Advances in Marine Biology, Volume 8

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Advances in

MARINE BIOLOGY VOLUME 8

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 8 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press

London and New York

*

1970

ACADEMIC PRESS INC. (LONDON) LTD. BERKELEY SQUARE HOUSE BERKELEY SQUARE LONDON, W l X 6 B A

U S .Edition published by ACADEMIC PRESS INC.

111 FIFTH

AVENUE

NEW YORK, NEW YORK 10003

Copyright

0 1970 by

Academic Prass Inc. (London) Ltd.

All rights reserved

NO PART O F THIS BOOK MAY B E REPRODUCED I N ANY FORM BY PHOTOSTAT, MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM T H E PUBLISHERS

S B N : 12-026108-1 Library of Congress Catalog Card Number: 63-1 4040

PRINTED IN GREAT BRITAIN B Y THE WHITEFRI4RS PRZSY LTJ). LONDON AND TONBRIIJGE

CONTRIBUTORS TO VOLUME 8 GORDONA. RILEY,Institute of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada. C. F. HICKLING, 95 Greenway, London N 2 0 , England.

A. NELSON-SMITH, Department of Zoology, University College of Swansea. Swansea. Wales. KOHMANY . ARAKAWA, Hiroshima Fi&eries E~perimentaZ Station, Ondo, Hiroshima, Japan.

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CONTENTS CONTRIBUTORSTO VOLUME8

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V

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1

Particulate and Organic Matter in Sea Water GORDONA. RILEY

I. Introduction

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11. Distribution of Particulate Organic Matter in the Sea .. .. .. .. .. A. Methods .. B. Visual Examination of Non-living Particulate Matter C. Particulate Organic Carbon . . .. .. .. I .

111. Chemical Composition .. A. Elementary Composition B. Biochemical Composition

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C. Relationships of Organic and Inorganic Materials..

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29 29 32 36

IV. Experimental Studies of Non-living Particulate Matter. . A. Adsorption on Bubbles .. .. .. .. €3. I n situ Production and Utilization . . .. .. .. .. ,. .. C. Sinking Rates . . ..

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.. .. .. .. V. General Discussion . . .. A. Re-examination of the Aggregation Process .. B. Dynamics of Production and Consumption of Nonliving Particulate Matter in the Sea .. ..

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VI. References

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40 49 66

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79 112

viii

CONTENTS

Estuarine Fish Farming C. F. HICKLING

1. Introduction . . .. .. .. .. .. A. From Primitive Fish-corral t o Fish Farin . . B. Definition of Estuaries as Sites for Fish Farms

II. Suitability of Estuaries as Sites €or Fish Farms . . A. Their Topography .. .. . . .. B. The Fertility of Estuaries . . .. .. 111. The Species Cultured .. . . .. A. Selection of Organisms by Salinity . . B. The Natural History of the Species..

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IV. Sources of Young Fish and Prawns .. A. Non-breeding and Artificial Breeding B. The Fish Fry and Prawn Fry Industry C. Care and Rearing of Fry .. ..

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V. The Food of Cultivated Fish and Prawns.. .. . . 164 A. Chams, Grey Mullet, Eels, Tilapia and Prawns . . 164 B. Culture of Algal Pasture . . .. .. .. 170 Vl. Management of Brackish-water Fishponds A. Tilapia . . .. .. .. .. B. Russian Limans .. .. .. C. Hawaiian Fishponds . . .. .. D. Brackish-water Ponds at Arcachon . . E. North Italian Lagoons .. .. F. Bheris of West Bengal .. .. G. Prawn Ponds of Singapore . . .. H. Fish and Prawn Culture in Paddy Fields

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178

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178 180 181

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CONTENTS

I. Chanos Culture in Java .. .. J. Chanos Culture in the Philippines . . K. Fishpond Management in Japan . .

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198

VIII. Profitability . . .. .. .. .. A. Need for a Large Pond Area.. .. B. The State of the Industry-Progress, . . .. . . and Decline . . C. Need for Long-term Credits . , ..

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199

L. Fish Culture in Taiwan

VII. The Rate of Fish Production

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193 194

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Stagnation

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201 204

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215

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219 224

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111. Properties of Petroleum Oils .. .. * . A. Physico-chemical Characteristics . . B. Behaviour of Spilt Oil on Sea and Shore . . C. Detection and Identification.. .. ..

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234

Effects of Oil Pollution .. .. .. A. Mode of Action and Toxicity of Oils

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IX. Is There a Future for Estuarine Fish Farming! X. References . . .. .. . . 1 .

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205

The Problem of Oil Pollution of the Sea A. NELSON-SMITH

1. liitroductioii

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11. Sources and Control . . . . .. .. A. Tanker Operation and General-cargo Shipping B. Harbours and Marine Terminals .. .. C. Coastal Industry and Other Sources .. a

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IV.

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234 236 240 243 243

B. C. D. E. V.

Effects on Marine Communities .. . . .. Carcinogenesis . . .. Rehabilitation of Oiled Birds .. Public Amenity and the Tourist Industry

Removal of Spilt Oil..

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A. Bacterial Degradation and Other Biological Processes 266 B. Dispersal, Sinking and Recovery at Sea . . .. 271 C. Problems in Cleansing Shores .. .. .. 274 D. Mode of Action and Toxicity of Solvent-emulsifiers 280

VI. Conclusions and Prospects . . VII.

References

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288

Scatological Studies of the Bivalvia (Mollusca)

KOHMAN Y. ARAKAWA

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307

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309

111. Morphology . . .. .. .. .. A. Classification of Faecal Pellets .. B. Definition of Pellet-Types . . .. C. Descriptions of Faecal Pellets .. I. Protobranchia (Gastroproteia) 11. Septibranchia (Gastrodeuteia) 111. Gastrotriteia . . .. .. IV. Gastrotetartika .. .. V. Gastropempta . . .. ..

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345

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Introduction

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11. Material and Techniques

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317 320 334

xi

CONTENTS

IV. Biological Significance of the Characteristic Form of .. .. .. .. .. . . 379 Faecal Pellets A. Relation of Faecal Characteristics to the Feeding Habit and Mode of Life of the Animal . . . . 379 B. Relation of Faecal Characteristics to the Structure and Function of the Digestive Organs . . .. 381 V. Use of Faecal Pellets as a Systematic Index

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VII. Biodeposition of Suspension Feeding Bivalves . . .. A. Factors Influencing Biodeposition .. .. B. Daily and Seasonal Aspects of Biodeposition . . C. Effects of Biodeposition upon Various Marine .. .. .. Environmental Conditions

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VI. Evolutionary Trends of Faecal Pellets

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TAXONOMIC INDEX ..

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459

CUMULATIVEINDEX OF AUTHORS. .

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VIII. Bibliography IX. Plates

AUTHOR INDEX

SUBJECTINDEX

CUMULATIVE I N D E X O F

TITLES

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facing page 436

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Arlu. mar. Biol., Vol. 8, 1970, 1-118

PARTICULATE ORGANIC MATTER IN SEA WATER GORDONA. RILEY Institute of Oceanography, Dalhousie University, Halifax, Nova Scotia, Canada

.. .. I. Introduction . . . . .. .. .. .. .. .. .. 11. Distribution of Particulate Organic Matter in tho Sea .. .. .. A. Methods .. .. .. .. .. .. .. .. .. T3. Visual Examination of Non-living Partirulnto Matter .. .. C. Particulate Organic Carbon .. .. .. .. .. .. 111. Chemical Composition . . .. .. .. .. .. .. .. A. Elcrncntary Composition .. .. .. .. B. Uiochemical Composition. . . . .. .. .. .. . . . . .. C. Relationships of Organic and Inorganic Materials .. .. .. IV. Experimontal Studies of Non-living Particulate Matter .. A. Adsorption on Bubbles . . . . . . .. .. .. . . B. In situ Production and Utilization .. .. .. .. .. .. C. Sinking Rates .. .. .. .. .. .. . . . . .. V. General Discussion .. .. .. .. .. .. A. Re-examination of tho Aggregation Process . . .. . . B. Dynamics of Production and Consumption of Non-living Particulate Matter in the Sea .. . . .. .. .. . . .. VT. References .. .. .. . . .. .. .. .. ..

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7 12 29 29 32 36 40 40 49 66

75 75

79 112

I. INTRODUCTION The non-living organic matter in sea water is ultimately derived from a variety of plant sources, including phytoplankton, attached aquatic vegetation in shallow waters, macroscopic pelagic algae, and waterborne and windborne materials of terrestrial origin. The relative importance of these various sources cannot be stated precisely, but there is little doubt that phytoplankton is the most important source. Phytoplankton production, as determined by C14 fixation, falls within the range of 50-15Og of carbon per m2 in a year in the major ocean basins ; however, some regions, notably the high arctic, are less productive than this and higher levels are attained in some coastal and estuarine waters and probably in oceanic areas of intense upwelling. Recent work suggests that present methods may underrate total 1

2

GORDON A. RILEY

production, but the range that has been given establishes a reasonable order of magnitude. Benthic algae and rooted aquatic vegetation of the shore zone can have a level of production that is an order of magnitude higher than the values given for phytoplankton, and the output from rivers and salt marshes can be very important locally. However, the area where such factors are important is less than 1% of the world oceans, and there is little doubt that phytoplankton provides 90% or more of the basic stock of oceanic organic matter. Although much of the organic matter is used quickly, the accumulated remains of non-living organic matter, particulate and dissolved, are larger than the annual production and much larger than the quantity of living organisms that is present a t any one time. Most of the published data for particulate organic carbon, as determined by passing the water through a filter with a pore size of 1 p or less and analysing the collected material for its carbon content, fall in the general range of 5-50 pg C/litre in deepwater samples and are somewhat higher in the surface layer. A reasonable average for total filterable carbon, summed from surface to bottom in an average water column of 4 000 m would be 100 g/m2. Filter-passing organic substances, commonly denoted as the dissolved fraction but obviously including colloids and any particles small enough to escape the filter, commonly have a carbon content of the order of 0.5 mg/litre as determined by wet oxidation, so that the total quantity in a water column of 1 m2 is about 2 kg. This is roughly two orders of magnitude higher than the amount present a t any one time in living organisms, and this may be a minimum estimate, for there are indications (Skopintsev, 1966) that dry combustion methods yield somewhat larger values. The fact that these organic remains have accumulated in such large quantities, even though most of the products of photosynthesis are consumed quickly by living organisms, is sufficient evidence that they have a slow rate of degradation. The reasons for this are not altogether clear, for biochemical characterization of the material has not proceeded far enough t o give us a detailed picture of composition. We know that some of the dissolved substances are highly refractory and have little biological utility. We also know that there are simple sugars, amino acids, and other substances which are potentially usable ; however, except in near surface waters the concentration of such substances appears t o be too low to provide anything more than bare subsistence for a scanty population of heterotrophs. The situation is similar with respect t o non-living particulate matter. The total stock is large, and some of it is assimilable; however, the

PAItTICULATE ORGANIC MATTER I N YEA \\ATER

3

concentration appears to be too low t o fulfill the requirements of pelagic filter feeding organisms in most of the deepwater column. Particles that sink to the bottom, and are thereby concentrated at the water-sediment interface, supply nourishment to a benthic population of bacteria and animals which is considerably more abundant than the bathypelagic assemblage. One can find many references in the early literature to the presence of abundant detritus in the sea and speculation about its possible utility as food. However, little serious attention was given to the nonliving fraction until the 1950s. Nishizawa et al. (1954) published an account of their observations of particulate matter from a submerged diving chamber and aroused considerable interest and curiosity by demonstrating that some of it was aggregated into much larger particles ,than had previously been described. Bathyscaphe divers reported similar flakes of " marine snow " in various oceanic areas. At that time no one had as yet questioned the traditional concept that nonliving particulate matter was derived by decay of dead organisms, but these observations demonstrated that it could clump into masses of considerable size rather than merely disintegrating into smaller fragments, and this stimulated further interest in the possible utility of this material to filter feeding organisms. Krey et ul. (1957) described a newly developed method for protein analysis and measurement of seston weights, and a series of papers followed, describing their results in various oceanic regions. Riley (1959) made a few measurements of particulate matter in Long Island Sound, including total seston weight, difference on ignition, and estimates of phytoplankton biomass. Some of this was fairly closely comparable t o the kind of data being collected by Krey and his associates. Baylor et ul. (1962) and Sutcliffe et al. (1963) discovered that organic particles could be formed experimentally by bubbling air through sea water. Baylor and Sutcliffe (1963) demonstrated that particles so formed would support the growth of Artemia. Riley (1963), in a further study of Long Island Sound, found particles in natural sea water which were similar in appearance t o the experimental product. All this began to cast serious doubt on the idea that the particulate and dissolved organic fractions in sea water are simple intermediary steps in the degradation of living matter into inorganic elements. Reversals in the process seem to be possible, and newly created particles might re-enter the food chain as bacterial substrates or food for filterfeeding animals. New data and new theories as to their meaning promoted further

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CORDON A. RILEY

work on this subject but did not lead to any real solution of the major problems. The validity of the experimental evidence on particle formation has been challenged. If such particles can indeed be formed in the sea, their natural rate of production remains essentially unknown. Opinions differ as to the suitability of non-living particulate matter as food. Menzel and Goering (1966) took the extreme stand that naturally occurring particles below the immediate surface layer are neutrally buoyant and refractory, neither sinking out of the water column nor being utilized. Riley et al. (1965), on the other hand, proposed the hypothesis that the particulate matter sinks slowly, with a mean residence time in the water column of the order of four years, more or less, and is subject during that time to both utilization and accretion, the two processes existing in a state of dynamic balance. One interpretation or the other seems necessary in order t o explain the observed fact that the concentration of particulate matter is relatively uniform with respect to depth and shows no evidence of decrease in deep water due to biological utilization. The paper that follows will attempt t o resolve some of these difficulties. It will survey existing data on the distribution of particulate organic matter in the sea, experimental work that has been done on processes of production and consumption, and the indirect evidence that is necessary in order t o put the subject into proper oceanographic perspective. The discussion will mainly deal with non-living particulate matter but will of necessity also be concerned with its relations with living organisms and filter-passing organic materials.

11. DISTRIBUTION OF PARTICULATE ORGANICMATTERIN

THE

SEA

A. Methods This section will deal with generalities about methods of collection and analysis. Details about the methods used by individual investigators will be taken up in later sections in connection with the discussion of their work. Measurements of particulate organic matter and studies of its chemical composition require the collection of fairly large water samples. Our laboratory uses Niskin bottles of 8 and 28 litre capacity, constructed of polyvinyl chloride. Menzel (1967) has described an all glass sampler which he built t o avoid any possibility of contamination by plastic materials. However, Gordon (1969) has used both kinds of bottles concurrently and has found no significant difference in the results. Collecting bottles need t o be cleaned frequently. There is a tendency for a bacterial slime film to grow on the inner surfaces, and

PARTICULATE ORGANIC MATTER IN SEA WATER

5

this can cause serious errors. Scrubbing and rinsing with isopropyl alcohol are recommended. Various kinds of filters have been used in this work. For purposes of microscopic examination Millipore filters ars commonly used. A sea water sample of 50-250 ml is filtered ; the pad is then dried and cleared and mounted with cedar oil or Permount. Scrupulous cleanliness is required. All glassware should be rinsed with isopropyl alcohol immediately prior t o use, and distilled water or any stains used in the preparation should be pre-filtered. Most distilled water supplies contain considerable quantities of organic matter which can be converted, on standing, into flake-like particles indistinguishable from some of the materials naturally occurring in sea water. The type of work done by Gordon (1970a), using histochemical stains t o characterize the kinds of particles found in the sea, requires fairly extensive treatment with reagents and rinses. He found it necessary to monitor the operation by running frequent reagent blanks and correcting his counts, if necessary, for the presence of any extraneous particles. Millipore filters also have been used frequently for any purpose requiring the water to be freed of filterable particles. Various pore sizes have been used, ranging from 0.22-5 p. If the filtered water is to be used for experimental purposes, the filter should be pre-rinsed. Glass fibre and more recently silver filters have been used to collect material for measurements of total carbon or any other analysis requiring a filter that is relatively free of organic matter. Actually neither type is ideal. They contain carbon that cannot be entirely removed by baking a t the relatively low temperatures that they can tolerate (about 40O0C), and in some cases baking has produced an undesirable increase in the pore size of silver filters. Experience has shown that 0.8 p silver filters contain less carbon than most of the others, and they may be used without baking. However, there is enough variation from one batch to another so that blank determinations on each batch are necessary, and fairly large water samples should be used in order to minimize errors due to variability of the blanks. Silver filters, like the Millipore filters, have the advantage of graded pore size, whereas the glass fibre filters have pores of varying sizes. However, the writer has found no marked difference in the total catch obtained by a fine glass filter as compared with 0.46 p silver filters, nor did Gordon (1969) obtain significant differences when he filtered aliquots of sea water samples through silver filters of different pore sizes. Sheldon and Sutcliffe (1969) examined this situation further, using

a Coulter Counter to determine the spectrum of particle sizes before and after filtration. They found that filters removed almost all of the particles larger than a given pore size, but they retained a considerable fraction of smaller particles that theoretically could have passed through. Thus the filters are not suitable for quantitative size fractionation. This result helps t o explain the observation (Menzel, 1966 ; Batoosingh et al., 1969) that immediate refiltration of a sea water sample will give an additional yield, presumably consisting of particles smaller than the pore size of the filter, which are retained imperfectly but to a measurable degree during subsequent filtrations. Menzel, in the paper cited and in subsequent ones, also suggested the possibility of adsorption of dissolved organic carbon, but this seems unlikely. P. J. Wangersky (personal communication) filtered sea water through a dialysis membrane which removed all organic materials except dissolved substances with a molecular weight of less than 10 000. He then passed the water through silver filters and found no significant increment in organic carbon; however, there was an indication of a slight amount of adsorption on glass fibre filters. After filtration the samples are kept in a dried or frozen state until analysis. Both wet oxidation and dry combustion have been used in the determination of total organic carbon. For a detailed description and discussion of these methods the reader is referred to Wilson (196l), Menzel and Vaccaro (1964) and Strickland and Parsons (1965). Strickland and Parsons also described methods for determining protein, lipid, carbohydrates and crude fibre with sufficient sensitivity to be used in the analysis of naturally occurring particulate matter. Krey et al. (1957) developed a method for determining protein in particulate matter by means of the biuret reaction. They then used a conversion factor t o estimate the quantity of living material. The difference between total dry weight and the calculated biomass was then regarded as detritus. This method, with some later elaboration, has been used widely by Krey and his co-workers and provides useful comparative data in the various regions studied. However, this work cannot be compared directly with the data of other investigators, for there is some protein in non-living particulate matter, and the detritus is by no means exclusively organic material. In addition to these general and widely used methods, there will be references in a later section t o various biochemical studies of a more limited nature, and the reader is referred to the original literature for the methods used.

PARTICULATE ORGANIC MATTER I N SEA WATER

7

B. Visual exam,ination of non-living particulate matter 1, General appearance Fig. 1 shows some common types of particles found in sea water. The most obvious ones, particularly in the surface layer, are amorphous masses of material, which will be familiar to everyone who has examined sea water samples. They have commonly been called detritus, although identifiable plant or animal remains are only occasionally evident, and generally as small inclusions rather than constituting the main mass of material. They appear to be flocculated masses of smaller particles rather than decomposing bodies and are similar in general appearance to bacterial slime films that are found growing on submerged surfaces. Riley (1963) called this material organic aggregates, a term that was purposely vague as to mode of origin but served to distinguish them from detritus of identifiable structure. As seen in this figure the aggregates have been flattened on the slide and dried, and they appear more consolidated than they really are. They have been observed in a free floating state in the chamber of an inverted microscope, where they appear as more or less rounded masses. They are delicate and tenuous, with internal spaces that harbour a flora of bacteria, small algae and sometimes protozoa. Pomeroy and Johannes (1968) have provided an excellent account of this assemblage of organisms, which they designated as ultraplankton. One suspects that these microcosms might have quite a different environment from that of the free water, although the quantity of organisms is not large enough t o suggest a rich supply of nutrients. The median diameter of these aggregates in most sea water samples is of the order of 25-50 p. However, there is a wide spectrum of sizes. Particles of one millimetre or more in diameter are not uncommon, and on rare occasions sheets of material and slimey strings of the order of centimetres long have been observed in tide rips. Gordon (1970a) reported that the aggregates stain heavily with Schiff reagent and apparently consist mainly of carbohydrate material. There was virtually no reaction t o lipid stains, and the protein reaction (brom phenol blue reagent) was variable and generally light, except in associated living organisms. Fig. 1 also shows some small, semi-transparent flakes, which are important components of the non-living particulate matter although much less obvious than the aggregates, Indeed the writer has found no reference t o them in the literature prior to his account (Riley, 1963) of their natural occurrence in sea water. They may have escaped the notice of earlier workers or may have been regarded as inorganic

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GORDON A . RILEY

FIG.1. Millipore filtor preparat'ions of part,iculatc organic matter, magnification x 200. (a) Surface sample, Nova Scotia coastal water, with two amorphous aggregates above and flakes below, indicatcd by arrows. (b) A similar surface sample treated with brom phenol blue (protein stain). Flakes show typical deep st,aining reaction. (c) A mid-depth collection (850 m, Slope Water south of Nova Scotia), also treat<ed with protein stain. (d) Particle format,ion in fi1t)eredsea water (carbohydratc stain). The aggregations that can be seen dimly in several parts of the slide are of the type charact,erizecl(section IV, B) as '' pale primordia *' of naturally occurring aggregat,es. There arc numcrons smaller particles which do not show clearly becrtuso of t>hofiltor background.

PARTICULATE ORGANIC MATTER I N SEA WATER

9

inclusions. I n fact the writer did not include them in routine counts until it became apparent that they were visually indistinguishable from experimentally produced organic particles of the type which Baylor and Sutcliffe (1963) demonstrated to be adequate food for the growth of Artemia. Later Gordon (1970a) showed that they react intensely to protein and carbohydrate stains. His counts of stained material were invariably larger than those of unstained aliquots. Some of this material is so nearly transparent that it eludes detection except by staining treatment. The median size of the flakes is about 25 p in their longest dimension. The size range is not large, and few of them are more than 50 p. Gordon categorized two types of larger particles that are found occasionally, which exhibited the same kind of staining reactions as flakes but otherwise were somewhat different in appearance. One type was long and narrow; the other resembled a clump of smaller flakes. It is still an open question as to whether they are different in any really significant way and whether the clumping is a natural phenomenon or an artifact of preparation. Aside from the aggregates and flakes, most samples contain a number of minor organic components such as more or less recognizable remains of phytoplankton and zooplankton, fibres, occasional faecal pellets, and starch grains. Bursa (1968) has described the starch grains that he has found in sea water and plankton samples, sometimes in great abundance a t Arctic stations, with which he was particularly concerned. Similar material was found a t inshore locations in tropical and subtropical waters. The writer has occasionally seen identifiable starch grains in offshore water although never in abundance. However, some of Bursa’s photographs of semi-hydrolyzed grains suggest that there might be difficulty in distinguishing between starch and flakes in some cases unless specific staining procedures are used. The problem of identifying non-living particles is certainly not easy, and further study is in order. Small particles of the order of 5 p down t o the limits of visibility are numerically more abundant than the larger particles. Many of them show organic staining reactions, but visual examination gives little clue as to their origin. Traditionally they have been regarded as breakdown products of larger remains. However, Sheldon et al. (1967) documented spontaneous formation by aggregation of smaller entities, and Chave (1965) has detected coatings of adsorbed organic matter on particles of calcium carbonate. Conceivably other minerals could be similarly coated. Thus the small particles probably are of diverse

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GORDON A . RILEY

origin and composition, but their appearance is not distinctive enough t o encourage attempts t o classify them. 2. Seasonal cycles in inshore waters

Riley (1963) described a two-year study of particulate matter in Long Island Sound based largely on counts and measurements of particles. The results were quite similar to earlier work by Krey (1961) whose examination of the seasonal cycle in the Kiel Bight consisted mostly of protein analyses and seston weights. The following generalizations apply t o both surveys : the level of non-living particulate matter was moderately high in midwinter, when the quantity of phytoplankton was small. It increased further to a peak that more or less coincided with the peak of the spring diatom flowering and thence declined to the lowest point of the year a t about the time of the termination of the flowering. The quantity was relatively small during most of the summer and autumn. The only major difference in the two seasonal cycles was an early summer peak in Long Island Sound, a period of the year when the quantity was low a t Kiel. Within the traditional view that non-living organic matter consists mainly of detritus derived from the death of organisms, certain aspects of these results would be puzzling. Lower values would be expected during the midwinter period of phytoplankton poverty, and increases associated with phytoplankton flowerings should be most pronounced during the terminal stages of the flowering rather than near the peak. However, these new developments cast another light on the problem. An increase coincident with the flowering would be expected if extracellular metabolites could be converted to particles, and mixing processes associated with winter storms might have been responsible for the observed increase in particulate matter during early winter. There was some evidence to support these hypotheses. The number of flakes was larger in winter than in summer, and the yield of particles obtained by bubbling filtered sea water more or less followed the seasonal trend of naturally occurring seston during winter and spring. However, in the absence of any really good methods for determining rates of particle production in nature such hypotheses remain speculatory. 3. Particle counts in offshore waters

The methods developed for counting and measuring particulate matter were subsequently applied t o a series of surface collections obtained on a transect from the Sargasso Sea south of Bermuda to the coast of Africa a t about SON (Riley et al., 1964) and a series of surface

PARTICULATE OKGANlC MATTER I N SEA IVATEIL

11

and deepwater samples taken off Bermuda on a more or less seasonal basis (Riley et al., 1965). I n the first paper cited the general range in particle number was 5-40 x 103 per litre. Lowest values were found in the Sargasso Sea and non-upwelling tropical areas ; the highest ones in a region of upwelling in the Guinea Current. There the number of particles intergraded with the general range of 30-100 x lo3 per litre which had been found in Long Island Sound. I n all of these studies the measurements of particles size were used in conjunction with counts to determine their total area as they appeared on the filter in mm2/litre. This was only a crude measurement and could not be converted into an estimate of the volume of material ; however, a measurement of this type was regarded as a necessary precaution against the possibility of variations in mean size of particles from one area to another. I n this set of data the general range of values was 6.3 t o nearly 40 mm2/litre as compared with about 20-160 mm2 in Long Island Sound. From these data on numbers and areas it is apparent that non-living particulate matter varies regionally in much the same way that phytoplankton does, and in fact in the subtropicaltropical transect there was a correlation of 0.95 between area of particulate matter and phytoplankton cell counts. The regression equation was

A

=

0.127C

+ 8.0

where A = organic aggregates in mm2/litre, and C = thousands of phytoplankton cells/litre. The form of the equation is indicative of the fact that even when phytoplankton is scarce there will be a considerable amount of non-living particulates present. The additional amount that is correlated with phytoplankton abundance may be detritus derived from dead cells or it might be particles that have been produced from extracellular metabolites. The latter point was examined experimentally by growing cultures of seven species of diatoms and one dinoflagellate in artificial sea water of minimal organic content and then removing the cells and bubbling the medium. The particulate carbon produced by the bubbling process averaged 20% of the carbon content of the diatoms that had been removed ; however, in the case of the dinoflagellate it was only 2y0. Riley et al. (1965) described six sets of observations obtained on a seasonal basis during the period from April 1963 t o April 1964. Three sets were obtained a t a station about 27 km southeast of Bermuda, a position routinely occupied by various oceanographers working at the Bermuda Biological Station. The other three sets were cruise data taken over a wide area and ranging between 21' and 36"N Lat.

12

G U S D O N -4. RILEY

Mean particle counts in all samples were as follows : surface 11.32 x 103/litre; 100-200 m, 9.20 ; 500-900 m, 7.51 ; 1 000 m 7-86. Measurements of the area of the aggregates and of particulate carbon gave a similar picture of vertical distribution, with a decrease in the upper layers and only slight and random variations in the water below about 500 or 800 m. There was some seasonal variation in particle counts and areal measurements, with largest values in winter and spring, more or less corresponding with seasonal variations in phytoplankton in that area. There was also a seasonal variation in deep water. Much of the discussion in the paper cited was devoted to an attempt to rationalize these deep water seasonal dhanges and the fact that there is not a systematic decrease in particulate matter with depth. Continuation of these discussions is relegated to later sections of this paper. Gordon (1970a) refined the earlier methods for microscopic investigation and expanded the regional coverage of the North Atlantic. He developed methods for cleaning the filtering apparatus and making blank determinations, because it became apparent that contaminants could be involved which were indistinguishable from naturally occurring organic particles. He also used histochemical stains, the mercuric bromphenol blue method of Mazia et al. (1953) for proteins and the Schiff reagent for carbohydrates. Gordon obtained significantly higher counts with stained slides than with unstained material. The flakes, in particular, are often so nearly transparent that they can be missed in routine counts. Therefore his counts are probably more accurate than previous ones but are not directly comparable with those in earlier work. Gordon’s sampling areas ranged widely from the Sargasso Sea to the Irminger Sea. Mean particle numbers were of the general order of 100/ml in near surface waters, and 12-27/ml in deep water. The Nova Scotia and Newfoundland shelf and slope areas were somewhat richer than offshore waters, as might be expected, but regional differences were not pronounced.

+,

C. Particulate organic carbon 1. Regional variations and vertical gradients Wangersky and Gordon (1965) obtained extensive data on particulate organic carbon in subtropical and tropical waters along two transects between the coast of Africa and a point several hundred miles southeast of Bermuda. This was a cruise of the “ Trident ” in 1963, during which the material for particle counts described by Riley et al. (1.964) was also collected.

