite amphitrite, 371 balanus, 364, 365, 368, 370, 371, 372 crenatus, 371 eburneus, 371 perforatus, 370, 371 Balistidae, 442 Bangia, 181 Bangiophycidae, 206, 220 Bankia australis, 291 gouldi, 291 Bathylasma alearum, 358 corolliforme, 358 Bathymodiolus, 292, 294 thermophilus, 292, 293, 294, 297 Batillaria multiformis, 411 Batrachoides, 442 Bdellovibrio, 88 Beggiatoa, 120 Belonidae, 421 Berndtia purpurea, 362
528
OCEANOGRAPHY AND MARINE BIOLOGY
Bivalvia, 416, 417, 466 Bildingia minima, 243, 249, 251 Bonnemaisonia, 186, 199, 240 Bothidae, 442 Branchiostoma, 438, 453 africae, 453 leonense, 453 nigeriense, 453 senegalense, 453 takoradii, 453 Byropsis, 189 Bullia, 409 melanoides, 411, 466
Calantica, 354, 358 calyculus, 360 spinilatera, 358 trispinosa, 358 villosa, 358, 359, 360 Calcinus, 450 Callinectes, 422, 467, 468 arcuatus, 451 Calyptogena, 293, 294 elongata, 295 laubieri, 294 magnifica, 291, 292, 293, 297 phaseoliformis, 294 ponderosa, 293 Campylobacter jejuni, 307, 310, 311 Campylosira, 156 Canuela perplexa, 424 Capitella capitata, 423, 424 Carangidae, 442 Cardium echinatum, 280 Carpophyllum, 194 maschalocarpum, 249 Caryophyllia clavus, 437 Caulerpa, 179, 204, 212, 420 Cellana, 236 tramoserica, 236 Centroceras, 189 Ceramiales, 197 Ceramium, 189, 210, 240, 243 rubrum, 183 Cerastoderma edule, 300 glaucum, 296 Ceratonereis, 411 hircinicola, 396 Cerianthus, 408 Cerithidea, 419 cingulata, 396, 397 Cerithium angulatus, 410 Chaetoceros, 99, 110, 156, 168 armatum, 156, 157, 159, 160, 161, 164, 168, 171 Chaetozone, 432 Champia, 221 Chanidae, 421 Chelonia mydas, 219 Chelonibia patula, 358 Chelonobia patula, 358 Chione cancellata, 466 Chionelasmus darwini, 358 Chlamydiae, 319
Chlorophlexis, 427 Chlorophyta, 179, 181, 182, 191, 192, 206, 210, 211, 220, 223 Chondria, 419 tenuissima, 218 Chondrus, 210, 221, 236, 249 crispus, 183, 222, 245 Chorda, 210, 211 tomentosa, 208, 211 Choromytilus meridionalis, 281, 282 Chthamalophilidae, 354, 363 Chthamalus stellatus, 364, 371 Cichlidae, 421 Cirolana, 410 mayana, 396, 411 parva, 396 Salvadorensis, 396, 397 Cirripedia, 353, 372, 374, 375 Citharidae, 442 Cladophora, 218, 419 Clathromorphum circumscriptium, 202 Clibanarius, 450 Clistosaccidae, 363 Clistosaccus, 356 Clithon ocualamensis, 396 Clostridium, 287 botulinum, 308, 310, 311, 315 perfringens, 307, 310, 311, 312, 313 Clupeidae, 421, 442 Clymene, 411 Clymenella mucosa, 397 Codakia costata, 295 orbiculata, 295 Codium dimorphum, 250 fragile, 196, 220 fragile tomentosoides, 219 Colpomenia peregrina, 226 Conchocelis, 189, 240 Conopea, 358 calceolus, 356 galeatus, 356 masignotus, 356 merilli, 356 Copepoda, 400, 401 Corallina, 239 officinalis, 239, 245 Corbicula fluminea, 324 Corynebacterium, 287 Costaria costata, 201 Cottus scorpius, 446 Crassostrea angulata, 305 commercialis, 303, 304 cuculata, 287 gigas, 282, 284, 286, 287, 288, 289, 298, 300, 302, 303, 305, 323, 324 virginica, 284, 286, 290, 298, 301, 303, 305, 323, 325 Cristispira, 289, 290 Crustacea, 353, 362, 467 Cryptophialus, 362 newmani, 366 wainwrighti, 363 Cryptopleura, 214 violacea, 222, 223
SYSTEMATIC INDEX
Ctenodrilus serratus, 122 Cultellus tenuis, 437 Cunicus profundus, 398 Cyclaspis, 411 Cynoglossidae, 421 Cynoglossus, 446, 447, 449 brevis, 446, 447, 449 Cystoseira, 193, 420 barbata, 218 osmundacea, 192 Cytophaga, 286
529
Engraulidae, 421 Enhydrosoma buecholtzi, 403 Enterobacteriae, 287 Enteromorpha, 113, 178, 179, 198, 210, 211, 213, 214, 215, 226, 234, 235, 252, 419 intestinalis, 203, 252 linza, 243 Ephippidae, 442 Erysipelothrix rhusiopathiae, 308 Erythrocystis, 210 Escherichia, 287, 302 coli, 95, 96, 98, 299, 300, 301, 303, 304, 307, 309, 311, 312, 313, 314, 315, 316, 322, 325 Eunice, 420 Euplotes, 444, 445, 447 antarcticus, 445 balteatus, 445 vannus, 445 Eurydice, 396, 411, 467 longicornis, 411 Euscalpellum, 358 rostratum, 358 Excirolana, 396, 409, 412, 445 braziliensis, 396, 411 latipes, 396, 408 natalensis, 398, 408, 410, 411 orientalis, 408, 410 Exosphaeroma diminutum, 397 laevisculum, 398
Dasybranchus, 420 Delesseria, 201 sanguinea, 197, 201 Dendrophyllia, 437 Dentalium, 437 Derxia, 87 Desmarestia, 198 aculeata, 241 Desmodora, 424 Dictyosphaeria, 208, 210, 212 Dictyota, 205 dichotoma 198, 202, 205 Diogenes diogenes, 411 Diopatra, 435 neopolitana, 411, 437 Donax, 396, 397, 409, 410, 444, 450, 452, 453, 468, 478 aemulus, 408, 410 denticulatus, 396, 452, 453 elegans, 408, 410 faba, 408, 409, 410 gracilis, 397 incarnatus, 396, 404, 411, 453, 466, 468 panamensis, 411 peruvianus, 407 pulchellus, 396, 408 roemiri, 397 serra, 170, 398, 411 spiculum, 396, 404, 411, 466, 468 Dorylaimus, 424 Dotilla fenestrata, 408, 410 Dumontia contorta, 199 incrassata, 196 Durvillea, 248 antarctica, 188
Facetotecta, 375 Fissurella barbadensis, 444 Flavobacterium, 286, 287 Flexibacter, 92 Florideophyceae, 196 Foraminifera, 418 Fosliella farinosa, 219 Fucales, 191 Fucus, 193, 197, 206, 208 mytilus, 218 serratus, 213, 230 spiralis, 251 vesiculosus, 218, 252 Furcellaria fastigiata, 218
Echinodiscus, 420 Ecklonia, 248 radiata, 192, 194, 241, 249 Ectocarpaceae, 220 Ectocarpus, 210, 211, 220 siliculosis, 198 Edwardsia gilbertensis, 411 zonesi, 397 Egregia, 248 laevigata, 248 Elizia orbicularis, 411 Elminius modestus, 371 Emerita, 410 analoga, 398, 411 asiatica, 396 holthuisi, 396, 404, 411, 450, 467, 468 rathbonae, 411 Endarachne, 214
Gafrarium pectinatum, 466 Gastropoda, 416 Gastrosaccus psammodytes, 170 Gastrotricha, 400 Geleia nigriceps, 444 Gelidiella acerosa, 195, 198, 203 Gelidiopsis, 202 variabilis, 195 Gelidium, 179, 180, 196, 202, 204, 214, 243 amansii, 195 chilense, 251 robustum, 195, 240 sesquipedale, 220, 221 Gerreidae, 442
530
OCEANOGRAPHY AND MARINE BIOLOGY
Geukensia demissa, 280, 285 Giffordia, 181 Gigartina, 221, 236, 249 acicularis, 186, 199, 218 stellata, 236 Gigartina-Petrocelis, 202 Gigartinaceae, 183, 185, 191, 207 Gigartinales, 181 Gitanopsis pusilla, 398 Gloiopeltis, 202, 214 Glossophora kunthii, 199 Glycera, 411, 435 alba, 396, 467 Gobiidae, 421 Gonyaulax, 156 Gracilaria, 179, 198, 202, 203, 204, 205, 221, 241, 249, 250 corticata, 202 debilis, 250 domingensis, 250 foliifera, 202 millardetii, 195 sjostedtii, 202 textorii, 202 verrucosa, 195, 222 Gracilariopsis, 214 lemaneiformis, 235 Gravierella multiannulata, 410 Griffithsia, 210 Gruvelialepas, 354 Gymnocongrus, 181
Haemulidae, 421 Halectinosoma curticorne, 403 Halichondria panicea, 86 Halimeda, 393 Halodule, 393, 458 Halophila, 398, 420 Halophrye dusumieri, 446, 449 Halymenia latifolia, 199 Haustorius, 397 Hedophyllum, 188, 253 Hemiaulus, 156 Herposiphonia plumula, 250 Heterodonax, 396 Hippa picta, 420 Hippidae, 409 Histriobdella homari, 122 Holothuria scabra, 450 Hormosira, 235 Hyale media, 205 nilsonnii, 206 Hydrobia, 409 Hypnea, 202, 240
Ibla, 362, 371 cumingi, 361, 362, 373 idiotica, 373 quadrivalvis, 361, 373
Iblidae, 361 Idotea wosnesenskii, 206 Iridaea, 178, 181, 183, 252 cordata, 181, 206 laminarioides, 183, 184, 192, 202, 205, 252 Isopoda, 397
Jania, 239 rubens, 239 Janua, 298 brasiliensis, 113, 298 Jasmineira, 397 Jullienella, 438 foetida, 437
Klebsiella, 90 Kochlorine bocqueti, 362 floridana, 362, 366 hamata, 362 ulula, 362
Lactobacillus, 119, 282 Lagocephalidac, 442 Laminaria, 192, 200, 240, 241, 248, 249, 253 angustata, 200 digitata, 186, 195, 200, 214, 249 ephemera, 194 hyperborea, 195, 197, 214 japonica, 251 longicruris, 177, 193, 195, 249, 251 saccharina, 186, 200 Laminariales, 193, 198, 241 Landsburgia, 194 Laophonte, 119 Laophontopsis secunda, 403 Leathesia difformis, 248 Leiocapitellides, 424 Leiognathidae, 442 Leitoscoloplos chilensis, 432 Lepadomorpha, 354, 358, 359 Lepas fascicularis, 364 Lepidactylus, 397 Lepidotrigla, 441 Leptocharias, 442 Leptocylindrus, 156 Lernaeodiscidae, 356, 362 Lessonia, 244, 249 nigrescens, 188, 240, 243, 248, 251, 253 Lessonia-Durvillea, 188 Lessoniopsis, 188 Lethrinidae, 441 Leuconostoc, 90 Levringiella, 210 Lingula, 410 anatina, 446, 451 Listeria monocytogenes, 308
SYSTEMATIC INDEX