PARTICULATE ORGdNIC MATTER IN SEA WATER

13

Wangersky and Gordon demonstrated that there was a major concentration of particulate carbon in the immediate surface layer, a t least under the calm conditions prevailing during most of their cruise. Surface bucket samples taken in the Guinea Current had concentrations ranging from 300 t o 800pgC/litre, in contrast t o about 55-2OOpg C/litre in water bottle samples from depths of 13-15 m. I n less productive areas most of the bucket samples had values of 20-120 pg C/litre. Slightly deeper collections, some with the bottles barely submerged or a t most a t a depth of 10 m, were of the order of 14-58 pg. Williams (1967) developed methods for collecting a thin layer of water near the surface and compared organic carbon and various other determinations in these samples with subsurface concentrations. His work confirmed and extended previous conclusions as to the existence of a large vertical gradient in near surface waters. There is of course a tendency for bacteria, nanoplankton and non-living particulate matter to become adsorbed a t the surface film, although pronounced vertical turbulence tends t o disrupt the film and drive some of this material into deeper water. A certain balance between these processes presumably is responsible for the observed vertical gradient. The observations that have been described were obtained mainly in calm weather, because surface film collection becomes increasingly difficult in rough water. Hence such observations represent an extreme development of near surface gradients. However, later evidence will indicate that there is a measurable and biologically important accumulation of particulate matter a t the sea surface a t higher sea states. Most of the investigations of organic carbon in the surface layer of the sea have employed serial casts of various kinds of collecting bottles, with the uppermost bottle a t a depth of a metre or more, so that surface film effects were slight or negligible. These investigations have not been extensive enough yet t o provide a clear picture of either regional or seasonal variations ; however, the available information should be summarized in order to give a general idea of areal coverage and degree of variation. Menzel and Ryther (1964) described some observations obtained in January 1962 between 41" and 37"N Latitude in the western Atlantic, which thus included both temperate and subtropical waters. Another cruise in April of the same year obtained a line of stations between 42'30" and 20"N along the 65"W Meridian. Their Fig. 1, which apparently includes only observations north of the Gulf Straam and includes all data taken in the upper l o o m , shows a total range in January of about 25-200 pg C/litre, with a large majority of observations between 35 and 95 pg. I n April the general range was of the

14

GORDON A. RILEY

order of 53-330 pg C/litre, with about two-thirds of the observations between about 110 and 220 pg. Riley et al. (1965) took about 20 near surface sampIm in the vicinity of Bermuda. The average of March-April samples, which probably represented spring flowering conditions, was 168 pg C/litre, and averages obtained during other seasons ranged from 46 to 111 pg C. Gordon (1970b) compiled data for some 60 surface layer analyses in various parts of the N. Atlantic. I n the Irminger Sea in April-May 1966, the mean of 11 samples was 44 pg C/litre. I n April-May 1967, a line of stations across the temperate N. Atlantic a t approximately 40"N averaged 87 pg. Three cruises were made t o Nova Scotia and Newfoundland shelf and slope waters, and cruise averages ranged from 41 t o 176 pgllitre, the largest values being obtained in April 1968. Five cruises t o the Sargasso Sea yielded averages of 29-142pg, and again the largest values were in April. A few surface water values have been reported for other oceans. I n general they fall within the same range and are similarly variable. One report of considerable interest is that of Szekielda (1967), whose study of the Somali Current off the east coast of Africa revealed a series of bands of high and low carbon content running parallel with the coast. These were believed to be associated with localized upwelling. I n areas where the temperature and salinity structure were indicative of vertical water movement there was an upward thrusting of mid-depth water of relatively low carbon content. I n the immediate surface layer the situation was less clear cut. Theoretically there wilI be a low particle content in newly upwelled water, but this will give way to high values as phytoplankton develops in the new water. Szekielda's data suggest that both phenomena may have been present in different parts of his profiles. This is clearly a case where one needs to know something about relative proportions of living and non-living matter in order t o understand the data on total carbon. Below the immediate surface layer there is almost invariably a decrease in total particulate carbon. The gradient may be quite sharp and of limited vertical extent or it may continue more gradually through most of the main thermocline, but a t some depth of the order of 200-800 m an essentially deep water situation is reached in which carbon concentrations generally are low and relatively uniform, although in some cases pronounced increases have been noted in association with particular water masses. However, there is little or no systematic decrease with depth. I n deep water a large proportion of the total organic carbon is non-living, so that quantitative assessment of that fraction is simpler

PAltTICULATE ORGANIC MATTER 1N S E A WATER

15

than in the sur€ace and transition layers. Also, the quantity found in any one area does not ordinarily vary seasonally, although certain exceptions will be noted, so that regional comparisons are possible, even though the amount of data available for the purpose is still fairly small. Thus the deep water observations deserve a more thorough analysis than was possible in the case of surface layer data. Most of the papers cited above in connection with surface observations also included deepwater data, and a few others are included in

'

+

+ 5 0

FIG.2. Deepwater values for particulate organic carbon (pgilitre) in the North Atlantic Ocean. Each number is an average of all values below 1 000 m at a station or in some cases a group of stations in approximately the area indicated. See text for further details and references to the original published data.

the general compilation of deepwater averages shown in Fig. 2. These numbers were obtained by averaging all values below 200 m for a given station or a group of stations of similar characteristics, so that a single average is derived for a given area. This is justified on the grounds that observed vertical variations in the North Atlantic Ocean tend to be of an essentially random nature. The variations often exceed the analytical error, but present sampling methods, which admittedly have not been as closely spaced as might be desired, have shown little indication of a systematic change with depth or maxima and minima

16

GORDON A. RILEY

that would imply an association with particular water masses. A single exception to this generalization is noted in a station figured by Menzel and Ryther (1964). This station was a t 38"N 65OW. The mean deepwater carbon was about 74 pgllitre ; there was a large variation of about 48-106 pg, with a pronounced maximum a t a depth of 2 000 m. The authors did not comment on possible water mass relations, but waters at this depth commonly lie within the upper limits of the North Atlantic Deep Water. The same investigators also graphed a station a t 36"N 6 5 " w , which is included in Fig. 2, and Menzel and Goering (1966) presented average data for two lines of stations in the western tropical and subtropical North Atlantic and a station in the Caribbean in which the concentrations were essentially constant with respect t o depth below 200 m and averaged about 18 pg C/litre. Wangersky and Gordon (1965) obtained observations in waters underlying the Guinea Current in a general depth range of 400-1 200 m, where large values were obtained. They also made deeper stations farther offshore in non-upwelling areas of the tropical Atlantic and in the southeastern Sargasso Sea. These declined toward levels of the sort observed by Menzel and Goering (1966) in the western Atlantic. Riley et al. (1965) published data obtained from waters near Bermuda on a more or less seasonal basis. Observations obtained between November and January were markedly higher than other times of the year in all deep water samples, and two values are given for this area, representing winter and summer averages. This rather remarkable seasonal change, later confirmed in other years by Gordon (1970b), will be discussed later. The latter author is credited with most of the remainder of the observations in the North Atlantic, but Duursma (1960), who did classical work on dissolved organic matter in the North Atlantic, provided data on particulate carbon at one station which is included in the figure. Observations in other oceans are inadequate for regional charting, but a brief review of the literature is in order. Parsons and Strickland (1962a) analyzed eight samples taken in depths of 500-3 000 m in the temperate North Pacific and obtained a mean value of about 5 0 p g C/litre. They also made a biochemical study of this material which will be discussed in a later section. Dal Pont and Newell (1963) reported carbon and nitrogen values for a station in the South Pacific a t approximately 34'5 153"E. Thirteen samples taken between 237 and 4 210 m averaged 96 pg C/litre. The total range was 36-207pg, and vertical variations in carbon content appeared t o be associated with particular water masses.

PARTICULATE ORGANIC MATTER I N SEA WATER

17

There was a sharp increase in carbon t o a maximum of 150 pg/litre at the level of t he intermediate salinity minimum, which presumably represents the core of the Antarctic Intermediate Water. Lower values of 36-82 pg/litre were found between about 1 400 and 3 300 in. The deep salinity maximum lies within this zone. This salinity maximum is believed t o be due t o the influence of North Atlantic Deep Water which leaves the Atlantic Ocean around the southern tip of Africa and traverses th e southern part of th e Indian and Pacific Oceans as a northern component of the general Antarctic circumpolar drift. Values at 3 763 an d 4 210 m were respectively 207 a n d 106 pg C/litre. Probably this is primarily Antarctic Circumpolar water. Holm-Hansen et nl. (1966) described a station off California, which also showed considerable vertical variation. There was a general increase at t he depth of the oxygen minimum layer with a maximum concentration of 100 pg C/litre. Most of the deepwater values were between 20 a nd 6 0 p g C/litre, b u t here too there was evidence of distinct layering. This station was taken in one of the deep basins off the California coast, and in several respects it was not quite typical of open oceanic conditions. There is a possibility t h a t the unusual amount of variability observed here was associated with peculiarities of basin circulation. However, in the present state of our ignorance an equal possibility exists t h a t closer sampling intervals at oceanic stations would reveal a similar degree of layering. Hobson ( 1 967) reported th e results of six cruises t o a n area in the North Pacific between 45" and 48"N and 135-140"W. There was a large range in deep water values, from 8-110 pg C/litre, with considerable layering and with systematic seasonal variations, which appeared to represent a movement through th e profile of discrete parcels of water with relatively high concentrations of 30-1 10 pg C/litre. Computed currents were more or less in accord with the concept of seasonal transport of water masses through th e area. Menzel (1964) published figures for two stations in the Arabian Sea. Individual analyses in waters of 200 m or more ranged from 17-80 pg C/litre, and the average values for the two stations were 32 and 35 pg. Menzel's work was primarily concerned with dissolved organic carbon in the western Indian Ocean, and his data on particulate matter were incidentaI t o the main purpose. Later work by Szekielda (1967) provided more extensive coverage of this region, including transects off the Somali coast an d one across the Gulf of Aden. I n general his values were higher t ha n those reported by Menzel. The lowest ones obtained were of the order of 60 pg C/litre, an d they ranged upward t o about 140pg in the core of the Red Sea outflow an d in near-bottom waters

18

GOItDON A. RILEY

of Antarctic origin. Thus there were definite indications of water mass effects in his profiles. 2 . Discussion of results

(a) Methods. The various investigators who contributed to present knowledge about the distribution of particulate organic carbon have used a variety of methods in almost every phase of the work. Thus the question naturally arises as t o whether the results really are comparable. This problem has largely been dealt with in the methods section in connection with the intercomparisons made by Gordon (1969) of various pore sizes of filters and of plastic versus glass Sampling bottles. I n no cases were there significant differences. His carbon analyses were carried out in part on an F. & M. Model 185 CHN analyser and partly in an apparatus assembled by P. J. Wangersky, which involved dry combustion and determination of the CO, in a Beckman infra-red analyser. He also arranged with D. IV. Menzel for an intercomparison of determinations by the method of Menzel and Vaccaro (1964). Again no significant differences resulted from differences in methods. This removes much of the uncertainty from regional comparisons of the type that is intended here. To be sure, great care must be exercised in maintaining cleanliness in sampling bottles and filtration techniques, and corrections for the carbon content of filters are always troublesome. Some investigations, and particularly the early ones, may be in error due to failure t o recognize all of these problems. However, there are no indications of gross error that warrant discarding any of the early data. But there is no simple solution to the problem of analysing particulate organic matter. Ranging in size from macroscopic particles t o colloids, it cannot be sampled quantitatively by any filter now in use, nor is there any present filter that effects a precise size fractionation. Further study of size spectra is needed, but for routine examination of regional variations the prime requirement is for general agreement on a standard method, and as is usual in such cases, some compromise is necessary. A fairly large quantity of water must be filtered in order to minimize errors in blank determinations, and this is inconsistent with the use of filters with very fine pores, which would be desirable in order t o retain small particles. I n practice, silver filters of 0.8 or 1.2 p pore size appear to be a good compromise. Menzel (1967) assumed that dissolved organic matter is adsorbed on filters and attempted t o correct this. Subsequent papers by Menzel and Ryther (1968a and b) did not provide details as t o whether similar

PARTICULATE ORGANIC MATTER IN SEA WATER

19

corrections were made. However, in all three papers the values reported for particulate organic carbon were considerably lower than most analyses previously reported. As indicated earlier, preliminary work by P. J. Wangersky (personal communication) has shown no evidence that dissolved organic materials with molecular weights of less than 10 000 are adsorbed t o an appreciable extent on silver filters. Thus a correction factor probably is improper, and in either case these analyses are not comparable with older data and cannot be included in the general regional analysis. (b) Regional variations in organic carbon. As far as the surface layer is concerned, present data are insufficient to draw conclusions about seasonal cycles or regional variations. I n areas where data are available for more than one season, large variations have been observed, and in most cases the highest values have been obtained in spring. This is to be expected. A spring diatom flowering in the open sea commonly has a chlorophyll concentration of the order of 2-10 pgllitre, and the carbon content of a phytoplankton crop of this size probably is about 60-300 pgllitre. Thus a large proportion of the total carbon reported during the spring season may be derived from living cells. However, the particle counts described earlier suggest that non-living organic matter also may increase a t this season. At other seasons the quantity of phytoplankton carbon is likely to be at least an order of magnitude lower than a t the height of the spring flowering. Referring again to particle counts, the non-living fraction may then be somewhat larger than the quantity of phytoplankton carbon. No great improvement in our knowledge of particulate organic matter in the surface layer will be obtained until more information is available on seasonal cycles of organic carbon and on fractionation into its different components. A semiquantitative estimate of phytoplankton carbon can be made on the basis of chlorophyll analyses; however, chlorophyll : carbon ratios are variable, and there is lack of agreement as to limits of variability. ATP analyses (Holm-Hansen and Booth, 1966) and DNA analyses (Holm-Hansen et al., 1968) possibly will supply a more precise separation of living and non-living fractions. Modern techniques seem more or less adequate for the task, but accumulation of data will be slow. After many years of phytoplankton investigation there are still only a few open ocean areas where we have a satisfactory knowledge of seasonal cycles and average abundance. The larger task of determining total organic matter and its components will also require years t o accomplish.

20

GORDON A . EILEY

While regional coverage of deep water is still fragmentary, there are enough observations for some generalities t o emerge. The total variation is large, but a major proportion of the observations fall between 15 and 100 pg C/litre. I n general there appears to be about a three-fold t o five-fold variation between poor areas and rich ones. Markedly high values have been found underlying the upwelling zone off the west coast of Africa, and the averages decrease to low and relatively constant values through most of the tropical and subtropical regions of the western North Atlantic. Dal Pont and Newel1 (1963) obtained fairly large values in the South Pacific, particularly in waters of Antarctic origin, which presumably are productive. Thus t o some extent, a t least, the magnitude of deep water carbon concentrations is associated with high levels of surface productivity. Temperate waters of the North Atlantic and North Pacific presumably have a level of primary productivity that is above average, and in those areas carbon values tend to be moderately large, although some low ones have also been obtained. Low values were obtained by Gordon (1970b) in the Irminger Sea, which probably is not highly productive on an annual basis, despite good phytoplankton flowerings during the short subarctic summer. More recently he has obtained extremely low values in tropical Pacific waters off Hawaii (personal communication). Menzel (1964) obtained intermediate values in the Arabian Sea, an area that is subject t o seasonal upwelling but probably is not as productive on an annual basis as the west African coast. The west coasts of the Americas should be productive, and moderately high values were recorded by Holm-Hansen et al. (1966) in the California offing. I n summary, there are substantial regional variations in deep water particulate organic matter, which appear t o be related a t least in part to primary productivity in the surface waters above. This presupposes that vertical transport of materials down through the water column is more rapid than horizontal displacement by deep water currents and diffusion. McGill ( 1964) obtained essentially similar results in studies of deep water distribution of organic phosphate, despite the fact that the latter was primarily in dissolved rather than particulate form. However, this is a broad generality, which is subject to exceptions. Deep water transport probably is not negligible, for variations have been reported in carbon concentrations which hardly can be explained in any way other than water mass transport. This will be discussed in the next section.

21

PARTICULATE ORGANIC MATTER I N SEA W A T E R

(c) Temporal variations in deep water. The work of Hobson (1967) in the North Pacific has been mentioned, in which seasonal changes in deep water particulate carbon were explained in terms of seasonal variations in computed currents. I n certain other areas that have been examined on more than one occasion, systematic differences have been noted, for example, in Slope Water south of Nova Scotia (Gordon, 1970b). These have not been examined thoroughly enough to determine whether they are of a seasonal nature or are associated with variations in transport systems. The best documented case of a consistent seasonal variation is in the north-western Sargasso Sea, in the vicinity of Bermuda and northward toward the Gulf Stream. There Riley et al. (1965) obtained a three-fold variation between winter and summer values with highest values in winter. These values, averaged and plotted in Fig. 2, showed similar variation throughout the whole deep water column. Vertical variations in T-S relations suggest that there are several fairly distinct water masses in this area, and the kind of generalized changes that were found obviously could not have been the result of intrusion of a particular water mass. These samples were taken in 1963-64. Subsequently Gordon (1970b) obtained another series of samples in 1966-67, with the results shown in Table I. Results were essentially identical with the earlier ones. TABLEI. NUMBERS OF DEEPWATER SAMPLES AND CRUISE AVERAGES GIVEN BY GORDON ( 1 9 7 0 ~ FOR ) THE NORTHWESTERN SARGASSO SEA No. January 1967 April-May June-July Jan.-Feb. 1968 April

11 61 24 17 20

pg

Cllitre 47.3 19.7 12.3 47-1 8.8

Other variation& of a somewhat similar sort have been noted. McGill et al. (1964) reported a seasonal variation in organic phosphorus in deep water off Bermuda, and to a lesser degree in other stations to the northwest. At Bermuda the highest values were found in winter and were accompanied by a slight increase in salinity. Subsequently Bricker (personal communication) has found seasonal variations in the ratios of Mg and Sr to total salinity, which again extend through the whole water column. .4.WB.-8

2

22

CORDON A. RILEY

The possibility that the observed seasonal change in organic carbon resulted from in situ biological events can be ruled out fairly quickly. The total seasonal increase is of the order of 100 g C/m2 of sea surface, which is equal t o or greater than net phytoplankton production a t the surface. The observed increase therefore cannot be accounted for in terms of sinking of organic matter from the surface, and even if i t could be, the seasonal cycle of phytoplankton production is not of a sort that would lead to a short winter maximum. The other possibility of in situ processes is conversion of part of the dissolved organic matter t o particulate matter. Later information will suggest that such transformations might be possible, but for them to occur on a seasonal basis in an essentially seasonless deep ocean seems unlikely. Moreover, this would not supply a reasonable explanation for the increase in organic phosphorus noted by McGill et al., which included dissolved and particulate fractions. The alternative to in situ changes is a seasonal movement of water of different composition through the area, and this must be a generalized movement from surface to bottom rather than an intrusion of particular water masses. The only presently known source of water with a sufficiently high content of organic carbon to account for the observed winter maximum is the area t o the north, where Menzel and Ryther (1964)reported fairly large concentrations in winter and spring just north and south of the Gulf Stream. The concomitant winter increase in salinity in Bermuda waters is in accordance with such movement, for there is a slight but significant north-south gradient in salinity in the great water mass lying between the Gulf Stream and the tropics. Direct evidence on current movements is fragmentary. This is not an area where estimates of deep currents by geostrophic rrethods are simple and reliable, and no direct current measurements have been made on a year around basis. Even information on surface currents is scanty. Day and Webster (1965) described a series of current observations obtained with a buoy moored a t about 28"N 65"W in which currents were recorded continuously from October 10, 1962 t o January 27, 1963. The long term drift a t this station, located some 250 miles south of Bermuda, was toward the north during the first part of this period, averaging about 8 km/day. I n early January the current veered t o the east and then to the south. During the last two weeks of the observation period the water was flowing south at an average speed of 14 km/day. If currents of this magnitude prevailed over a considerable area, they could move surface water from the vicinity of the Gulf Stream to the latitude of Bermuda in about a month.

PARTICULATE ORGANIC MATTER IN S E A WATER

23

The measurements ended too soon t o determine the length of the period when the water was drifting south. Nor is there any assurance that this kind of event occurs every year or in deep water as well as the surface layer, However, there is evidence of an indirect sort that a flow from the south is re-established by early spring. Some years ago the writer attempted t o calculate coefficients of vertical eddy conductivity based upon temperature data taken in the vicinity of Bermuda. These were to be used for computations of biological rates of change of essential micronutrients. The attempt failed because temperature increases in waters underlying the surface layer were Iarger than the solar input during the spring and early summer and were patently the result of advection of warmer water from the south, so that the problem could not be treated in simple terms of vertical transfer. A hypothesis can be proposed that there is a net northward transport of water past Bermuda during most of the year, with a short period of reversal in winter, and that this is a generalized phenomenon involving the whole water column. This hypothesis does not violate any of the information available, although admittedly the evidence is tenuous. Furthermore, a movement of this sort, which is distributed through the water column rather than involving intrusions of particular water masses, probably is indicative of a change in major circulation patterns in that part of the Atlantic Ocean. Iselin (1936) and Sverdrup et al. (1942) noted that Gulf Stream transport increases northward toward the New England offing and decreases thereafter. Principles of mass continuity are best satisfied by a theory that all of the Sargasso Sea is in a state of slow, clockwise motion around a central high that is located far toward the northwestern edge of the area. Sverdrup’s transport diagram shows about a tenth of the Gulf Stream water peeling off in a tight little gyre in the vicinity of Bermuda. This was only a diagrammatic sketch, which was drawn without any real knowledge of the trajectory of the water past Bermuda, and it merely serves as a reminder that the Sargasso Sea is an integral part of the eddy rather than dead water within the encircling currents of the North Atlantic gyre. The actual geometry of the system can be expected t o change with variations in Gulf Stream transport. Iselin (1940) analyscd all of the information available a t that time which had a bearing on transport variations in the Gulf Stream. There was clear evidence of systematic seasonal variations. His compilation of geostrophic computations and tide gauge records from Miami and Charleston showed that transport was minimal in mid-

24

GORDON A . KILEY

autumn and rapidly rose to a peak in mid-winter. This was followed by a gradual and irregular decline, with a tendency toward a secondary maximum in late summer, and then a rapid drop to mid-autumn. Iselin proposed that an increase in transport would tighten and deepen the central eddy, and Stommel’s (1948) theory of westward intensification suggests that an acceleration of the system could move the position of the centre closer to the Stream. A relatively small shift in the centre could place Bermuda either in the northward drift between the centre and the Stream or in the part of the gyre that moves toward the southwest. Furthermore, expansion and contraction of the central eddy could involve displacements of deep water throughout the whole eddy system as well as in the Gulf Stream itself. This hypothesis provides a framework that can logically contain all of the fragmentary evidence on seasonal variations of conservative and non-conservative properties in the Bermuda area. It also provides a possible reason for a systematic seasonal change which involves only a slight geographical displacement rather than a profound change in circulation patterns. However, this is a limited view of a very complex problem, as will be apparent to anyone who reads Iselin (1940) and other works involving the broad implications of changes in Gulf Stream transport. More thorough study is needed, over a broader area, and until that is done any conclusions are speculatory. If there is any validity in the hypothesis that has been proposed, one would suppose that oceanic areas subject to that kind of seasonal variation would be quite limited. Variations due t o intrusions of particular water masses are likely to be more common. I n the long range view the Bermuda case may seem trivial, hardly warranting the present long and diffuse discussion. However, in the present state of our knowledge a difficult problem such as this one cannot be neglected. Finally, it should be pointed out that although only a few cases have thus far been documented of either seasonal cycles in deep water or vertical variations which can be correlated with specific water masses, other instances are likely to arise. Many oceanic areas are subject t o random or seasonal transgressions of water masses. These movements are not well understood by physical oceanographers, and there are indications here that properties such as organic carbori and phosphorus and ratios of major ions may be more sensitive tools for tracing water mass movement than ordinary T-S relations. Clearly we should move toward a more inter-disciplinary approach to these problems. (d) Small-scale variations in distribution. The earlier account of organic carbon concentrations indicates that there is a large concentration in the surface film and a rapid decrease in the waters immedi-

PARTlClLlLATE ORGANIC MATTER 1N SEA WATER

25

ately underneath. In deeper water there have been occasional indications of microstratification, as in the work of Holm-Hansen et al. ( I 966). Most studies of particulate organic carbon have been based on collections in which the bottles were spaced much too far apart for microstratification t o be detectable as such. However, concentrations frequently vary with depth in an irregular manner. Gordon (1970b) found that most of the observations a t his stations in the North Atlantic were significantly non-random. I n other words, present data indicate that vertical variations exist at all levels from surface to bottom, even though the form of the variation remains obscure. I n Gordon’s comparison of PVC sampling bottles with the Menzel glass-teflon sampler, the bottles were spaced 15 m apart. Here, too, there were significant differences in some of the pairs, although the overall averages were not significantly different, and this suggests that some of the vertical variations may be quite abrupt. Thus the available data on organic carbon provide only hints about small-scale variations in particulate organic matter. However, a t the present time there is increasing interest in non-random distributions of filter feeding organisms and their particulate food, so that a discussion of the problem and an account of indirect evidence on the subject are in order. Baylor et al. (1962) and Sutcliffe et al. (1963) brought forward evidence that organic particles could be produced by adsorption of organic materials on near-surface bubbles. There were indications that phytoplankton and bacteria might also be trapped on bubbles. The net effect would be a concentration of organic materials in the surface, and this could be a t least part of the reason for the near-surface gradients in organic carbon which were discussed above. This local concentration a t the surface is subject to gradual removal by vertical turbulence and convection cells. These are long cells oriented more or less downwind, in which the surface layer moves laterally and downwind into narrow, parallel lines of convergence. Sutcliffe et al. (1963) measured the sinking speed of the water in these convergences and obtained values of the order of 3-6 cm/sec. Between the narrow curtains of descending water, principles of mass continuity require a corresponding upward movement. This is presumably slow and diffuse, for the area between the convergences is much broader. The trajectory of any particular parcel of water in such a cell is probably a spiral motion downwind, although little is actually known about these cells except the surface water movements (Woodcock, 1944) and the downdrafts. In an area such as the Sargasso Sea, where convergences are marked

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GORDON A. RILEY

by accumulations of Xargassum and floating debris, the configuration of the cells can be determined visually over a considerable distance, and the situation is seldom as diagramatically simple as might be implied from the foregoing account. Broad and well-established weed lines are likely t o be interspersed with small and discontinuous ones, and a t wind speeds of about 15 mjsec or more these are in turn interlarded with foam lines and irregular spume patterns which might be the result either of small-scale convective sinking or turbulent exchange. Indeed McLeish ( 1968) has presented theoretical and experimental evidence in support of the hypothesis that turbulence can be responsible for all of the observed surface phenomena and has expressed doubt as to the reality of the classical picture of the Langmuir spiral. For present purposes, the exact form of the circulation pattern is not particularly important. The existence of downdrafts is well substantiated. Commonly, although not always, the water in the downdrafts is slightly cooler than the surrounding water, and when these movements occur in an essentially homogeneous mixed layer, they probably can extend down to the top of the thermocline and can create a vertical transfer of plankton and particulate matter that is biologically significant and is more important than the question of what the remainder of the circulation looks like. For convenience the rest of the discussion will assume the validity of Langmuir circulation, but the conclusions would not be seriously altered by qualifications about the character of the motion. Sutcliffe et ul. (1963) believed that organic particles accumulating in the surface layer would drift into the convergences, providing curtains of particle rich water which might serve as sources of abundant food for zooplankton. They found an increase in turbidity and phosphate in the convergence lines. There was evidence that zooplankton did in fact congregate in such areas, and a paper by Baylor and Sutcliffe (1963) suggested that particles formed a t the surface might provide useful food, for particles produced experimentally in the laboratory supported the growth of Artemia. These results were exciting t o biologists on two counts. I n the first place, although our knowledge of the biochemistry of sea water was limited, and still is, it was apparent that many substances known t o exist in soluble or colloidal form in sea water would be suitable food for filter feeding animals if the material could be aggregated into sufficiently large particles t o be retained by their filtering apparatus. This kind of non-living material appears more promising as food than semi-decayed detritus. Secondly, since the evidence is fairly good that there is a physical

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mechanism which concentrates phytoplankton as well as non-living particles into convective downdrafts, and moreover since zooplankton appears to congregate in these areas, the real environment of zooplankton with respect to its food supply is very different from the impression that we get with our ordinary crude sampling devices. We can expect that the usual zooplankton tow will cut across a number of lines of convergence and will provide a realistic estimate of average zooplankton abundance, although it tells us nothing about microdistribution. Phytoplankton samples are commonly taken from a string of water bottles, They are almost never taken in sufficient abundance to give a true picture of micro-distribution, and by the law of averages most of the samples will be taken in the broad areas between convergences rather than in the convergences themselves. Neither type of observation is realistic with respect t o phytoplankton-zooplankton relations as they exist in nature, but one suspects that the true abundance of zooplankton food materials has been seriously underrated. This should give some comfort to the investigators, too numerous to cite by reference, who have examined zooplankton grazing rates and food requirements in the laboratory and found that the estimated requirements often exceeded the amount of food that appeared to be available in nature. One can hardly deny nature, and there seemed to be some flaw in the experiments. Now it seems likely that the flaw may be in our observations of nature-that food may be more abundant than we realized in the micro-habitats where it is being consumed. What has been said about horizontal micro-distribution in the surface layer applies equally to horizontal layering in underlying thermoclines. There is increasing evidence (Stommel and Federov, 1967 ; Lovett, 1968; Tait and Howe, 1968) that thermoclines are not smooth gradients but rather are laminar structures in which thin, almost homogeneous layers alternate with transitional zones of steep temperature gradient. Theoretically, sinking particles will accumulate in any gradient strong enough t o cause a significant reduction in sinking speed. Many writers have described accumulations of phytoplankton in thermoclines, although seldom in sufficient detail to reveal fine structure. Biggs and Wetzel (1968) found concentrations of particulate carbohydrate, presumably mostly non-living particles, in discontinuity layers. Limbaugh and Rechnitzer (1955) reported that this layering can be sufficiently dense t o be detected visually when diving. Moreover, Harder (1968) demonstrated experimentally that copepods and some other marine plankton organisms tend to congregate a t discontinuity layers. Thus there is abundant qualitative evidence that physical processes

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concentrate small particles in shear zones-vertical convective movements in the surface layer and horizontal shear zones in the thermocline-and that zooplankton tends to congregate in gradients. Interest in this problem is giving rise t o incraasingly sophisticated devices for examining micro-distribution of plankton. However, a t the present time there is still little quantitative information on the physical dimensions of these loci of abundance or the absolute magnitude of the concentrations. The temperature-depth curves given by Lovett (1968) indicated that layering decreased with depth in the main thermocline. Deviations from the mean gradient were small, below 1 000 m, but were detectable t o a depth of about 2 000 m. Tait and Howe (1968) found quite distinct layering to a depth of 1500 m in the vicinity of the Mediterranean outflow. The writer is indebted to Henry Stommel and W. F. Simmons for permission t o examine unpublished records of a similar sort which were taken with a Salinity-Temperature-Depth recorder in the Sargasso Sea. On two occasions the instrument was raised and lowered continuously between 1 000 and 1 200 m, more or less, for a period of about half an hour, while the ship drifted freely. Marked layering was observed, including temperature inversions. The same pattern was repeated with only minor differences throughout each half-hour period, indicating that the discontinuities extended horizontally for some distance, although their true size remains an open question. A single lowering a t another station to a depth of about 1 900 m showed irregularities in temperature structure throughout the column, although the amount of variation in the gradient decreased with depth. There was virtually no variation in the salinity gradient below 1 000 m. Paramonov et al. (1966) measured optical characteristics of the water column as determined by lowering an instrument which bore a fixed light source and a photocell and hence was able to determine vertical variation in optical attenuation as the instrument was lowered through water. Theoretically the attenuation would include both absorption by dissolved materials and absorption and scattering by particles ; however, the effect of particles is likely to be the dominant feature in deep water and should provide a semi-quantitative indication of variations in particulate organic matter. These authors found that there were pronounced variations in attenuation in the surface layer and in the main thermocline. I n the deep ocean there were no sharp peaks. Minor variations were found, but they were gradual changes in the level of the attenuation coefficient rather than sudden shifts. Thus there is considerable likelihood that the thermal structure of

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the main thermocline concentrates particulate food into micro-habitats which are favourable for filter feeding animals. The evidence is less clear for the deep ocean. Some thermal structure certainly exists. In boundaries between water masses of markedly different T-S characteristics, as in the Mediterranean water mass described by Tait and Howe (1968), considerable vertical variation may occur in the deep ocean. This is a matter that deserves further attention, for, as will be seen later, the concentrations of particulate organic matter that have been observed in routine sampling programmes are minimal for the support of bathypelagic organisms.

111. CHEMICAL COMPOSITION There have been excellent and well documented reviews (Provasoli, 1963; Parsons, 1963; Degens, 1968) of the chemical composition of particulate and dissolved organic matter. The present account will not repeat the whole story but will merely summarize the salient facts. Collecting methods have involved centrifugation or accumulation 011 filters of moderate pore size, and the discussion centres on particles of the order of 0-5 to 1 p or larger. The so-called dissolved fraction obviously contains smaller particles, including colloids. Little is known of their composition or even of the quantity of such substances, as compared with materials in true solution. Fox et al. (1952) examined the properties of various filters and effected a reasonable separation of colloids and dissolved materials. The quantity of organic carbon retained on their ultra-fine filters ranged from 0.16-0.47 mg C/litre in a series of samples taken a t depths of 100-600m off the California coast. By way of comparison, Holm-Hansen et al. (1966) found that the particulate carbon removed by ordinary glass fibre filters was 30100 pg C/litre a t comparable depths at their station in the California offing, and the dissolved organic carbon was about 0.45-0.60 mg/litre. This type of comparison is crude, but the results suggest that a considerable fraction of the so-called dissolved component may actually be filter-passing particles and colloids. Thus the section that follows deals with only a fraction of the total particulate matter, and possibly a minor part of it. However, it is the part that is most immediately concerned with animals and bacteria.

A. Elementary composition Parsons and Strickland (1962b) measured carbon and nitrogen in samples obtained from surface and deep waters a t several stations in the temperate North Pacific (about 19-50°N, 132-145OW). The mean

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C : N ratio by weight was 5-7 :1 in the surface layer and 3.6 :1 in waters of 300-3 000 m. Menzel and Ryther (1964) obtained essentially similar results in surface waters of the temperate North Atlantic. I n some of their deep water analyses the ratios were as little as 2.7 : l . Values reported by Duursma (1960) in the North Atlantic and Dal Pont and Newel1 (1963) in the South Pacific fell within this same general range. Duursma (1960) and others had found that C : N ratios in dissolved organic matter in sea water also were of a similar order. Provasoli (1963) called attention to the fact that these ratios were much lower than in fresh wat,er or soils, and the results suggested that humic materials, which ordinarily have a C : N ratio of 8 :1 or more, may be scanty in the sea. However, recent work indicates that the situation is more complicated and variable than it appeared to be in the early 1960's. HolmHansen et al. (1966) obtained a ratio of 5.5 : 1 in the surface layer of their station off the California coast, but the ratio increased below the surface, and the average for the whole water column was 1 2 . 5 : l . Subsequently Gordon (1970b) analyzed three sets of cruise data obtained in temperate and subtropical waters of the North Atlantic. Altogether about 120 samples were analyzed, and the means were 7-8 :1 and 8.3 :1 in the first two cruises and 15-5 :1 in the third. The possibility that the apparent variability was due to differences in analytical technique cannot be entirely ruled out, although this seems unlikely. All except the last author cited used wet oxidation methods, which are possibly suspect on the grounds that oxidation of carbon may not have been complete. Gordon used dry combustion, and his higher ratios could have been due t o differences in method. However, Holm-Hansen et al. also obtained markedly high values by wet oxidation methods. Here one might argue further that conditions might have been atypical in the isolated basin that these investigators were studying. However, the argument is not very convincing, because high ratios were obtained well above the level of the sill depth of the basin. Handa (1968) also obtained moderately high C :N ratios a t a station in subtropical waters off Japan (35"N, 139"36'E), and he found that the ratio increased with depth. He regarded this as indicating that protein is utilized more readily than carbohydrate as the material sinks into deep water. His biochemical analyses, which will be summarized later, indicated that a large proportion of the carbohydrate existed as polysaccharides which one would expect to be refractory. There is no longer much doubt that observed variations in C : N

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ratios are real, but more investigation will be needed in order to determine limits of variation and regional aspects if any. Handa’s evidence of a systematic increase in C : N ratios with depth cannot be accepted as a general phenomenon without more thorough examination in other regions. Data from the North Pacific by Parsons and Strickland (1962a) and from the south-eastern Indian Ocean (Newell, 1966) show no such evidence. There is some possibility that these variations can be ascribed to differences in the relative proportions of amorphous aggregates and flakes, the former consisting mostly of carbohydrate, while the latter are also rich in protein. Counts now available do not reveal marked differences in the proportion of these components ; however, counts are somewhat deficient in their assessment of large aggregates, which are few in number but might have sufficient mass to influence bulk chemical analyses. Holm-Hansen et al. (1966) found that the ratio of particulate carbon to phosphorus in thc surface layer was about 33 :1 by weight. A considerable fraction of this particulate matter presumably consisted of living phytoplankton, and they regarded the observed ratio as being fairly typical of phytoplankton growing in a nitrogen deficient medium. The C : P ratio declined t o a minimum a t mid-depths and increased in near-bottom waters. The average C : P ratio for the vertical column was about 50 : l . The average ratio for the dissolved fraction was about 90:l.