Lithoglyptes, 362 indicus, 366 Lithoglyptidae, 362 Lithophyllum, 205, 251 incrustans, 192 yesoense, 251 Lithothamnion, 251 Lithothrix, 210, 212 Lithotrya dorsalis, 364 Littorina littorea, 206, 248 neglecta, 248 unifasciata, 248 Liza richardsonii, 170 Lovenia, 420 Lucina costata, 295 floridana, 295 multilineata, 295 radians, 295 Lucinacea, 296 Lucinidae, 293, 295, 296, 297 Lucinella divaricata, 296 Lucinoma annulata, 294, 295 borealis, 295, 296, 297 Lumbriconereis latreilli, 467 Lumbrinereis, 397, 411 meteorana, 411 Lutjanidae, 441, 442 Lyrodus medilobata, 291 pedicellatus, 291
Macoma, 415, 437 balthica, 106, 118, 283, 285, 328 Macrocystis, 180, 184, 188, 210, 215, 219, 226, 240 241 243 245 248 249 251 pyrifera, 192, 193, 195, 219, 232, 244, 245 Macropetasma africana, 170 Macrophthalamus grandidieri, 408, 410 Mactra olorina, 420, 466 veneriformis, 287, 300 Magelona phyllisae, 432 Marginopora, 438 Mastocarpus papillatus, 189 stellatus, 191, 196 Mastocarpus-Petrocelis, 189 Maxillopoda, 353, 374 Mediomastus, 424 californiensis, 398 Mercenaria, 323 campechiensis, 325 mercenaria, 284, 299, 300, 301, 302, 303, 304, 305, 324, 325 Meretrix casta, 448, 449 Mesodesma, 420 donacium, 407, 411, 466, 469 Mesopodopsis slaberri, 170 Metalinhomoeus setosus, 403 Micrococcus, 286, 287
531
Microprotopus, 424 Minuspio cirrifera, 423 Modiolus modiolus, 280 Moira atropus, 467 Monachus schauinslandi, 291 Monhystera denticulata, 122 Monochrysis lutheri, 284 Monostroma, 205, 214 nitidum, 202 Moraxella, 287 Mugil, 442 Mugilidae, 421 Mullidae, 442 Muraena, 442 Murex, 420 Mustelis, 442 Mya arenaria, 287, 300, 304 Mycobacterium tuberculosis, 299 Mycoplasma, 319 Myrtea spinifera, 296, 297 Mystacocarida, 401 Mytilicola intestinalis, 122 Mytilidae, 289 Mytilus californianus, 278, 285, 326 coruscus, 287, 300 edulis, 281, 282, 283, 287, 288, 289, 299, 300, 302, 303, 304, 323, 324, 325, 326 galloprovincialis, 286 provincialis, 284 viridis, 287
Nannopus palustris, 403 Navicula, 156 Neisseria 287 Nematoda, 400, 401, 418 Nemipteridae, 442 Neogaimaridia kowiensis, 398 Nephthys, 435 impressa, 411 Nereis, 435 Nereocystis, 221, 221 Nerine cirratulus, 396 Nerita, 444 tesselata, 444 Nitocra spinipes 403 Nitophyllum punctatum, 203 Nitzschia, 156 Noctiluca, 156 Notomastus, 420 Nuculana minuta, 449
Octopus fontaneanus, 432
532
OCEANOGRAPHY AND MARINE BIOLOGY
Ocypode, 408, 410, 411, 453 arenarius, 410 gaudichaudii, 398, 411, 412 hippeus, 408 Oliva, 420 Olivaricella, 409 Olivella, 409 Onuphis, 411, 435 eremita, 467 Operculina gaimardi, 420 Ophelia, 411 Ophiactis kroyeri, 432 Ophionephthys limicola, 467 Ophiuroidea, 467 Orbinia anagrapequensis, 398 Ostracrontidae, 442 Ostrea edulis, 281, 284, 289, 298, 301 Owenia, 435, 437 fusiformis, 410
Pachymeniopsis, 240 Padina, 420 jamaicensis, 241 Pagurus, 450 Palmaria, 221 Paphia malabarica, 449 Paracomesoma dubium, 403 Paraonides, 411 Parapionsyllis longicurata, 397 Paraprionospio pinnata, 398, 432 Parvilucina multilineata, 295 tenuiscalpa, 297 Patella, 248 vulgata, 247 Patelloidea latistrigata, 248 Patinopecten yessoensis, 282 Pavlova lutheri, 283, 284 Pecten maximus, 283, 284, 285, 298 Pectinaria, 420 Pelagophycus, 188, 221 Pelecyora trigona, 404 Peltogasteridae, 356, 362 Pelvetia, 178, 206, 208, 241 canaliculata, 206 fastigiata, 206 Penaeidae, 421 Penaeus, 122 Perciformes, 441 Perinereis, 410, 420 Perna viridis, 288, 448 Petalonia fascia, 189, 198, 199 Petrocelis middendorffii, 189 Phacosoma japonicum, 287, 300 Phaeophyta, 179, 181, 182, 191, 206, 207, 209, 210, 211, 220, 223, 249
Photobacterium, 287 Phycolimnoria, 219 Phyllochaetopterus, 408 elioti, 410 Pilayella, 210 Pinna, 408, 410 Platycephalidae, 441 Platycephalus, 441 Platyischnopus, 398 Plesiomonas shigelloides, 307 Pleuronectes, 446, 447 platessa, 446, 447 Pleuronectidae, 442 Plicarcularia leptospera, 397 Plocamiocolax, 210 Plocamium cartilagineum, 197 Pollicipes cornucopia, 370 elegans, 432 polymerus, 364 Polychaeta, 397, 416, 417 Polydora aggregata, 432 citrona, 398 Polygordius, 398 Polynemidae, 421, 441 Polynices, 420 Polysiphonia, 181, 210, 219 platycarpa, 195 Polystomella, 420 Pomadasyidae, 442 Pontogeloides latipes, 398 Porphyra, 184, 189, 204, 206, 210, 240 gardneri, 209 variegata, 211, 212 Porphyra-Conchocelis, 204 Postelsia, 221 palmaeformis, 188, 221 Prasiola stripitata, 243 Priacanthidae, 442 Pringsheimiella scutata, 219 Prionotus, 441 Protodrilus, 400 Psettodidae, 442 Pseudogloiophloea, 202 Pseudomiltha, 293 Pseudomonas, 89, 90, 92, 97, 119, 286, 287, 288, 319, 321, 322 aeruginosa, 96, 310 atlantica, 80, 96, 119 enalia, 319 insolita, 86 Pseudopolydora, 424 Pseudostenhelia secunda, 403 Psiloteredo healdi, 291 Pterocladia, 179, 196, 202, 204 capillacea, 185, 186 Pterosiphonia dendroidea, 250
SYSTEMATIC INDEX
Pterygophora californica, 193 Ptilota serrata, 183 Pyura stolonifera, 280, 281
Ralfsia, 189 Rhizobium, 81 japonicum, 86 Rhizocephala, 353, 354, 362, 366, 374 Rhizoclonium, 189 Rhizosolenia, 156 Rhodocorton, 240 purpureum, 179, 187, 198, 200 Rhodomela larix, 183 Rhodophyta, 179, 181, 182, 183, 185, 189, 190, 206, 209, 210, 211, 212, 218, 220 Rhodymenia, 221 californica, 250 pertusa, 209 Rickettsia, 319 Rickettsiae, 319 Riftia, 292 pachyptila, 297 Rotalia, 420 Ruditapes philippinarum, 283 Ruppia, 419
Sabatieria, 424 intermissa, 424 Sabellaria cementarium, 435 Sacculina carcini, 354 Sacculinidae, 356, 362 Salicornia, 419 Salmonella, 90, 300, 301, 302, 303, 304, 307, 308, 311, 314, 315, 316, 317 charity, 304 foecalis, 301 hadar, 310 paratyphi, 307 thyphimurium, 301 typhi, 307 Sarcodiotheca gaudichaudii, 223 Sargassum, 179, 198, 204, 218, 233, 252 fluitans, 218 herporhizum, 194 heterophyllum, 198 johnstonii, 194 muticum, 192, 215, 219, 220, 221, 226, 251 natans, 218 plagiophyllum, 252 polyceratium, 194 sinclairii, 192, 193, 249 sinicola, 194 Scalpellum, 358, 360, 373 bengalense, 360, 361 californicum, 358 discoveryi, 360 elongatum, 360 gigas, 360 gracile, 360 intermedium, 360 longirostrum, 360 luteum, 360 ornatum, 360 peronii, 359, 360 pilsbryi, 360 retrieveri, 360
533
rostratum, 360 rutilum, 360 scalpellum, 358 scorpio, 360 squamuliferum, 360, 361 stearnsi, 360 striatum, 360 stroemii, 358 tritonis, 360 villosum, 360 vulgare, 360 woodmasoni, 359, 360 Scapharca broughtonii, 287, 300 cornea, 288 Schizammina, 437 Sciaenidae, 421, 441, 442 Scillaelepas, 354 Scolelepis, 396, 424 agilus, 397 madagascarensis, 411 squamata, 397, 398, 411 Scoloplos, 411 marsupialis, 467 Scorpaeniformis, 441 Scrobicularia plana, 300 Scyphomedusae, 443 Scytosiphon, 184 lomentaria, 180, 189, 200 Scytosiphon-Petalonia, 189 Semibalanus, 372 balanoides, 364, 365, 366, 367, 368, 369, 370, 371, 372, 373 Serranidae, 441, 442 Shigella, 307 dysenteriae, 310 Sigambra bassi, 432 Siliqua patula, 170 Siphonaria, 206 lessoni, 234 Smilium, 358, 360 Smithora, 210, 211 naiadum, 208, 211, 212, 214 Soleidae, 421, 442 Solemya 293 panamensis, 294 reidi, 294, 295, 297 velum, 297 Solen, 408 corneus, 410 Solidobalanus 356 Solieria chordalis, 220 Sparidae, 442 Sphacelaria, 180, 243 Sphaeroma annandalii, 397 Spirillina, 420 Spisula, 415 subtruncata, 296 Spongomorpha, 243 Spyridia, 240 filamentosa, 240 Squilla paramenis, 432 Staphylococcus, 310 aureus, 307 Steineria sterreri, 444 Stenhelia longifurca, 403 madrasensis, 403 Stenothyra glabrata, 409
534
OCEANOGRAPHY AND MARINE BIOLOGY
Stichopus, 119 Streblospio benedicti, 87 Streptococcus, 90, 287 pneumoniae, 94 Strombus, 420 Sylon, 356 Sylonidae, 363 Synechococcus, 279 Synodidae, 442 Synodontidae, 421, 442
Tachidius discipes, 403 Tagelus divisus, 466 Talorchestia, 408, 410 quadrispinosa, 411 Taniada, 417 Tapes japonica, 300 philippinarum, 287, 300 Telescopium telescopium, 445 Tellina, 415 martinicensis, 466 Terebra, 409 Teredinidae, 290 Teredo bartschi, 291 furcifera, 291 navalis, 290, 291 Teredora malleolus, 290 Terschellingia longicaudata, 403 Tetraclita squamosa, 444 Thais chocolata, 432 Thalassia, 393, 394, 397, 401, 419, 456 testudinum, 456 Thalassodrilides, 423 gurwitschi, 423 Theristus floridanus, 444 Thetya, 280 Thioplaca, 426, 427 Thoracica, 353, 354, 366, 374 Thyasira, 296 flexuosa, 296, 297 obsoleta, 297 sarsi, 296, 297 Thyasiridae, 296, 297 Tilapia, 128 melanotheron, 420 Timoclea imbricata, 466 Trailiella, 186 Trefusia schiemeri, 444 Trevus, 289 Trichurus, 442 Triglidae, 441 Trissonchulus oceanus, 403 Trygon, 442 Trypetesa (=Alcippe), 363 (=Alcippe) nassarioides, 370 habei, 363, 366 lateralis, 362 nassarioides, 363, 372 spinulosa, 363 Turbellaria, 400, 401