Menzel and Ryther (1964) found essentially no phosphorus in deep water particulate matter. McGill ( 1964) was particularly concerned with total organic phosphorus, particulate and dissolved, in his monographic treatment of phosphorus distribution in the Atlantic Ocean. The concentrations were of the order of 0-0.15 pg a t P/litre and averaging about 0.05 pg, suggesting that the C : P ratio by weight might be several times higher than that obtained by Holm-Hansen et al. (1966) for the dissolved fraction. These observations, admittedly scanty, suggest that deep water particulate matter is poor in phosphorus as compared with plankton and the general assemblage of particulate matter in the surface layer. Much of the phosphorus in living organisms is regenerated quickly after their death, and apparently only a few components are resistant t o biological utilization. Holm-Hansen et al. (1966) suggested that most of this deep water phosphorus is in nucleic acids, and thought that the increase in C : P ratios which they observed in near-bottom waters was due to the fact that nucleic acids were more resistant to decomposition than protein.

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B. Biochemical composition The work of Parsons and Strickland (1962a) is the most complete of the early accounts of the biochemical composition of oceanic particulate matter. Their analyses of carbon and nitrogen were discussed in the previous section, and the remainder of the work will be outlined now. Measurements of carbon, nitrogen and carbohydrate were obtained a t three stations. These comprised two samples from the surface layer and nine samples a t various depths from 300-3 000 in. I n addition, a composite sample from 400 m was used for more detailed biochemical study. Seven amino acids were identified in the protein hydrolysate. Glycine and alanine predominated, with lesser amounts of aspartic acid, lysine, arginine, serine and proline. There were indications that a considerable fraction of the total nitrogenous components was not recovered. I n the carbohydrate fraction, 70% was crude fibre. Glucose constituted 50% of the carbohydrate hydrolysate. Other sugars included galactose, mannose, arabinose, and xylose. No glucosamine was detected, indicating that chitin is not an important constituent, nor hexuronic acids. Fat content was less than 1%. The two surface samples averaged 202 pg C/litre, equivalent t o about 400 pg of organic matter. Carbohydrate, calculated as glucose, was 115 pg. Protein, estimated as N X 6.25, was 219 pg, leaving an unidentified remainder of roughly 65 pg of organic matter per litre. The deep water samples averaged 40.7 pg/litre of glucose equivalent and 87.3 pg of protein, calculated in the same way as indicated above. These two fractions added together would account for more than the organic matter that could reasonably be expected to be present since the total carbon averaged 50 pg/litre. Attempting to resolve this dilemma in another way, the carbohydrate is subtracted out, leaving an average of 34 pg of non-carbohydrate carbon. The C : N ratio of this material would be 2.4 :1, which seems anomalously low for proteins but is not entirely out of reason in view of the predominance of nitrogen rich amino acids such as glycine and alanine. This helps t o resolve the dilemma but does not imply that it is the whole story. Some of the " crude fibre )' may be complex polysaccharides containing nitrogen. The paper by Holm-Hansen et al. (1966), which was discussed a t some length in the previous section, contained notes on biochemical composition which will be summarized here. They assumed that organic phosphorus was present as a nucleic acid component because

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Strickland and Solozano (1966) had failed to find carbohydrates containing phosphorus. I n the case of deep water particulate matter, they reported that large quantities of carbon remained unaccounted for after correcting for carbohydrate determined by direct analysis and subtracting likely values for protein carbon. They suggested that there must be “ either a high proportion of non-nitrogenous material or an inert organic residuum with a very high carbon to nitrogen ratio.” This of course is very different from the situation that Parsons and Strickland (1962) had found earlier in offshore waters of the North Pacific. Hobson (1967) determined carbohydrates in particulate matter collected a t his three stations in the North Pacific. Deep water values for carbohydrate-carbon in his various cruises averaged 13-28% of total carbon. These are slightly lower than the average obtained by Parsons and Strickland. Handa (1968), whose studies of C :N ratios in the waters off Japan have already been reported, was particularly concerned with the biochemical characterization of the carbohydrate fraction and has provided the most detailed information on that subject which is thus far available. His paper also contains incidental information on the ratio of amino N to total organic N, which is summarized briefly in passing by saying that amino N was more than 85% of the total and tended t o increase slightly and irragularly with depth. The total particulate carbohydrate carbon was of the order of 20 pg C/litre in surface waters and 4-6 pg between 100 and 1 000 m. The most important monosaccharide components were glucose, galactose, mannose, xylose, and glucuronic acid. D-glucose was the most important one in the immediate surface layer, decreasing gradually in the upper 200 m. Otherwise there was little change in relative proportions with depth. One hundred litre samples were taken a t depths of 20, 500 and 700 m for detailed analysis. Soluble carbohydrate was removed from the particulate matter with a hot aqueous solution followed by ethanol and acetone treatment for further fractionation. The remaining particulate matter was treated with Schweizer’s reagent t o extract polysaccharides. The material so obtained was examined by standard methods t o determine the monosaccharide composition and the degree of polymerization that was involved. Two of the soluble fractions gave only D-glucose upon acid hydrolysis. One of these was specified as containing D-glucose and two oligosaccharides ; the other was D-glucan. A third fraction contained galactose, glucose, mannose and xylose. The water insoluble fraction

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yielded these four plus glucuronic acid. Glucan and the water insoluble polysaccharides were the most important constituents a t all depths and were virtually the only significant ones in deep water samples. Handa used periodate oxidation to determine types of linkage. His results will not be discussed in detail, but some generalities emerge. He identified a 1,3-glucan which is similar t o laminarin, and this general class of compounds probably is derived from algal storage carbohydrates. The water insoluble carbohydrate is a mixture of polysaccharides having 1,2- or 1,4-linkages. The latter is a common constituent of algal cell walls, and Handa believed that these polysaccharides are a mixture of algal remains. Such material is more resistant to bacterial attack than storage polysaccharides and is the chief component of deep sea particulate carbohydrate. Degens (1968) has presented a detailed examination of nitrogenous compounds in particulate and dissolved matter and sediments a t several collection points in both the Atlantic and Pacific oceans. Total amino acids in deep water particulate matter ranged from 5.3-1 8.6 pg/litre and constituted more than 50% of total particulate matter. Major amino acids included glycine, serine, glutamic acid, alanine, arginine, lysine, and aspartic acid. The amino acid composition of particulate matter was not markedly different from that of the so-called dissolved fraction, and indeed the distinction between them is somewhat arbitrary. With regard to this subject and also the structural relations of the nitrogenous molecules, a quotation from Degens is pertinent : “Much confusion has also been generated due to the arbitrary separation of particulate and dissolved matter into distinct classes of compounds. Chemically speaking, such a classification has little information content with regard to the elucidation of the molecular nature of the organic compounds in the sea. The so-called dissolved organic matter is composed of more than 90% of material that has a molecular weight (MW) greater than 400. The bulk of the organic compounds with MW > 400 falls in the 3 000-5 000 MW-range as ascertained by molecular sieve techniques. Hydrolysation of this material will release substantial amounts of monomers ; yet, some high molecular weight products are still intact after this treatment. “ The generally low C : N ratios of dissolved organic matter, the presence of urea even after hydrolysis, the high abundance of amino acids and aromatic compounds in connection with the high yields of oxygen, suggest that oxygen and nitrogen are used in the structural stabilization of the high molecular weight fraction. Peptides do account for some of the materials. Urea may easily react with aldehydes and produce long-chain polymers ; alternatively, its oxy-

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gen may be used for co-ordinative purposes. The molecular structure of urea . . . easily renders itself for such molecular work assignments. . . . “ Aside of arrangements involving peptides or urea condensates, oxygen may also be organized in the form of chlathrates. Thus phenols, quinones, amino acids, amines, sugars, fatty acids, alcohols, and their respective polymers may coexist within the same polymer by virtue of their oxygen functions. Further molecular stabilisation can be achieved by metal ions involving ion co-ordination polyhedra.” Degens’ paper also contains information on CI3/Cl2 ratios in particulate and dissolved organic matter and in sediments. Evidence is presented of isotopic fractionation associated with metabolic use of the organic matter, and these data will be discussed in a later section which deals with biological transformations. The use of histochemical stains by Gordon (1970a) has beel mentioned earlier. The mercuric bromphenol blue method (Mazia et al., 1953) combines directly with free amino groups and by coupling with mercury to sulphydryl, aromatic and free carboxyl groups. Thus all classes of proteins are stained, and staining of non-proteins is reported to be virtually negligible. The Schiff reagent is specific for 1,2-glycol groups and therefore is a generalized carbohydrate stain. These stsins have been useful in determining general classes of components in different kinds of particles. As indicated earlier, flakes and many smaller particles stsin heavily with the protein stsin as well as with the Schiff reagent. Amorphous aggregates chiefly take the carbohydrate stain. Any protein staining in the latter, aside from bacteria and other small inclusions, tends to be a light greenish blue rather than the intense reds and blues that characterize the staining reactions of flakes. Thus the protein reaction of aggregates is either quantitatively small, or, as suggested by Gordon, it may indicate a qualitative difference in the type of protein. The further question of availability to biological attack was studied by Gordon (1970a) under simplified laboratory conditions by treating collections of naturally occurring particulate matter with digestive enzymes. Duplicate samples were prepared by simultaneous filtration of measured amounts of a water sample through paired silver filters. One filter was used for determination of organic carbon content before treatment. The second filter was treated with a mixture of trypsin, chymotrypsin and a-amylase. The filters were then washed t o remove hydrolyzed materials and analyzed for carbon, and the difference between controls and the residue after hydrolysis provided an indication of the amount of digestible organic matter.

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Commonly 30-60y0 or more of the total material in surface collections was hydrolyzed, although in one cruise the mean was only 10%. In deep samples, comprising a total of about one hundred analyses, cruise averages varied from 19-26y0. Hydrolyzed material was examined microscopically after treatment with the usual histochemical stains. Protein was largely removed, but the carbohydrate was not noticeably altered. As Gordon pointed out, the digestive processes of filter feeders may be more effective in the hydrolysis of this material than the simple in vitro treatment. How much of the organic matter can really be used remains obscure. Earlier work by Parsons and Strickland ( 1 962a) suggested that the percentage might be very much higher. Their values for crude fibre averaged about 25% of the total, and the composition of the remainder suggested that most of it might be assimilable. The later work by Holm-Hansen et al. (1966),as described above, was more nearly in line with the concept that a large fraction of the total might be biologically inert. This is another case in which it is impossible, in the present state of our knowledge, to distinguish clearly between differences in methodology and real differences in composition of the organic matter. It is tempting at this point t o suggest that the different kinds of substances described by Handa and by Degens may be largely segregated morphologically into the two major types of non-living particles that have been observed in the sea. There are indications that amorphous aggregates may represent a conglomeration of refractory remains of phytoplankton and other detrital material and that bacteria living on these particles may be dependent primarily upon dissolved organic matter rather than the aggregates themselves for their sustenance. On the other hand, the proteinaceous substances described by Degens and ranging in size from macromolecules t o flakes would appear to be not only more usable metabolically but also chemically more susceptible to polymerization and cementing into flake-sized particles. The proposition probably is stated more categorically than is fully deserved but present information and experimental evidence t o be introduced later suggest that there is some validity in the generalization.

C. Relationships of organic and inorganic materials Wangersky (1965) remarked. that " aggregates are called organic only by courtesy and precedent, since their organic fraction seldom exceeds 30% ". This is quite true. Biologists have recognized for some time that organic matter is a minor fraction of the total particulate matter in sea water, but they took little interest in the inorganic fraction.

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Chemical oceanographers have paid some attention to a few of the inorganic constituents, but as yet there is no clear picture of the overall composition of the inorganic component. Riley (1959) used the relatively crude technique of measuring dry weight and difference on ignition of samples of particulate matter filtered from Long Island Sound waters. The difference on ignition averaged less than half of the dry weight. Riley et al. (1965) measured the dry weight of samples of surface and deep water from the Sargasso Sea and then proceeded to carbon analysis. Deep water carbon averaged only about 2% of total seston dry weight. These collections from relatively unproductive waters probably represent minimum limits for organic content. Gordon (1970b) used similar methods on a broader regional scale and concluded that the organic content, estimated as twice the carbon, averages about onethird of the total dry weight. Hobson (1967) used a Coulter counter to measure the volume of particulate matter a t his North Pacific stations and then estimated the weight of particulate matter by assuming a specific gravity of unity. His results indicated that organic carbon averaged 20% of the total particulate matter or more in most of his groups of deep water samples. The method of Krey et al. (1957) and a subsequent series of papers by Krey and his associates had been mentioned earlier. A good general summary of their work is given by Krey (1967). Tabular data are given for a series of stations in the North Atlantic in the general latitudinal range of 45-55"N. Groups of stations were averaged, and deep water values for total particulate matter ranged from 25-141 pgllitre. The protein fraction was 15-45 pgllitre. Krey regarded this latter fraction as living substance, but biochemical studies cited above would suggest that some non-living protein also is involved. The results do not give a clear separation between organic and inorganic materials, but they suggest that the total organic matter would be a t least 30% of the total and probably more. Wangersky and Gordon (1965) found that calcium carbonate in their open ocean collections was about equal to the organic carbon, with the majority of deep water samples falling between 30 and 80 pg/litre. Chave (1965, 1968) has found that naturally occurring flakes commonly have crystals of calcite embedded in them. Moreover, particles of calcium carbonate adsorbed a coating of organic matter which was sufficiently impermeable t o protect them from re-solution in undersaturated water. Suess (1968) has presented further studies of the physical chemistry of this process.

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Most of the naturally occurring aggregates also contain particles which appear to be clay. This is particularly true of inshore collections but generally can be seen in oceanic material as well. X-ray diffraction analysis of Long Island Sound material showed clear evidence of clays. More remarkable, sodium chloride was present, although the material had been well washed before analysis. Moreover, one occasionally sees crystals in organic aggregates which appear to be sodium chloride. Wangersky (1965) described experiments which may help to explain these strange results. He prepared solutions of each of the major sea water salts in distilled water and bubbled them. The inorganic material was carried into the air above the water surface as an aerosol and fell back as a collection of fine crystals which floated on the surface until they gradually redissolved. I n another series he found a sudden increase in the yield of inorganic material together with appreciable yields of organic carbon. Further investigation showed that the distilled water contained organic material which apparently was the result of a spring diatom flowering in a local reservoir and had survived treatment with alkaline permanganate and triple distillation. These and other experiments suggested that crystals of any of the sea salts might be stabilized by the adsorption of organic skins, possibly of denatured protein. Indeed it would be difficult to account for the large inorganic content of the particles in any other way. This is particularly true in the case of flakes produced by experimental bubbling of filtered water, although even there the possibility exists of a contribution by inorganic solids that are small enough to pass the filters which are ordinarily used. The truth of the matter awaits further analysis. Wangersky’s theory about the process of particle formation is a little different from the one postulated by Sutcliffe et al. (1963) which will be described later. Experimental evidence will be introduced which will require further modification of present viewpoints. However, these theories are not mutually exclusive, and the later discussion will attempt t o pull the evidence together into a generalized picture which fits all of the available facts. Organic particulate matter is of considerable potential interest to geochemists. Sebba (1962) described a process which he called ion flotation, whereby bubbling air through a solution contsining surfaceactive organic materials resulted in the concentration of ions in particulate matter formed in the foam. He demonstrated that aluminium, uranium, alkaline earths, iron, nickel, and traces of other metals could be concentrated in this way.

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Wangersky (1965) and Wangersky and Gordon (1966) were particularly conceriied with the geochemistry of calcium carbonate and manganese. Their calculations indicated that the carbonate fraction of organic particles could contribute significantly t o the fine fraction of carbonate in deep water sediments. Manganese was particularly interesting. The presence of abundant deposits of manganese dioxide as nodules, crusts, and layers in sediments has been a subject of debate for many years. No known mechanism could account for the existence of soluble manganous ion which could be oxidized in bottom waters to produce these deposits. However, Wangersky and Gordon found that organic aggregates in deep water contain manganous ion in concentrations of 0.0 1-0.06 pgllitre, and decomposition of this material could liberate Mil++, which would then be available for oxidation and precipitation. The ability of particulate matter and associated clay particles to adsorb trace elements is well known, yet little of the geochemical literature shows much awareness of this problem. Some geochemists use whole water samples for analysis ; others filter their samples. In some cases various kinds of collections are indiscriminantly mixed, and often the exact procedures are not stated. This lack of realization that many of the problems are biogeochemical rather than merely geochemical has slowed the development of the field. The occurrence of inorganic substances in oceanic aggregates obviously can result from either adsorption of ions or scavenging of solid materials. The presence of manganous ion presumably is the result of direct adsorption. Calcium carbonate could be scavenged from the water column or formed as crystals on bubble surfaces or possibly adsorbed. Wangeraky and Gordon (1966) reported that experimentally produced aggregates had a calcium carbonate content that averaged about 2.5% of the dry weight. However, Siege1 and Burke (1965), using tracer methods t o study the uptake of various cations on particulate matter formed by bubbling, found essentially no calcium uptake. They reported that zinc, strontium, and manganese were adsorbed t o a slight degree on particles that were formed both by bubbling and on standing, but the amount was invariably less than 1yoof the amount added. The amount added was not stated specifically but was said to be negligible compared with the natural concentration of the cation in sea water. This raises questions about the interpretation of their results. I n the case of calcium carbonate, for example, the amount that Wangersky and Gordon found in their aggregates was a significant component of the aggregates but was generally less than 0.2% of the amount normally found in sea water. I n this case one

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would expect a tracer experiment to give a low yield, and a high yield could not be expected unless both naturally occurring and added cation are present in such low concentxation that a significant fraction of the total would be adsorbed during the bubbling period.

IV. EXPERIMENTAL STUDIES OF NON-LIVING PARTICULATE MATTER A. Adsorption on bubbles Earlier sections have mentioned the experiment31 finding of Baylor et al. (1962) and Sutcliffe et al. (1963) that particles can be produced by adsorption on bubble surfaces, and this process will now be considered in some detail. Their experimental work was not the first indication that this process might occur, but for the first time attention was focused on the possibility that such substances might be biologically important. Their work had been preceded by about forty years of study of atmospheric sea salt nuclei, a subject that has been ably reviewed by Blanchard (1963) and is mentioned here only as background information. These nuclei are formed and flung into the air by bubbles breaking at the surface, and there have been indications that they contain adsorbed organic materials and organisms as well as sea salts (Woodcock, 1948 ; Wilson, 1959, and others). Fox and Herzfeld (1955) suggested that bubbles in the water column could be stabilized by the presence of a skin of adsorbed organic matter. Moore (1953) found that sea foam was stabilized by an organic skin of protein. Baylor et al. (1962) called attention to a peculiar distribution of phosphate which has often been noted in near surface waters, in which the concentration in the immediate surface layer is slightly higher than in the underlying mixed layer. A biological explanation for the observed negative gradient seems unlikely although not impossible. Baylor et al. (1962) developed a more sophisticated hypothesis which probably was suggested by the work on sea salt nuclei and certainly drew supporting evidence from those studies. They made an experimental examination of the proposition that phosphate is transported toward the surface by adsorption on rising bubbles. Their evidence supported the hypothesis and they further found that organic matter was associated with the adsorption process. The experimental apparatus consisted of a sea water column with a stream of air bubbles entering a t the bottom and a sloping glass surface above the liquid which collected droplets of aerosol produced by bursting bubbles and allowed them to accumulate and flow off by gravity into a catchment flask. With this

PARTICULATE ORGANIC MATTER IN SEA WATER

41

apparatus phosphate was removed exponentially. They furthermore found that preliminary extraction of the sea water with xylol reduced the effectiveness of the bubbling process and suggested that organic substances adsorbed on the bubbles served as anion binders. Their conclusion was that phosphate could be transported toward the surface by rising bubbles. Part of it could be ejected with the aerosol droplets, but materials remaining in the surface film or released by dissolution of bubbles before they reached the surface could produce the observed vertical gradient in phosphate. Sutcliffe et al. (1963) pursued this subject further, and their attention was now focused primarily on the organic component and its possible biological significance in the sea. Experiments testing the surface activity of the adsorbed material and partitioning of the phosphate by dialysis led to the conclusion that some of the phosphate is bound to organic substances with a molecular weight in excess of 300. Their hypothesis regarding the mode of formation of organic particles was as follows : " Such large organic-active molecules adsorb t o bubbles and produce monomolecular films which may be aggregated into insoluble organic particles in the following way: in the foam produced by aeration the ever increasing area of the adsorbed monomolecular films causes them to fold into polymolecular layers and to form colloidal micellae or to collapse into fibers (Goldacre, 1958). The agitation of foaming produces repeated collisions and results in multiple-layer coalescence of colloidal particles t o produce a semi-stable suspension of organic material. Many of the larger particles undergo further aggregation and settle out." Subsequent studies have brought to light certain aspects of the aggregation process which are not fully in agreement with this early hypothesis. The evidence will be examined in a later discussion; however, the experimental work and theoretical implications developed by these investigators were directly responsible for a rapid expansion of programmes of enquiry into various aspects of this subject. Because of the fact that these experimental studies stemmed from earlier meteorological work, it was natural that the problem was approached from an aerosol point of view. Experimental devices were designed to catch droplets above the water surface or t o drain off surface foam. We now know that methods of this type give the largest continuing yield of any method thus far discovered. As primary interest shifted from studies of the immediate surface film t o problems involving a larger portion of the water column, experimental methods changed. Most investigators bubbled a volume of water for a given length of time, allowing the particles to accumulate

42

CORDON A. R I L E Y

in the water. Invariably the rate of production was smaller, and under some experimental conditions the yield was negligible. Hence some doubt began to arise as to the validity of the earlier work. The matter became further confused by the fact that a variety of techniques was used, with little knowledge as to the effects that they might have on experimental results. Various kinds and pore sizes of filters were employed. Plastic containers have been used because of ease in fabrication, but they have been criticized on the grounds of possible introduction of contaminants. Air supplies are always suspect. Furthermore the quantity of carbon obtained is small, so that analytical errors are troublesome. The above section on " Methods )'has outlined precautions that are necessary for good analytical results ; this kind of information has accumulated gradually over the years, and early investigations did not include all of the precautions that are now regarded as necessary, nor did they always include enough replications for good statistical tests of the results. However, the results of earlier work should be summarized, and insofar as possible they will be reexamined in the light of more recent information about possible errors. Riley et al. (1965, Table 5) described the results of bubbling experiments on surface and deep water from the Sargasso Sea. The water was first filtered through 0.45 p Millipore filters in 15-20 litre lots into polyethylene carboys, bubbled for 3-6 hours with filtered ambient air supplied through an aquarium pump, and then re-filtered through glass fibre filters for measurements of particulate carbon. The conclusion a t that time was that all of these waters, surface and deep, contained filter passing material which could be converted into particulate matter by the bubbling process. The use of polyethylene and ambient air and the lack of unbubbled controls have been criticized and raise some doubt as to absolute values ; however, the whole series was done under essentially the same kind of conditions, permitting internal comparison. There were 44 experiments in all, about equally divided between samples taken in the upper 200 m and those obtained a t various depths from 500 m t o 3 000 m. The mean yields in these two series were 70 and 39 pg C/litre, respectively, and the difference was significant to the 1% level. Any errors due t o artifacts or lack of control should be about equal in the two sets. Thus, while one cannot say with certainty that bubbling produced particles in the deep water samples, the higher values obtained in the surface layer were a definite indication that this process was significant, even though the region under investigation is relatively poor in organic productivity. The other question, whether organic matter in deep water also can be converted into particles by the bubbling process,

PARTICtTLATEORGANIC MATTER I N SEA WATER

43

has no practical significance. It would be more interesting to find out whether other adsorption processes which could operate in situ in the deep ocean could increase the quantity of particulate matter. The paper in question had examined a good deal of oceanographic evidence, direct and indirect, as to probable causes of the lack of a systematic decrease in particulate matter with depth in the deep sea. The most reasonable explanation seemed to be a dynamic balance between utilization by bacteria and other biological processes and renewal by adsorption from the dissolved fraction. Preliminary experiments were undertaken t o explore the adsorption problem, and results looked promising. Subsequent work has enlarged this subject to the point where it deserves a separate subsection later. Riley et al. (1964) explored the question of whether extracellular substances produced during phytoplankton growth could be converted t o particulate matter by experimental bubbling. Seven species of diatoms and one dinoflagellate were grown in pure culture in an artificial medium in which the only organic additives were minimal quantities of vitamins which are necessary for growth of most of these forms. They were grown under varying conditions of light and temperature which were believed to be optimal for the species in question ; in general the light intensity was 500 ft. c. or less. At approximately the end of the log phase of growth the cultures were filtered through glass fibre filters. The medium, generally one litre, was bubbled for 24 hours in a pyrex flask using the laboratory air supply, and then was filtered again. The yield was highly variable, ranging from 2-75% of cellular carbon. The dinoflagellate was at the lower end of the range ; the diatoms averaged 20%. The mean carbon yield in all experiments was 1.16 mg C/litre. These results are open to criticism on the grounds of possible contamination by the laboratory air supply. However, during the same period another series of experiments was carried out with natural sea water and using the same air supply and other experimental equipment, so that any errors due to artifacts should be about the same in both series. Results obtained with natural sea water were an order of magnitude lower than the yield from culture experiments. Thus there is no evidence that the latter were seriously vitiated by contamination. Hellebust (1965) described the kinds and amounts of organic excretion obtained from 22 species of algae. His results also were highly variable, although his maximum yield of 25% was exceeded by about a third of the experiments listed by Riley et al. (1964). However, Hellebust’s yields represented only a 48-hour experiment rather than the week or more required for growth to the end of the log phase. Only two species

were duplicated in the two lists. Hellebust obtained a total carbon excretion of 9% from the diatom Skeletonema costatum and 4.4% from the dinoflagellate Peridinium trochoideum in the series grown a t 3 000 Lux. Figures obtained by Riley et al. (1964) for particle production in these species were respectively 31 and 2%. Possibly not all of the particulate matter was formed from dissolved extra-cellular metabolites. The coarse filtration used in these experiments would perhaps permit fragments of broken or dead cells to pass through and subsequently become incorporated in the particles. However, the procedure more or less simulated natural conditions in that surface waters of the sea can be expected to contain an array of dissolved metabolites, cell fragments, and possibly cell sap exuded during zooplankton grazing. All such phytoplankton products conceivably can be aggregated and were believed to contribute toward the observed relationship between phytoplankton concentrations and non-living particulate matter observed by Riley et al. (1964). About this time the writer began to find evidence of peculiarities in yield, depending upon the type of bubbling process used. Several experiments were designed to explore this situation. The series was interrupted before sufficient data had accumulated for publication, but some of the results warrant a brief account here. One experiment, for example, involved filtration of three lO-lit,re samples of essentially identical Long Island Sound water through 0.45 p Millipore filters into glass carboys. The first one was bubbled for 3 hours with filtered air from the laboratory compressed air supply and filtered through a glass fibre filter. The yield was 50 pg C/litre. The second was passed continuously through a 250 ml bubbling chamber, entering the bottom and draining off a t the surface into a filter. The yield was 61 pg C/litre, a t least equal to that of the first experiment, although the mean time in the bubbling chamber was only 12 minutes. The third one was bubbled for 24 hours, and the yield was 110 pg C/litre. The first carboy was rebubbled and filtered twice more during the first 24 hours, with additional yields each time, and the total yield was 184 pg, considerably more than that attained by continuous bubbling. Six more periods of rebubbling and refiltration for a total of 140 hours increased the total yield to 474 pg. Three additional experiments involving alternate bubbling and filtering were carried out with surface water taken near Bermuda. These were done in glass carboys, using ambient air introduced with aquarium pumps. One relatively short experiment of 21 hours duration gave a total yield of 157 pg C/litre. Two longer ones of 40 and 80 hours, each involving six periods of bubbling and subsequent filtration yielded

PARTICULATE ORGANIC MATTER IN SEA WATER

45

417 and 438 pg. No measurements of dissolved organic carbon were made, but these amounts were not markedly less than some of the figures for total dissolved organic carbon in oceanic waters as determined by wet oxidation methods (for example, see Duursnia, 1960). These results suggested (a) that the rate of production of particles by bubbling is very high initially and rapidly decreases with time, and

/

0

20

40 TIME

60 IN

00

I00

120

HOURS

Fm. 3. Comparison of total carbon yields in different kinds of bubbling experiments performed with aliquots of the same sample of Nova Scotia coastal water. A. Water was continuously circulated through EL bubbling chamber, through a filter, and back into the chamber. Filters were harvested a t intervals indicated by dots on the curve, and the amounts of carbon obtained were summed to give the integrated curve shown in the figure. B. Sample was alternately bubbled, filtered and rebubbled, and yields were integrated as in A. C. A sample was bubbled continuously for the entire period. If the yield during the first six hours was similar t n that of the other two aliquots, the subsequent yield was as indicated by the dotted line.

(b) that the reduction in rate is due to some process of inhibition by the particles produced, for their periodic removal permitted extensive further formation. There were indications in experiments described by Wangersky (1965) that excessive collection of particles at the surface inhibited further formation. If this is correct, there should be some advantage not only in draining away the surface layer continuously but also in having a large surface to volume ratio in the bubbling chamber. An

46

QORDON A. RILEY

apparatus was constructed consisting of a flat polyethylene pan with inlet and bubbling stone a t one end and an outlet a t the other a t a level permitting a 2-litre capacity with a surface area of about 550 om2. Water from the outlet passed through a glass fibre filter into a small collecting bottle and thence was pumped a t a rate of 2 litre/hr back through the bubbling chamber. Yields obtained with this device were compared with the results of alternate bubbling and filtering of an aliquot of the same sample. I n all cases continuous harvesting increased the yield. The results of one such experiment, conducted with Nova Scotia coastal water, are shown in Fig. 3. Each point represents the time when a filter was removed and the total yield up to that time; the latter obtained by adding all of the carbon analyses together. The form of the curve is typical. The quantities obtained were higher than average, and the sample presumably had an unusually rich supply of organic matter. Unfortunately, however, no data on dissolved organic matter are available for this series of experiments. The work was not completed and published a t that time, because there was evidence that organic contaminants in air supplies could be serious enough to produce spurious results, and further examination of possible errors was necessary. Menzel (1966) found that bubbling with his laboratory air supply for three hours increased the dissolved organic carbon by a factor of 2-4. He therefore developed a method for combusting his air supply in order to get rid of airborne organic material. He also developed an all glass apparatus. With this he conducted some twenty-five experiments using local coastal water (Woods Hole), surface and deep water from the Sargasso Sea, and culture media in which algae had been grown. The water was triple-filterzd through 0-8p silver filters prior t o the experiments, and he then compared the results of 3-6 hours of bubbling with unbubbled controls. I n all cases small quantities of carbon (1836 pg C/litre) werz retained 011 the filters, both experiments and controls, but the difference between them was statistically insignificant. Menzel’s work was done with considerable car3 with r3spect t o cleanliness in all materials used arid statistical design. His bubbling chamber was a glass cylinder, which is relatively inefficient for particle production, and a longer bubbling time might have been used ; however, these factors in themselves should not have been sufficient to prevent significant particle production. The discrepancy between his results and earlier ones that have been described required re-examination of various factors which might affect the bubbling process. I n addition t o questions of technique and artifact, the role of bacteria also needed t o be examined, for Barber (1966) had reported that he was unable t o

PARTICULATE ORGANIC MATTER I N SEA WATER

47

get significant formation of organic carbon in experiments that were effectively sterilized by filtration through 0.22 p filters. An evaluation of some of the major problems was published by Batoosingh et al. (1969). A prerequisite for such work was of course the development of an air supply that was reasonably free from contamination and, incidentally, a comparison of this air with the ordinary supply of laboratory compressed air as an aid in evaluating previous results. Combustion of the air seemed an unnecessary refinement. Instead, a small volume of air (about 0.5 litre) was recirculated. One method was simply to carry out the experiment in a tightly stoppered pyrex bottle with magnetic stirring sufficiently vigorous to introduce subsurface bubbles. The other was t o introduce a bubbling stone and circulate the air via silicone tubing and an AC vibratory pump. The latter provided more efficient mixing with little likelihood of serious contamination. Results showed that the laboratory air supply in current use was not objectionable, so that previous experiments such as the one described above on yields obtained with Nova Scotia coastal water were not invalidated. The use of a polyethylene bottle instead of a glass one did not introduce a significant error. A major factor in determining the yield was the pore size of the filters. Highly significant yields were obtained by bubbling sea water that had been prefiltered through silver or Millipore filters of 1.2 p pore size or glass fibre. The yield declined t o a very slightly significant level when 0.22 p filters were used for pre-filtration. The results implied that particles in the size range of 0.22-1 - 2 p, and possibly larger, are important as nuclei in the formation of larger particles. Further tests compared triple filtration through 0.8 p filters, as practised by Menzel (1966), with single filtration, and the latter gave higher yields, indicating that part of his difficulty in producing particles was due simply t o the fact that triple filtration, even through filters of medium pore size, removes a considerable fraction of the small particles that facilitate aggregation. However, Batoosingh et al. (1969) found that even after triple filtration the yield was not entirely insignificant. They used a 24-hour bubbling period, as contrasted with 3-6 hours in Menzel’s experiments, and the bottle used as a bubbling chamber had a larger surface : volume ratio than his cylinder. These factors may have been responsible for the difference. Barber’s (1966) conclusion that bacteria are necessary for the aggregation process was not confirmed, but it was not categorically denied. Batoosingh et al. (1969) found that samples filtred through 0.22 p filters were sterile, as judged by plating test, yet there was a slight

48

GORDON A. RILEY

amount of particle formation. However, if samples treated in this manner proved not t o be entirely sterile, growth of bacteria might provide nuclei for further aggregation and therefore might lead t o larger yield of particles. There is no doubt that bacteria become incorporated in particles, and indeed prolonged bubbling is an effective means for sterilizing sea water, but there is no evidence that bacteria play a physiological role in the process. Thus it was suspected that bacteria or any organic particles of a similar size might be equally effective as nuclei for aggregation. This matter can be tested further by coarse filtration and some kind of sterilization of the filtrate. However, most kinds of sterilization are suspect on the grounds that they might introduce artifacts into the experiment. Treatment with cyanide seemed to be one of the least objectionable methods. This was tried in a series of replicates using 1.2 p pre-filters in which one set was bubbled for 24 hours in the usual way, and replicate pairs were given identical treatment except for an addition of 50 mg KCN/litre. There was no significant difference in the results. The experiments did not fully prove the point because the KCN treatment did not establish complete sterility. Plate counts indicated that there could be as many as 100-200 bacterial cells/ml a t the end of the experiment. However, this was one to two orders of magnitude less than the quantity in untreated controls, and if living bacteria were very important one would expect t o find some difference in experimental results. Having demonstrated that air supplies did not contribute significantly t o particle formation, Batoosingh et al. (1969) carried out a few experiments of longer duration in further examination of time relations involved in particle formation. One experiment involved continuous bubbling for 15 days, with daily removal of an aliquot for carbon analysis. A concentration of 227 pg C/litre was attained on the second day, and no further increase was observed thereafter. Earlier experiments on alternate bubbling and filtering were repeated with better controls and more thorough replication and with essentially the same kind of results that had been obtained earlier. I n a series of nine experiments the mean total yield for four successive oneday bubbling periods was 492 pg C/litre and this was 3.3 times the mean yield for the first day, indicating that particle formation can continue for some time with only slight diminution if the particles are removed a t intervals. Another experiment was devised to provide continuous yield, and the amount obtained during one day was larger than in four days of alternate bubbling and filtering. I n short, the results reaffirmed

PARTICULATE ORGANIC MATTER I N S E A WATER

4!)

previous conclusions that the rate of particle formation is rapid a t first but cannot be maintained unless the particles are removed. Certain aspects of experimental particle formation in sea water have not yet been thoroughly studied. For example, quantitative studies of the effects of variations in air flow and bubble size are still lacking. More important, the physical chemistry of the aggregation process remains obscure, and information about the kinds of compounds involved is little more than anecdotal. These basic problems probably could be studied more effectively with artificial sea water of known composition, both organic and inorganic, than with natural sea water. Wangersky (1965) began a programme of this sort but was unable to continue it because of difficulties in removing organic contaminants from his distilled water. The problem still awaits study, and little further progress can be made until the basic facts become clearer. A second kind of problem, of a different and perhaps even more difficult sort, is the assessment of natural rates of particle production at the sea surface and attempts to synthesize laboratory results and field observations into a coherent picture of what is actually happening a t the sea surface. These problems will be considered in a later discussion, but the discussion will raise more questions than it answers.

B. I n situ production and utilization 1. Organic carbon

Riley et al. (1965) proposed the hypothesis that the lack of a systematic vertical gradient in particulate matter in the deep sea could best be explained as an expression of a dynamic balance between utilization and further adsorption from the filterable fraction. To test whether such adsorption might occur, particles were produced artificially by bubbling, and small quantities of this water were seeded into carboys of filtered deep sea water and were allowed to stand without disturbance for a day. The carboys were then filtered for analyses of particulate carbon, and there was in fact more carbon present than had been added. Further experiments involved additions of experimentally produced particles and natural particulate matter to filtered deep sea water, and the water was allowed to stand for several days. The same kind of results was obtained, but there was also a significant accumulation of carbon in controls that were simply filtered, with no addition of substrate for adsorption. This suggested the existence of some sort of process whereby particles could be produced by aggregation of filter

50

OOKUON A. RILEY

passing materials. The experiments were not published a t that time, pending further study of the problem. Sheldon et al. (1967) were the first to publish an account of the early events in this aggregation process. They followed the course of particle formation in filtered sea water with repeated Coulter Counter measurements of the total volume of particles in a graded size series between 1-58 and 5 p. Initial particle formation was rapid, leveling off after a few days. The smallest sizes were most abundant a t first, and there was a gradual shift toward a maximum concentration a t a particle size of about 4 p. The process could occur in the light or in the dark ; it was stimulated by addition of glycine and inhibited, a t least temporarily, by mercuric chloride. They suggested that bacterial action probably was implicated in the formation, but this could not be established beyond question. When the sample was filtered after equilibrium concentration had been raached, another cycle of production occurred, and as many as four cycles were induced in one sample by repeated filtration. They estimated that the concentration of particulate organic carbon might be of the order of 25 pg/litre a t the time of equilibrium. The writer has followed the course of particle formation in filtered sea water by means of carbon determinations and to a lesser extent by visual examination. The initial increase described by Sheldon et al. (1967) is near the limits of sensitivity of the carbon method, and during the first 2-3 days the results generally are not significantly higher than those obtained by immediate refiltration. However, after about five days a difference can generally be notc3d, and the quantity is more or less in agreement with the estimate made by Sheldon et al. (1967). The quantity of particulate organic carbon continues to increase in these experiments, commonly reaching a peak in 10-20 days, and a t that time the carbon concentration is likely to be a t least an order of magnitude higher than the equilibrium value estimated by Sheldon et al. (1967). Visual examination shows that the most important constituents are hazy, amorphous masses of material in the general size range of about 25 p , which stain heavily with Schiff reagent. The protein staining reaction is generally less marked and may be absent. Bacteria are associated with this material ; their protein staining reaction makes them clearly visible. Presumably these are two chapters of the same story. The so-called equilibrium stage described by Sheldon et al. ( 1 967) probably is merely an equilibrium of small particles within the size range that he was particularly concerned with, but these particles gradually coalesce into larger masses, are worked over by bacteria, and are gradually

PARTICULATE ORQANIC MATTER I N SEA WATER

51

transformed into materials that look like pale primordia of the aggregates found in nature. I n short, the writer suspects that the equilibrium condition is a dynamic steady state rather than a static situation. Otsuki (1968) has described the formation of aggregates in fresh water during the course of bacterial utilization of dissolved organic matter produced by addition of dried algae of the genus Scenedesmus. There are photographs of these aggregates in the paper, and they are indistinguishable from the marine material that has been described. I n one experiment of 185 days’ duration the dissolved organic carbon decreased from 213 to 87.1 mg/litre, due t o the combined effects of bacterial utilization and conversion of dissolved t o particulate carbon, but no estimate was made of the amount of particulate carbon formed. There was a concomitant decrease in the carbon : nitrogen ratio from 11.1to 5.9 (atoms). Similar decreases in C : N ratios were noted in many other decomposition experiments. Parsons and Seki (1968) have described aggsegation phenomena in both filtered and unfiltered sea water. They mentioned having seen several different kinds of particles, but special attention was focused on clumping of bacteria. The size of the clumps was of the order of 4 p , more or less, and these authors apparently felt that the clumps consisted primarily of bacterial biomass although there was a suggestion of cementing action by excreted polymers together with inclusions of other materials. The writer is aware of this clumping phenomenon, but again this appears to be a stage in the production of larger aggregates in which the major part of the organic matter is non-living. Admittedly the early stages in the development of aggregates are not very noticeable without the aid of staining procedures, and they are so delicate that they may be broken up during Coulter Counter measurements. Two special cases of i n situ aggregate formation are mentioned in passing. Sieburth and Jensen (1968) described extracellular production of organic matter by Pucus and other littoral brown algae, and they found that some of the end products of decomposition of the exudates condensed into organic aggregates. The authors described this material as “ polyphenol tanned carbohydrate and proteinaceous material ”. A second example was reported by Johannes (1967), who found a marked increase in organic aggregates in shallow water passing over an atoll reef. The aggregates apparently were formed from mucus secreted by the corals; however, this probably was a result of fragmentation of pre-existing materials rather than in s i t u condensation from smaller particles or dissolved substance. Hence the example is not quite comparable with other studies that are being reviewed in this section.

52

ClOCDOX A . EILEP

The rather surprising finding that particles form spontaneously in filtered sea water deserves study in an attempt to determine the processes that are involved and to try to find out whether this is a phenomenon that is likely t o occur in nature. The writer began such a study several years ago. At the same time other experiments were underway in an attempt t o find out something about rates of utilization of particles produced i n situ or by experimental bubbling. As it turned out, all of these converged into a single problem. One of the first experiments involved bubbling two 10-litre samples of water, addition of a small amount of an actively growing culture of

01 0

10 TIME

IN

I

I

20

30

DAYS

FIG. 4. I n situ formation and utilization of particulate organic matter. Duplicate samples were bubbled to produce particulate matter and then were inoculated with Pseudomonas sp. Curves show ensuing concentrations of organic carbon with respect to time.

a marine bacterium, Pseudomonas sp., and removing one-litre samples initially and a t intervals thereafter for measurements of total particulate carbon. The results are shown in Fig. 4. The initial values were 0.13 and 0-16mg C/litre. There was a three- t o five-fold increase in the first two days. Estimates of the increase in bacterial cell substance, based on plate counts and known carbon content of the original inoculum, indicated that 20% or less of the observed increase was due to bacteria per se. If these estimates were realistic the results could only mean that additional organic carbon from the filter passing fraction was being converted into particulate form. Subsequently the quantity decreased and more or less levelled off for a considerable period. After the 24th day (the last analysis shown in Fig. 4) there was only a little

53

PARTICULATE ORGANIC MATTER I N SEA WATER

water left. It was held for a final analysis twenty days later, and a t that time the level of particulate carbon had gone up again and was 0.61 mg C/litre in one bottle and 1.08 mg in the other. Some of the water was plated, and it was found that the original inoculum had been contaminated by growth of about five other species. It remains uncertain as t o whether the increase a t the end of the experiment represented a second cycle of growth by these other species or was simply the result of suspension of materials which previously had been adhering too tightly t o the carboy t o be included in the analysis. Visual examination from time to time had revealed the presence of bacteria, flakes, and amorphous aggregates. The form of the curve for

0

5 TIME

IN

10 DAYS

15

FIG. 5. I n situ formation and utilization of particulate organic matter. This experiment is similar to the ones shown in Fig. 4 except that Pseudomonas was added directly to filtered water without prior bubbling.

total carbon suggested a typical laboratory cycle of bacterial growth, with an initial phase of logarithmic increase followed by decline and senescence, yet all evidence pointed toward the conclusion that living bacteria were a minor part of the total organic matter. Thus it seemed likely that bacterial growth was basically responsible for initial aggregation of organic matter and for utilization of the portion that could be metabolized readily, so that the living and non-living fractions varied together. Fig. 5 shows the results of an experiment in which Pseudomonas was added to filtered water which had not been bubbled. A similar curve A.M.B.-8

3

54

UORDON A . RILEY

was obtained, but the peak was reached more slowly. I n this experiment the dissolved organic carbon was initially 2.7 mg C/litre. At the time of the peak it had declined to 1.95 mgllitre. Thus about half of the observed decrease represented conversion to particulate matter, living or dead, and the remainder can be ascribed to metabolic utilization. During the remainder of the experiment the dissolved organic carbon remained constant within the limits of error of the analytical method. Thus the decrease in particulate carbon after its peak is presumed to be due to bacterial utilization, and this is followed by a steady state situation in which the metabolism of the bacteria proceeds at a rate that is too low to be detected by the methods employed. Studies of in situ accumulation of particulate matter have been carried out by filtering sea water through Millipore or silver filters with a pore size of 0-45 p or larger, which allow part of the bacterial flora t o pass through and repopulate the water. Filtration has been carried out by gravity, or sometimes using pressure generated by a peristaltic pump. I n an attempt to reduce air-water interfaces as much as possible, most of the experiments have utilized polyethylene bags as experimental containers. These bags were of about 4-litre capacity and were sealed at the top, with a polyethylene tube sealed into each corner. One tube extended to the bottom and served as an inlet. A short tube at the other corner was used to evacuate the bag slightly. Thus the inflowing water gradually filled and expanded the bags and had no contact with air except for occasional accidental bubbles. Glass bottles were used in some experiments for comparison with results obtained in bags and also for experiments involving long period storage. The bottles were filled by gravity filtration with as little disturbance as possible and were allowed to overflow before sealing, in the same way that bottles are filled for oxygen analysis. Fig. 6 shows two examples of the kind of results obtained in bag experiments, using water that was filtered but with no bacteria added. Each point represents the mean carbon content of a bag that was refiltered at the time indicated on the graph. The particulate carbon during the first few days was indistinguishable from the amount obtained when water is refiltered immediately. Subsequently the carbon content increased to roughly the same value that was found when samples were inoculated artificially, the only difference being in the length of time required to reach the peak. Other experiments that lasted longer have shown that in this type of experiment, as in others described above, the particulate carbon decreased later and tended to level off. However, in both types there have been a few experiments which did not follow the usual pattern in that the carbon increased and

55

PARTICULATE ORGANIC MATTER I N SEA WATER

levelled off without showing a definite peak. Hence the experiments as a whole show a large variation in maximum concentration. I n an attempt t o find out whether bacteria are essential to this process, some of the experiments have been poisoned with potassium dichromate (1 mg/litre) or potassium cyanide (50 mg/litre). No peaks were observed in these experiments, but there was some slight increase

P

“Oi

b

10 TIME

20

30

IN DAYS

FIG. 6 . In situ formation of particulate organic matter. allowed t o stand, with no further treatment.

Samples were filtered and

to a “ steady state ” a t a lower level than would be expected when bacteria are allowed to grow freely. However, the results were equivocal, for bacteria were not completely eliminated, particularly in the case of dichromate treatment. TABLE11. AVERAGECONCENTRATIONOF PARTICULATE ORGANICCARBON (MG C/LITRE) OBTAINEDIN STUDIESOF BACTERIAL EFFECTS ON BUBBLED WATERAND in situ PRODUCTION AND UTILIZATION

Bubbled ; bacteria added In aitu, with or without bacterial inoculation In situ, poisoned _____

~_____

Maximum

Steady State

0.44 & 0.25

0.20 f 0.06 0.15 f 0.08 0.10 0.02

0.41 f 0.30 -

*

~ ~ _ _ _ _

Table I1 summarizes the results of fifteen experiments with inshore waters taken near the Nova Scotia coast, showing maximum observed concentrations averaged for each type of experiment and the “ steady state ” concentration attained after the peak.

56

GORDON A. RILEY

The question of bacterial effects was reopened a t a later time with somewhat more conclusive results. The work by Batoosingh et al. (1969), involving comparison of bubbling tests with water that was refiltered immediately, provided the necessary material, for it was found that two filtrations in rapid succession were a fairly effective means of sterilizing the water. Two sets of experiments were performed in which this was held for 5 days and for 12 days and then was filtered a third time, and the 12-day set was plated t o determine the degree of sterility. A duplicate set was given an immediate third filtration to serve as a control to gauge the amount of additional formation during the 5-12 day periods, and a fourth set had 1 ml of raw sea water added to the doubly filtered water to examine the question of whether double filtration would in itself affect the normal process of aggregation. Plate counts indicated that the filtration procedure was reasonably effective. Some plates were completely negative and none had more than a few bacteria per ml. The observed increase in organic carbon averaged 19 pg C/litre in five-day experiments and 6 pgllitre in the twelve-day set. The general range in values was such that these averages were not significantly different from each other nor from the controls. If one chooses to believe that the increase is real, it is no more than might be expected from incipient aggregation of the type described by Sheldon et al. (1967), which may be entirely a physical phenomenon, although this is not as yet definitely established. I n contrast, inoculated 12-day experiments showed a mean increase of 155 pg C/litre, which was significantly higher than controls or the accompanying experiments, although it is somewhat lower than is commonly obtained in water that has been filtered only once. A cruise on the Canadian oceanographic ship “ Hudson ” in JuneJuly 1967 provided an opportunity for experiments with samples taken from a variety of water masses off the eastern Canadian seaboard. Complete time series were difficult under shipboard conditions, for it was desirable to process as many different samples as possible within the limited time available. Most of the experiments were of 6-8 days’ duration, which should be long enough to determine whether particle formation was occurring but probably not long enough to establish a maximum concentration. Samples were filtered by gravity through silver filters (0.45 or 1.2 p ) into four-litre polyethylene bags. Approximately one week later the water was removed through filters of the same pore size used initially, and these were frozen for later analysis ashore. Results are summarized by area and depth range in Table 111. The area listed as coastal and bank waters includes the Scotian Shelf, one station each on the Grand Banks and Flemish Cap, and one

57

PARTICULATE ORGANIC MATTER I N SEA WATER

TABLE111. MEAN PARTICULATE CARBON ( pC/LITRE) IN 6-8 DAY dn S i t U AGGREGATION EXPERIMENTS WITH WATER SAMPLES TAKEN FROM THE AREASAND DEPTH RANGES LISTED. NUMBER OF EXPERIMENTS IS SHOWN I N PARENTHESES

Depth Range 1-150 500-1 200 2 000-4 000

Coastal and Bank Waters

Slope Water

168 ( 6 )

67 (2) 159 (6)

~

68 (4)

Sargasso Sea 46 (1) -

102 ( 1 )

station at the eastern edge of the Grand Banks in the core of the Labrador Current. The Slope Water stations were made in various locations between the Scotian Shelf and the edge of the Gulf Stream. The station labelled Sargasso Sea was in the northern fringe of that area or possibly in the southern edge of the Gulf Stream. For purposes of statistical analysis the data were lumped into two groups of approximately equal size, comprising all samples taken between the surface and 600 m and all those in the 1 000-4 000 m depth range. No samples were immediately refiltered on this cruise to provide paired samples for comparison. Alternatively they were compared with a set of refiltrations of inshore water (Batoosingh et al., 1969) which yielded values of 46 f 20 pg C/litre when 1.2 p filters were used. The means for shallow and deep samples were respectively 127 f 87 and 115 65 pg C/litre. Using the " t " test for unpaired samples, the differences between these means and the ones obtained upon immediate filtration were significant to the 2% level of probability. This is regarded as a reasonably acceptable test in view of the fact that the method is not as critical as comparisons of paired samples. One five gallon carboy of water from this cruise and two from a previous one have been used t o examine the so-called steady state which develops after the initial burst of bacterial growth. The first two were obtained from depths of 2 000-3 000 m in the Sargasso Sea, the third from 900 m in Slope Water south of the Grand Banks. All were filtered immediately on collection. The first carboy was seeded with 1 ml of an actively growing culture of Pseudomona,s. A week later a sample of 1 litre was withdrawn for carbon analysis, and this was followed by successive one-week samplings, 17 in all, until the supply was exhausted. The mean particulate carbon during this period was 63 f 30 pg/litre. There was no obvious upward or downward trend. The variations possibly were real or may

58

GORDON A. RILEY

have been due to sampling errors, for the particulate matter sinks to the bottom of the carboy and may not be thoroughly detached during the mixing process prior t o sampling. Nevertheless, there was an indication of the maintenance of general level, if not a true steady state, for a considerable period. The second carboy was subjected to overnight bubbling to create an initial substrate. Pseudomonas was then added as before, and carbon was again determined a t weekly intervals. During the first 1 2 weeks the average was 98 f 37 pg C/litre. At the end of the 13th week there was an anomalously high value of 1.29 mg C/litre. Probably the filter was grossly contaminated. The possibility of a second cycle of bacterial growth seemed unlikely; there was no evidence of it in plate counts made concurrently. During the remaining four weeks the organic carbon was somewhat higher than it had been in the early part of the experiment (140-170 pg C/litre). The third experiment was inoculated with 10ml of unfiltered surface water. The first sample taken a week later had a concentration of 191 pg Cjl. Subsequently the level declined, and there was a more or less steady state of 106 34 pg C/litre until the end of the 15th week. During the last two weeks there was an increase in organic matter (270-300 pg C/litre). The experiments described thus far indicated that newly formed aggregates in filtered sea water are subject to a rapid increase initially, followed by rapid bacterial utilization, so that by the time the stable phase has been reached the concentration of particulate organic carbon will be roughly half the earlier maximum. At this point the remaining organic matter would appear to be resistant to further attack, although persistence of living bacteria implies either further utilization a t a very slow rate or some slight degree of further aggregation of filterable materials or direct utilization of dissolved organic matter by bacteria. Some variability has been noted in the so-called stable phase in some experiments, and the level varies somewhat from one experiment to another. However, the variation is not large, and the general level of the experimental product is more or less the same as that of naturally occurring particulate matter in the sea and is also similar to that attained in bubbling experiments. The bubbling experiments and in situ production appear to be somewhat analogous in that the rapid rate of initial particle production quickly gives way to a situation in which further formation appears t o be inhibited. This might be a physical inhibition of the sort postulated for bubbling experiments, or it might be caused by exhaustion of substances suitable for aggregation. If this is simply a matter of physical inhibition by the standing

PARTICULATE ORGANIC MATTER I N SEA WATER

59

stock of particles, partial removal of the stock should lead to further formation, as it did in the ca.se of continuous harvesting in bubbling experiments. However, bacterial aggregation is a slower process than adsorption on bubbles, so that a relatively slow rate of harvesting would be necessary in order to test this point. A bottle of freshly filtered inshore water was inoculated with 5 ml of unfiltered water. The bottle was wrapped with dark cloth to eliminate any possibility of autotrophic growth. Water was pumped from the bottle at a rate of 0-6 ml/minute via silicone tubing to a glass fibre filter and thence was returned to the bottle. Every four days a filter was harvested and replaced by a fresh one. During this period the calculated flow through the filter was 3.45 litres. The total volume in the experiment was 4.3 litres, so that the rate of harvesting was 20% of the total volume in a day. I n calculating results the measured amount of organic carbon on the filter could then be used to determine the total amount harvested and also the mean concentration in the bottle during each four-day period. Table I V shows the mean concentrations and the total yield, the latter obtained by summing successive four-day yields. AND TOTAL YIELDIN TABLEIV. ORGANICCARBONCONCENTRATION MG C/LITRE UNDER CONDITIONSOF CONTINUOUS,SLOW HARVESTING

T i m e in Days

Mean Concentration

Total Yield

0-4 4-8 8-12 12-16 16-20 20-24 24-28 28-32 32-36 36-40

0.31 0.12 0.12 0.13 0.10 0.14 0.11 0.08 0.09 0.09

0.25 0.34 0.44 0.55 0.63 0.75 0.83 0.89 0.96 1.03

The mean concentration during the first four days was indicative of an initial burst of bacterial growth. Subsequently there was a more or less uniform concentration until the end of the fourth week and a slight decline thereafter. The concentrations were only slightly smaller and probably were not significantly different from the value of 0.15 f 0.08 mg C/litre reported in Table I1 (p. 5 5 ) for steady state situations in

60

GORDON A . RILEY

experiments using essentially the same kind of water but with no harvesting procedure. This experiment was repeated, using a surface sample taken from the Slope Water area well offshore. Other samples from the same collection were used for additional experiments of a comparative nature. One of these was a 14-litre sample which was stored in a polyethylene carboy. On alternate days 1 litre was removed and filtered for carbon analysis, and the filtered water was then returned to the carboy. Practically speaking, this approximated t o a continuous yield experiment but the daily rate of removal averaged only about 3.5% instead of 20%. The third was a control carboy in which there was no cropping, but 1 litre was removed each week for carbon analysis, and the filtered water was then discarded. Preliminary filtration was carried out a t sea, and the water stood for five days before the experiment began. Initial experiment readings were about 0-40 mg C/litre, and the concentrations declined as the experiments proceeded. Table V shows the mean concentration of carbon during the first four weeks and the total yield.

v. MEAN CONCENTRATION AND TOTALYIELD O F PARTICULATE ORGANICCARRON(MG C/LITRE)WITH THREEDIFFERENT LEVELSOF CROPPING

TABLE

No removal 776 removal, alternate days 20% daily removal

Concentration in Suspension

Total Yield

0.23 0.20 0.13

0 0.24 0.74

Results show that the lower rate of cropping can lead to a significant yield over a period of time with little reduction in the amount of particulate matter in suspension. The higher rate of 20% cropping reduced the concentration by an amount that appeared to be slightly significant (P falls between 0.05 and 0.02). However, a t the expense of only a slight decrease in concentration the yield was substantially increased and was only slightly less than was obtained during the first four weeks of the experiment with inshore waters. During the fourth week there was a general decline in the amount of particulate carbon in all bottles. The concentration in the control bottle was 0.17 mg C/litre at the end of this period, and the averages for the fourth week in the other two bottles were respectively 0.23 and 0.06 mg.

PARTICULATE ORGANIC MATTER I N SEA WATER

61

At the end of the fourth week 1 ml of raw sea water was added to each bottle to find out if a fresh and active supply of bacteria could alter the trend. It did not do so. When the experiment was terminated at the end of the fifth week the concentrations in the three bottles were 0.14, 0.1 I , and 0.05 mg C/litre, respectively. I n summary, the maximum sustained concentration of particulate organic carbon, either in long term bubbling experiments or in situ aggregation, is seldom much more than 0.2 mg C/litre. This concentration tends to be maintained for a considerable period even when part of the product is removed. However, a downward trend has been noted, particularly in cases of heavy cropping, and deep sea samples frequently have a lower steady state concentration than surface samples. A hypothesis has been proposed that particle formation inhibits further formation and that this is responsible for the upper limit of concentration, but there are further indications that the supply of filterable organic matter can be reduced to a point where a maximum concentration of particles cannot be attained or maintained. 2. Bacteria

Most of the experiments were accompanied by plate counts of bacteria. Aliquots of water from experimental bottles were diluted serially in autoclaved water and the series was plated on enriched sea water agar. The plates were then incubated for 3-5 days at 1 5 O C . The dilutions ranged through several orders of magnitude. Ideally the investigator can discard plates which have too few colonies for a good count, or are so heavily overgrown that there is danger of fusion of colonies, and can base his judgement on one or two plates in the middle of the range. There are subjective elements in this procedure, and replication is not as precise as might be desired. Moreover, as everyone who has dealt with this problem is well aware, plate counts commonly give much lower values than direct visual examination. These and certain other difficulties will have to be taken into account in evaluating the results that are to be described. The early series of experiments, for which carbon values are given in Table 11, were mostly of short duration. Some involved an initial inoculation with Pseudomonas sp., and in other cases a natural flora was allowed to develop. I n the former case the method was simply to introduce a small quantity of an actively growing culture of bacteria in the proportion of 0.1 ml of culture per litre of filtered sea water. The actual number of bacteria was not determined in each case, but on two occasions when samples of sea water were plated immediately after inoculation, the count was of the order of lo3 cells/ml.

62

GORDON A . RILEY

I n all cases examined, higher values were obtained subsequently. The maximum count recorded was 87 x l o 3 cells/ml. Most experiments had maximum readings of 30 x l o 3 or higher, but a few were lower. The sampling interval may not have been frequent enough t o record true maxima, and this may have accounted for some of the variability. However, there was an extreme case in which the maximum bacterial count was only 8 x 103 cells/ml, and this was one of the experiments in which organic carbon did not exhibit a n early peak either. The maximum observed concentration during the 10-day experiment was 140 pg C/litre. The earlier discussion indicated that addition of an inoculum of bacteria is not necessary for formation of particulate carbon. Aggregation occurs more slowly when bacteria are not added, but there is little difference in the peak concentration that is eventually achieved. Plate counts showed that there was in fact an abundant increase of bacteria in filtered sea water, but maximum concentrations were seldom as large as those obtained when an inoculum had been introduced. This is best demonstrated in six pairs of experiments which were replicates with respect to the original source of sea water and mode of handling and differed only in that one set was inoculated with Pseudomonas and the other was not. Maximum observed concentrations averaged 39 x lo3 cellslml in the first set and 16 x lo3 in the second. I n experiments inoculated with Pseudomonas, plate counts declined rapidly after the early maximum, and by the end of the first week most counts were of the order of I2 x lo3 cells/ml or less. The total range was of the order of 1-12 x 103, and a reasonable average for the series is about 8 x 103. There was considerable variation from one plate count to another in the same experiment, but comparisons of replicate plates and successive dilutions suggest that the variation can be ascribed largely t o sampling error rather than to real variation in the size of the population. I n cases where the bacterial population was derived from natural flora which escaped the filter, the experiments generally did not last long enough to permit a good estimate of the population level subsequent t o the maximum. This matter will be taken u p in connection with long term experiments to be described later. The relationship of plate counts t o the real population is always problematical. Direct counts in natural sea water commonly range from 1t o 4 orders of magnitude larger than plate counts (Jannasch and Jones, 1959). The culture medium and often the physical conditions of the laboratory environment are not suitable for the growth of a large majority of naturally occurring species. However, the Pseudo-

PARTICULATE ORGANIC MATTER IN SEA WATER

63

monas that was used as an artificial inoculum had been grown in the laboratory for some months and had demonstrated that it was one of the species that thrives under such conditions. Hence there is little reason t o doubt that it could be monitored by plate counts with a fair degree of accuracy. If these counts are accepted as realistic they can be used to evaluate the biomass of bacteria in relation to total particulate carbon. HolmHansen and Booth (1966) estimated that average carbon content of bacteria is about 4 x 1 0 - 7 pglcell, and rough computations based on the measured volume of Pseudomonas suggest that this is a reasonable value t o use for present purposes. Thus the largest observed population of 87 x 103 cells/ml should contain about 35 pg C/litre, and in the later period after the maximum, an average figure would be about 3pg. Thus the living fraction would appear t o be less than one-tenth of total particulate carbon a t all times, and to anyone who has examined the material visually, this is not an unreasonable conclusion. Earlier estimates of 20%, based on direct carbon analysis, possibly are too large, for the inoculum contained some non-living flocculated material. There is a possibility that these figures represent a slight underestimate on the grounds that the Pseudomonas inoculum probably was contaminated by the growth of adventitious bacteria introduced by the filtering process, and some of these may not have been susceptible to detection by plating methods. However, the experiments themselves impose a selective process for bacteria which can grow at room temperature, and in the absence of an artificial inoculum the plate counts for such bacteria were half as large a t the time of the maximum as in the Pseudomonas experiments. If the difference had been an order of magnitude or more, the possibility of the existence of a large undetected population would seem more likely. The paper by Holm-Hansen and Booth (1966) which was cited above was particularly concerned with the development of a method for measuring adenosine triphosphate (ATP) and using it to determine relative proportions of living and non-living particulate organic matter. They established the fact that ATP disintegrates almost instantly upon death of the organisms, and the concentration varied within reasonably narrow limits in various organisms examined, so that the method appeared to be thoroughly suitable for its intended purpose. I n deep water, where bacteria are believed to constitute the major living component, the method was used to estimate the number of viable bacteria. The average for the depth range of 183-1 025 m a t a station off the California coast was 6 x 103 cells/ml, and the authors pointed out that these results were in good agreement with direct counts reported

64

GORDON A.:RILEY

by Kriss (1963) in various deep water situations. The values obtained by these authors are similar to the estimated population of Pseudomonas during the stable phase after the early maximum, suggesting that the balance between living and non-living fractions in these experiments is essentially similar to that which occurs in the sea. Plate counts were made during the experiments involving long term storage of deep water and in two of the three experiments summarized in Table V. The third experiment in Table V, involving continuous circulation and a 20% cropping rate, was not monitored. These experiments included inoculation with Pseudomonas, inoculation with raw sea water, and simple filtration with no additions, but in all cases results were essentially the same, differing only in minor details of timing and relatively insignificant variations in population level. The early maximum was observed in some experiments and not in others, as indicated in the earlier account of carbon concentrations. There was a stable phase with populations of the order of lo4 cells/ml, more or less, which was approximately the same as in short term Pseudomonas experiments described earlier. This persisted for 2-4 weeks, and then the plate counts began to increase steadily. The number of dilutions required for suitable counts had t o be increased. Errors were suspected, and the water used for dilution was examined frequently and found to be negative. The increase continued to the end of experiments lasting 17 weeks, and the concentration at that time was of the order of 10" cells/ml or more. No good reason has been found to reject the plate counts. On the other hand, the quantity of bacteria found, if they had a " typical " carbon content of 4 x 10-7 pglcell, would total 0.4-1 mg C/litre. This is about an order of magnitude higher than the total carbon that was demonstrated t o be present. Moreover, visual examination gave no indication of a marked increase in bacteria. Careful microscopic counts were not attempted but any such increase would be clearly evident. If the plate counts are valid, the bacteria would have to be small enough t o be unrecognized as such in these examinations and of a size to permit their total carbon content t o fall within reasonable limits. This probably means a size range of 0.2-0.4 p for much of the p o p lation. There is a common impression that most marine bacteria are of the order of 1-3 p (ZoBell, 1946). However, water that has passed through 0-45 p filters is almost never sterile, and the most rigorous precautions do not always prevent growth in water that has gone through 0.22 p filters. Later examination of such filtrates commonly shows the presence of bacteria that are too large to pass through the filters.