Turritella terebia, 420 Tympanotonus radula, 420
Uca, 397 Ulothrix pseudoflaca, 243, 252 Ulva, 178, 198, 202, 210, 211, 212, 252 lactuca, 189, 190, 192, 198, 214, 245, 252 mutabilis, 203, 215 pertusa, 213 Umbonium, 409 vestiarium, 446, 466, 468 Undaria, 204, 214 Ungulinidae, 297 Urothoe grimaldi, 396
Valonia, 212 utricularis, 218 Vaucheria sessilis, 203 Venerupis semidecussata, 287 Venus, 437, 438 japonica, 289 verrucosa, 282, 283 Verruca stroemia, 364, 371 Verrucomorpha, 358 Vesicomya cordata, 293 Vesicomyidae, 291, 293 Vibrio, 286, 287, 288, 319, 321, 322, 327 aestuarinus, 321 alginolyticus, 319 anguillarum, 319, 321, 322 cholerae, 307, 309, 311, 315 fisheri, 321 harveyi, 303 parahaemolyticus, 303, 304, 307, 308, 309, 310, 311, 315, 325 tubiashi, 321 Vibrionaceae, 287, 288
Weltneria, 362 exargilla, 362
Xanthomonas, 90
Yersinia, 317 enterocolitica, 307, 310, 316
Zeidae, 442 Zonaria farlowii, 183 Zoogloea, 97 Zostera, 460
SUBJECT INDEX References to complete articles are given in heavy type; references to sections of articles are given in italics; references to pages are given in normal type.
Acrothoracica males, 362, 363 Africa, 411 tropical continental shelves, 425, 426 African shelf fauna, 438 Agglutinins, 324 Alaska, 247 Algae grazers, 409 Algoa Bay, S. Africa, surf-zone diatoms, 167, 169, 170 Amazon, 388, 389, 392, 429, 430 outwelling, 440 American Public Health Association (APHA), 314 Americas, tropical estuaries, 424 Amino acids, 127, 128, 283, 284, 464, 465 in mangroves, 464, 465 Amoebocytes, 323 Anaerobic bacteria, 295 mineralisation, marine micro-heterotrophs, 457 Andaman Islands, Indian Ocean, 387, 400 Sea, 429, 430, 434 Angola, 387 Anoxic habitats, Chile, 427 Fosa de Cariacao, Venezuela, 425 Golfo Dulce, Costa Rica, 425, 427 Indian estuaries, 425 South West Africa, 427 Antarctic sea-ice ciliates, 444, 445 species, metabolic rates, 446, 447 Antibiotics, use in bivalve culture, 284– 285 Apomeiosis, 181, 185 APS reductase, 295 Aquaba, Jordan, 398, 401 Arabia, 387 upwelling, 441 Arabian Gulf, 414, 416 Sea, 429, 434 Arctic species, metabolic rates, 446 richness, 438 Ascorbic acid, cirripedes, 355 Ashtamudi Lake, India, 417, 420 Association Française de Normalisation (AFNOR), 314 Atchafalaya River, 436 Atlantic beaches, 413 demersal fisheries, 441 no surf-zone diatoms, 158 Ocean, 186, 218, 219, 388 trough, high waves, 166 Atlantic-East Pacific fauna, 383
ATP reductase, 294 sulphurylase, 294, 295 Australia, 196, 200, 204, 232, 236, 247, 248, 385, 390, 391, 393, 402, 406, 458, 459 benthic chlorophyll, 457 demersal fisheries, 441 gastroenteritis in, 311 salinity maximum zones at river mouths, 386 standards for shellfish, 313 growing waters, 313 Australian beaches, surf-zone diatoms, 156 Autotrophic bacteria, 296 carbon dioxide fixation, 292, 294, 295 sulphuroxidising bacteria, 293 Axenic culture of bivalves, 284 Bacillary necrosis, 320 Bacteria, accumulation factor, 301 and hydrothermal vents, 117 as a food resource, 125 as disease agents in bivalves, 319–320 as food for bivalves, 278–285 associated with bivalve larval culture, 284–285 benthic depositfeeders, 125 impact of bivalve faeces on, 327–328 contaminating bivalves, release of, 303–306 digestion by bivalves, 282– 283 enrichment factors in bivalves, 300– 302 experimental uptake by bivalves, 282 faecal, as potential trophic resource, 329–330 food source, amino acids, 125 polyunsaturated fatty acids, 125 vitamin B complex, 125 heterotrophic, associated with bivalve tissues, 285–291 interactions with bivalve molluscs in the marine environment, 277–352 in the ocean, 73 kinetics of accumulation by bivalves, 299–300 lack of sterols, 125 location of accumulation in bivalves, 302 marine, size of, 280 retention by bivalves, 280–282 symbiotic, autotrophic in bivalve gills, 291–297 uptake and production of DOM, 283– 284 yield in natural environment, 278– 280 Bacterial cells and secreted exopolymers, schematic diagram, 75 expolymer secretions, carbohydrate components, 90–91 composition of, 89–95 isolation from laboratory cultures, 101–104 isolation of
536
OCEANOGRAPHY AND MARINE BIOLOGY
polysaccharide, 103 non-carbohydrate components, 91–92 removal of lipid, 104 removal of protein, 103–104 role of adsorbed components on composition, 93 tight capsular EPS, 102–103 growth measured by thymidine uptake, 402 populations and surface sediment temperature, 463, 464 Bacteriocytes, 292, 293, 294, 295, 296 Bacterioplankton, 278, 279, 280, 285 Bahamas, 390 Baja California, 428, 458 upwelling, 459 Balanomorpha, males, 356, 357 Barbados, West Indies, 428, 438 Bashi Channel, 13, 18, 20, 21, 22, 23, 25, 26 water exchange through, 22– 23 Strait, 14 Bay of Bengal, 385, 387, 400, 429, 430 fish fauna, 421 Bay of Brest, 280, 288 Bay of Panama, hermit crabs, 450 Belize, 241, 390 Benguela, 398, 407 Current, 387 upwelling, 407, 468, 469 Benthic biomass, and flux of pelagic detritus, 472 deposit-feeders and bacteria, 125 ecosystems, ecology of tropical soft bottoms, 381–496 feeders, 443 fisheries, 473 Bermuda, 395, 444, 470 Bidyadhari River, India, 417, 425 Bight of Biafra, 390 Biotic comparisons of tropical and temperate intertidal habitats, 474, 475 Biscayne Bay, Florida, 465 sewage pollution, 423 Bivalve larvae, bacterial diseases of, 320–323 culture, associated bacteria, 284–285 growth without bacteria, 285 retention efficiency of bacteria, 281 Bivalves as indicators of pollution, 317–318 autotrophic gill symbionts of, 291–297 bacteria as food for, 278–285 commercial evaluation of quality, 312– 317 microbial contamination of, 299– 306 consumption, human health risks from, 310–312; 306 sanitary aspects of, 306–308 depuration, 303–306 digestion of bacteria, 282–283 digestive enzymes, 282–283 digestive tract, microflora of, 285–289 ecosystem, physico-chemical
characteristics of, 326–327 enrichment factors for bacteria in, 300–302 environmental interactions with bacteria, 326–330 experimental uptake of bacteria, 282 haemocytes, adhesion to target, 325 attraction to target, 325 endocytosis by, 325–326 heterotrophic bacteria associated with tissues of, 285– 291 immunology, cellular effectors, 323–324 humoral effectors, 324–325 of, 323–326 indication of metamorphosis by bacteria, 297–299 interactions with bacteria in the marine environment, 277–352 kinetics of accumulation of bacteria by, 299–300 location of accumulated bacteria in, 302 microbial diseases in, 318–323 microflora associated with, 285–299 pathogens associated with, 308–310 retention efficiency and pumping rate, 281–282 of bacteria, 280–282 spirochaetes associated with, 289–290 teredinid, microbiol flora associated with, 290–291 uptake and production of dissolved organic matter (DOM), 283–284 viruses in, 316–317 Blue crabs, 422, 468 Boca Ciega Bay, Florida, 455, 459 Bohai Sea, 42 Bombay, 401 Botulism, 308, 311 Boundary layer, 217, 227, 241 Bowling Green Bay, Australia, 392, 395 Brahmaputra River, 388, 389 Bramble Bay, Queensland, Australia, 415 Branchiostoma, adaptor to stress, 453–454 Brazil, 387, 392, 438, 442, 458, 470 Bream, 442 Brilliant Green Bile lactose broth (BGB), 314 British Isles, 192 Brittany, 218 Brown shrimp, 122 Brunei, crude oil terminal, 424 Cabo Frio, 387 Calatagan, Philippines, 450 Calcareous algae, 393 Calcium-specific chelant [ethylenebis(oxyethylenenitrilo)] tetraacetic acid [EGTA], 95 California, 181, 188, 231, 232, 240, 245, 250, 251, 253, 387 Current, 12 Calvin-Benson cycle, 292, 293, 295 Canada, 200, 219 Current, 387
SUBJECT INDEX