PARTICULATE ORG-4NIC MATTER I N SEA WATER

65

Hence, while there may be marine bacteria that fall within this size range in their normal vegetative state, some of them must have nonactive stages of a smaller size. Senescent stages are commonly reduced in size. The writer can find no information as to whether any marine bacteria are known to produce filterable " L phases ", although certainly many of them are highly pleomorphic. Thus the existence of viable, filterable bacteria in sea water is established beyond reasonable doubt, but the form in which they occur is open to question, and their quantitative abundance is not known. They are possibly a small percentage of the total biomass. The ATP analyses described by HolmHansen and Booth (1966), indicated that total biomass was essentially in agreement with observed numbers of cells of normal size. The situation described in long term experiments is clearly different, but experimental procedures induce an artificial selection of filterable forms and eliminate any bacteria that require special conditions such as low temperature or high pressure. The ones that survive and multiply in the experiments have a good chance of being suitable for detection in plate counts. Although these considerations supply a possible explanation for astronomical numbers of bacteria despite the relatively low value for particulate carbon, they do not provide much insight into the dynamics of the situation. The early part of the experiments suggested a stable state in both bacteria and particulate matter. The latter remained more or less constant thereafter, although increasing slightly during the final few weeks of some experiments, while the bacterial population was anything but stable. However, there is a question as to how many of these bacteria were in an active physiological state. There was a small, continuing p o p lation of bacteria of normal size, which was readily detectable by visual examination. One can postulate that these were existing on the verge of senescence, some being able to divide normally and others being transformed into smaller forms which gradually accumulated in a viable but inactive state. I n summary, the early stages of the so-called stable state seem realistic in that carbon levels and bacterial counts approximate those found in the sea. The later sequence of events remains realistic only with respect to maintenance of a reasonably stable carbon level, and problems involving dynamic relations with bacteria require further study by more exacting methods. Here again, as in bubbling experimenfs, there is a need for an examination of basic problems, preferably with defined artificial media. Moreover, the experiments are deficient in that data are largely

66

GORDON A. RILEY

lacking on dissolved organic carbon. The ordinary method for determining organic carbon by wet oxidation is not precise enough to provide useful information on some of the small changes that are involved here, and as indicated earlier there is considerable doubt as to whether all of the organic carbon is oxidized. Methods for carbon determination by dry combustion are under development in this laboratory by P. J. Wangersky, but data are not yet available for incorporation in the present account. C. Sinking rates 1. Introduction to the problem Various problems involving the biological and geochemical significance of non-living particulate matter require some knowledge of its residence time in the ocean and its sinking rate. Thus far no direct measurements of sinking rates have been published. Riley et al. (1965) made an indirect calculation based upon estimated food requirements and availability of assimilable organic matter in deep water. The results implied an average residence time of four years and an average sinking rate of 2 miday, with a general range in likely estimates of 1-7 m/day. This estimate was of course dependent on the validity of several assumptions about biological relationships. In particular, recent work by Gordon (1970b) on enzymatic hydrolysis of particulate organic matter suggests that the assimilable fraction may be less than was assumed by Riley et al. (1965), and if this is so, the sinking rate was over estimated. I n contrast with these estimates Menzel and Goering (1966) postulated that the particulate matter below a depth of about 200m is unassimilable and neutrally buoyant. Some experiments were described in which water samples were filtered, and the filter pads were inoculated with surface water. No significant decrease in carbon was found after 90 days’ storage. The further postulate that the particles are neutrally buoyant was not supported by data but was regarded by these authors as the simplest explanation for observed patterns of distribution. Hobson (1967) used a Coulter Counter to measure the size-frequency distribution of deep water particulate matter, and with certain assumptions about the specific gravity of the particles he was able to calculate sinking rates, using a modified version of the Stokes equation. He concluded that most of the rates should be within the general range of 0-1-10 m/day. This large range resulted from a variety of assumptions about specific gravity ; there was no certainty about the correct value to be used, and the range was too large to be very useful.

PARTICULATE ORGANIC MATTER I N SEA WATER

67

Direct measurements clearly are needed. The present section will deal with a few measurements that have been made on naturally occurring surface and deep water particulate matter and experimental preparations. The quantity of data is not large, but it is enough for present purposes. 2. Methods

This work was done with an inverted microscope, using a counting cell 1-5cm in diameter and 4.5 cm high, which was merely a lucite tube with a cover slip cemented to the bottom. Lucite was used because it has a lower rate of thermal conductivity than glass, and it is important in experiments of this sort to reduce convective mixing as much as possible. A cover slip was laid on top to inhibit evaporative cooling. Preparation of the material presented some problems. I n the beginning an attempt was made to follow the method used by Smayda and Boleyn (1965, 1966a and b) to measure the sinking rate of diatoms. These investigators filled their tubes with sea water of a salinity of 32%, and introduced a diatom population at the surface in a medium of 30%,. Initially all of the diatoms were within the upper boundary layer, and the bottom of the cell was then scanned at intervals thereafter to determine the rate of sinking from surface to bottom. There were practica1 difficulties in applying this method in the present case. I n order to get enough material for a good count, the particulate matter had to be concentrated into a small volume. Under these conditions the aggregates tended to coalesce, and the sizefrequency distribution was unrealistic. Thus it was necessary to use whole water samples or slightly concentrated ones and to fill the entire cell with uniformly mixed material. The method sacrificed any possibility of determining sinking rates of individual particles but permitted a statistical estimate of the average rate of passage of the various kinds of particles through a mean vertical path. Repeated examinations were made of the same area on the bottom of the cell, consisting of a strip 0-3 mm wide and 10 mm long, under a magnification of x 300. The ocular grid that was used as a guide in counting was subdivided into smaller squares equivalent to 30 p and 6 p, which served as convenient references for estimating particle size. The categories that were recorded were flakes, four size ranges of amorphous aggregates, and miscellaneous particles in the size range of 2-6 p. The character of the latter could not be clearly distinguished in all cases. Phytoplankton and bacteria were excluded, of course, but the less structured material which was counted probably included

68

GORDON A. RILEY

particles that were primarily silt or minerals rather than organic matter. Initially the cell was filled to a height of 4 cm with a well mixed suspension, and the chosen area was scanned rapidly at intervals of 5-15 minutes in order to get as much information as possible on the arrival time of large and rapidly falling particles. After the first hour or so the counting interval was gradually increased. The time required for scanning also was longer with the arrival of increasing numbers of small particles on the bottom. I n each case the time was recorded as the mid point of the scanning period, but the actual time involved varied from 2-20 minutes. Counts ordinarily continued for a total elapsed time of 6-8 hours, with a final check at the end of 24 hours. Further increases between 8 and 24 hours were slight and were only in the smallest size category. 3. Results

Figs. 7 and 8 show examples of the kinds of results obtained. The counts were made on a sample of surface water taken just offshore in the area near Halifax. Arrival times of four size ranges of amorphous

0

100 TIME

FIG.

200 IN MINUTES

300

400

7. Sinking speeds of organic aggregates. The number of particles of the size range indicated is plotted against the times when they appeared on the bottom of the counting chamber. These data were used to compute generalized sinking rates shown in Exp. 1, Table VI. Short vertical lines indicate points arbitrarily chosen for determining variations in sinking speed. See text for further details.

PARTICnLATE ORGANIC M-4TTER I N SEA WATER

69

5OOr

8 12 16 20 24 TIME IN HOURS FIG.8. Sinking speeds of small particles and flakes. Format is similar to Fig. 7 and again refers t o Exp. 1. Table I7I. 0

4

aggregates are illustrated in Fig. 7 , and Fig. 8 shows the results for flakes and miscellaneous small particles. The interpretation of experimental results for flakes and small particles is fairly simple. The curves rise in a linear fashion and tend to level off abruptly. This is what one would expect if the particles have a uniform sinking rate, and the latter is calculated simply as the total length of the column of water divided by the time required to reach the break in the curve. The curves in Fig. 7 are more complex, indicating a spectrum of sinking rates. Maximum and minimum values can be determined roughly from the initial slope and the final point of leveling. In these experiments and others there have tended t o be sharp inflection points in the curves, so that with only slight over-simplification they can be broken into two or more linear segments, implying that the curve is compounded of two or more kinds of particles, each with uniform sinking rates. I n such cases we can postulate a simple solution which is illustrated diagrammatically in Fig. 9. Here there are two kinds of particles, X and Y , each with a constant sinking rate, so that all of X reaches the bottom of the cell a t time tx and all of Y at time t , as indicated by dotted lines in the figure. Then X+Y=B where B is the total number at time t,, and the number A a t time t, is

70

GORDON A. RILEY

From these equations individual values for X and Y can be computed. The inflection points serve to establish maximum and minimum values for the sinking rate, and the two rates can be combined into a single mean value by appropriate weighting of the relative numbers of X and Y . A more sophisticated analysis would be possible, but elaborate treatment is hardly warranted. The size-frequency distribution of particles varies somewhat from one sample to another, and other variables and experimental errors are such that precise evaluation of any one experiment is not very meaningful.

0

I00

ZOO

TIME

11.1

300

400

MINUTES

FIG.9. Diagrammatic exposition of methods used for estimating ranges and mean values for sinking rates. For further details see text.

Two other experiments were performed with inshore water, all collected during early summer, and the results are given in Table VI. The methods that have been described served to establish a general range of sinking rates and a mean value for each category. Four samples were taken at a station in Slope Water at various depths from the surface to 3 000 m. Some difficulties were encountered in sinking rate experiments with this material because the number of particles was minimal for good counts, and flakes were not easy to distinguish in the natural, unstained condition. Counts of flakes are omitted, for successive counts were inconsistent. The remainder of the results are shown in Table VII. This clearly is not as consistent a