Cape Blanc, Spanish Sahara, 429, 431 Blanco, Oregon, surf-zone diatoms, 158 Hatteras, 442 of Good Hope, surf-zone diatoms, 159 Padronne, surf-zone diatoms, 159 Peninsula, S. Africa, 280 Shionomisaki, 44, 45, 54 York Peninsula, 391, 392 York, Queensland, Australia, 460 Capsular and slime EPS, physical structure of, 93–94 Carbohydrase, 283 Carbohydrate, 390 Carbon dioxide fixation, 292, 293, 294, 295, 296 Carbon fixation, marine microheterotrophs, 457 14 C-labelled EPS, labelling and isolation of, 104 Carbon sink hypothesis, 464 tropical soft bottoms, 391–392 Caribbean, 198, 241, 384 benthic communities, 438 nearshore lagoon, 419 Sea, 442, 455, 469, 470 Carnivores, 422 Carrie Bow Cay, Belize, 397, 455, 456, 459 Catfish, 421 Cebu, Philippines, 400 Cellular detritus as a food resource, 126 Cellulose degradation, 291 Central America, 384 Chakara, 384 definition of, 389 or mudbanks, 435 Changjiang, East China Sea, 429 River, 36 delta, 436, 437 Charleston Bump, 51 Cheju Island, 43 Chemical defences of plants, 443 “Chemical warfare,” seaweeds, 207 Chemoreception in cirripedes, 355 Chesapeake Bay, 286, 304, 309 Chile, 188, 192, 232, 244, 250, 253, 387, 388, 398, 409, 411, 412, 428 sulphide-rich sediments, 426 Chilka Lake, Bay of Bengal, 416, 418, 420 China, 11 -Japan Joint Research Program on the Kuroshio (JRK), 12 Seas, 36, 37 Chinese oceanographers, 36 ports, icefree, 42 Chitinase, 290 Chitobiase, 290 Chlamydiae in bivalves, 319 Chlorophyll, 213, 455
537
Chlorophyll a, 399, 455, 456, 457 Cholera, 307, 311 Chunda Bay, Queensland, Australia, 405 bacterial production, 458, 461 Cintsa Bay, North East London, surfzone diatoms, 159 Cirripedes, anatomy and function of penis, 363–366 androdioecy, 372 apertural males, 356, 358 burrowing, 354, 372 complemental males, 354, 356, 358, 375 copulation in, 354– 356 cryptogonochorism, 373 description of copulation, 355, 356 dwarf males, 354, 356, 375 fate of penis after copulation, 366–369 fundamentals of insemination in, 353–379 future research, 374–375 hermaphroditism, 354, 372, 373 male cyprids, 356 males, anatomy and morphology, 356–363 penis, degeneration of, 367, 368 regeneration of, 368, 369 place of attachment of males, 354 prospects of evolution, 372–374 pseudocopulation, 354, 355 selffertilisation, 373, 374 sexuality, 353 spermatozoa, 369–372 schematic representation of, 370 type of reproduction, 354 Clay species in surf-zone diatom platelets, 157 Cochin, India, 392, 396, 408, 467, 468 Coconut husks, retting of, 424 Cold seeps, bacterial symbionts in bivalves associated with, 293–294 Conforms, 301, 302, 304, 312, 313, 314, 315, 316, 318 Colombia, 396, 397, 413 Colombian lagoon, 458 Colonisation by seaweeds, 180, 197, 233, 253 Commercial prawn trawling, 438 Concepcion, Chile, 426 Cooperative Study of the Kuroshio andAdjacent Regions (CSK), 11 Copulation in cirripedes, 354–356 Coral mucus, 117 and coral reef zooplankton, 117 Coral reefs, 241, 382, 390, 391, 393, 413, 414, 454, 477 Coralline algae, 251 Costa Rica, 397, 404, 409, 413, 425, 459 Dome, 387 Crabs and coral mucus, 117 Critical tidal factor hypothesis, 243
538
OCEANOGRAPHY AND MARINE BIOLOGY
Croakers, 441 Cryptogonochorism, cirripedes, 373 Crystalline style, 289 Cuba, 390 Cyanobacteria, 279, 391, 427 and stromatolites, 109 Daito Ridges, 13 Davies Reef, Great Barrier Reef, 392, 395, 455, 459, 460 Dawhat as Sayh, Arabian Gulf, high saline lagoons, 420, 421 Deep-sea fish and luminescent bacteria, 87 hydrothermal vents, 294 Demersal fish, 422, 468, 471 classified according to diet, 422 communities, tropical sea bottom continental shelves, 441–443 fisheries, 426, 473 tropical estuaries and lagoons, 421–422 Denmark, ciliates, 445 Density dependent mortality, seaweeds, 222, 243 Deposite-feeders, 404, 406, 409, 440 Depuration of commercial bivalve shellfish, 303–306 Detritus-feeders, 285, 422 Diarrheic poisoning, 307 Diatom, EPS isolation of, 105 Diatoms, 229, 236, 247, 251, 252 and microalgae as a food resource, 126 and microbial mucilage, 99–100 composition of, 99 synthesis of, 99– 100 as source of fatty acids, 126 Digestive enzymes, bivalves, 282–283 tract microflora of bivalves, 285–289 Dispersal of seaweeds, 216–227 shadows, seaweeds, 225, 226, 230 Dissolved organic carbon (DOC), 465 matter (DOM), 73, 76, 78 production and uptake by bivalves, 283–284 production by bacteria, 283–284 uptake by bacteria, 283–284 DNA, exogenous, 132 synthesis, 458, 460 marine micro-heterotrophs, 457 Donax, adaptor to stress, 452–453 as resource exploiters, 453 LDOPA, 298 Drums, 441 Dysentry, 307 East China Sea, 11, 12, 14, 17, 18, 25, 26, 27, 28, 32, 33, 34, 35, 36, 39, 41, 42, 43, 48, 63, 64, 436 East Pacific Rise, Galapagos, 291, 293
Ébrié lagoon, Ivory Coast, 455 Ecology of tropical soft-bottom benthic ecosystems, 381–496 benthic-pelagic coupling, 470–473 continental shelves, 474–477 energy transfer in benthic food chains and latitudinal comparisons, 473–477 growth, 448– 449 heterotrophic microbial activity and fate ofbacterial production, 457– 465 intertidal habitats, 474 macrofauna, 465–470 microalgal productivity, 454–457 physiological and behavioural adaptations to stress, 443–454 reproduction, 449–452 demersal fishes, 451–452 invertebrates, 449–451 superb adaptors, 452–454 temperature and salinity tolerances, 443–446 compensation and metabolism, 446– 448 Ecotone point, 423 Edge effects, algal settlement, 245 Eels, 442 Eliminases (lyases), 122 Elimination of bacteria from bivalves, 304–305 El Niño, 387, 407 El Niño-Southern Oscillation (ENSO), 63, 64, 387, 469 and crab fishery, 432 and soft-bottom macrobenthic communities, 432 Bay of Ancon, Peru, 432, 433 Peru, 431 South and Central America, 431 Endocytosis, 292 Endopeptidase, 283 Endosymbiotic bacteria, 295 England, 185, 197, 200, 218, 241 Enshunada, 56 Enterobacteria, 300, 310 Enteropathogenic strains, 310 Enterotoxin producers, 309, 310 Environmental characteristics of tropical soft bottoms, 383–393 Enzymes in animals, 122 which degrade EPS, 121 Epidemiology, 310–312 Epigrowth-feeders, 404, 406 Equatorial Countercurrent, 14 Erosion by ice movement in temperate zones, 425 Erythrocytes, 325 Esteros, narrow winding sea channels, 414 Estimates of production and fish yield to man, 476, 477
SUBJECT INDEX
Estopa, microbial mats, 426 Estuaries and lagoons ecology of tropical soft bottoms, 414–425 high sulphides, 414 high temperatures, 414 oxygen and nutrients, 414 polyphenolic acid, 414 salinity, 414 turbidity, 414 Estuaries, India, 415 Estuarine macrobenthos, Brisbane, Queensland, Australia, 415 Eulerian measurement, 41 Europe, 186, 219, 407 standards for shellfish growing waters, 313 Exoenzymes, 78 and EPS, 76 in proximity of the cell, 78 Exopeptidase, 283 Exopolymer capsules, 78 binding mechanisms, 79 metal-binding to, 79–81 Exopolymer secretions (EPS) N-acetylDgalactosamine, 91 UDP-N-acetyl glucosamine, 98 N-acetyl-Dglucosamine, 91 O-acetyl groups, 91 acyl groups, 91 alanine, 81 alginases, 122 alginate, 122 amino acids, 89, 93 analysis of by magnetic resonance imaging (MRI), 101 arabinase, 99 arginine, 81 as adsorptive sponge for sequestering DOM, metal and toxins, 78–82 as carbon source for bacteria, 89 as dispersant and for temporary attachment, 84–85 as DOM or POM, 112 as energy source for protozoans, 76 as general adhesive for microbial cells, 82–84 as storage reserves for nitrogen-fixing bacteria, 88 ATP, 93 generating systems, 84 bacteria, 78, 83, 84, 85, 86, 87, 93, 94, 97, 104, 105, 106, 108, 110, 111, 113, 114, 115, 118, 119, 120, 124 bacterial aggregates, 109 bicinchoninic acid assay, 103 binding of organic compounds to, 81–82 cadmium, 79, 80 cobalt, 79, 80 copper, 79 iron, 79, 82 magnesium, 79 manganese, 79, 82 nickel, 79 lead, 79, 80 silver, 79, 80 strontium, 79 zinc, 79, 80 biofouling, 76, 113 biosynthesis of, 97–99 influence of physiological conditions, 97–98 can reduce frictional drag on fish, 87 capsule attachment to bacterial cell, 95 capsules, 88, 94 and utilisation of microbial cells as food, 128–129 layer, 78 carbohydrases, 123
539
carbohydrates, 89, 93, 97, 100, 101 carbon substrate, 97 cellulose digestion, 115 chromium, 119 composition, regulation and structural aspects of, 89–110 concentration of nutrients, 76, 77 coral reef zooplankton, 117 coral reefs, 117 cyanobacteria, 85, 86 deacetylases, 122 degradability by enzymes, factors affecting, 123–125 degradation of detritus, 77 degrading enzymes, 121, 122 isolated from bacteria, 122–123 dental plaque, 115 diffusion of nutrients, 114 DOC-POC fluxes, 77 DOM, 82, 83, 93, 101, 109, 111, 112, 118, 125, 126, 127, 128, 129, 130, 131 DNA, 91, 93, 96, 116, 117 downward transport of metals, 81 endopolysaccharases, 123, 124 enzymes which degrade, 121 examination by electron microscopy (EM), 94, 95, 109 examined by interference reflection microscopy (IRM), 83 exchange of nutrients in sediments, 109 exoenzymes, 76, 77, 81, 91 exoglycosidases, 123 exopolysaccharases, 123 exopolysaccharides, 84, 92, 98, 102, 119, 122, 124 extracellular enzymes, 77 feeding by zooplankton, 106 feeding experiments, harpacticoid copepods, 105 holothureans, 105 fishery resources, 113 food value of, 118–121 food webs, 77 freshwater bacteria, 79 from natural systems, analysis of, 100–101 from various bacterial strains, 92–93 fructose, 97 fucose, 99 functional roles of microbial cells, 77–89 galactose, 92, 99 UDP-galactose, 98 galactouronic acid, 91, 92 genes, 96 genetic regulation of capsule production, 96 gluconate, 97 glucose, 89, 92, 97, 99, 101, 104, 113 UDP-glucose, 98 glucuronic acid, 92, 99 UDPglucuronic acid, 98 glycanohydrolases, 122 glycerol, 97 glycoproteins, 84, 85, 89, 91, 92, 95, 103, 104, 106 glycosidases, 123 glycoside hydrolases, 123 glycosidic acid, 122 bonds, 103 heteropolysaccharide capsules, 84 heteropolysaccharides, 90, 98, 123 homopolysaccharides, 90, 119 hyaluronic acid, 106 hyaluronidases,
540
OCEANOGRAPHY AND MARINE BIOLOGY
122 hydrothermal vents, 117; 76, 108 bacteria, 82 in attachment of microbial cells to surfaces, 76, 77 in benthic systems, 76 in feeding experiments, 105–106 “Initial Reversible Sorption,” 83 in intestinal flora, 115 in non-marine systems, 74, 77 in protection against heavy metals, 76, 77 in protective effects of, against toxic compounds, 82; 76, 77 in relation to other food resources, 125–126 in tight capsules, 76 in water column, role in aggregation and flocculation, 109– 112 iron, 111 isoprenoid alcohols (IP), 98 act as a transferase, 98 lectins, 85, 86, 113 lipids, 103 lipopolysaccharides (LPS), 85, 95, 98, 102 magnetic resonance imaging (MRI), 107 maintenance of symbiotic relationships, 78 manganese, 111 mannose, 97, 99 mannuronic acid, 91 marine snow, 76 metal-binding and pH, 80 metal corrosion, 115 methane digestion, 115 methods for analysis of, 100–107 microbial cells, 76 molecular regulation, 96–97 molecular weight, 89 monosaccharide donors, 98 monosaccharides, 90, 91, 95, 122 mucopolysaccharides, 106, 107, 121, 122 nuclear magnetic resonance (NMR), 107 nucleoside diphosphate sugars (NDS), 98 occurrence and effect on sediments, 108–109 in natural systems and their interactive roles in oceanic processes, 107–118 oligosaccharides, 97, 98, 122, 123, 124 particulate organic matter (POM), 112 pentose, 101 peptidoglycan, 98 phosphates, 81 phytoplankton, 109, 110 polypeptides, 103 polysaccharases, 124 polysaccharides, 78, 79, 80, 82, 84, 86, 89, 93, 96, 99, 104, 106, 107, 111, 113, 116, 123, 124 potential roles in food webs, 118– 129 protection from grazing and digestion by consumer animals, 87– 88 protects bacteria against antifouling copper paints, 82 protein, 99, 103, 104 proteoglycans, 106 protozoan grazers, 106 reef corals, 106 released by diatoms for locomotion, 108, 109 rhamnose, 99 ribose, 99, 101 RNA, 91, 93 role in
development of biofilms and microbial consortia, 115–117 role in symbiosis and syntrophic relationships, 86–87 role of ions in the structural integrity of, 94–95 radiolabelling, 104 sedimenting of phytoplankton, 76 settlement and metamorphosis of marine larvae, 112–114 of abalone, 113 of oysters, 113 similar to DOM complex for binding, 81 sinking rates of cells, 110 specific binding to exuding surface, 85–86 succinate, 97 sucrose, 97 sugar nucleotides, 98 summary and future research, 129–132 synthesis, site of, 98–99 techniques for future work, 107 uronic acid, 79, 84, 89, 90, 91, 92, 95, 99, 111, 122, 123 use of microscopy to examine, 106–107 utilisation as a direct food resource, 118–126 vehicle to transfer adsorbed DOM and metals to higher trophic levels, 126–128 what they are, 73–77 xylose, 97, 99 Faecal coliforms, 300, 301, 304, 313, 314, 315 pellets, 234; 225 streptococci, 300, 301, 314, 318 Faeces, mineralisation of, 327–329 False Bay, S. Africa, surf-zone diatoms, 156, 169 Filter-feeders, 206, 228, 229, 230, 231 Finisterre, France, 186 Fish locomotion assisted by bacteria, 87 predation, 422 Flexibacteria, 427 Florida, 309, 390, 402, 442, 458 ciliates, 445 Current, 35, 36 escarpment, 293 Keys, 419 Flounders, 421 Flower Garden Banks, Caribbean Sea, 429, 430 Form-function hypothesis, seaweeds, 188 France, typhoid in, 311 French Guiana, 387, 390 Fulvic acid, 125 Fundamentals of insemination in cirripedes, 353–379 Fungi, production of in marine sediments, 457 tropical production estimates, 465 Galapagos, 291, 292 Gambia, coast of, 453 Gastroenteritis, 307, 308, 311
SUBJECT INDEX
Gautami-Godavari estuary, India, 418 GEK observations, 18, 28, 29, 31, 41, 48, 57, 58 Geostrophic velocity sections, 45, 47 Ghana, W. Africa, 387, 428, 437 demersal fisheries, 441 lagoon, 420 Ghost crab, 408, 412 Gibberellins in seaweeds, 203 Gilbert Islands, cholera in, 311 Gland of Deshayes, 290–291 ß-glucanases, 122 Glucosamine-containing lipid, 95 Glucose-6-phosphate dehydrogenase, 103 ß-glucuronidase in nematode, 122 ß-glutamic acid in some sulphatereducing bacteria, 465 Glycoprotein in seaweeds, 211, 215 Goa, India, 392, 393, 396, 401, 402, 417, 430, 468 Godavari estuary, India, monsoons, 415 Gold coast, N.W. Africa, 396, 408 Golfo Dulce, Costa Rica, 392, 429 Golgi apparatus, 99 Gram negative bacteria, 287, 291, 292, 294, 295, 296, 325 Gram positive bacteria, 287, 325 Grand Banks Bahamas, 438 Grazing of seaweeds, 246–248; 178, 187, 205, 206, 228, 229, 232, 233, 238, 239, 250 Great Barrier Reef, 390, 393, 395, 399, 411, 429, 430, 438, 439, 453, 455, 458, 459, 462, 463 cyclones, 440 trawling, 440 Great Britain, 192, 219 Greenland, shelf ecosystem, 474 Groupers, 441 Grunts, 442 Guam, 16 Guarapina, Brazil, 459 Guiana, 387, 390 Current, 390 demersal fish stocks, 442 trawl-caught fish, 443 Guinea and Senegal, W. Africa, 428 shelves, 437, 438 Gulf of Carpentaria, 387 Chiriqui, no upwelling, 431 Elat, 414 Guinea, Ivory Coast, 385, 387, 390, 414 demersal fish stocks, 442 Mexico, 22, 390, 413, 438, 442, 470 demersal fisheries, 441 hypoxia, 436 Nicoya, Costa Rica, 387, 398, 401, 412, 417, 419, 451 Panama, 385, 387, 429 upwelling, 431 Thailand,
541
435 demersal fish stocks, 442 fish fauna, 421 Gulf Stream, 11, 12, 25, 36, 45, 51, 62 Haemocytes, 323, 324, 325, 326 Hake, 442 Hatcheries, bivalve, 320–323; 298, 299 Hawaii, 63, 64, 218, 458 Heavy metals, effect on respiration of bivalves in Indian estuary, 448 Helland-Hansen method for measuring dynamic heights, 23 Hemolysin from Vibrio culture, 322 Hepatitis, 307 Herbivores, 184, 188 Herbivorous fishes, 206 Heteroauxins in seaweeds, 203 Heterotrophic bacteria, 282, 288, 293 bacterial communities, 395, 457 flagellates, 285 metabolism, 297 nanoplankton, 285 Heterotrophy in tropical ecosystems, 456 Hexulose phosphate synthetase, 293 Hinchinbrook Island, Australia, 392, 395, 458, 460, 463, 475 Holocene sea level, rise of, 390 Hong Kong, 398 harbour, 435 shelf, 429 Hooghly River, India, 417, 418 Huizache Caimanero lagoon, Mexico, 416 Human diseases and epidemiology, 310– 312 Humic acid, 125 Hungho River, Vietnam, 386 Hydrothermal activity, 293 vents, 108, 120 and bacteria, 117 and sulphide deposits, 117 bacterial symbionts in bivalves associated with, 291–293 Juan de Fuca, 292 Hypersaline lagoons, 382, 414, 421, 477 Hypoxia of tropical sediments, 436 Iblidae, males, 361, 362 Immunology of bivalves, 323–326 India, 203, 204, 385, 387, 389, 399, 402, 403, 411, 414, 428, 429, 434, 451, 470, 471 benthic chlorophyll, 456, 457 demersal fisheries, 441 tropical continental shelves, 426 wedge clams, 450 Indian beaches, 474 estuaries, 425 meibenthos densities, 418 coasts, organic pollution, 424 sewage pollution, 423 Ocean, 388, 426, 429,
542
OCEANOGRAPHY AND MARINE BIOLOGY