71

PARTICULATE ORGANIC MATTER I N S E A WATER

TABLEVI. SINKING RATEI N MIDAY OF VARIOUS SIZES AND KINDS OF PARTICLES FOUND IN INSHORE SURFACE WATERS Range ~~

~~~

~

0.78-1'4 0.31-0.93 0.31-0'57

Exp. 1. Aggregates >60 p 30-60 15-30 6-15 Mist. particles 2-6 p

-

2.9 1.1 0.70 0.50 0.10 0.17

0.24-2.6 0.24-1 '6 0.10-0.97 -

1-0 0.44 0.19 0.15 0.18

0.97-2.1

1.a 0.54 0.45 0.31

-

Flakes

Exp. 2. Aggregates >30

Mean

~

p,

15-30 6-15 Misc. particles 2-6 p

Flakes Exp. 3. Aggregates >60 p

-

30-60 15-30 6-15

0.32-0.54 0.22-0.54

set of data as the other set, but it shows that there is a general similarity between the sinking rates of surface and deep water particles. A few comparative studies were made of experimental material. Flakes produced artificially by bubbling had a mean settling rate of 0.30 m/day. The fact that they had a slightly faster sinking rate than natural flakes is not surprising, for many of the natural ones are filmy in appearance and presumably have been partly degraded by bacteria. Measurements were also made of aggregates produced experiment ally by bacterial activity. The material was taken from an experiment described earlier in which the particulate matter was routinely cropped TABLEVII. MEAN SINKING RATESOF AGGREGATES AND SMALL PARTICLES IN SURFACE AND DEEPWATERS OFF THE SCOTIAN SHELF. ALL VALUES ARE LISTED

Size range >60p 30-60 15-30 6-15 2-6

0

1.1 0.83 0.32 0.26 0.27

500

0.48 0.29 0.19 0.12

AS METRESIDAY

1000

3 000

0.58

0.43 0.34 0.29 0.38 0.22

0.38 0.26 0.25

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GORDON A. RILE1

a t a rate of 7 % on alternate days, and the test was done a t the time when the experiment was terminated after a period of about five weeks. The following rates were obtained : 15-30 p, 0.82 m/day ; 6-15 p , 0.50 ; 2-6 p, 0-20. These are in general higher than the rates for natural particles of comparable size, but the difference is not marked.

4. Discussion Observed sinking rates of different kinds of particles vary by more than an order of magnitude, and within any particular size category there is some variation from one experiment to another. Further variation is introduced by size-frequency differences between one sample and another, so that there is no simple answer to the question of what the sinking rate of non-living particulate matter in the sea may be. The largest particles measured here could sink from the surface t o the deep ocean bottom in a little more than two years if they maintained their integrity that long. The smallest ones would require fifty years or more. I n general the largest particles in these counts are volumetrically the most important constituents. The large volume of individual particles in the upper size ranges more than compensates for the fact that they are minor elements numerically. This is illustrated by a volume computation based upon data obtained in Exp. 1, Table VI. Particles larger than 60 p are assumed t o have a mean volume equivalent to a spherical particle with a diameter of 80 p. The other aggregates are calculated as spheres with mean volumes equivalent to the size ranges listed. Most of the aggregates appear to be more or less spherical in the free floating condition, so that this is not a serious over-simplification. Flakes are calculated as disks with a diameter of 25 p and a thickness of 5 p. The latter is a guess, for they are seldom oriented in a position that permits measurement of their thickness with any degree of accuracy. TABLEVIII. VOLUME COMPUTATIONS Amorphous aggregates

Size range >60 p 30-60 15-30 6-15 Misc. particles 2-6

Flakes

Number

6 16 38 58 420 75

BASEDUPON DATAFROM Vol./particle

EXP. 1

1 0 3 p3

Total Volume (X 103 p 3 )

270 63 7.9 0.96 0.058 2.4

I620 1008 300 56 24 180

PARTICULATE ORGANIC MATTER I N SEA WATER

73

The results are shown in Table VIII. In this particular set of data particles with a diameter of more than 30 p constituted only 3.6% of the total number but represented over 80% of the total volume. One can go a step further, multiplying the total volume in each size range by its mean sinking rate, summing, and dividing by the total volume of all particles, and thus arriving a t a mean sinking rate for the assemblage as a whole. I n the present case it is 1.4 miday. A similar computation for Exp. 2 gives a value of 0.8 m/day. Mean sinking rates for the three deep water samples in Table VII ranged from 0.41-0.50 m/day. These results suggest that most of the organic matter is concentrated in larger particles and sinks at a rate that is near the upper limit of experimentally determined values. However, this conclusion must be qualified by adding that the organic content of the particles probably is not precisely proportional to volume. Most of the large masses are visibly less compacted than the small ones. I n the free floating state they are loose conglomerates of material, with open spaces in which bacteria and microflagellates can be seen circulating freely. Thus the overall volume is not a good index of the actual volume of solid material. Moreover, there are large numbers of particles that are smaller than 2 p, ranging down toward the limits of visibility and presumably beyond, into the colloidal range. As indicated earlier, the quantitative aspects of this size spectrum have not been described in a satisfactory way. Thus a significant but essentially unknown fraction of the total particulate carbon occurs in small particles with a sinking rate that is probably less than 0.1 m/day. Experimentally determined sinking rates were used to estimate the specific gravity of the various size ranges of particles. This calculation was based on Stokes’ Law which may be stated as

W

=

219 g

Pz

--

P1 r z

~

P

where W is the sinking speed, g the acceleration of gravity, p1 and pz the density of the water and of the particle, respectively, and p is the dynamic viscosity of the water. All values are in the c.g.s. system. For application to present experimental conditions we can assign values of p1 = 1.02 and p = 0.01. W has been measured experimentally, and r is designated as the median value for each of the size ranges that has been examined. Table I X shows results obtained by application of the formula to data from Exp. 1. The increase in specific gravity with decreasing size is consistent

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GORDON A. RILEY

but slight down to the 6-15 p size range, and that particular result may be atypical, for the observed sinking rate was unusually high. A similar computation based on the observed sinking rate of 0.19 m/day in Exp. 2 gives a value of 1.070 for particles in this size range. The slight variation in specific gravity with size is in accord with visual indications that the larger particles are less compacted, tending to have larger water-filled interstices. There is no reason to suppose that there is any real difference in the organic matter itself. TABLEIX. COMPUTATIONOF SPECIFIC GRAVITY AS DETERMINED FROM MEASUREDSINKINGSPEEDSIN EXP. 1 Aggregates >60 p 30-60 15-30 6-15 Misc. particles 2-6

Assumed Radius

Sinking Speed

Specific Gravity

40 22 11 5

2.9 1.1 0.70 0.50

1.033 1.034 1.057 1.146

2

0.10

1.152

Observed sinking speeds of 2-61” particles have varied from 0.100.25 m/day in the various experiments, and the estimate of specific gravity in Table I X is a minimum figure. Some of the estimates run as high as 1.40. These small particles cannot be seen easily at the magnification that was used, and their nature is open to question. Some of them undoubtedly are minerals and clay particles with an organic coating. Flakes are omitted from the present discussion. Stokes’ Law is of course inapplicable. There are methods for dealing with disks and plates (Munk and Riley, 1952), but they require better estimates than are now available of the thickness of the flakes. Experimental material appears to be more variable than naturally occurring particles. Some sinking rates were mentioned above which were obtained from an experiment that had been underway for some weeks, and calculated specific gravities of amorphous aggregates were 1.05-1.13. These aggregates probably were lying on the bottom of the container much of the time and may have been more compact than free floating material. I n contrast, one measurement was made during the early stages of an experiment in which the aggregates were diffuse and only barely visible. The sinking rate of 25 1“ particles was 0.19 m/ day, and the calculated specific gravity was 1.027.

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I n looking over the results as a whole, a good many ambiguities remain. The complete spectrum of sizes and sinking speeds has not been examined. Most of the particle counts described in earlier parts of the paper were based on samples of not more than 250 ml of sea water. These commonly contain a few particles of the order of 100200 p in diameter, which could have sinking rates of as much as 5-10 m/ day, The " marine snow ') which has been reported by direct observation probably is still larger and can have a correspondingly faster sinking rate, but the concentration is too small for them to appear in small samples except on rare occasions. However, in certain circumstances they may be important. Aggregates predominate in the surface layer, and the larger sizes are volumetrically the most important. They are presumably delivered into deep water in the same proportions as they exist in the surface layer, and the apparent decrease in abundance is due in large part to the fact that they have a rapid sinking rate and a relatively short residence time in the deep water column. The rate of delivery t o animals in deep water or t o the deep ocean bottom will be proportional to the product of the sinking rate and the concentration in the water. Dynamic considerations of this sort will seriously underrate the importance of large particles if one considers them only in terms of observed concentrations in the water. The relationship between temperature and sinking rate has not been examined experimentally. This would be desirable, but temperature effects are minor compared with some of the other variables that have been discussed above. I n the case of small particles with a specific gravity of 1.1 or more, the effect of increased density of the water would be less than the differences recorded in individual experiments. The most important temperature dependent variable would be the increase in the viscosity of the water, which could reduce sinking rates nearly 50% in deep ocean waters. Since the reduction in specific gravity of large particles is believed to be due mainly t o water inclusions, temperature equilibration as particles sink would tend to maintain a constant difference between the specific gravity of particles and water except in strong temperature gradients. Again the main variable is expected to be increased viscosity.

V. GENERALDISCUSSION A. Re-examination of the aggregation process The original aggregation process as described by Baylor et al. (1962) and Sutcliffe et al. (1963) involved migration of surface active substance toward the surface via bubbles and the formation of particles containing

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organic compounds with molecular weights in excess of 300. This much was well documented. Their hypothesis that particle formation involves the compression of monomolecular surface film into a polymolecular complex seemed at that time to be the simplest explanation of further events. However, Garrett (1968) has questioned whether film compression occurs to a significant degree, and other findings suggest that processes acting a t the sea surface are more complicated than was originally supposed. Wangersky ( 1965) believed that adsorption of organic matter on crystals of sea salts was an important feature of the process, and apparent stabilization of the crystals indicated that the organic " skin " was relatively impermeable. Further evidence supporting these results was the demonstration by Chave ( 1 965, 1968) and Suess (1968) that calcium carbonate can be protected from solution by absorbed organic coatings and that naturally occurring particles frequently contain calcite crystals. Papers by Garrett (1964), Jarvis (1965), Jarvis et al. (1967) and several others by this group of investigators have examined the physical and chemical characteristics of surface films in the sea, using a collecting device which picks up the upper 0.15 mm of water and associated surface film materials. The materials were used for chemical analysis and experiments on physical properties. Garrett (1964) reported the presence of free fatty acids, fatty acid esters and alcohols, and probably nonpolar hydrocarbons. Small quantities of carbohydrates and polypeptides or amino acids (as determined by anthrone and ninhydrin reagents, respectively) were reported. These latter materials were passed through a Sephadex column which had an exclusion limit of about 5 000 molecular weight units. The majority of the carbohydrate material was in the high molecular weight fraction, and most of the ninhydrin reactive substances had molecular weights of less than 5 000. Jarvis (1965) reported that surface active material can be transported to the surface and collected there by either bubbling or stirring. Jarvis et al. (1967) found in experimental studies of film pressure that the calculated average film thickness of some of their samples was a s much as 300& more than an order of magnitude larger than the calculated thickness of a monomolecular film. They concluded that there is a selective process involved in which initially all of the organic materials arriving a t a clean water surface would be adsorbed a t the interface, but with further addition only the more surface-active molecules such as long-chain fatty acids would remain strongly adsorbed, and more weakly adsorbed and water soluble molecules would be displaced.

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This interesting series of papers helps to broaden our knowledge of surface film processes. Some of the facts they report may have a direct bearing on problems of particle formation. There is a possible mechanism here for fractionation of materials and for concentration of the carbohydrate and protein components, which appear to be particularly important in flake formation. These authors presumably were thinking of downward displacement of the less surface-active materials. However, it is equally possible that water droplets derived from bursting bubbles and carrying the usual array of surface film organics and inorganic ions could, when they fall back into the sea, release the most surface-active molecules to the interface and leave the other substances floating on a ‘‘ dry ” surface. Such phenomena could be involved in the kind of flake formation described by Wangeraky (1965). Other investigators, cited in an early section of the paper, thought that particulate matter formed as little skins of organic matter on submerged bubbles. This is a distinct possibility ; flakes can form very quickly. The writer has collected flakes by holding a microscope slide over filtered sea water, turning on an air supply, and removing the slide as soon as it collected a few droplets. Typical flakes could be seen, sometimes still adhering to intact bubbles. Several investigators have mentioned the fact that bubbles can scavenge bacteria and nanoplankton as well as non-living particles. These materials have been shown to accelerate flake formation and presumably are incorporated within them. However, there is little visible evidence of this. The flakes are not a mere conglomeration of small particles. Enough other materials have been added to give them a emooth surface and essentially homogeneous appearance. This implies additional adsorption of colloids and/or polar molecules. The impermeable nature of the material formed and the presence of molecules of high molecular weight suggests that synthesis is occurring. Electrical charges a t air-water interfaces are an obvious source of energy for organic synthesis. If these are the main factors involved, then the various sites and modes of formation mentioned above are not mutually exclusive. I n contrast with the flakes, most of the particles that form spontaneously in filtered water have a granular appearance, suggesting that they are merely an aggregation of discrete smaller particles, and as indicated earlier their reactions to histochemical stains are also different. However, some flakes are invariably found in these experiments on i n situ aggregation. The most careful precautions to eliminate airwater interfaces during and after filtration do not entirely prevent their formation. Moreover, there is circumstantial evidence that they are

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formed in deep ocean water, although it is not obvious how they could be provided with the necessary energy for organic synthesis or moulded into the characteristic leaf-like shape under these circumstances. However, within the general size range of 15-35 p, flakes are the most abundant particles in deep water (Gordon, 1970a). Gordon also showed that most of their protein can be removed by enzymatic hydrolysis, and present work indicates that they are readily attacked by bacteria in experiments of some weeks’ duration. They are found in deep water in various stages of decay, and some look as fresh as newly produced particles. If they were produced only in the surface layer and sank through a typical vertical column of 4000m, the residence time would be more than 50 years. Since some of them are being degraded by bacteria, a t least t o the point of virtual invisibility if not complete destruction, one would expect a decrease with depth, but this is not the case. There seems to be no reasonable alternative to some mode of formation in deep water. The other type of in situ aggregation, by simple amalgamation of smaller particles, is not so mysterious, although certain aspects have not been fully worked out. The study of early stages of formation by Sheldon et al. (1967) leaves some doubt as to whether the initiation of the process requires bacteria or is entirely a physical process. The later production of large quantities of aggregated material requires a bacterial flora in the experiments that have been described. The general principles have been known for years and have been used to practical advantage by sanitary engineers in the treatment of sewage. The problem appears to be simply one of reducing the electrical charges which ordinarily keep particles dispersed, and sewage effluents are aggregated and precipitated by chemical or bacterial treatments which accomplish this purpose. I n summary, observations and experiments with natural sea water indicate that particulate matter can be formed on air-water interfaces and within the water column by aggregation of smaller particles, together with adsorption of colloidal and probably dissolved organic material. Adsorption of organic matter on inorganic particles has been demonstrated. Biochemical synthesis and incorporation of inorganic ions appear to be important. Formation of particles on air-water interfaces by compression of monomolecular films remains as a possible mode of formation but has not been undeniably established. The complexities of the natural sea water system have placed several constraints on attempts t o sort out the various processes that are involved. Attempts to examine the physical chemistry and biochemistry of simplified artificial systems have been abortive because of difficulties

PARTICULATE ORGANIC MATTER I N SEA WATER

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of preparing artificial sea water that is sufficiently pure for the purpose ; however, basic studies of this type are essential for further progress. B. Dynamics of production and consumption of non-living particulate matter in the sea 1. Physical process of movement and dispersal (a) The surface layer. The fact that particulate matter is concentrated in the immediate surface layer of the sea and in convective downdrafts is sufficient evidence that production of particles a t the surface is effective ; but we know very little about actual rates of production. Batoosingh et al. (1969) found that when unfiltered sea water was bubbled, the yield was not significant. This was presumably due to the same phenomenon that is observed in any other bubbling experiment ; the accumulation of particles inhibits further formation, and natural sea water contains a large enough concentration of particles to be inhibiting. One would suppose then tha,t the rate of formation is just sufficient under ordinary circumstances to replace losses, although seasonal variation in the non-living fraction indicates some degree of imbalance between production and removal. The sea surface presents some of the features of a continuous yield experiment, and this is primarily responsible for continued production of flakes. Vertical turbulence in the surface layer tends t o counteract upward flux on bubbles: and convective processes drain off the surface water and transfer it to a deeper level, in some cases all the way to the bottom of the mixed layer. The discussion would profit from a better knowledge of the rate of convective overturn. As indicated earlier there is some doubt as t o whether Langmuir convection cells are as simple and well organized as has been indicated in some of the literature, and there is little real knowledge of either volume transport or depth of penetration of the downdrafts. However, the mere fact that downdrafts exist, removing surface materials t o a deeper level, is biologically significant, and with some possible over-simplifications an order of magnitude estimate should be attempted. Sutcliffe et al. (1963) measured the sinking speed in convective downdrafts associated with Langmuir cells by measuring the vertical displacement of a slightly buoyant disk 20 cm in diameter. They obtained values of the order of 3-6 cmisec. The sinking speed was correlated with wind speed, the higher values being obtained with winds of about 6 m/sec. The width of the downdrafts is somewhat variable but commonly

80

GORDON A . RILEY

is not much more than the diameter of the disk that was used for measurement. I n order to make a rough estimate of the rate of coilvective circulation, the downdraft is assumed to be exactly 20 cm wide with a vertical velocity of 6 cmisec. The wind speed is assumed to be 6 misec, and according to Faller and Woodcock (1964) the distance between convergences would be about 30 m, and the depth of the mixed layer would be about 24m in temperate latitudes. If the downdraft went all the way to the bottom of the mixed layer, the time required would be 400 seconds. Between the convergences there would be a return movement toward the surface of a more diffuse nature, and if it were uniform throughout the 30 m distance between convergences the speed would be 1.4 rn/hour. The time required for complete overturn would be about three-quarters of a day. This rate of upward movement is many times faster than observed sinking rates, and particles caught in the upward movement would be carried back toward the surface. Stommel (1949) developed a mathematical model of the behaviour of sinking particles in these convection cells. The model possibly is somewhat idealized in that he postulated a symmetrical rotation, and the actual cells appear to be very assymmetrical, with strong downdrafts and much more diffuse upward motion, but the general principles should hold. Stommel showed that when the velocity of upward motion exceeds the sinking rate there is an " area of retention " in the ceiitre of the cell, in which the upward motion of water is sufficient to overcome natural sinking tendencies, and particles within this area will be trapped. Theoretically they would remain there permanently. I n actual fact, as Stommel pointed out, there would be turbulent exchanges between this area and surrounding regions. However, the important point is that the rate of loss by sinking from the surface layer would not depend simply on the sinking rate of the particles but would be determined by all the variables involved in the convective system. The smaller the sinking rate is in relation t o the velocity of the water, the larger the area of retention will be, and in the present case it would be quite large. The net effect is presumed to be that only a small proportion of the particle content of the mixed layer will be subject to loss a t any one time, and this loss will occur as water reaches the bottom of the convective layer and spreads laterally and before it begins to rise again. The form of the convective movement can be traced more easily in the columnar cells that occur in calm weather than in Langmuir cells. These are often seen in the Sargasso Sea, where the Sargasso weed

PARTICULATE ORGANIC MATTER I N SEA WATER

81

drifts into more or less circular patches five or ten metres across, which readily identify these areas as points of convergence and confirm the fact that convection cells are indeed columnar. The temperature is commonly 0-1-0.3°C cooler in the convergences than in the surrounding water, and the temperature is essentially constant with respect to depth. I n the water between the convergences a slight negative temperature gradient is likely to develop during these calm periods. Often, particularly during the night and early morning hours, a temperature inversion can be found just a t the top of the thermocline. This is a thin layer, generally less than half a metre thick, in which the temperature is slightly warmer than that immediately above it but generally cooler than the surface water. I n order to be stable in the position in which it is found, this water also must be slightly more saline than the water just above it. On one occasion the writer took a series of closely spaced bathytherms as the ship drifted slowly across and beyond one of these convergences. The temperature in the downdraft was the same as in the inversion beyond, and the profile gave the impression that the latter was derived by spreading from the base of the convergence. There seems to be little doubt that this water is the product of surface cooling and evaporation. Particulate matter in a thin layer of this sort will not have to sink very far in order to be trapped in the thermocline, and it will be apparent that the rate of loss from the mixed layer will depend more on the rate of convective overturn than on the actual sinking rate of the particles. A direct estimate of rates of loss is impossible in the present state of our knowledge. However, the problem is essentially the same as that of removal of phytoplankton from the mixed layer, a subject that has been given some attention over the years. Riley et al. (1949) developed some mathematical models of the vertical distribution of phytoplankton, and in order to obtain a realistic vertical distribution it was necessary to assume a sinking rate of about 3 m/day in temperate waters and 6 m/day in the subtropics. Steele (1958) and Riley (1965) used similar assumptions in further models that have been developed. The assumption of a regional variation in mean sinking rates was adopted on the grounds that variations in viscosity associated with regional temperature differences could have this effect. However, measured sinking rates of phytoplankton vary enormously, and most of them are less than the values postulated here. The idea that average sinking rates of natural populations should be so nearly constant, or

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GORDON A. RILEY

should vary so precisely with changes in viscosity, is questionable. Riley (1965) suggested alternatively that this apparent sinking rate might actually be due to convective overturn, a concept which has been developed more fully in the present discussion. If this concept is correct, regional variations in apparent sinking rate would be related to thermal structure of the water rather than to differences in viscosity. I n general, the seasonal thermocline tends to be somewhat deeper in tropical and subtropical waters than in higher latitudes. Many local exceptions can be found, such as the shallow thermoclines associated with upwelling. However, when the thermal structure develops as it simple function of wind stress, the depth of the mixed layer for any given wind speed theoretically should be inversely proportional to the sine of the latitude (Rossby and Montgomery, 1935). This kind of variation was implicit, though not explicitly stated, in the model of regional variations of phytoplankton (Riley, 1965). The assumption of a regional variation in sinking speed could have been stated alternatively as an advective removal of a certain fixed proportion of the population in the mixed layer each day, and the results would have been essentially the same. I n order t o get numerically realistic results one would have to assume that about 5-7% of the mixed layer loses its population each day. Convective motion obviously deserves more thorough study, both as a physical process and in respect t o its biological implications. The hypotheses proposed here remain tentative, but they provide possible explanations for problems that eluded solution for a long time. There are further implications with regard to non-living particulate matter. Particles which have the same spectrum of sinking rates as phytoplankton should have approximately the same area of retention and the same rate of loss from the mixed layer, and this rate of loss could be several times larger than observed sinking rates. Of course this must be qualified by saying that there are times when negative gradients in the surface layer are too strong to permit convective overturn, and at such times both phytoplankton and non-living matter will be removed at their natural sinking rate. A correlation has been noted between the quantity of phytoplankton and non-living matter. Moreover, flakes and aggregates are of a size that should make them susceptible t o removal by indiscriminate filter feeders to about the same degree as phytoplankton. These similarities in processes of removal suggest that rates of production also are probably more or less similar. I n general this means that the daily increase in particles of 5 p or larger could be about 5-15% of the amount present.

PARTICULATE ORGANIC MATTER I N SEA WATER

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Particles smaller than 5 p in diameter will be taken less efficiently or not at all by indiscriminate grazers, and they are not likely to be transferred downward very effectively either by ordinary sinking or by the mediation of convective downdrafts. A thin layer of water spreading laterally from these downdrafts will not remain in contact with the thermocline very long and is unlikely to lose an appreciable quantity of particles that have sinking rate of 0.1 m/day or less. The analogy with phytoplankton dynamics is inapplicable, and small particles may be subject to other processes, such as aggregation into larger particles, which cannot be estimated quantitatively. As indicated earlier, the amount of organic carbon in the various size categories cannot be stated precisely, and this creates a major difficulty in arriving at a quantitative treatment of this subject. Some approximations will be presented in a later section as to likely rates of transfer into deep water, and these will be compared with independent estimates of rates of utilization. (b) T h e transition zone. I n certain respects deep ocean conditions begin at the top of the thermocline. Here convective flux ceases to be a factor. Further transport into deep water will be essentially a sinking phenomenon, somewhat augmented by vertical eddy diffusivity, for there is usually a negative gradient in particle concentration. Bubbles at this depth are most unlikely, and any formation of new particles should proceed according to processes described in experiments on unbubbled samples. However, there is a zone underlying the mixed layer which differs from the deep sea in several important respects. This transition zone is best defined as that part of the vertical column in which there is a marked decrease with depth in particle number and total organic carbon. The maximum limit of this zone has been found at depths of as little as 200 m (Menzel and Goering, 1966) or as much as 900 m in some other sets of observations (Riley et aZ., 1965). Below this depth variations tend to be smaller and of a random nature, or occasionally there may be larger variations associated with particular water masses, but there are no systematic negative gradients. Particles enter the top of the transition zone a t a rate that is at least equivalent to observed sinking rates of near-surface material and may be somewhat larger, if there is any validity in the hypothesis presented above with regard to speeds of convective transfer. If this rate of transfer between the mixed layer and the transition zone is greater than the natural sinking speed, there will be an increase in the concentration of particulate matter in the upper part of the thermocline. This kind of distribution is well known in the case of phytoplank-

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GORDON A. RILEY

ton distribution, but sampling for non-living organic matter has not been conducted a t sufficiently close intervals to reveal the fine detail of vertical distribution. An earlier discussion of micro-distribution cited the work of Paramonov et al. (1966) which demonstrated marked vertical variations in transparency. These probably were associated with thermal discontinuities. The decrease in organic carbon that has been noted in the transition zone presumably is merely an indication of a general trend, and the gradient is by no means a smooth one. I n the surface layer aggregates constitute the bulk of the material. Below the transition zone small particles and flakes are predominant. This may be due to selective consumption of large particles in the transition zone by animals, or it may be simply a matter of physical sorting. Large particles with a rapid sinking rate will spread downward through the layer more quickly than small ones, and their concentration per unit volume will be proportionately reduced. The rate of decrease of organic matter in the transition zone cannot be determined with any degree of generality, for few areas have been sampled in sufficient detail to provide a representative spectrum of vertical profiles. A sample analysis will be presented here, based on data obtained by Riley et al. (1965) in the Sargasso Sea. The results will be useful in a later discussion of biological problems in this area, but it serves no other function except as an exposition of method. I n this area the mean concentration of particulate organic carbon was about 100pg/litre a t 100 m and 30pgllitre a t a depth of 900m. These figures can be regarded as representing the upper and lower limits of the transition zone. A first approximation t o consumption is simply the decrease in organic matter between the top and bottom of the transition zone. This can be converted to a rate of consumption if the residence time is known. Experiments suggest that the mean sinking rate is of the order of 0.25 m/day, allowing for a decrease in sinking rate with increasing viscosity, and this leads to an estimate of 0-022 pg C.litre - 1.day- 1. This kind of computation is applicable t o a static situation ; however, in the present case we can assume that organic matter is imported into the top of the transition zone faster than it is exported from the bottom, so that total consumption is greater than is indicated by mere decrease in concentration. If the concentration exists in a steady state, the mean rate of decrease can be determined simply as the difference between the two vertical fluxes. The flux F , directed positively downward, is given as AC F = d C - A - AX

85

PARTICULATE ORGANIC MATTER IN SEA WATEK

where S is the mean sinking rate of organic carbon C, A is the coefficient of vertical eddy diffusivity, and AC/Az is the mean vertical gradient in organic carbon in the depth range in question. The mean sinking rate S is assumed to be 1 m/day at the top of the layer. This is approximately the observed value in experiments with inshore water and surface Slope Water. A sinking rate of 0.24 is postulated for the bottom of the layer. This again is obtained from experiments on Slope Water, using mid-depth values and correcting for a change in viscosity. These obviously are crude estimates. No experimental observations are available for the area in question, and there is no good way to make allowance for the possibility that the rate of delivery of large particles may be enhanced by convective movement or that there may be a significant quantity of small particles with a negligible sinking rate. Eddy coefficients are generally small in the thermocline. A value of 1 cm2/sec is postulated for the upper part of the zone and 0.5 for the lower boundary. The mean decrease in carbon content between 100 and 200 m is about 25 pg C/litre, and between 500 and 900 m it is about 20 pg C/litre. These values are used to compute eddy flux. The calculation is carried out in the c.g.s. system, but results are translated into terms of daily flux in Table X. TABLEX. COMPUTATIONOF VERTICAL FLUXOF CARBONIN THE TRANSITION ZONE (WG C . C M - ~ . D A -l) Y AND CARBONLoss WITHIN THE LAYER( P G C.LITRE DAY - l ) . FORFURTHER DETAILS SEE TEXT

S( W a y ) A(cm2/sec)

cs

Eddy Flux Total Flux (F) Carbon loss

100 rn

900 rn

1 1 10 0.9 10.9

0.25 0.5 0.75 0.2 0.95 0.12

The total flux F in the table is in terms of pg C passing downward through a horizontal area of 1 cm2 in a day. It will be noted here that the eddy flux is relatively insignificant and might have been omitted ; however, it could be important in areas where gradients in organic carbon are steeper. The difference in flux between the upper and lower limits of the zone represents total carbon loss. This difference, divided by the volume of water in which it occurs, gives an estimate of carbon loss of 0.12 pg C.litre-l.day-l, which is shown as the last entry in the A.H.B.-S

4

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GORDON A . RILEY

table. This is about five times the earlier estimate, which considered only the observed decrease with depth. These results will be discussed later in relation t o biological problems in the transition zone. The values that have been obtained suffer from all of the qualifications that have been made about the difficulties of relating experimental determinations of sinking rates to the mean rate of sinking of total particulate carbon. Examination of biological processes within this layer provides an independent method of calculating carbon consumption which will be useful for comparative purposes. (c) The deep ocean. Data presented in earlier sections of this report indicate that particulate matter in the deep ocean varies regionally in a manner that is more or less in accord with the productivity of the surface layer. Thus it would appear that the residence time of particulate organic matter in the deep ocean is short enough for the influence of surface conditions at the point of formation to be more important than later horizontal movements of deep water masses. However, the latter can be important occasionally, as indicated by the fact that Dal Pont and Newel1 (1963) found maxima and minima associated with particular water mass characteristics of the south Pacific Ocean. More commonly vertical variations appear to be of an essentially random nature, although admittedly the sampling intervals have seldom been close enough to delineate vertical gradients realistically. The residence time of much of this material is fairly long, but McGill (1964) has reported a similar pattern of distribution of organic phosphorus, most of which was present in the dissolved fraction and probably had an even longer residence time. Menzel and Ryther (1968b) have reported similar regional variations in dissolved organic carbon. The reason for the slow rate of horizontal dispersal in deep water lies in the fact that the major transport systems in the deep ocean are localized, to a degree that was not realized until recent years, and further mixture of the main mass of deep water is a slow diffusion process. This was clearly demonstrated in an analysis by Wiist (1955) of currents in the South Atlantic Ocean based on Meteor data, in which major north-south currents were concentrated along the eastern slope of South America. Stommel and Arons (1960) applied the theory of westward intensification of ocean currents to the deep ocean system, and their conclusions indicate that this kind of localization is to be expected in all of the major ocean basins. Even non-conservative properties of an inorganic nature are somewhat localized in their distribution despite the fact that this distribution is developed during the entire residence time of the water itself. Riley (1951) examined oxygen distribution in the Atlantic Ocean, based

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mainly on expedition data of the " Discovery '), " Dana )', " Meteor ", and " Atlantis ", and found that the oxygen minimum layer is quite complicated in its structure, being compounded of several loci of marked oxygen depletion which are imperfectly diffused and show evidence of regional variation of the same kind that has been noted in connection with particulate organic matter and organic phosphorus. Oxygen minima are most strongly developed off the West African coast a t the roots of the North and South Equatorial Currents. They are centred at a depth of about 400 m on ut surfaces 26.9-27.0. There is also a secondary minimum a t a depth of only 100m in the Guinea Current according to " Dana " data. Another locus of low oxygen concentration is found in the Sub-Antarctic a t about ut 27.5. This tends t o spread northward but remains separate from the tropical oxygen minimum above, so that stations between 25" and 40'5 Lat. sometimes show double minima a t about 400 and 1 800 m. I n the tropical North Atlantic the oxygen minima spread westward across the ocean and are centred a t a ut surface of 27-0-27.1, indicating that some local consumption occurs along the way a t a slightly deeper level. The great mass of northern water that drifts down to the central North Atlantic has a weak and diffuse oxygen minimum layer, and individual stations have minimum oxygen values at various ut surfaces from 27.3-27.7. I n the vicinity of the Mediterranean outflow the minimum is also weak and is centred around the 27.5 surface. These waters of various origins meet and mix in the western North Atlantic, where current systems are relatively strong. Because two of the sources have oxygen minima that are vertically diffuse, no secondary minima are formed. Instead there is coalescence into a single well defined minimum a t ut surface 27.2-27.3. To the southward it grades upward toward the tropical minimum, while to the east and north it grades toward denser water. The fact that the oxygen minimum layers occur on different density surfaces in different parts of the ocean is indicative of a more or less local origin. More recently Menzel and Ryther (1968a) have suggested that this layer is derived from the upwelling area of the tropical eastern Atlantic and spreads from there by isentropic mixing. However, this is clearly not the case except in a very limited area, and even in their short north-south profile (ca 8-36"s) in the South Atlantic, which was the main subject of their analysis, the northward intrusion of the deep Antarctic oxygen minimum layer can be seen a t the southern end. In deep ocean waters vertical turbulence is believed to be slightly stronger than in the mid-depth region of maximum stability. This

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tends t o facilitate the maintenance of a fairly uniform vertical distribution and to accentuate regional differences in particulate organic matter and other properties. However, evidence has been presented of the existence of thermal discontinuities in the deep ocean. These could lead to the development of layers of particle rich water, although the somewhat inadequate data now available suggest that the distribution is only slightly non-random (Gordon, 1970b). Vertical turbulence can have some effect in dispersing any local concentrations that develop, but it cannot produce a systematic downward flux, for the mean vertical gradient of particulate carbon is essentially nil in most areas that have been examined. Thus particulate matter sinks passively from the main thermocline to the ocean floor and seems to be influenced very little by any of the physical oceanographic processes of the deep ocean except in a few local situations that have been described. 2. Biological relationships Having brought together available information on physical movements of particulate organic matter in the sea, we come now to questions of the character and magnitude of the biological processes which can be expected to affect the concentration and distribution of the non-living matter. This involves a consideration of the degree of balance between production and consumption at various depths in the sea. Theoretically, of course, total carbon fixation by photosynthetic plants is expected t.0 equal total respiratory utilization of ca,rbon by animals and heterotrophic plants, neglecting the residue that remains unoxidized in sediments or in the water column. This residue is large in its total accumulation, but it has accrued during a long period of time and is believed to be a small percentage of total carbon production. For practical purposes we can assume a balance over a period of a year or several years. During shorter periods there are seasonal imbalances in the surface layer, so that the discussion must be limited to areas where the information is available on mean annual production and consumption. This balance between total production and consumption is of course realized only by considering the total vertical column from surface to bottom. At any particular depth there is an imbalance. All photosynthesis occurs in a thin surface stratum which seldom exceeds 125 m in depth and generally is less. Much of the consumption also occurs here, and the remainder of the surface production, once it has been delivered to deep water by one means or another, provides minimal sustenance for the sparse deep water fauna and flora.

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Various estimates have been made of production and consumption in near-surface waters, and by difference we can estimate the amount of food available for deep water organisms, allowing the assumption of total balance. Some attempts have also been made to evaluate deep water consumption rates. These are of a lower order of validity, but they deserve comparison with other items in the overall balance sheet. Riley et al. (1965) developed this kind of balance sheet in connection with studies of non-living particulate matter in the Sargasso Sea, with particular emphasis on respiratory rates and food requirements of the deepwater population. Four essentially independent analyses were presented : ( 1 ) Menzel and Ryther (1960) measured C14 uptake by phytoplankton in the surface layer off Bermuda and found that the mean daily production, averaged over a period of a year, was 200 mg C.m-2.dayThe same authors (1961) made quantitative collections of zooplankton to a depth of 500 m, obtaining an average value of 1.08 g dry weight/m2. The mean respiratory requirement was determined experimentally and averaged 0.12 g C/g dry wt of zooplankton. Thus the total requirement of zooplankton in the upper 500 m was estimated t o be 130 mg C.m-2. day-l. This leaves an excess of 70 mg C/day which might be available to deep water organisms ; however, there are two ambiguities : (a) no allowance is made for bacterial metabolism in the upper water, and (b) part of the photosynthetic product may be liberated to the water in dissolved form and hence is not measured as production by the C14 method. Thus there is some doubt as to whether the amount of food materials available to populations in deep water might be more or less than 70 mg. (2) Riley (1957) used observed vertical gradients of oxygen and computed eddy coefficients t o estimate net organic production in the upper 300 m of the Sargasso Sea. This method theoretically measures the difference between oxygen production by phytoplankton and oxygen consumption by all components of the population. Hence it is free of some of the difficulties mentioned in item ( l ) , but the method of computation is indirect and is subject t o considerable error. The results indicated that net oxygen production between the surface and the compensation depth was equivalent, on a mean annual basis, to 134 mg C.m - 2.day- l. The net decrease from the compensation depth to 300 m was 81 mg. The difference of 53 mg C.m-2.day-1 provides an estimate of potential deep water consumption. (3) Riley (1951) used similar but somewhat more complicated methods t o compute deep water oxygen consumption. This was a generalized calculation for the central Atlantic basic and might be an