433, 434, 435, 442, 451 no surf-zone diatoms, 158 shelf benthos, 433–435 Indigenous fishermen, 422 Indoleacetic acid, 203 Indolecarboxylic acid, 203 Indonesia, 385 fish fauna, 421 Indo-Pacific, 422 area, 391 fish fauna, 421 Indo-West Pacific, 451 demersal fisheries, 441 fauna, 383 Industrial wastes, tropical estuaries, 425 Infaunal groups and sedimentary characteristics, Amazon, 440 Great Barrier Reef, 440 Inhaca Island, Bay of Lourenco Marques, Mozambique, 408 Insemination, fundamentals of in cirripedes, 353–379 Intermediate water, 16 Intertidal communities, seaweeds, 178 habitats, 234, 236, 243, 246, 251 Intertropical Convergence Zone (ITCZ), 387 Iraq, 434 Ireland, 185 Irrawaddy River, Burma, 386, 436 Isle of Man, 200 Isle of Sylt, 474, 475 Italy, cholera in, 311 Izu-Ogasawara Ridge, 13, 16, 44, 45, 51, 57, 59, 60, 61, 62, 63 Izu Peninsula, 44 Jackson Turbidity Units (JTU), 304 Jamaica, 205 Japan, 11, 12, 13, 14, 15, 16, 43, 44, 45, 46, 48, 49, 50, 52, 62, 63, 64, 65, 218, 219 Sea, 27, 39 subduction zone, 293, 294 Japanese Navy, 52 oceanographers, 11, 36, 41, 56 Java, 429, 435 Kakinada Bay, India, 401 Kali estuary, India, macrobenthic densities, 425 Karwar, India, 418, 430 Kelp, 188, 218, 226, 234, 243, 245, 246, 250, 251, 253 Kerala, India, 389, 430 backwaters, pollution of, 424 coast, 450 Kiel Bight, 279 Fjord, 279 Kii Peninsula, 44, 47, 49, 53, 56, 60 Kinetins in seaweeds, 203 Kingston, Jamaica, 428
Korea Strait, 27, 39, 41, 42 Korean oceanographers, 41 Krishna River, India, 417, 418 Kulti River, India, 417, 425 Kuroshio and circulation in South China Sea, 22–26 and circulation in East China Sea, 36–43 beginning of, 17– 26 circulation in Western North Pacific, 14 Countercurrent, 14, 45, 47, 48, 49, 51 currents and volume transport, 17–20 dark cobalt-blue colour, 11 discovery of, 11 Exploitation and Utilization Research (KER), 12 Extension, 12, 14, 16 in East China Sea, 26–43 currents and volume transport, 27–52 temperature and salinity distribution, 32–36 Loop, 22 meaning black current, 11 physical features, 11–71 large scale, 12–17 South of Japan, 43–64 causes of bimodality, 62–64 Kuroshio cold eddy, 59–62 large meander in 1975– 1980, 56–59 large meander mode, 51–64 path patterns, currents and volume transport, 44–49 temperature and salinity distribution, 49–51 ‘trigger ’ meander and development into a large meander, 53–56 Subsurface Water, 39 temperature and salinity distributions, 20–22 topographic features, 13–14 volume transport, 31, 32 Kyucho, 64–65 Kyushu, 36, 41, 42, 47, 48, 53, 54, 55, 62, 63 Kyushu-Palau Ridge, 13 Kyusyu, 56, 57 Ladyfish, 442 Lagoonal studies, Australia, 415 Florida, 415 Middle East, 415 Lagos lagoon, Guinea coast, W. Africa, 420, 422, 453 Lagrangian measurements, 47 Laguna Joyuda, Puerto Rico, 422 La Jolla, USA, 395 Land plants, comparison with seaweeds, 182, 217, 228, 237, 238, 242, 249 Lanthanum inhibits calcium transport into cells, 95 Las Maritas, Venezuela, 396, 455, 459 Latitudinal variations in reproduction, 451 Lebanon, 400 Lectin-binding mechanism, 113
SUBJECT INDEX
Lectins, 298, 324 Lepadomorpha, males, 358, 359 Life cycles, diplohaplontic, 181 heteromorphic, 179, 190 isomorphic, 179, 190 Light intensity responses, seaweed spores, 202, 203 Lignin, 125 Lima, ENSO, 469 Limpets, 234, 247 Limpopo River, Mozambique, 386 Lipase, 283 Listeriosis, 308 Lizard Island, Great Barrier Reef, 460 Longshore currents and surf-zone diatoms, 164, 165, 166 Loop Current in Gulf of Mexico, 22 Louisiana coast, hypoxia, 436 slope, 293, 294 LST, a new bacterial strain, 298 LST-D, a mutant, 298 LST-like bacteria, 298, 299 Lunar cycles, 449, 451 rhythms, adaptation to, 451 Luzon, 11, 12, 14, 17, 18, 19, 20 Lysozyme activity, 282 from bivalve crystalline style, 283 -resistant bacteria, 282 Lysozymes, 283, 294, 326 MacConkey Broth, 314 Macrofauna, tropical and subtropical continental shelves, 428, 429 Macroinfauna, Great Barrier Reef, 439 Mactan, Philippines, 395, 459 Madagascar, 409, 410, 438, 455 Mahanadi River, India, 417, 418 Maitland beach, surf-zone diatoms, 167 Malabar coast, India, 386, 387, 428, 435 sole, 446, 447 Malacca Strait, Indian Ocean, 387, 429, 430, 435 Malay Archipelago, 435 Malaysia, 402, 409, 410, 460 benthic chlorophyll, 456, 457 cholera in, 311 Mandovi River, India, 416, 449 Mangrove creeks, Australia, 386 Mangroves, 382, 387, 390, 391, 393, 399, 403, 405, 421, 445, 454, 456, 458, 461, 462, 463, 477 bacterial biomass, 464, 465 tannins, 414 Mariana Ridge, 13 Marine micro-heterotrophs, 457 poikilotherms, 448 snow, 76, 109, 112
543
Mariscos, commercially exploited invertebrates, 431 Mauritania, 387 Mediterranean, 286, 469, 470 Meiobenthic communities in tropics, organic pollution, 424 Meiofauna, Great Barrier Reef, 439 tropical and subtropical shelves, 430, 431 Mekong River, Vietnam, 386, 389 Melanin-producing bacteria, 298 Metamorphosis, induction by bacteria, 297–299 Methanogenesis, marine microheterotrophs, 457 Methanotrophs, 293 Methylotrophs, 293, 294, 297 Mexico, 387, 396, 414 coastal lagoons, 419, 422, 455, 459 Miami, Florida, 400 Microalgae in the ocean, 73 Microbial consortium hypothesis, 115 Microbial contamination of commercial bivalves, 299–306 Microbial exopolymer secretions in ocean environments, their role(s) in food webs and marine processes, 73– 153 Microbial flora associated with teredinid bivalves, 290–291 Microbiogeochemical processes and degradation of detrital particles, 114– 115 Microflora associated with marine bivalves, 285–299 Microzones characterised in sediments, 106 Mindanao Current, 14 Minicoy, Lakshadweep, 397, 401 Missionary Bay, Queensland, Australia, 392, 395, 460 Mississippi River, 436 Mole crab, 404, 450 Molluscs, man as main predator, 468 Mombassa, Kenya, 397, 401 Monk seal, Hawaiian, 219 Monsoons, 389, 404, 406, 414, 415, 419, 420, 425, 426, 443, 450, 468, 477 and cyclones, India, 415 Montmorillinite in surf-zone diatoms, 167 More Probable Number (MPN) method, 314 Moreton Bay, Queensland, Australia, 460
544
OCEANOGRAPHY AND MARINE BIOLOGY
Morocco, 387, 400 Mozambique, 409, 410 Channel, 428, 453 Mucilage in seaweeds, 208, 212, 221, 222, 223, 224, 234, 235, 236, 252 Mucopolysaccharides in seaweeds, 215, 235 Mucus-expolymers (EPS) extracellular slimesecretions, 73 Mud in fish and prawn guts, 390 Mulki estuary, India, 417 Mullet, 170, 308, 442 Mycoplasma in bivalves, 319 Nagasaki Marine Observatory, 28, 29 Namibia, 387 Namibian coasts, surf-zone diatoms, 158 Naos Island, Panama, Pacific, 396 Naphthalene acetic acid, 203 Naples, 205 Narmada estuary, India, 417, 418 National Shellfish Sanitation Programme (NSSP), 313 Negros Oriental, Philippines, 435 Netherlands, 186, 218 New England, 470 New South Wales, Australia, 251 New Zealand, 192 productivity of surfzone diatoms, 156 surf-zone diatoms, 169 Nha Trang Bay, Vietnam, 429, 435 Nitrate reductase activity, 167 reduction, marine micro-heterotrophs, 457 Nitrogen fixation by bacteria associated with subduction zones, 294 teredinid bivalves, 290 tropical soft bottoms, 391–392 Non-red tide flagellates, 156 Non-upwelling areas, 477 Normandy, 218 North America, 188 Atlantic, 16 Current, 39 Carolina, 205 Equatorial Countercurrent, 12 Current, 12, 14, 17, 18 Pacific anticyclonic gyre, 11 bottom water, 16 Current, 12 Deep Water, 16 Intermediate Water, 15 Ocean, 11, 12, 15, 16 Subtropical Mode Water, 16 surface circulation, 12 Tropical Water, 15 North Penang, Malaysia, 408 North Sea, 226 shelf ecosystem, 474 North West Africa, 430 upwelling, 441 Norwegian fjord, 296 Nosy-Be, Madagascar, productivity of sediment, 457
Nova Scotia, 197, 251 Oil platforms, 226 Okinawa Trough, 13, 14, 29, 32, 34 Olympic Peninsula, USA, surf-zone diatoms, 161 Omnivore-predators, 404, 406, 422 Opportunists, 432 Opsonins, 324 Oregon, 251 coasts, USA, surf-zone diatoms, 158, 159 subduction zone, 293 Organic pollution, Indian coasts, 424 meiobenthic communities in tropics, 424 Osumi Current, 28 Strait, 28 Oyashio Current, 12, 14, 65 Undercurrent, 59 Pacific coasts, 413 Ocean, 14, 22, 26, 32, 65, 279, 388, 435 Pakistan, 385, 428, 434 Palo Alto salt marsh, lead in surface layers, 80 Panama, 411 upwelling, 441 Papua New Guinea, 385, 387 Paralytic shellfish poisoning, 307 Paratyphoid, 307 Parrot-fishes, 219, 241 Pathogenic spore-forming bacteria in bivalve shellfish, 310 Peak of opportunists after pollution, 423 Pearl River, China, 386 Peck’s Cove, Canada, 475 Pelagic compared with demersal fish yields to man, 477 primary production and benthic biomass, 473 shrimp-feeders, 443 Penang, Malaysia, 468 Penis anatomy and function of, in cirripedes, 363–366 fate of, after copulation in cirripedes, 366–369 Percoll-sorbitol mixture (silica gel) extraction technique for sediments, 395 Persian Gulf, 387, 390, 428, 451 Peru, 387, 388, 390, 392, 428, 470, 471 Current, 387 demersal fisheries, 441 infaunal biomass, 427 shelf, 429 Peru-Chile Subsurface Countercurrent, 426 Peruvian upwelling, 407, 428, 432, 441, 469 Phaeopigment, 390 Phagosome, 325
SUBJECT INDEX
Pheromones of seaweeds, 207, 215, 228 Philippine Basin, 13, 17 Sea, 11, 12, 13, 14, 15, 22 T-S diagrams, 15, 16 water masses, 14–17 Philippines, 11, 13, 385, 387, 458 Phosphatase, 283 Photoperiodism in seaweeds, 198, 199, 200 Photosynthesis, seaweeds, 213, 214 Photo taxis in seaweed propagules, 215, 216 Phuket Island, Thailand, 446, 455, 459 Physical features of Kuroshio, 11–71 Phytoplankton, 190, 222, 223, 224, 225, 234 Plaice, 446, 447 Plankton-feeders, 422 Plant-herbivore interactions, seaweeds, 239 Plastids, seaweeds, 211, 212 Pleistocene glaciations, 414 Plio virus, 301 Pollution, bivalves as indicators of, 317–318 catastrophic effect in tropical marine environments, 423 Ébrié lagoon, 414 Kerala backwaters, 424 tropical soft bottoms, estuaries and lagoons, 422–424 Polyphenols (tannins), 236 Polysaccharides, 76, 224 Polyunsaturated fatty acids (PUFA), 285 Ponyfish, 442 Porto Nova, India, 396, 400, 418 Predatory-omnivorous forms, nematodes, 404 Production/biomass ratios (P/B) in tropics, 465, 466, 467, 468, 469, 470 Production rates in Thalassia beds, 456 Propagule production by seaweeds, 190– 201 release by seaweeds, 201–216 Proteinase from Vibrio culture, 322 Protozoans, production of in marine sediments, 457 tropical production estimates, 465 Pseudo-copulation in cirripedes, 354, 355 Puerto Rico, 395 Queensland, Australia, 401, 403, 404, 445, 451 r- and k-selection, 179, 187, 189, 190 Rays, 442 Razor clam, 408
545
Recruitment of seaweeds, 237–254; 207, 225 “Recruitment windows”, seaweeds, 244 Red Sea, hypersaline lagoons, 386 Red-tide organism, 156 Reef fish and coral mucus, 117 Remane’s classic species-salinity relationship, 425 Reproduction patterns of seaweeds, 179– 216 type of in cirripedes, 354 Resource-allocation theory, 190, 201 Reynolds number, 63 Rhythms in spore release, seaweeds, circadian, 204 daily, 203, 204 lunar, 204, 205 semilunar, 205 tidal, 204, 205 Ribulose-1, 5-biphosphate-carboxylase, 292, 294, 295 Ribulose-biphosphate-carboxylase activity, 294 Ribulose-5-phosphate kinase, 292 Rickettsiae in bivalves, 319 Rip currents, surf-zone diatoms, 164, 165, 166, 167, 169 River Amazon, Brazil, 385, 386, 388, 390 delta, 436, 437 Bamu, Papua New Guinea, 386 Brahmaputra, 386, 388 Chira, Peru, 386 Choshui, Taiwan, 386 Damodar, India, 386 Fly, Papua New Guinea, 385, 386 Gambia, 437 Ganges, Bangladesh, 386, 389, 436 Godavari, India, 386 Haulien, Taiwan, 386 Indus, Pakistan, 386 Kaoping, Taiwan, 386 Kikori, Papua New Guinea, 386 Magdalena, Colombia, 386 Mehandi, India, 386 Niger, Nigeria, 386 Nile, Egypt, 386 Orinoco, Venezuela, 386, 388, 389, 390 Purari, Papua New Guinea, 386 Rufiji, Tanzania, 386 Sepik, Papua New Guinea, 386 Sulima, 437 Zaire, 385, 386, 388 Zambesi River, Mozambique, 386 RNA synthesis, marine microheterotrophs, 457 Roaring Forties, 166, 167 Rossby number, 22, 63 Ryukyu Islands, 13, 48, 63 Ridge, 14, 34 Sabkhas, marine terraces round saline lagoons, 384, 390, 414 “Safe site” concept, 237 Sakishima Depression, 13, 14, 18, 27, 29, 31,34, 39
546
OCEANOGRAPHY AND MARINE BIOLOGY
Salinity and surf-zone diatoms, 167 Salmonellosis, 311 Samar, coast of, 14 Sandy beach, schematic diagram, 157 San Francisco River, Brazil, 386 San Luis, Venezuela, 396, 455, 459, 465, 466, 467 Santa Barbara Basin, 294, 295 Santa Maria del Mar, south of Lima, 407 Satellite Gemini X, 22 imagery studies, 36 Saudi Arabia, 385 Scabbard fish, 442 Scallop fishery, 432 Sealpellum males, 358, 359, 360, 361 Scavengers, 409, 412 Scottish beaches, 474 Scottish-Indian International Biological Programme (IBP), 399, 403, 408, 474 Scribu Island, Indonesia, 429, 435 Sea catfish, 441 Sea-mounts, 22 Sea scorpion, 446 Sea urchins, 206, 219, 236, 247, 251, 253, 420 Seaweed propagules, ultrastructure, 210 Seaweeds, alternation of generations, 181–182 differences among reproductive phases, 183 dispersal, 216–227 agents, 217–220 external surfaces of animals, 219–220 faecal pellets, 220 floating substrata, 218– 219 water masses, 217–218 units, 220–222 plant fragments, 220–221 propagule packages, 221–222 unicellular propagules, 222 dispersion patterns, 225–227 longdistance, 225–226 short-distance, 226–227 sinking and floating of propagules, 222–225 changes in the water, 224 mechanisms accelerating sinking, 225 morphological adaptations, 223–224 sinking in water, 224–225 heteromorphic and isomorphic life cycles, 182–184; 199 patterns of propagule production, 190–201 patterns of propagule release, 201–216 ecophysiology of propagules, 213–216 attachment abilities, 214–215 spore viability, 213–214 tactic responses, 215–216 environmental control, 202–207 abiotic factors, 202–205 biotic
factors, 205–207 morphology of propagules, 210–213 nature of release mechanism, 208–210 patterns of reproduction, dispersal and recruitment, 177–276 patterns of spore production, 193–201 environmental control, 198–201 ontogenic, 193–194 seasonal, 196– 198 specific, 194–196 recruitment, 237–254 bank of microscopic forms, 240–242 experimental studies, 242– 254 abiotic factors, 243–244 factor interactions, 252–254 grazing, 246– 248 interspecific interactions, 250– 252 intraspecific interactions, 248– 250 substratum effect, 244–246 relative abundance of gametophytes and sporophytes, 184–185 of sexual and asexual reproduction, 185–187 relative allocation of resources to reproduction, 187–190 reproductive bodies, fertile structures and reproductive efforts, 191–193 settlement, 227–237 attachment, 255–257 settler mortality, 235–237 sexual and asexual reproduction, 179–181 spore cloud, 228–231 spatial patchiness, 230–231 temporal patchiness, 229–230 spore production measurements, 195 spore rain, 231– 234 faecal pellets, 234 previous vegetation, 233 sea foam, 234 sediments, 233 substratum, 233 water depth, 232 water movement, 232 Sediment types on World’s inner continental shelves, 389 Sedimentary chlorophyll, 431 Seep mussel, 294 Sek Harbour, Papua New Guinea, 435 Selangor, Malaysia, 397 Senegal shelves, 437 Seto Island Sea, 65 Settlement of seaweeds, 227–237 Sewage-polluted areas, 286, 307 Biscayne Bay, Florida, 423 Indian coasts, 423 tropical estuaries, 425 Victoria Harbour, Hong Kong, 423, 424 Visakhapatnam Harbour, Bay of Bengal, 423 Shamal winds, 414 Shannon-Wiener function H’ of species diversity, 413, 423, 425, 433 Shark Bay, Western Australia, 109, 391, 460 Sharks, 442
SUBJECT INDEX
Sheepshead, 442 Shelf benthos, Indian Ocean, 433–435 Shellfish-borne diseases, epidemiology of, 311–312 pathogens associated with, 307–308 prevention of, 312 Shellfish-borne poisoning, incidence of, 307 Shellfish-growing waters, microbiological standards for, 313 Shellfish, microbiological standards for, 313–314 relation between pathogens and indicators, 315–317 techniques, 314–315 Shertallai, India, 408, 468, 475 Shikoku Basin, 13, 16, 17, 47 Shimmery Beach, Panama, Atlantic, 396 Ship hulls, biofilms, 115 Shrimp and coral mucus, 117 Sicily, 197 Sierra Leone, 437, 477 demersal fisheries, 441 Siluroid catfish, 441 Sinai Peninsula, Red Sea, tropical shores, 420 Singapore, 396, 411 Site 13°N, 292 Skeleton coast, S.W. Africa, 398, 401 Snake-eels, 442 Snappers, 441 Somali coast of Africa, 387 South Africa, 253, 407 fish faunas, 421 upwelling, 468 South African coasts, surf-zone diatoms, 158, 159, 167, 168, 170 South America, 197, 384, 389, 390, 407, 409 surf-zone diatoms, 159 South Atlantic Bight, 35, 36 South China Sea, 13, 14, 21, 22, 23, 24, 25, 26, 27, 385 circulation in, and Kuroshio, 22–26 Warm Current, 24, 25, 26, 36, 37 and Kuroshio ‘branches’, 23–26 South Equatorial Current, 12 South Gujarat estuaries, India, 417 Southern Ocean, circumpolar westerlies, 168 Soybean plant, 86 Spadefish, 441 Spain, 186, 220 standards for shellfish, 314 Spanish Sahara, coast of, 392, 453 Species diversity of surf-zone diatoms, 156–157 Spermatozoa, cirripedes, 369–372 Spirochaetes, associated with bivalves, 289–290