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over-estimate for the relatively poor waters of the Sargasso Sea, but in view of other possible errors this is a quibble. Results indicated that total oxygen consumption between 300 m and the bottom averaged 48 mg C.m-2.day-1, a figure in good agreement with the one obtained in item (2). Most of this utilization occurred in the mid-depth region. The estimated consumption between 1 000 m and the bottom was only about 8 mg C/day. (4) Riley (1951) compiled data on deep water zooplankton from Leavitt (1938) and estimated what the respiratory requirements might be if they were similar to experimental results obtained with surface water forms a t low temperatures and surface pressure. I n the absence of any solid information about respiratory rates of deep water animals under normal environmental conditions, this is the best that can be done, and the results seemed more or less realistic. The total for the depth range between 300 m and the bottom was 38 mg C.m-2.day-1. An additional 4 mg C/day were estimated as the requirements for benthic bacteria and animals. Riley et al. (1965) pointed out that although each calculation has obvious deficiencies or possibilities of error, the four independent methods yield a range of only 42-70 mg C/day, suggesting that this is considerably better than an order of magnitude estimate for deep water consumption. An obvious deficiency in these estimates is the failure t o specify the respiratory needs of bacteria and other small heterotrophs. Their inclusion would tend t o lower the estimate in item ( I ) , which is the highest one, and increase item (4),the lowest one. There was no attempt to do this in the paper cited, because the results appeared t o be adequate for the purpose that was in mind at that time, namely to attempt to evaluate the residence time of particulate organic matter in deep water. However, further examination of the biological system seems desirable a t the present time. Some of the published views represent a piecemeal approach to the problem. Menzel and Ryther (1961) concluded that zooplankton in the Sargasso Sea were capable of consuming virtually all of the phytoplankton production, whereas Parsons and Strickland (1962) suggested equal capabilities for small heterotrophs. A compromise must be chosen between these extremes, for total phytoplankton production must be shared between the two kinds of populations. Moreover, in the period since Riley et a,Z. (1965) published their analysis several papers have appeared containing data which are in marked disagreement with values used in the earlier analysis. The whole subject needs to be reopened t o further discussion. Thus the

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problem of heterotrophy will first be reviewed, and then the problem of the general balance between production and consumption will be reconsidered. (a) Heterotrophy. Until recently most estimates of the numbers of bacteria in deep ocean waters were based on plate counts, which greatly underestimate the total population. Sorokin (1964) examined some stations in the central Pacific by direct counting methods, and a t a depth of 2 000 m his numbers ranged from 0.8 t o 1.03 x l o 6 bacteria per litre. Other investigators have obtained more or less similar results. Water samples from the deep ocean commonly contain a few algae. Most oceanographers have supposed that they represent merely a remnant that has sunk into deep water and is doomed to quick death. However, Wood (1956) demonstrated viability of diatoms taken from ocean depths. More recently Fournier (1966) and Hamilton et al. (1968) have found that large concentrations of small cells (2-4 p ) of somewhat uncertain systematic position are regular inhabitants of ocean deeps. Bernard (1967) reported large numbers of coccolithophores in Mediterranean waters, but Fournier ( 1 968) has cast serious doubt on the validity of these observations. An earlier section mentioned a paper by Holm-Hansen and Booth (1966) who developed a method for assessing relative quantities of living and non-living organic matter by means of ATP analyses. They listed data for fractional partition of this kind a t a station located approximately a t 33"N, 119"W. Cellular organic carbon at depths of 10 and 30 m was respectively 33.6 and 95 pgllitre, constituting 42 and 79%, respectively, of total particulate carbon. At 103 m corresponding figures were 4.6 pg C/litre and 14%. With minor exceptions deep water samples fell within fairly narrow limits and averaged 1.7 pg C/litre and 3.7% of total carbon. Hamilton and Holm-Hansen (1967) extended the examination of the ATP content of marine bacteria, and Hamilton et al. (1968) published additional data from several stations in tropical and subtropical waters of the Pacific Ocean. There were clear indications of a middepth maximum in ATP and a decrease in deep water. The amount of carbon in living organisms, as indicated by the usual ATP conversion factor, was of the order of 1-2% of total particulate carbon in waters below 1000 m. These authors apparently believed that the small coloured cells were quantitatively more important than bacteria. They also mentioned the fact that small green cells from deep water collections had been established in autotrophic culture, but they stated that " the nature of the coloured spheres seen on the membrane filters

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remains an enigma and more work is needed to establish their identity and assess their importance, if any, in the bathypelagic food web ”. Holm-Hansen ( I 968) found a distinct decrease in ATP with depth in the deep ocean, suggesting a corresponding decrease in the biomass of heterotrophs. Possibly it is too early to generalize on these results, but there are indications that although total organic carbon does not decrease systematically with depth, its capabilities for the support of living organisms may decline as it sinks toward the bottom. Nevertheless, one must conclude from this brief summary of recent literature that the quantity of heterotrophs in deep water is much larger than has been supposed in the past. Most of these organisms have not been identified, and there is still little information available on the kinds of substrates that they depend upon. Some information is, however, now being obtained about possible rates of uptake of organic substances and minimum concentrations required to support growth. Parsons and Strickland (1962b) undertook an investigation of heterotrophic processes by measuring the uptake of C14 labelled glucose and acetate, Sophisticated biochemical and microbiological concepts were involved, which will not be elaborated here. It suffices to say that they established beyond reasonable doubt that natural substrates of 10-7 moles or less of glucose or acetate were adequate for heterotrophic growth. Their experiments were performed with natural sea water taken off the coast of British Columbia (49”12’N, 123”58’W). Most of the samples were taken from depths of 5-35 m, and the rate of uptake varied from 0.004-0-3 pg C/litre in an hour, averaging 0.015. Two samples from a depth of 175 m had values of 0.003 and 0.007. I n discussing their results the authors concluded: “ Values for a Michaelis-Menton type constant of less than 10- M have been reported but are uncommon. Yet it should be reasoned that marine microorganisms must have evolved so as to utilize substrates a t the concentrations occurring in nature, with possibly the mediation of an adsorptive concentration onto particulate matter. More work with a wider variety of samples and substrates is required to decide . . . but the method looks promising.” Further work along these lines was reported by Vaccaro and Jannasch (1966). They used both pure cultures and natural populations in studies of glucose assimilation and obtained results similar to the earlier ones in that natural substrate levels appeared t o be of the order of 10-7 M or even as little as l o - * . They were also able t o estimate the in situ rate of substrate removal. At five stations in the tropical North Atlantic, samples collected in the upper 50 m gave values

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of 0.01-0.18 pg C/litre in an hour, and four samples from 100 m ranged from 0.001-0.062 pg, with three of the four toward the lower end of the range. These results were on the whole somewhat higher than the ones obtained by Parsons and Strickland, and clearly more data are needed in order to give us a clear idea of natural ranges of variations and their reasons. Also these tracer methods, though elegant and provocative, do not yet provide a generalized picture of heterotrophic absorption of the complex array of carbon sources existing in sea water. Parsons and Strickland found that the rates of uptake of glucose and acetate were quite different, and a few experimental results cannot be extrapolated to generalities. However, if as much as l-lOyo of the total dissolved organic matter is biologically usable and is as readily available as glucose, this would provide a substrate concentration of 10-8-10- M. Thus it is not entirely unreasonable to suppose that the dissolved fraction might supply most or all of the necessary substrates for heterotrophs, and also, again quoting Parsons and Strickland, " the mediation of an adsorptive concentration onto particulate matter '' is a distinct possibility, particularly since that is where most of the bacteria are living. Hamilton et al. (1968) dealt with some of these problems and quoted unpublished references t o experiments on heterotrophic uptake by deep water organisms. One of these experiments was credited to J. D. H. Strickland (ref. Antia et al., 1962) who showed that the rate of uptake from 500 pgllitre of radiocarbon-labelled glucose, acetate, succinate and citrate a t i n situ temperatures was less than 0.001 pg C/litre/hr a t depths greater than 1 0 0 0 m. Similar results were also obtained by Hamilton, using 20 pg/litre of radiocarbon-labelled glucose, proline and glycine. These experiments were mentioned in passing without further details and presumably will be described more extensively in a later publication. Hamilton et al. had reported that the biomass of deep water heterotrophs in terms of organic carbon was of the order of 0.3-0.5 pgllitre. Thus if the uptake is less than 0.001 pg C/hr, the daily consumption will be less than 10% of the weight of the organisms. This is a remarkably low rate of turnover for small organisms ; however, in an environment that is obviously marginal for the support of heterotrophs one would expect a low metabolic rate, and these results may be realistic. Some algae are much less eficient in heterotrophic uptake than bacteria. For example Wright and Hobbie (1965) found that some freshwater algae they were studying required substrate concentrations several orders of magnitude larger than those required by bacteria.

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They concluded that the algae were lacking in active transport systems and were dependent upon simple diffusion for heterotrophic growth. However, Hellebust (1968) reported that some species are capable of heterotrophic uptake a t substrate concentrations comparable to the minimum levels required by bacteria, and there now seems to be little doubt that some algae at least have effective transport systems. Relative biomasses of the different kinds of cells, as reported by Hamilton et al. (1968), might even suggest that deep sea algae are more effective than bacteria in their competition for available substrates, although admittedly there is still considerable question as to what proportion of the small coloured cells reported by these authors are actually living algae. (b) Variations in production and consumption with depth. Returning t o the problem of allocating the available production in the marine environment to the various kinds of consumers, the situation in the Sargasso Sea will be examined once more, for this area provides more complete data than any other place in the open ocean. This is largely a matter of reworking and amplifying the analyses described in items (1) to (4)of the introductory section. Unfortunately, however, the problem seems more difficult now than it did when Riley et al. ( I 965) published the original a,nalyses, and the results will be less clear cut. Item (1)was an estimate of net phytoplankton production obtained by Menzel and Ryther (1960). Their average was 200 mg Cam-2.day-1 on a mean annual basis. I n recent years the C14 method has been criticized because of the difficulty of proper correction for self absorption on filters, and the International C14 Laboratory a t Charlottenlund Slot has recommended that all of the older values should be increased 45% t o bring them more nearly in line with modern information, Whether this correction is really adequate remains to be seen. Goldman (1968) has recommended burning the material and determining absolute activity by gas counting methods. He compared the two methods, using cultures of various algae. Results varied considerably, but in general the values obtained by absolute counts were about three times as high as those analyzed by the traditional method. The fact that there were systematic differences among different species of algae raised some doubts as to whether the results obtained with natural populations might also vary in a rather unpredictable way depending upon the species composition of the population. This is where the situation stands at the moment. It remains to be seen whether the accumulated C14 data can be salvaged by application of an arbitrary correction factor or will have to be discarded. I n

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the present case the correction factor recommended by the C14 Laboratory is applied provisionally t o the Sargasso Sea data, bringing the mean value to 290 mg C.m-2.day-1. I n the light of Goldman’s recent results, the correct figure might be as high as 600 mg C, but the writer is inclined to doubt this. Even the old light and dark bottle oxygen techniques, which have been criticized for giving results that are too high, indicated that the general range of net production in oceanic waters is of the order of 400-1 000 mg C.m-2.day-l (Riley, 1944), and the Sargasso Sea should be near the minimum limit of the range. The total estimate for usable organic production by phytoplankton also should include extracellular metabolites, which would not be included in measurements of productivity by routine C14 tests. Hellebust (1965) reported experimental results on the production of external metabolites by a large number of algal species. The list included Coccolithus huxleyi, an important species in the Sargasso Sea. At nominal light intensities of 3-10 x lo3 lux, 1.3-4*4y0 of the photoassimilated carbon was released, and the value increased to 1 7 % in full sunlight. Dinoflagellates ranged from 4.4-1070. Values of up to 25% were obtained for some of the diatoms, but these algae are not important constituents in the Sargasso Sea except in winter and spring. From these data one might suppose that a reasonable estimate for extracellular release might be of the order of 10% of photoassimilated carbon. However, (2.1. Choi of this laboratory (personal communication) has obtained considerably higher values in experiments with natural populations. These were in situ C14 experiments performed a t a series of depths a t stations between the Newfoundland-Nova Scotia shelf and the Gulf Stream, followed by measurements of organic C14 in the particulate matter and in the filtrate. At the three southernmost stations filterable organic C14 averaged 25% of the C14 incorporated in particulate matter. Even higher values were common a t the more northerly stations. I n short, extracellular release in the natural environment can be 1 0 - 3 0 ~ 0 or more, and the total organic productivity a t the Sargasso Sea station under present consideration is estimated to be 320-380 mg C.m-2.day-1, with some possibility that the true value might be more. The next step is t o attempt to equate organic production in the surface layer with consumption in the water column as a whole. The two physical oceanographic computations in items ( 2 ) and (3) gave closely concordant values of 48-53 mg C.m-2.day-1 for consumption below 300 m, and the others varied around these values. As a guide to the remainder of the analysis, it will be assumed that these

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numbers are approximately correct, and for convenience a value of 50 mg will be chosen arbitrarily, although the later discussion will indicate that this may be an underestimate. An additional simplification arises from the fact that the analyses were not quite comparable as to depth ranges that were selected. Zooplankton data by Menzel and Ryther (1962) were based on tows made from 500 m t o the surface, so that their calculation of zooplankton consumption was lumped into a single estimate for this depth range. I n item (4),deep water estimates of zooplankton Consumption were calculated from 300 m to the bottom, of which about 20 mg can be assigned t o the depth range of 300-500 m. To avoid counting part of the zooplankton twice, this number will be subtracted from the estimate based on the data of Menzel and Ryther. The estimates for consumption by zooplankton will then be 110 mg C in the upper 300 m, and the remainder of vertical column will remain the same. Data for estimating heterotrophic consumption are scanty, as was evident in the last section. Observations by Vaccaro and Jannasch (1966) yield the following averages: 1-10 m, 0.045 pg C.litre-l.hr-l; 35-50 m, 0.061 ; 100 m, 0.004 (excepting one anomalously high value of 0.062). Further, assuming that consumption from 100-300 m is about 0.001, their lowest value for 100 m, the daily carbon requirement for the upper 300 m would be 120 mg C/m2. A similar treatment of the observations of Parsons and Strickland (1962) gives a value of 45 mg C/day. The agreement is not particularly close, and of course neither estimate is directly applicable to the area in question. There is the further question of whether experimental results of this type are indicative of the natural rate of absorption of the more complicated array of substances available in nature. Nevertheless, for what it may be worth, the combined estimate for consumption by zooplankton and heterotrophs in the upper 300 m plus the assumed deep water value of 50 mg comes to 205-280 mg C, which is about two-thirds to threequarters of the postulated surface production. Direct measurements of consumption by heterotrophs would be desirable, but there are grave dangers of introducing experimental artifacts into such determinations. Ordinary dark bottle incubation is useless because of the well known problem of extensive bacterial growth in bottles of stored sea water. Pomeroy and Johannes (1968) have attempted to get around this problem by developing a method for gentle filtration of large volumes of sea water, permitting short term measurements of oxygen consumption in the concentrate. Their paper contains an interesting descriptive account of the collections, which has been mentioned earlier, in addition t o the experimental

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measurements. The latter were obtained from collections off Peru and in subtropical latitudes of the western North Atlantic, an area well to the west of the Bermuda station that is under present consideration and which probably is somewhat richer biologically. The results that they obtained were considerably higher than the present writer’s estimates of in s i t u oxygen consumption in the central Atlantic basin as determined by physical oceanographic calculations, and the question is not fully resolved as to whether this represents real regional differences or is due t o errors in one method or the other. Pomeroy and Johannes determined changes in rate of oxygen consumption with varying concentrations of their material and found that the curves extrapolated to the origin. Thus there were no obvious indications of density dependence in the results. Even their minimum values are equivalent to a carbon consumption of about 300 mg.m-2.day-l in the upper 300 m and 500-600 mg in the whole of the surface and mid-depth column. These figures do not fit comfortably into the carbon balance sheet for the Sargasso Sea, but as indicated earlier, they were dealing with more productive regions. There is another way to look at the situation which might be more informative. Their measurements in the Peru offing were accompanied by experiments on C14 uptake and they obtained a mean P / R ratio of 1 - 5 : 1 , where P is uncorrected C14 uptake, and R is total carbon consumption in the upper 500 m as determined by measurements of oxygen consumption. Their experiments in the Atlantic did not include C14 measurements, but they reported that there was about a 1 : l ratio between earlier C14 estimates in the area and their determinations of respiratory requirements. If the same sort of ratio is applicable to the Bermuda region, the carbon consumption by ultraplankton in the upper 500 m would be about 133-200 mg.m-2.day-1. Total utilization in the water column would then be 290-360 mg, a range that is essentially in agreement with production figures, although the indirect methods used t o derive it leave much to be desired. Below 300 m there are three major oceanographic regimes, biologically speaking. There is a mid-depth zone which includes the oxygen minimum layer and a mid-depth assemblage of animals which comes up close to the surface a t night, and migrates downward some hundreds of metres to a daytime position that more or less corresponds with the depth of the oxygen minimum layer. Below the main thermocline the species composition changes and the total quantity of animals is much reduced. The deep water animal population will be referred t o here simply as bathypelagic animals

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although this is an over-simplification, for a detailed study of populations requires subdivision into several depth zones. Finally there is an assemblage of benthic and epibenthic animals and an associated bacterial flora. The benthic population of deep ocean waters is not large, but it is probably about equal to the total quantity in the sparsely inhabited bathypelagic zone. The mid-depth zone properly includes the whole thermocline region. Drawing an arbitrary dividing line at 300 m as was done above is an artificiality imposed by the nature of the analyses. Physical oceanographic analyses were predicated on assumptions of a steady state and had to be limited to waters in which there were no seasonal changes in properties, and analyses of the upper 300 m cannot be partitioned with enough precision to fill in the gaps in a very satisfactory way. There is of course the further difficulty that the top of the thermocline varies seasonally from 50 m or less to more than 150. However, with some slight over-simplification a range of estimates of biological consumption can be obtained for the depth range of 100-900 m, which constitutes the major part of the mid-depth zone in this area. This depth range will be examined briefly, and a more detailed balance sheet will be drawn up later for the whole of the vertical column below 300 m. A generalized estimate for oxygen consumption within this layer can be derived from physical oceanographic analyses. The net decrease in oxygen from the compensation depth to 300 m (item 2 above) plus the decrease from 300-900 m (the same data used in compiling item 3) are equivalent t o a total carbon consumption of 119 mg.m-2.day-1. For reasons given below this figure may be too small. A further estimate based upon respiratory rates requires an assumption about partitioning of zooplankton respiration within the upper 300 m. The total utilization of 110 mg C/day as described above is assumed to be uniform with respect t o depth on the grounds that the population is subject t o diurnal migration, so that 73 mg can be allotted to the 100-300 m depth range. To this is added 28 mg for animalrespiration bet,ween 300 and 900 m and an allotment for heterotrophs and associated ultraplankton which could be as much as 70-100 mg if the vertical variations in this segment of the population are comparable .to those described by Pomeroy and Johannes (1968). Vertical flux into this layer (Table X, p. 85) was estimated to be 109 mg C.m- 2.day- l, and the flux into deep water below was 9.5 mg ; thus the loss within the layer was estimated to be about 100 mg. This again is a crude and possibly minimal estimate. From the earlier discussion of this problem it will be apparent that as in the case of phytoplankton, the larger particles may be lost from the surface layer a t a

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rate several times that of their apparent sinking rate, although there is some question as to what proportion of total carbon will be so affected. So again there is a considerable range in possible estimates, from about 109 to 200 mg C.m-2.day-1 in the 300-900 m depth range. The most likely value is toward the upper end of this range, and a major proportion of the consumption is believed t o occur between 100 and 300 m. With regard to deep water below the transition zone, physical oceanographic computation of oxygen consumption (Riley, 195 1 ) indicated that carbon utilization in the bathypelagic zone and on the bottom totalled 9.4 mg C/m2. A somewhat higher value of 14-16 mg is indicated for metabolic consumption by bacteria and animals in the bathypelagic zone and on the bottom. Again there is some variation in results, but this amount of agreement is reassuring, because the earlier estimate based on oxygen consumption was drastically over-simplified. The problem is simply that oxygen consumption in deep water is so slight that extensive averaging is necessary in order to get a body of data that will yield consistent results. I n this case data were combined into a single north-south profile of the Atlantic Ocean. Within this profile the deep water showed an apparent oxygen utilization, as defined by Redfield (1942), which averaged about 2 ml/litre. If this were due entirely to biological utilization, the rate of consumption could be calculated in terms of the age of the sea water. The age probably falls within the general range of 250-750 years. Calculated carbon utilization in the whole deepwater column would be about 12-33 mg C.m-2.day- l . These are maximum values because part of the loss in oxygen is due to transfer upward toward the oxygen minimum. The analysis utilized estimates of vertical and horizontal eddy coefficients derived from the salinity distribution to correct for physical dissipation of oxygen, and the residual value was the estimate given above. It will be apparent from the method of calculation that this is a generalized statistic, and its application to any particular area is questionable. However, it is the only information of its kind available. This analysis possibly should be reworked, incorporating new data and using a finer network of stations. The broad grid that was used failed to delineate narrow, deep ocean currents, which indeed were not known to exist a t that time, so that total advective circulation was underestimated. Sverdrup et al. (1942) and Riley (1951) computed the average age of the deep water as about 1000 years, which now appears to be an over-estimate, and in both cases this was due to the assumption that the advective pattern was broader and more diffuse.

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Correction of the figures for advection would require adjustments in coefficients of eddy diffusivity in order t o maintain a conservative balance of salt, and this would lead in turn to alterations in estimates of biological rates of change. Possibly the alterations would be quite local, in association with major deep water currents, or they might be more general. Intuitive methods are not equal to the problem, but conceivably all of the mid-depth and deep water biological rates of change that have been listed here should be doubled, more or less. I n deep water the values are so small that no conclusions would be seriously altered. I n the mid-depth region from 100 to 900 m it makes some difference as to whether consumption is one-third or two-thirds of the total surface production. This discussion makes it quite apparent that the writer does not subscribe to the viewpoint expressed by Menzel and Ryther (1968a), who regarded the oxygen distribution in lower mid-depths and deep water as being essentially conservative. Their hypothesis seems to be that oxygen deficits develop in the upper reaches of the thermocline and are translated horizontally and to greater depths by isentropic mixing, and apparently they regarded the whole of the oxygen minimum layer of the Atlantic Ocean as having been derived from Equatorial upwelling areas off Africa. Reasons why this conclusion is unacceptable have been presented earlier. Their conclusion that oxygen consumption in deeper water is conservative requires further discussion. They analyzed the distribution of oxygen along the axis of the Antarctic Intermediate water in the South Atlantic, a water mass lying just above the upper boundary of the deep water that is under present consideration. In their north-south profile, which extended from approximately 10’ to 36’5, there was a decrease in oxygen of about 2.65 ml/litre from south to north. They used the so-called core ” method to analyze oxygen at intermediate points. This method assumes that mixing takes place only along the axis, so that the salinity at any intermediate point can be determined as percentage mixtures of water at the two ends. These percentages are then applied to the two end values for oxygen to determine intermediate concentrations. Menzel and Ryther found that these more or less agreed with observed values and concluded that oxygen is a conservative property. Earlier Riley (1951) had obtained a n estimate for annual oxygen consumption of about 0.01 ml/litre in this water mass, a modest amount although considerably larger than the deep water average quoted above. However, even this small rate of change could lead t o 66

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a considerable oxygen deficit during the slow northward movement of the water. The difficulty with the core method is that it is incapable of detecting this biological deficit except under certain special circumstances. The observed oxygen concentrations a t the two ends of the profile are arbitrarily chosen to compute intermediate values. These concentrations show an apparent oxygen utilization, but whether it has taken place locally or a t the point of origin or how rapidly it has occurred are unknown. Menzel and Ryther begin with values that do not deny their hypothesis but do not support it either. And if local utilization has occurred, the use of arbitrary reference values will hide any utilization that has taken place a t intermediate points, provided this utilization proceeds a t a reasonably constant rate with respect to time and mixing rates along the path of flow. Only pronounced anomalies and non-linearities can be detected. There is, unfortunately, no solution to this problem except the treatment developed by Sverdrup et al. (1942), requiring evaluation of advection and diffusivity in terms of conservative properties and application t o non-conservative distributions to derive a residual rate of biological change. Ideally this is done as a three-dimensional problem, although a two-dimensional profile can serve the purpose. This type of analysis, developed by Riley (1952), is not a very dependable solution, because there are so many complexities and uncertainties in the application. However, vertical and horizontal diffusion are both important enough so that one-dimensional analysis of deep water is seldom effective, even aside from pitfalls of the kind described. Returning to a consideration of biological problems in waters below 300 m, total consumption was postulated t o be of the order of 50 mg C.m-2.day-1, and earlier estimates indicated that 38 mg are consumed by pelagic animals and 4 mg on the bottom. However, no real confidence can be placed in these figures. They are largely derived by extrapolation of experiments on surface water forms. Little is known about effects of pressure and nutritional state on the respiratory rates of these organisms. Some speculation is necessary in order to try t o fit the pieces of the puzzle together. One can suppose that animal respiration might consume as much as 38 mg C/day, or perhaps it might be only half that much. This would leave 8-27 mg/day for heterotrophs. Converting to more familiar terms, this is 1-4 x 10-4pgC.litre-l.hr-l as an average for the deep water mass as a whole, a range that is one order of magnitude less than observed uptake a t depths of 100-175 m, two orders less than in near-surface waters, and essentially similar to the

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value of <0.001 quoted by Hamilton et al. (1968) for deep water. The daily uptake would be less than 10% of the carbon content of the organisms (judging the latter by ATP analyses). This consumption is small compared with metabolic rates that are commonly reported for bacteria, but it is in accord with the low levels of bacterial activity associated with long term laboratory experiments, as well as with the experiments on heterotrophic utilization by natural populations. Presumably both particulate and dissolved organic matter provide carbon sources for these heterotrophs, and the latter is the larger potential supply, although not all of it is likely to be assimilable. Nevertheless, these rates have some bearing on the question of the residence time of dissolved organic matter in the deep sea. Analyses of dissolved organic matter by wet oxidation methods have indicated a carbon content of 0.5 mg/litre more or less. Its distribution in the North Atlantic (Duursma, 1960) shows some slight indications of a relation with oxygen distribution ; for example, there is a reduction in the region of the oxygen minimum layer. I n view of the general similarity but less extreme variation, Riley et al. (1965) suggested that the mean residence time is fairly long but not as long as that of the water itself. I n retrospect this conclusion seems too simple, and it should be modified. Heterotrophic carbon utilization is directly related with oxygen consumption, but this is not true of animal metabolism, which is more likely t o increase the dissolved organic content than to decrease it. Some investigators have felt that mid-depth concentrations of animals are very largely responsible for the development of the oxygen minimum layer, and it is perhaps significant in this respect that the decrease in dissolved organic matter is slight or lacking. For example, Menzel and Ryther (1968a) found no mid-depth reduction in dissolved organic carbon in the tropical South Atlantic where animal populations are known t o be unusually large (Jespersen, 1935). As to the average age of the dissolved organic matter, the length pg C.litreof time required to use 0.5 mg C/litre a t a rate of 1-4 x is 140-570 years. The larger value falls within the somewhat elastic range of estimates that has been proposed as the age of the deep water of the Atlantic Ocean. As a generalized statistic this range seems reasonable ; however, the true situation is likely to be a rapid rate of turnover of a small fraction of readily assimilable substances and a much longer residence time for more refractory compounds. Webb and Johannes (1967) and Johannes and Webb (1968) have investigated the kinds and quantities of dissolved organic compounds that are released by copepods and other invertebrates. The product

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includes free amino acids and other substances which should be readily utilizable by heterotrophs. Thus the general stock of dissolved organic matter in the deep sea includes materials that have been recently produced in situ by the local assemblage of bathypelagic animals. Theoretically, such things as amino acids could either be utilized directly by heterotrophs or could be adsorbed on particulate matter, which would make them available either to bacteria or to filter feeders. The general concept that dissolved organic matter originates a t the surface and has a long residence time in deep water is true as a generalization, but these recent observations suggest that internal recycling of “ young ” materials could be a significant aspect of the biological economy of the deep sea. However, measurements of excretory rates thus far have been limited to zooplankton collections taken in the surface layer, and the results cannot be extrapolated to a quantitative estimate of excretion under the semi-starvation conditions of the bathypelagic zone. As indicated earlier, most of the nitrogenous material in deep water is in the form of amino N, yet much of the older material must be combined in forms that make it resistant t o biological attack. The low concentration occurring in nature cannot be the only reason for its inability to support active heterotrophic growth. Barber (1968) increased the concentration by pressure dialysis but found no significant utilization in experiments of 1-2 months’ duration. Of course the method is not precise enough t o detect small changes with certainty. Rakestraw (1947) reported small but significant reductions in oxygen in long term B.O.D. experiments. The carbon equivalent of this consumption was of the order of 0.1 mg/litre in experiments lasting considerably longer than Barber’s. While this amount is small compared with the B.O.D. of surface waters, it is in fact much more rapid than estimated in situ rates of consumption. Presumably the bacteria were growing more effectively in the bottles than they do in the sea, as is usual in this kind of experiment. Degens (1968) has noted that ratios of C13 t o C12 are essentially similar in living plankton, in non-living particulate organic matter and in recent marine sediments, and there is a reduction in the ratio in dissolved organic matter and in ancient marine sediments. Biological utilization of the organic matter presumably has resulted in isotope fractionation. For example, Degens quoted evidence that the CO, released during decarboxylation of amino acids can be significantly enriched in C13 in relation to the remainder of the molecule, and the remaining organic matter of course will be correspondingly depleted. Degens concluded that the sediments were derived primarily from

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particulate matter in the water column rather than from the dissolved fraction. There is a further implication in his results that the dissolved matter is older and has gone through more metabolic transformations than the particulate fraction. This sort of conclusion could be valid as a generalization without denying the concept developed above that a small fraction of the dissolved material is new and metabolically usable. The problem of estimating zooplankton food requirements and feeding rates is not an easy one. Experimental estimates vary widely, and probably there are similar variations in nature. The problem is particularly difficult in the present case because most of the experimental information has been obtained from surface forms. Our opinion about what bathypelagic organisms eat is largely a matter of inference, based upon the character of their mouth parts. The question is largely unresolved as to whether there are local concentrations of food that ameliorate the average picture of extreme scarcity. There is as yet no clear answer to the question of whether food requirements and metabolic rates in the deep sea are essentially similar to those of nearsurface waters. Attempts to investigate pressure effects have led to somewhat equivocal results. Napora (1964) reported that pressure slightly increased the respiratory rate of Xystellaspis debilis, a prawn which is a member of the mid-depth population that migrates to the surface a t night. He was working with animals that live in the Sargasso Sea, where the thermocline is not particularly steep, and the effect of decreasing temperature as the animals moved downward was approximately balanced by the pressure effect, so that the animals maintained an essentially constant respiratory rate a t all depths. Teal and Carey (1967) found a significant pressure effect with Thysanopoda monocantha, a euphausiid which normally lives a t mid-depths and apparently does not come t o the surface a t night. However, they tested several migratory euphausiids and found that pressure effects were operative only a t temperatures that were too high to be of any significance a t the daytime level. Pearcy and Small (1968) examined two euphausiids and a prawn, all migratory forms, and found no significant pressure effects. I n short, no consistent pattern emerges among the mid-depth forms, and the writer has failed to find any information on truly bathypelagic animals. Provisionally the problem must be considered in terms of what is known about surface forms although the deep sea environment may have a significant effect on physiological rates. Present estimates of zooplankton respiratory requirements have been based upon measurements of oxygen consumption of surface

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forms a t low temperature as indicated in item (4) of the introductory section, together with data from Leavitt (1938) on the quantity of zooplankton in deep water. The latter collections were made with a twometre stramin net. Recent work with finer mesh sizes indicates that there is a significant fraction of small zooplankton that would not be included in the present estimats. The true value for deep water consumption by animals probably is somewhat larger than the one given here, and as indicated above, physical oceanographic computations may also underrate total consumption. However, present information provides a basis for a general discussion of feeding problems in deep water. One of the early attempts to express grazing rates of herbivorous plankton in a simple form suitable for quantitative application was that of Riley et al. (1949). The formula, restated in a slightly different notation, was G = 235 R where G is a grazing coefficient indicating ml/day of water swept clear of particulate food by a quantity of zooplankton containing 1 mg C, and R is the respiratory consumption in mg C/mg of zooplankton carbon. This formula as expressed conformed with experimental observations that grazing rates increased with temperature in much the same way that respiratory rates do, and the constant in the equation was more or less in the middle of the observed range of grazing coefficients. The equation was used with a fair degree of success in theoretical computations of regional plankton abundance in various areas of the western North Atlantic, including the Sargasso Sea. Recent work has added a great deal of knowledge about grazing and assimilation rates and respiratory requirements under various conditions, but these investigations have not yet produced a definitive statement of quantitative relationships, so that the formula given above still serves as a rule of thumb in gauging the effectiveness of a given food supply in supporting a crop of herbivorous zooplankton. With regard t o the surface layer of the Sargasso Sea, Menzel and Ryther (1961) found that the respiratory requirement of the zooplankton in terms of carbon was about 12% of zooplankton dry weight so that R = ca 0.06 mg C/day, and G = 1.4 litres. The general range of particulate organic carbon as determined by cruise averages for various seasons (Riley et al., 1965) was 46-168 pg C/litre. A reasonable annual mean would be about 85 pg, leading to an estimated daily consumption of 120 pg C/mg of zooplankton carbon. This is probably an adequate food supply, on the average, for a t least half of the particulate carbon in the surface layer is likely to be assimilable. During the poorer part of the year the supply would seem to be somewhat inadequate, but as

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indicated earlier, there are likely t o be micro-concentrations of food in convective downdrafts that are not clearly demonstrated by routine sampling procedures. Most of the mid-depth organisms in this area perform long diurnal migrations of some hundreds of metres. Varying food habits are represented. The herbivorous fraction presumably gets most of its nourishment in the surface layer a t night. At the daytime level there is probably little more particulate food available than in the deep sea, although there may be layering in small discontinuities in the main thermocline as indicated earlier. Food relations of bathypelagic animals have been discussed by many authors, but this remains as one of the most poorly understood problems in biological oceanography. Early investigators wrote that deep sea animals are fed by a " rain of detritus from the surface layer )', a phrase that has been quoted too often, for it is a superficiality that tends to sweep the problem under the rug. It is presumably a simplistic expression of the valid concept that all deep sea life is supported directly or indirectly by surface production, but the statement was made with essentially no knowledge of the quantity or food value of detritus sinking from the surface, or of the further transformations that must occur in order t o develop the observed assemblage of deep sea animals. A considerable proportion of this assemblage is of course carnivorous or necrophagous. Wheeler (1967) has found that dead zooplankton constitutes a significant fraction of total net catches in deep water. This is not generally the case in near-surface catches, where presumably the population is sufficiently concentrated so that any animals dying a natural death will be consumed very quickly. The implication in Wheeler's finding is that bathypelagic organisms which die a natural death may not be found and eaten immediately and in the meantime will sink into deeper water. Even in the case of capture of living prey, vertical movement of animals and random capture a t different depths can lead t o a sort of " biological diffusion " of food materials from middepths down into the sparser deep waters, a concept mentioned by Riley (1951) and developed more fully by Vinogradov (1962). Some bathypelagic copepods have foliaceous appendages which appear t o be suitable for a filter feeding habit. Animals with mouthparts of this type probably are more common than has been suspected, because most of the collections of deep water zooplankton have been made with coarse nets that do not catch small copepods effectively. However, it remains an open question as t o whether indiscriminate filter feeding in the bathypelagic zone will supply an adequate amount

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of food. Work by Conover (1964) on Calanus hyperboreus is useful in evaluating this problem. This copepod is a surface form in high latitudes and is a minor constituent of the bathypelagic fauna of lower latitudes. It is well adapted to the rigors of its normal habitat a t the surface, where food is abundant in summer but virtually absent during much of the year. Conover has demonstrated that there is a high rate of accumulation of stored fat when it is fed a t an optimal level, and it can survive starvation for some months with a reduced rate of metabolism that conserves its stored food. Conover found that the normal daily food requirement a t low temperature is about I yo of the weight of the animal ; under starvation conditions carbon consumption is reduced to as little as 0.4%. According to average grazing estimates presented earlier a 1yo respiratory requirement would be accompanied by a filtering rate of about 235 ml of water per milligram of zooplankton carbon in a day. This filtration rate would require a concentration of 17 pgllitre of assimiIable carbon to supply a maintenance ration even a t a reduced level approaching starvation metabolism. Most of the values that have been reported for deep water particulate carbon fall within the general range of 1050pgC/litre, which appears t o be inadequate unless it is more completely assimilable than is indicated by experiments with enzymes (Gordon, 1970b). As far as present information is concerned, there is little likelihood that bathypelagic organisms can support themselves solely by indiscriminate filter feeding. According to Conover ( I 964) C. hyperboreus is capable of either selective capture or filter feeding, and the present discussion points toward a tentative conclusion that this kind of feeding habit is essential for bathypelagic copepods with foliaceous appendages. Possible food materials would include smaller zooplankton, living and dead, large aggregates, and faecal pellets. Reports by divers of " marine snow " indicate that there are organic aggregates of visible size in the deep ocean. These presumably have a fairly rapid sinking rate, and the number delivered into deep water may be much greater than might be inferred from the relative scarcity of large aggregates in water samples. Faecal pellets of visible size can sink at rates of 50-375 m/day (Smayda, personal communication). They, too, may be a source of particulate food that is much more important than would be suspected on the basis of their relative abundance. These various sources can only be mentioned in passing. Little can be said about their nutritive value or rate of supply. Certainly the sparse nature of the bathypelagic population is sufficient evidence that the food supply is minimal.