547
Spore production by seaweeds, 193–201 releasing factors, seaweeds, 202 Stable environment and localisation of exoenzymes in proximity of the cell, 78 Stalked barnacles, harvesting of, 432 Standards Association of Australia (SAA), 314 Sterols lacking in bacteria, 125 Storm effects on seaweeds, 253 Streptococci, 301, 312, 313, 315, 318 Streptomycin, 284 Stress avoidance by benthic organisms, 444 Stromatolites, 382, 477 and cyanobacteria, 109 of Shark Bay, Australia, 109 Subarctic Gyre, 15 Subduction zones, bacterial symbionts in bivalves associated with, 293–294 Subtropical Countercurrent, 14 Mode Water, 32, 49 transition zones, 388 Sulphate-reducing bacteria, 295, 465 Sulphate reduction, marine microheterotrophs, 457 Sulphide biome, caused by retting, 424 Sulphide in sediments, 294, 296, 434 oxidation, enzymatic activity, 294, 295, 296 Sulphide-enriched coastal areas, bacterial symbiont in bivalves associated with, 294–297 Sulphide-oxidising symbionts, 297 Sulphide-rich sediments, 424 Sulphidic blue mud, 390 Sulphur oxidation, 293, 294 Sumatra, 435 Sundays River Beach, S. Africa, surfzone diatoms, 156, 157, 161, 165, 167, 170 Sunderbans, India, 397, 403 Surface drogues, 169 Surf clams, 404, 407, 408 Surf zone, 232 Surf-zone diatoms, Algoa Bay, S. Africa, 167, 169 anatomical considerations, 157 and rip currents, 164, 165, 166, 167, 169 Australian beaches, 156 biogeography, 158–159 Cape Blanco, Oregon, 158 Cape of Good Hope, 159 Cape Padronne, 159 Cintsa Bay, 159 diel periodicity, 159, 160, 163, 164 patch formation and decay, 162, 163 distribution of recorded sites, 158 ecological role of, 169–170 ecology
548
OCEANOGRAPHY AND MARINE BIOLOGY
of, with special reference to Anaulus australis, 155–175 effect of salinity, 167 wind, 166, 167 False Bay, S. Africa, 156, 169 frequency of patch occurrence, 159–161 hypotheses concerning geographical distribution, 165–168 longshore currents, 164, 165, 166 Maitland beach, 167 montmorillinite, 167 muciloginous covering on frustules, 157 Nambian coasts, 158 New Zealand, 169 Olympic Peninsula, USA, 161 Oregon coast, USA, 158 patches, oil production by, 156 patch dynamics, 161–165 and diel periodicity, 162– 163 early views, 161 floatation, 161– 162 mesoscale variance, 163–165 platelets contain illite, 157 contain montmorillinite, 157 on frustules, 157 productivity in New Zealand, 156 seasonality, 159, 160, 161 South African coasts, 158, 159, 167, 168, 170 South America, 159 spatial features in relation to rip currents, 168–169 species diversity, 156–157 storm-calm-storm cycle, 159, 160, 166 Sundays River Beach, S. Africa, 156, 157, 161, 165, 167, 170 Surf-zone flora, 155 patches, Washington coast, USA, 156, 158, 159, 161, 164, 167 Surinam, 390, 397 Survival strategies, seaweeds, 188 Suspension-feeders, 409, 440 Swarmers of seaweeds, 206, 234 Sweden, 327 Symbionts, autotrophic bacteria in bivalve gills, 297–297 Taiwan, 11, 12, 14, 17, 18, 19, 20, 21, 22, 24, 25, 26, 29, 32, 38, 39 Strait, 24, 27, 36 Warm Current, 36–39; 43 Tasmania, 219 Tehuan-tepec, Venezuela, 387 Temperature-salinity (T-S) diagrams, 25 Teredinid bivalves, associated microbial flora, 290–291 Tertiary period, global cooling, 383 Téthys Sea, 383 Texas, 397, 429 Thailand, 385, 456 shelf ecosystem, 474 Thermocline Water, 16 Thiosulphate-oxidising bacterium, 294 Thorson’s “parallel-level bottom” community concept, 415
Threadfin breams, 442 Threadfins, 441 Tidal currents in tropical coastal waters, 387 Tigris-Euphrates, Iraq, 386 Tilapia, diet and growth of, 128 Toadfish, 442, 446 Togo, 387 Tokara Strait, 13, 14, 27, 28, 63 Tokyo Bay, 287 Torch Bay, Alaska, 247 Total organic carbon (TOC) in sediments, 108 Transmission electron microscopy (TEM), 291, 293, 294 ‘Trash fish’, 422 Tropic of Cancer, 382 of Capricorn, 382 Tropical benthic communities, effect of monsoons, 383 effect of river discharge and hydrology, 383, 384 effect of upwelling, 384 major climatic zones, 383 sedimentary patterns, 384 Tropical benthic ecosystems, bacterial densities and production, 460, 461, 462, 463, 464 Tropical benthic habitats, total community aerobic respiration, 457, 459 Tropical biosphere, 381, 383 Tropical ecosystems, primary production and chlorophyll a concentrations, 455 Tropical estuaries, macrobenthic communities, 416, 417 fisheries, 473, 477 intertidal fauna, effect of torrential rain, 402 invertebrates, effect of pollution on respiration, 448 macrofauna, intertidal zonation, 410, 411 Tropical soft bottoms, benthic standing stocks, distribution and community structure, 393–443 carbonate-dominated shelves, 437–441 conservation, 383 continental shelves, demersal fish communities, 441–443 effect of major rivers, 436–437 including marine coastal regions, 425–443 mudbanks, 435–436 upwelling, 426–433 special case, ENSO, 431–433 dissolved inorganic nutrients, 392–393 ecology of, climatological and hydrographical conditions, 384–388 ecosystem dynamics, 454–477 production, 454–470 environmental characteristics of, 383–393 estuaries and lagoons, 414–425 demersal fisheries,
SUBJECT INDEX
421–422 distribution and abundances, 414–421 pollution, 422–424 species diversity and richness, 424–425 fish yields, 381 general ecology, 381 intertidal habitats, 393–414 climatic disturbances, 407 diversity and species richness, 413–414 dry tropics, 404–407 seasonally, 402–407 wet tropics, 402– 404 zonation, 407–412 mangroves and coral reefs, 381 organic carbon and nitrogen, 391–392 particulate dissolved sedimentary nutrients, 391–393 pollution and management, 381, 383 sedimentary patterns, 388–391 wetlands, 381 Tropical water, 16 Tropics, Africa, 384, 385 boundaries of, 382 coastal gypsum lakes, 391 coastal upwelling, 387 definition of, 382 demersal fish, 422 divisions of, 384, 385 effects of monsoons, 402, 403 estuarisation, 384, 385 formation of a lutocline (fluid mud layer), 387 hypersaline lagoons, 391 Indian, Atlantic and Pacific Oceans, 385 macrofaunal densities, 393, 395, 396, 397 macro-predators, 412 meiofaunal densities, 395, 400, 401 monsoonal patterns, 385 oxygen, 385, 386 polyphenolic acids in mangroves, 399 rainfall, 385 salinity, 385 sediment and water discharges into, 386 shelf lagoons, 390 shell-crushing predators, 412 South and Central America and Caribbean, 384 southeast Asia and northern Australia, 385 stromatolites, 391 temperature variations, 385 upwelling, 385 areas, 388 Tsushima Current, 39–41; 42, 65 transport, 41 water, 41 Tulear, Madagascar, 408 Tunisia, 400 Turbidity, tropical estuaries, 425, 457 Turtle, green, 219 Typhoid, 307, 311 Tyrosin hydrolysis, 321 Underwater microscopes, 235
549
United Kingdom, standards for shellfish, 313–314 United States of America, 191, 192, 219 botulism in, 311 Pacific coast, gastroenteritis in, 311 standards for shellfish, 313 shellfish growingwaters, 313 Upwelling, 440, 441, 477 African coast, 431, 458, 468, 469 Benguela, 468 Gulf of Panama, 431 Peru, 432, 469 Van der Waals forces, 83 Vellar estuary, Porto Novo, India, 391, 415, 417, 418 Venezuela, 410 Vestimentiferans, 291, 292, 297 Vibrios, 288, 303, 308, 309, 311 Victoria Harbour, Hong Kong, sewage pollution, 423, 424 Viruses in bivalves, 316–317 Visakhapatnam Harbour, Bay of Bengal, sewage pollution, 423 Vitamins, 127, 283, 284, 285 Vizhemjam, India, 417 Voltra and Congo, W. Africa, 428 Wales, 185, 205 Waltair coast, India, 400 Walvis Bay, S. Africa, 398, 401 Washington coast, USA, surf-zone patches, 156, 158, 159, 161, 164, 167 Water pipes, biofilms, 115 Wedge clams, 450, 468 West Africa, 218, 415, 422, 438 food for demersal fish, 443 West African coast, 453 shelves, 437 West Mariana Basin, 13, 16 Western Australia, 412 Wind and surf-zone diatoms, 166, 167 Xanthin degradation, 321 Yakushima, 53 Yap Ridge, 13 Yeasts, pathogenic, 310 Yellow coral, 437, 438 Yellow Sea, 26, 41, 42, 43 Warm Currents, 41–43; 36, 37 Yucatan, 390