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Coming back to the earlier comments about a “ r a i n of detritus from the surface ”, faecal pellets derived from the surface can sink quite rapidly and conceivably could arrive in the bathypelagic zone before their organic content, such as it is, has been seriously depleted by bacterial activity. Most of the other suspended matter would have a residence time ranging from one year t o many years, and there is little likelihood that any biologically usable fraction of it could escape consumption by one means or another during that period. The continued existence of particles containing a significant fraction of usable substances (as indicated for example by hydrolysis experiments quoted above) must be due to in situ processes. There are indications that particles can form de novo. There are also indications of interchanges of simple molecules such as amino acids between the dissolved organic pool and various kinds of particulate matter, living and dead. The pathways are complex and probably have not all been properly identified. Our knowledge of probable rates of exchange is very limited. The rates are low, due to the dilute nature of the medium, and it will be a very difficult job indeed to obtain realistic information on natural rates of exchange. Possibly carnivorous activity is quantitatively more important than heterotrophic processes in energy transfer and vertical flux of materials toward the bottom. This remains t o be seen. Present information is crude and equivocal. However, heterotrophy is more important than was realized until recently, and by the same token there is opportunity for complexity and diversification of food web relations t o a degree perhaps approaching that of the surface layer. Finally we come t o a consideration of deposition and utilization of organic matter on the bottom. Analyses of the carbon content of deep water particulate matter have indicated that it is probably of the order of 10-30% of the dry weight, although some records of as little as 1% have been reported. However, bottom sediments in deep ocean basins commonly contain only a fraction of 1 % of organic carbon, so that most of this material must be consumed on the bottom. The ocean bottom is of course a more favorable site for organic consumption than is the water column. Abundant surfaces are provided for bacterial growth, and presumably dissolved materials are more highly concentrated in the interstitial water than in the free water above. Compaction of organic matter into a relatively small volume makes it readily available to sediment feeders, and although the bottom fauna is sparse in the deep ocean compared with shallower areas, it is more concentrated than the bathypelagic assemblage. Estimates of biological activity of the benthic population are no

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better than any other calculations for deep sea fauna and flora, and they vary by an order of magnitude or more. Riley (1951) noted that the oxygen concentration decreases toward the bottom, indicative of utilization on or near the bottom. Computations of eddy diffusivity combined with observed oxygen gradients indicated that transfer of oxygen toward the bottom was equivalent t o a utilization of 0.4mg C/m2 of bottom in a day. ZoBell and Morita (1956) arrived a t a larger estimate based upon observed quantities of bacteria in deep sea sediments. They postulated an annual yield of 0.5 g of bacterial carbon/m2 of deep ocean sediment (1.4 mg/day). The bacterial population probably would have to utilize about 3 mg of organic carbon per day in order to maintain this level of production, and in a steady state situation their production would be utilized by benthic animals. Thus Riley et al. (1965) concluded that this kind of estimate involves a total utilization of about 4.4 mg C.m - .day This calculation is subject t o the same kind of difficulties that were apparent in the discussion of bathypelagic populations. It is based on a realistic estimate of the biomass of bacteria in deep ocean sediments, but there is no assurance that their metabolic rate is assessed properly. Kriss et al. (1966) have noted some alterations in metabolic processes of bacteria that are induced by high pressure, but there is little information on total oxygen consumption and energetic requirements of the natural population. The wide discrepancy between these two estimates given above might be resolved if we knew more about the biomass and food requirements of deep sea benthic fauna. Vinogradova (1962) has summarized much of the available information on quantitative collections. She found that the biomass is generally between 0.1 and 1 g/m2 wet weight a t depths in excess of 2 000 m, although samples of 0.05 g/m2 or even less have been obtained, particularly in deep tropical waters. The range is large enough so that an average may not be very meaningful, but Vinogradova suggested that the " approximate mean biomass " in waters of greater than 3 000 m is about 0.2 g/m2. This presumably would correspond to a carbon content of about 20 mg, and a general range of 10--100 mg C/m2 is indicated for most deep ocean communities. Normally one would expect the daily food requirement to be a t least 1-2% of the biomass of the fauna, so that the average consumption might be of the order of 0.2-0.4 mg C.m-2.day-1, and the total range might be about 0.1-2 mg/day. These numbers are of the same order of magnitude as the estimates derived earlier for total utilization. The minimum estimate of

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0.4 mg C.m-2.day-l appears t o be adequate to support a minimal population of bacteria and animals, and the maximum estimate of 4.4 mg probably would take care of the largest populations ordinarily found in the deep ocean. This still does not establish a reasonable average value, and possibly it is premature to attempt to do so. However, if we accept Vinogradova’s approximate figure for average biomass of the fauna, total utilization by these animals and associated bacteria possibly would be of the order of 1 mg C.m-Z.day-l. The rate of delivery of organic matter t o the bottom can be estimated with some degree of confidence. The materials most frequently seen in deep water samples are flakes and small particles. Under laboratory conditions these have a sinking rate of about 0.2 m/day, and in cold waters the rate might be reduced to around 0.1 m. Thus if the bathypelagic concentration is of the order of 10-50 pg C/litre, the rate of sedimentation would be 1-5 mg C.m-2.day-l. Quantitatively this seems adequate to satisfy utilization rates described above, and this may be a minimum estimate in view of the fact that there may be some larger particles raining down faster. The faunal assemblage has been reported by Vinogradova and others to consist of seston feeders, indiscriminate detritus feeders, and carnivores. As far as seston feeders are concerned, the problem would seem t o be much the same as that posed earlier in connection with the bathypelagic population. The rate of supply is adequate, but a concentration of 10-50 pg C/litre is minimal for filter feeders. However, the published literature indicates that the relative proportions of mud feeders and seston feeders are quite variable, and the latter are most abundant in certain limited zones where suspended organic matter is also most abundant. These zones are often located on or near continental rises or on the slopes of trenches, suggesting that the amount of suspended material may be increased in such areas by turbidity currents or the stirring action of deep water movements of a local nature. There is little reason to suppose that the supply of organic matter from above would vary in a way that would lead to strongly demarcated local zones of abundance of sufficiently permanent nature to affect faunal distribution, and variations in the benthic environment are a more likely explanation. As indicated earlier, collection of sinking particles a t the mudwater interface provides an abundant concentration of organic matter there, in contrast to the scarcity in concentration per unit volume in the overlying water. Thus it is not surprising to find that sediment feeders are more important than seston feeders on much of the deep ocean floor. There is not any good information as to what proportion

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of their sustenance is derived directly from noii-living particles. Some particles must be digestible, but earlier calculations also suggest that if bacteria were solely responsible for utilization of this material, their productivity could approximately satisfy animal needs. Some of the organic matter is of course highly resistant to attack by either animals or bacteria, so that although most of it is used up eventually, it takes a long time. Thus the organic content of the sediments declines slowly with depth even in the deep ocean where sedimentation rates are slow. The foregoing discussion, necessarily long because of the many problems and uncertainties in this kind of analysis, does not reduce to a precise balance sheet of production and consumption. A few concluding generalizations are likely to be more useful than a recapitulation of numerical values. Primary productivity occurs within the upper 100 m, more or less, in the Sargasso Sea, and the level of productivity is believed t o be considerably higher than was indicated by so-called standard methods of measuring C14 fixation. Net production plus extracellular production ara believed to be of the order of 320-380 mg C.m-2.day-1. About 75-80% of this production is utilized in the surface layer and upper mid-depths by zooplankton and ultraplankton. The latter term as defined by Pomeroy and Johannes (1968) includes bacteria, small heterotrophic algae, and protista. This is primarily a microcosmic assemblage within organic aggregates, and its total consumption is probably slightly greater than that of zooplankton. Approximately 20% of total Consumption is allocated to zooplankton and heterotrophs in the lower mid-depth region, the bathypelagic zone, and the bottom. The major part of this consumption occurs a t mid-depths, down to and including the level of the oxygen minimum layer. Total amounts consumed in the bathypelagic and benthic zones are probably about equal, but in the one case it is thinly spread through hundreds of metres and in the other it is concentrated into a small depth range on and in and just over the bottom. Together they probably account for less than 5% of the total consumption. Throughout these deeper waters flakes are numerically more important than amorphous aggregates. They are colonized by bacteria but do not develop complex microcosms. There are various indications, although the evidence is not entirely convincing, that heterotrophy is relatively less important in lower mid-depths and the bathypelagic zone than it is in upper waters or on the bottom. Higher carnivores have not been considered in this analysis, and quantitative assessment of their importance in the whole of the deep

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water column is a task beyond present oceanographic capabilities. From general energetic considerations they probably constitute less than 5% of the total consumers. Comparative analyses of other areas would be desirable, but available data are too fragmentary to warrant the attempt. The Sargasso Sea is of course relatively unproduct,ive. Phytoplankton production in temperate and boreal waters probably is of the order of three times that of the Sargasso Sea, and tropical upwelling areas perhaps are even more productive. These more productive areas also appear to have larger concentrations of non-living particulate matter, herbivorous zooplankton, macrozooplankton of primarily carnivorous habit, fishes and bottom fauna. Data could be compiled t o show in a semi-quantitative way that all of the elements which have been considered here can be expected to increase in more productive waters, although not necessarily in exact proportion. However, t o use the Sargasso Sea as an example of the relations between living and non-living matter seems quite justifiable. It is not an average oceanographic situation, but there is no reason to think that the inter-relationships are atypical. These inter-relationships are infinitely more complicated than was realized until recently, and our study of these problems is in approximately the same naive state as plankton studies of perhaps thirty years ago. This review has required a rambling discussion of a good many matters that could be stated more concisely if we understood them better, but hopefully it will be of some help in focusing attention on important problems that need further study. VI. REFERENCES Antia, N. J., Stephens, K., Tripp, R. B., Parsons, T. R. and Strickland, J. D. H. (1962). A data record of productivity measurements made during 1961 and 1962. R e p . Xer. Oceanogr. L i m n o l . Fish. Res. B d . C a n . 135, 33. Barbcr, R . T. (1966). Interaction of bubbles and bacteria in the formation of organic aggregates in sea-water. N a t u r e , L o n d . 211, 257-258. Barber, R. T. (1968). Dissolved organic carbon from deep waters resists microbial oxidation. N a t u r e , L o n d . 220, 274-275. Batoosingh, E., Riley, G. A. and Keshwar, Barbara. (1969). An analysis of experimental methods for producing particulate organic matter in sea water by bubbling. Deep S e a Res. 16, 213-219. Baylor, E. R., Sutcliffe, W. H. and Hirschfeld, D. S. (1962). Adsorption of phosphates onto bubbles. Deep S e a Res. 9, 120-124. Baylor, E. R. and Sutcliffe, W. H. (1963). Dissolved organic mattcr in seawater as a source of particulatc food. Limnol. Oceanogr. 8, 369-371. Bernard, F. (1967). Research on phyt#oplankton and pelagic protozoa in the Mediterranean Sea from 1953 t o 1966. Ocean. M a r . Biol. Ann. Rev. 5, 205229.

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Biggs, R. B. and Wetzel, C. D. (1968). Concentration of particulate carbohydrate at the halocline in Chesapeake Bay. Limnol. Oceanogr. 13, 169-171. Blanchard, D. C. (1963). The electrification of the atmosphere by particles from bubbles in the sea. I n " Progress in Oceanography ". (M. Sears, ed.) 1, 71-202. Pergamon Press, Oxford. Bursa, A. S. (1968). Starch in the Oceans. J . Fish. Res. BtE. Can. 25, 1269-1284. Chave, K.E. (1965). Carbonates: association with organic matter in surface sea water. Science, N . Y . 148, 1723-1724. Chave, K.E. (1968). Carbonate-organic interactions in seawater. University of Alaska Symposium on Organic Matter in Natural Watcrs.* Conover, R. J. (1964). rood relations and nutrition of zooplankton. Proc. Symp. on Ezp. Mar. Ecol., Occas. Pub. No. 2, Grad. School of Oceanogr. U. Rhode Isl. 81-91. Dal Pont, G. and Newell, B. (1963). Suspended organic matter in the Tasman Sea. Austral. J . mar. Freshwat. Res. 14, 155-163. Day, C. G. and Webster, F. (1965). Some current measurcmerits in the Sargasso Sea. Deep Sea Res. 12, 805-814. Degens, E. T. (1968). Molecular nature of nitrogenous compounds in sea water and recent marine sediments. University of Alaska Symposium on Organic Matter in Natural Waters. Duursma, E. K. (1960). Dissolved organic carbon, nitrogen, and phosphorus in the sea. Nethed. J . Sea Res. 1, 1-148. Faller, A. J. and Woodcock, A. H. (1964). The spacing of windrows ofSargassum in the ocean. J . mar. Res. 22, 22-29. Fournier, R. 0. (1966). North Atlantic deep-sea fert,ility. Science, N . Y . 153, 1250-1252. Fournier, R. 0. (1968). Observations of particulate organic carbon in t,he Mediterranean Sea and their relevance to the deep-living Cyclococcolithusfragilis. Limnol. Oceanogr. 13, 693-697. Fox, D. L., Isaacs, J. D. and Corcoran, E. F. (1952). Marine leptopel, its rccovery, measurement and distribution. J . mar. Res. 11, 29-46. Fox, F.E. and Herzfeld, K. F. (1955). Gas bubbles with organic skins as cavitation nuclei. J . ucoust. Sac. Amer. 26, 984-989. Garrett), W. D. (1964). The organic chemical composition of the ocean surface. N.R.L. Rep. 6201, 1-14. Garrett, W. D. (1968). Organic chemistry of natural seasurface films. University of Alaska Symposium on Organic Matter in Natural Waters. Goldacre, R . J. (1958). Surface films, their collapse on compression, the shapes and sizes of cells and the origin of life. I n " Surface phenomena in chemistry and biology ". (K. G. A. Pankhurst and A. C. Riddiford, eds.). Pergamon Press, New York. 278-298. Goldman, C. R . (1968). Thc use of absolute activity for eliminating serious errors in the measurement of primary productivity with C1*. J . Cons. int. Explor. Mer, 32, 172-179. Gordon, D. C. (1969). Examination of current methods of particulate organic carbon analysis. Deep Sea Res. 16, 661-665. Gordon, D. C. (1970a). A microscopic study of non-living organic particles in the North Atlantic Oceaii. Deep Sea Res. 17, 175-185. *Date given for University of Alaska Symposium throughout refer8 to insuc of preprint manuscript. Publication in preparation, D. W. Hood, editor.

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Gordon, D. C. (1970b). Some studies on the distribution and composition of partJiculate organic carbon in the North Atlantic Ocean. Deep Sea Res. 17, 233-243. Hamilton, R. D. and Holm-Hansen, 0. (1967). Adenosine triphosphate content of marine bacteria. Limnol. Oceunogr. 12, 319-324. Hamilton, R.D., Holm-Hansen, 0. and Strickland, J. D. H. (1968). Notes on the occurrence of living microscopic organisms in deep water. Deep Sea Res. 15, 651-656. Handa, N. ( 1 968). Dissolved and particulate carbohydrates. University of Alaska Symposium on Organic Matter in Natural Waters. Harder, W. (1968). Reactions of plankton organisms to water stratification. Limnol. Oceanogr. 13, 156-168. Hellebust, J. A. (1965). Excretion of some organic compounds by marine phytoplankton. Limno2. Oceanogr. 10, 192-206. Hellebust, J. A. (1968). The uptake and utilization of organic substances by marine phytoplankters. University of Alaska Symposium on Organic Matter in Natural Waters. Hobson, L. A. (1967). The seasonal and vertical distribution of suspended particulate matter in an area of the Northeast Pacific Ocean. Limnol. Oceanogr. 12, 642-649. Holm-Hansen, 0. (1968). Determination of microbial biomass in deep ocean waters. University of Alaska Symposium on Organic Matter in Natural Waters. Holm-Hansen, 0. and Booth, C. R. (1966). The measurement of adenosine triphosphate in the ocean and its ecological significance. Limnol. Oceanogr. 11, 510-519. Holm-Hansen, O., Strickland, J. D. H. and Williams, P. M. (1966). A detailed analysis of biologically important substances in a profile off southern California. Limnol. Oceunogr. 11, 548-561. Holm-Hansen, O., Sutcliffe, W. H. and Sharp, J. (1968). Measurement of deoxyribonucleic acid in the ocean and its ecological significance. Limnol. Oceanogr. 13, 507-514. Iselin, C. O’D. (1936). A study of the circulation of the western North Atlantic. Pap. phys. Oceanogr. Met. 4(4), 1-101. Iselin, C. O’D. (1940). Preliminary report on long-period variations in the transport of the Gulf Stream system. Pap. Phys. Oceanogr. Met. 8(1), 1-40. Jannasch, H. W. and Jones, G. E. (1959). Bacterial populations in sea water as determined by different methods of enumeration. Limnol. Oceanogr. 4, 128-139. Jarvis, N. L. (1965). Adsorption of surface-active material at the surface of seawater samples from the Bay of Panama. N . R . L . Rep. 6325, 1-20. Jarvis, N. L., Garrett, W. D., Scheiman, M. A. and Timmons, C. 0. (1967). Surface chemical characterization of surface-active material in sea water. Limnol. Oceanogr. 12, 88-96. Jespersen, P. (1935). Quantitative investigations on the distribution of macroplankton in different oceanic regions. Dana Rep. 7, 1-44. Johannes, R. E. (1967). Ecology of organic aggregates in the vicinity of a coral reef. Limnol. Oceanogr. 12, 189-195. Johannes, R. E. and Webb, K. L. (1968). Release of dissolved organic compounds by marine and freshwater invertebrates. University of Alaska Symposium on Organic Matter in Natural Waters.

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Krey, J. (1961). Der detritus im Meere. J . Cons. int. Explor. Mer, 24, 263-280. Krey, J. (1967). Detritus in the ocean and adjacent sea. I n “ Estuaries ”. (George H. Lauff ed.), AAAS Pub. No. 83, 389-394. Krey, J., Banse, K. and Hagmeier, E. (1957). Uber die Bestimmung von Eiweis im Plankton mittels der Biuretreaktion. Kieler Meeresforsch. 20, 18-29. Kriss, A. E. (1963). ‘‘ Marine Microbiology (deep sea) ”. (Translated by J. M. Shewan and Z. Kabata.) Oliver and Boyd, London. 536 pp. Kriss, A. E., Chumak, M. D., Mishustina, I. E. and Mitzkevich, I. N. (1966). Changes in marine bacteria activity under high pressure. Abstr. 2nd Int. oceanogr. Con,gr. Moscow, 208-209. Leavitt, B. B. (1938). The quantitative vertical distribution of macrozooplankton in the Atlantic Ocean basin. Biol. Bull. mar. biol. Lab., Woods Hole, 74, 376-394. Limbaugh, C. and Rechnitzer, A. B. (1955). Visual detection of temperate density discontinuities in water by diving. Science, N . Y . 121, 253. Lovett, J. R. (1968). Vertical temperature gradient variations related to current shear and turbulence. Limnol. Oceanogr. 13, 127-142. McGill, D. A. (1964). The distribution of phosphorus and oxygen in the Atlantic Ocean, as observed during the I.G.Y., 1957-1958. I n ‘‘ Progress in Oceanography ”. (M. Sears, ed.) 2, 127-211. Pergamon Press, Oxford. McGill, D. A., Corwin, N. and Ketchum, B. H. (1964). Organic phosphorus in the deep water of the western North Atlantic. Limnol. Oceanogr. 9, 27-34. McLeish, W. (1968). On the mechanisms of wind-slick generation. Deep Sea Res. 15, 461-469. Mazia, D., Brewer, P. A. and Alfert, M. (1953). The cytochemical staining and measurement of protein with mercuric bromphenol blue. Biol. Bull. mar. biol. Lab., Woods Hole, Mass., 104, 56-67. Menzel, D. W. (1964). The distribution of dissolved organic carbon in the western Indian Ocean. Deep Sea Res. 11, 757-765. Menzel, D. W. (1966). Bubbling of sea water and the production of organic particles : a re-evaluation. Deep Sea Res. 13, 963-966. Menzel, D.W. (1967). Particulate organic carbon in the deep sea. Deep Sea Res. 14, 229-238. Menzel, D. W. and Goering, J. J. (1966). The distribution of organic detritus in the ocean. Limnol. Oceanogr. 11, 333-337. Menzel, D.W. and Ryther, J. H. (1960). The annual cycle of primary production in the Sargasso Sea off Bermuda. Deep Sea Res. 6, 351-367. Menzel, D. W. and Ryther, J. H. (1961). Zooplankton in the Sargasso Sea off Bermuda and its relation to organic production. J . Cons. int. Explor. Mer, 26, 250-258. Menzel, D. W. and Ryther, J. H. (1964). The composition of particulate organic matter in the western North Atlantic. Limnol. Oceanogr. 9, 179-186. Mcnzel, D. W. and Ryther, J. H. (1968a). Organic carbon and the oxygen minimum in the South Atlantic Ocean. Deep Sea Res. 15, 327-338. Menzel, D. W. and Ryther, J. H. (1968b). Distribution and cycling of organic matter in the oceans. University of Alaska Symposium on Organic Matter in Natural Waters. Menzel, D. W. and Vaccaro, R . F. (1964). The measurement of dissolved organic and particulate carbon in seawater. Limnol. Oceanogr. 9, 138-142. Munk, W. H. and Riley, G. A. (1952). Absorption of nutrients by aquatic plants. J . mar. Res. 11, 215-240.

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Napora, T. A. (1964). The effect of hydrostatic pressure on the prawn, Systellaspis debilis. S y m p . o n E x p . Marine Ecol. Narragansett Marine Lab. Occas. Publ. NO. 2 ; 92-94. Newell, B. S. (196G). Suspended organic matter in the south eastern Indian Ocean. Abstr. 2nd Int. oceanogr. Congr. Moscow, 269-270. Nishizawa, S., Fukuda, M. and Inoue, H. (1954). Photographic study of suspended matter and plankt,on in the sea. Bull. Pac. Fish. Holclcaido Univ. 5, 36-40. Otsuki, A. (1968). Biogoochemical studies o n the production of the dissolved organic matter in relation to food chain of hydrosphere. Thesis, Tokyo Metropolitan University. 79 pp. Paramonov, A. N., Neumen, 0. G. and Efumov, B. B. (1966). Some results of measuring fluctuations in trmsparency in ocean water (in Russian). Acad. Sci. Ukrain. S.S.R., Marine Hydrophys. Inst., 18th cruise of the Michael Lomonosov, Spec, Inform. No. 3, 86-98. Parsons, T. R. (1963). Suspended organic matter in sea water. I n “ Progress in Oceanography ”. 1, 205-239. Pergamon, Oxford. Parsons, T. R . and Seki, H. (1968). Importance and general implications of organic matter in aquatic environments. university of Alaska Symposium on Organic Matter in Natural Waters. Parsons, T. R. and Strickland, J. D. H. (1962a). Oceanic detritus. Science, N . Y . 136, 313-314. Parsons, T. R . and Strickland, J. D. H. (196213). On the production of particulate organic carbon by heterotrophic processes in sea water. Deep Sea Res. 8, 211-222. Pearcy, W. G. and Small, L. F. (1968). Effects of pressure on the respiration of vertically migrating crustaceans. J . Fish. Res. B d . Can. 25, 1311-1316. Pearse, A. G. E. (1960). “ Histochemistry ”, J. and A. Churchill, London. Pomeroy, L. R. and Johannes, R . E. (1968). Occurrence and respiration of ultraplankton in the upper 500 meters of the ocean. Deep Sea Res. 15,381-391. Provasoli, L. (1963). Organic regulation of phytoplankton fertility. I n ‘‘ The Sea ” (M. N. Hill et al. eds.). Interscience Pub., London. 2, 165-219. Rakestraw, N. W. (1947). Oxygen consumption in sea water over long periods. J . mar. Res. 6, 259-263. Redfield, A. C. (1942). The processes determining the concentration of oxygen, phosphate and other organic derivatives within the depths of the Atlantic Ocean. Pap. Phys. Oceanogr. Met. 9(2), 1-22. Riley, G. A. (1951). Oxygen, phosphate, and nitrate in the Atlantic Ocean. Bull. Bingham oceanogr. Coll. 13(1), 1-126. Riley, G. A. (1957). Phytoplankton of the north central Sargasso Sea, 1950-52. Livnnol. Oceanogr. 2, 252-270. Riley, G. A. (1959). Note on particulate matter i n Long Island Sound. Bull. Bingham Oceanogr. Coll. 17, 83-86. Riley, G. A. (1963). Organic aggregates in seawater and the dynamics of their formation and utilization. Limnol. Oceanogr. 8, 372-381. Riley, G. A. (1965). A mathematical model of regional variations in plankton. Limnol. Oceanogr. 10 (suppl.), R202-R215. Riley, G. A., Stommel, H. and Bumpus, D. F. (1949). Quantitative ecology of the plankton of the western North Atlantic. Bull. Bingham Oceanogr. Coll. 12(3), 1-169.

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Riley, G. A., Wangersky, P. J. end Van Hemert, D. (1964). Organic aggregates in tropical and subtropical snrface waters of tho Nort'h Atjlantic Oman. Limncd. Oceanogr. 9, 546-550. Riley, G. A., Van Hemert, D. and Wangersky, P. J. (1965). Organic aggregates in surface and deep waters of the Sargasso Sea. Limnol. Oceanogr. 10, 354363. Rossby, C. G. and Montgomery, R. B. (1935). The layer of frictional influence in wind and ocean currcnts, P a p . Phys. Oceanogr. Met. 3(3), 1-101. Sebba, F. (1962). '' Ion flotation ". Elsevier Pub. Co., New York. Sheldon, R. W., Evelyn, T. P. T. and Parsons, T. R. (1967). On the occurrence and formation of small particles in sea water. Limnol. Oceanogr. 12, 367375. Sheldon, R. W. and Sutcliffe, W. H. (1969). Retention of marine particles by screens and filters. Limnol. Oceanogr. 14, 441-444. Sioburth, J. M. and Jensen, A. (1968). Production and transformation of extracellular organic matter from littoral marine algae ; a r6sum8. University of Alaska Symposium on Organic Matter in Natural Waters. Siegel, A. and Burke, B. (1965). Sorption studies of cations on " bubble produced organic aggregates " in sea water. Deep Sea Res. 12, 789-796. Skopintsev, B.A. (1966). Up-to-date data on the content of organic matter in the waters of the Atlantic Ocean. Abstr. 2nd I n t . Oceanogr. Congr. MOSCOW, 340. Smayda, T. J. and Boleyn, B. T. (1965). Experimental observations on the flotation of marine diatoms. I. Thalassiosira cf. nana, Thalassiosira rotula and Nitzsehia seriata. Limnol. Oceanogr. 10, 499-509. Smayda, T. J. and Bolcyn, B. J. (196th). Experimental observations on the flotation of marine diatoms. 11. Slceletonema costatum and Rhizosolenia setigera. Limnol. Oceanogr. 11, 18-34. Smayda, T. J. and Boleyn, B. J. (1966b). Experimental observations on the flotation of marine diatoms. 111. Bacteriastrum hyalinuwz and Chaetoceros lauderi. Limnol. Oceanogr. 11, 35-43. Sorokin, J. I. (1964). A quantitative study of the microflora in the central Pacific Ocean. J . Cons. int. Explor. Mer, 29, 25-40. Steele, J. H. (1958). Plant production in the northern North Sea. Mar. Res. 7, 1-36. Stommel, H. (1948). The westward intensification of wind-driven ocean currents. Trans. Am. geoph. U n . 29, 202-206. Stommel, H.(1949). Trajectories of small bodies sinking slowly through convection cells. J . mar. Res. 8, 24-29. Stommel, H. and Arons, A. B. (1960). On the abyssal circulation of the world ocean. 1. Stationary planetary flow patterns on a sphere. Deep Sea Res. 6, 140-154. Stommel, H . and Federov, K. N. (1967). Small scale structure in temperature and salinity near Timor and Mindanao. Tellus. 19, 306-325. Strickland, J. D. H. and Parsons, T. R. (1965). A manual of sea water analysis. Bull. Fish. Res. B d . Can. 125, (2nd ed., revised), 1-203. Strickland, J. D. H. and Solozano, L. (1966). Determination of monoesterase hydrolyzable phosphate and phosphomonocsterase activity in sea water. I n " Some contemporary studies in marine science". (H. Barnes, ed.). Allen and Utiwin, London. 665-674. A . M . 13 .-8

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Suess, E. (1968). Calcium carbonate interaction with organic compounds Doctoral dissertation, Lehigh University. 163 pp. Sutcliffe, W. H., Baylor, E. R. and Menzel, D. W. (1963). Sea surface chemistry and Langmuir circulation. Deep Sea Res. 10, 233-243. Sverdrup, H.V., Johnson, M. W. and Fleming, R. H. (1942). “ The Oceans Prentice-Hall, Inc. New York. 1087 pp. Szekielda, K.-H. (1967). Some remarks on the influence of hydrographic conditions on the concentration of particulate carbon in sea water. I n “ Chemical environment in the aquatic habitat ”. Proc. I.B.P. S y m p . Amsterdam and Nieuwersluis. 10-16 Oct. 1966, 314-322. N.V. Noord-Hollandsche Uitgevers Maatschappij, Amsterdam. Tait, R. I.and Howe, M. R. (1968). Some observations of thermo-haline stratification in the deep ocean. Deep Sea Res. 15, 275-280. Teal, J. M. and Carey, F. G. (1967). Effects of pressure and temperature on the respiration of euphausiids. Deep Sea Res. 14, 725-733. Vaccaro, R. F. and Jannasch, H. W. (1966). Studies on heterotrophic activity in seawater based on glucose assimilation. Limnol. Oceanogr. 11, 596-607. Vinogradov, M. E . (1962). Feeding of the deep-sea zooplankton. Rapp. P.-P. Rdun. Cons. perm. int. Explor. Mer, 153, 114-120. Vinogradova, N. G. (1962). Some problems of the study of deep-sea bottom fauna. J . oceanogr. SOC.Japan. 20, 724-741. Wangersky, P. J. (1965). The organic chemistry of sea water. Am. Scient. 53, 358-374. Wangersky, P. J. and Gordon, D. C. (1965). Particulate carbonate, organic carbon, and Mn + + in the open ocean. Limnol. Oceanogr. 10, 544-550. Webb, K.L. and Johannes, R. E. (1967). Studies of the release of dissolved free amino acids by marine zooplankton. Limnol. Oceanogr. 12, 376-382. Williams, P. M. (1967). Sea surface chemistry: organic carbon and organic and inorganic nitrogen and phosphorus in surface films and subsurface wat>ers. Deep Sea Res. 14, 791-800. Wheeler, E. H. (1967). Copepod detritus in the deep sea. Limnol. Oceanogr. 12, 697-701. Wilson, A. T. (1959). Surface of the ocean as a source of air-borne nitrogenous material and other plant nutrients. Nature, Lond. 184, 99-101. Wilson, R. F. (1961). Measurement of organic carbon in sea water. Limnol. Oceanogr. 6, 259-261. Wood, E . J. F. (1956). Diatoms in the ocean deeps. Pacif. Sci. 10, 377-381. Woodcock, A. H. (1944). A theory of surface water motion deduced from the wind-induced motion in the Physalia. J . mar. Res. 5, 196-205. Woodcock, A. H. (1948). Note concerning human respiratory irritation associated with high concentrations of plankton and mass mortality of marine organisms. J . mar. Res. 7, 56-62. Wright, R. T. and Hobbie, J. E. (1965). The uptake of organic solutes in lake water. Limnol. Oceanogr. 10, 22-28. Wust, G. (1955). Stromgeschwindigkeiten im Tief- und Bodenwasser des Atlantischen Ozeans auf Grund dynamischer Berechnung der Meteor-Profile der Deutschen Atlantischen Expedition 1925127. Deep Sea Res. 3 (suppl.), 373-397. ZoBell, C. E . (1946). “Marine Microbiology”. 240 pp. Chronica Botanica, Waltham, Mass. ZoBell, C . E. and Morita, R. Y. (1956). Barophilic bacteria insome deep sea sediments. J . Bact. 73, 563-568.

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ESTUARINE FISH FARMING

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.. . . A. From Primitive Fish-corral t o Fish Farm . . . . .. B. Definition of Estuaries as Sites for Fish Farms .. . . Suitability of Estuaries as Sites for Fish Farms . . A. Their Topography . . .. . . .. .. .. B. The Fertility of Estuaries .. .. . . . . . . .. .. The Species Cultured . . .. .. .. . . .. .. A. Selection of Organisms by Salinity . . .. .. .. B. The Natural History of the Species . . .. .. .. Sources of Young Fish and Prawns . . .. .. .. .. .. A. Non-breeding and Artificial Breeding .. .. .. B. The Fish Fry and PrawnFry Industry .. .. C. Care and Rearing of Fry .. .. .. .. The Food of Cultivated Fish and Prawns . . .. .. .. .. A. Chams, Grey Mullet, Eels, Tilapia and Prawns .. .. B. Culture of Algal Pasture . . .. .. Management of Braskish-water Fishponds .. .. .. A. Tilapia . . .. .. .. .. .. .. .. .. .. .. .. B. Russian Limans C. Hawaiian Fishponds . . . . .. . . .. . . .. .. D. Brackish-water ponds a t Arcachon . . .. .. .. E. North Italian Lagoons .. .. . . .. F. Bheris of West Bengal .. . . . . .. .. .. G. Prawn Ponds of Singapore . .. .. . .. .. H. Fish and Prawn Culture in Paddy Fields I . Chams Culture in Java .. .. .. .. .. . . .. J. Chams Culture in the Philippines . . .. K. Fishpond Management in Japan . . .. .. .. L. Fish Culture in Taiwan . . . . .. .. .. .. .. The Rate of Fish Production .. .. .. .. Profitability . . .. . . .. .. . . . . .. A. Need'for a Large Pond Area . . .. .. .. B. The State of the Industry-Progress, Stagnation. and Decline C. Need for Long-term Credits . . .. .. .. .. I s There a Future for Estuarine Fish Farming? . . .. .. References .. .. .. .. .. .. .. . .

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I. INTRODUCTION A. From primitive ,fish-corral to fish farm A comparative study of brackish-water fish culture shows all gradations from the most primitive fish-catching devices t o advanced culture operations, and it is difficult to say at what point capture ends and culture begins. For instance, stone or rock barriers to catch fish have been used for millennia by primitive man the world over. These are just walls of stone or rubble, usually built on a beach in the form of a semicircle 119

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with the open side facing the land. Fish and other edible animals which come up on the rising tide, and pass over the low barrier wall to continue their feeding, may be stranded behind it as the tide falls, and can be easily picked up. The barrier is of loose structure, so that the water can easily pass through it as the tide rises and falls. Such fish-corrals have been described by Hornell (1950) and there are even traces of them in Britain (Davis, 1923). Culture does not occur in such cases, since the fish are retained behind the barrier for the duration of the falling tide only, and are removed before the tide rises again. The barrachois of Mauritius are slightly more elaborate and permanent versions of the fish-corral (Hornell, 1926). I n Mauritius, there is only a small rise and fall of tide. A wall of coral rubble is put across the mouth of a small bay or creek ; in this wall are one or more gaps, closed by removable grilles. Through these, and the porous walls, the water in the barrachois is renewed with each tide, but the fish are barred from escaping. When these barrachois were in use, they were stocked with fish seined from the neighbouring lagoon; there was no selection of the fish nor were any measures taken to improve their rate of growth. The predictable result was that the few fish ultimately produced were the predators, chiefly Barracouta. On a much larger scale are the tidal fishponds of Hawaii. These are very large enclosures (up to 250 acres each*) bounded by walls of basalt rock, and equipped with sluice gates (Cobb, 1901). When Cobb wrote his account there were some 3 217 acres of these ponds still in active use, chiefly on Oahu. The gates were opened at favourable times of the season and tide to take in fish, especially young Chanos and mullet. When enough fish had entered, the gates were closed to prevent their escape, but the water could be freely renewed through the porous basalt wall. If insufficient fish had been taken, the pond operator would engage fishermen t o catch young Chanos and mullet to place (alive) in the pond. The fish would grow for some months until they had reached commercial size, feeding on the resources of the pond, so that, though culture measures are almost non-existent, these enclosures come near to the definition of fish farming. Another line of evolution is the pond enclosed by non-porous walls of earth. A simple case is the pupukan of Luzon, in the Philippines. This is a small earth enclosure with an area of about 2 hectare, which has a wooden or bamboo screen gate. A mixture of transient or migra-

* Weights and measures are given as quoted by the author. For convenience the following conversions are supplied. l l b = 0 * 4 5 kg; 1 kg=2.2 lb; 1 quintal (qt)=100 kg; 1 acre=0.405 ha; 1 ha=2.47 acres; 1 Ib/acre=1.12 kg/ha; 1 kg/ha=0.89 lb/acre.

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tory species such as Scatophagus, Tarpon, Epinephelus sp., Teuthis sp., Mugil cephalus L. and Lixa macrolepis (Blkr) is allowed to enter the enclosure on the rising tide, and is retained when the gates are shut. The fish are kept for 6-8 months, feeding chiefly on the resources of the pond, but are given some supplementary food if necessary. I n view of the list given above, the harvest must consist mostly of predators. These simple and inexpensive ponds are the predecessors to the large areas of fully-embanked pond-systems of the Philippines, Java, Taiwan and Italy, in which a true fish culture takes place. Intermediate in position are the Russian and Rumanian limans in the Black Sea. As Antipa (1937) has pointed out, the action of waves and currents on the north-west coast of the Black Sea (following a natural law by which seas try to rectify irregularities in their coastline) has set up long sand-bars which close off bays and small estuaries (limans). These are used for raising fish, the Russims referring t o them, in fact, as fish (mullet) farms. A channel connecting the enclosed lagoon with the sea is maintained through this bar by dredging and revetting. As the sea tries to restore the bar, as much as two thirds of the cost of the fishery exploitation of these limans is spent on keeping open the channel, which may be an artificial one (Ilin, 1954). Young fish, chiefly golden grey mullet, Liza aurata (Risso), enter the lagoon in spring, but when they try to return to the sea in autumn they are caught in traps placed in the channel. The valli of the north Adriatic are operated in the same way, and in both cases fish which, at the end of the growing season are still too small to be marketed, may be kept over winter in hibernacula t o continue their growth in spring. Another industry which comes close t o fish farming is the use of traps in some of the Mediterranean lagoons. Belloc (1938) describes the fishery a t Biguglia in Corsica. This lagoon has an area of 1 500 hectares, and has only one effective entrance, which is kept open by groynes and by dredging. Near the entrance is a barrage made of stout posts driven into the bed of the lagoon, which is very shallow, and this barrage has gaps through which, in the spring, fish swim in from the open sea. At the beginning of summer, these gaps are closed. The trapped fish continue t o grow fast in the very good feeding conditions. During the summer, some fishing is done with various kinds of net, but the chief fishery is in autumn, when the fish seek to return to the sea. The gaps in the barrier are now furnished with elaborate traps in which the fish are caught. The fish will represent a greater weight a t capture than on admission, but the growth will be a t the expense of the natural fertility of the lagoon, and fish culture is hardly involved,

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though the results are impressive. The barrier of posts, and the traps, are derived from a very primitive fishing device called a fish fence. A further evolution is the now-superseded semi-arginate valle of the north Adriatic, in which the fish were enclosed within palisades to grow ; and also the great pounds, made largely of netting supported on concrete piling, in which the Japanese cultivate intensively the yellowtail (Seriola),puffer (Fugu),and prawn. The free access of water allows a far greater weight of fish than could possibly be supported by the natural fertility of water and soil, so intensive feeding is done with cheap trash fish. The final stage in the evolution is the floating cage in which the fish are very intensively grown, and fed artificially, and in which the water plays no part except to provide living space and oxygen, and to remove waste products. With this method the natural fertility of the estuary is not used. Pillay (1966a) has published a useful bibliography of brackishwater fish culture. I n this article, the culture of molluscs will not be treated, but only that of fish and prawns.

B. Definition of estuaries as sites for fish farms A recent definition of an estuary is “ a semi-enclosed coastal body of water having a free connection with the sea, and within which the sea water is measurably diluted with fresh water derived from land drainage. . . . Associated with an estuary are transition zones, salt marshes, coastal marshes, intertidal areas, sounds, and other coastal water areas, plus the vital tidal fresh water habitats above the upper limits of salt water intrusion, so important as spawning and nursery areas for many anadromous species ” (quoted by Smith, 1966). A rather wider definition of an estuary is, “ a n environmental system consisting of the estuary and those transitional areas constantly influenced or affected by water from the estuary ”. For example, fine silt carried down by a river may be deposited by coast-wise currents beyond the strict geographical limits of the estuary, and may lead to accretion of land where conditions are suitable. These definitions are more applicable to north temperate conditions than t o tropical or sub-tropical conditions. Day (1967) describes the St. Lucia Estuary in South Africa. I n summer, there are floods and low salinities, while in winter the rivers cease to flow, and the headwaters of the estuary may then become more saline than the sea. d’Ancona (1954) writes that all littoral lakes undergo variations in salinity due to fresh water run-off and evaporation. Hardenberg (1950) thought that in the conditions of south-east Asia estuarine conditions

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could extend far out to sea, depending on the strength of the river outflow. I n this wider definition, the word estuary can be applied to the lagoons of the Adriatic, now the site of an important fish culture industry, and t o many Mediterranean lagoons in France, Spain, and Tunis, and in fact to almost any kind of coastal water-bodies in permanent or intermittent communication with the sea. I n the Black Sea are the Russian limans, a word translated in the dictionaries as " estuary " though liman refers to a wide range of inlets mostly cut off by sand bars. Some have a permanent connection with the sea, others had such connections in historical times and were in use as seaports (Ilin, 1954) but are now in direct communication with the sea only when flood or spring melt-water breaks through the bar, or when the bar is breached by storms or changes of water level caused by the wind. Still other limans may be connected with the sea only through seepage through the sand, and in these tha salinity rises so high in summer that salt will crystallize out. Such limans can only be kept a t a range of salinity suitable for fish culture by making and maintaining a permanent artificial connection with the sea. Even so, their salinity may rise t o 50%, which is nearing the limit for fish life. It should still be possible to speak of an estuary even when the volume of fresh water is small in comparison with that of sea water. Small as this may be, it may still attract migrating fish such as the salmon, and would justify those who hold that the estuary should even include areas of continental shelf affected by estuarine waters. Estuaries, in this wide sense, are the actual or potential sites for fish farms, both because of their topography and of their fertility. These will be discussed in turn. The total area of brackish-water fish farms is far from negligible. SOfar as can be ascertained from the literature, the approximate areas are as follows: TABLEI Hawaii (Cobb, 1901) India (Pakrasi et al., 1964) Arcachon (Arn6, 1938) Italy (Beadle, 1946) Philippines (Rabanal, 1961) Java (Schuster, 1952) Celebes (Schuster, 1952) Sumatra (Schuster, 1952) Taiwan (Lin, 1968) Elussia, Black Sea (Ilin, 1954) Totals, approximately

3 217 acres 2 2 2 3 0 ,, 741 ,, 2 4 7 0 0 0 ,, 2 9 6 4 0 0 ,, 2 0 0 0 0 0 ,, 50 000 ,, 9 5 0 0 ,, 39 520 ,, 101 270 ,, 969 900 acres

1 300 hectares 9000 ,, 300 ,, 100000 ,, 120000 ,, 80970 ,, 20240 ,, 3 850 ,, 16000 ,, 41 000 ,, 392 660 hectares

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11. SUITABILITY OF ESTUARIES AS SITESFOR FISHFARMS A. Their topography 1. Enclosed nature

The generally enclosed nature of estuaries, and especially the presence of bars or middle grounds, ensure fairly well-sheltered water with resulting absence of heavy surf liable to damage the farms. An exception is the liman of the Black Sea, where the natural sand bar which defines the lagoon faces the sea and is liable to be damaged and eroded with the mass-transport of sand.

FIG.1. Repairing the banks in a Javanese fishpond. Note shallowness of water, and sluice gate with turnbuckle, screened against the escape of fish. Main feeder canal t o left, with a wading cast-net fisherman.

Even in enclosed estuaries, erosion due to the rise and fall of tide, to flooding, and the strong currents associated with them, and to the ceaseless lapping of small waves, may entail much upkeep, such as, for example, rebuilding and revetting embankments (Fig. 1). This is the more so, because a close cover of plants, such as can easily be grown on the banks of fresh water ponds, is not always possible on the embankments of saline or brackish ponds.

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2. Accretion of soil

A further favourable factor is the transport into the estuary, by its rivers, of soil brought down from the watershed. The thousands of tons of material become sorted out in the estuary ;the coarser particles are deposited in the upper deltaic areas (and may be responsible for delta formation) while the finer clay part,icles start to settle by flocculation where the river water becomes mixed with sea water. The process is well described by Schuster (1952). These clay deposits gradually rise t o mean high-water level, where they form mud banks which are exposed a t low tide. On these banks vegetation starts t o grow. At first these are lowly forms such as filamentous algae and diatoms, many of which secrete mucous sheaths and films which help to bind the mud surface, just as, on the land, algae such as Nostoc may play an important part in land reclamation, binding the surface of soils, and contributing organic matter and nitrogen to so important a degree that their growth is encouraged by tilling (Round, 1965). At a later stage in the formation of mud banks, salt-tolerant higher plants (especially mangroves in warmer latitudes and grasses such as Spartina, low semi-recumbent plants such as Suaeda, (the samphire) and Ruppia in temperate climates) become established and entrap and hold yet more of the drifting silt, until the mud bank rises above mean high tide level. Then many other salt-tolerant plants can become established, and the mud flat becomes a salt marsh or mangrove swamp. I n this way, extensive areas of flat ground arise, in a certain relation to tide levels, and with a basis of clay especially suitable for making firm and impermeable embankments. The rate of accretion of soil may be considerable. Schuster (1952) estimated that in the area of the estuary of the Brantas River on the north coast of Java, the rate of increase of newly-risen ground suitable for pond construction may be as much as 26 yards annually. I n estuaries in West Africa and South America, the formation of mudbanks, their rise to high tide level and their colonization with mangroves to form islands, is happening so fast that banks and middle grounds charted in maps of only a few decades ago are now mangrove forests. The process may be hastened by the rapid increase in human population, which always causes a need for more land. The felling of forest cover and the cultivation of the new land leads to erosion which hastens the transport of soil down t o the estuaries, and so to more rapid mud bank formation.

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New estuarine environments can be the result of movements and changes in the level of the land. Estuaries may be drowned river valleys in which subsequent silt deposition proceeds apace. Again, the land may slowly tilt and so become submerged. Taiwan, for example, is tilting to the east-ward so that the flat land on the west coast is slowly rising (Lin, 1968). Over the centuries, the present salt flats on the west coast, on which there are important brackish-water fish farming industries, will rise above sea level to the point where they will become free of salt and fit for agricultural use, while new accretions of land to seaward will be reclaimed for fish farming. I n the northern Adriatic, vast engineering works were undertaken by the Romans, and, later, by the Venetian Republic, to prevent the silting up of the lagoon which protected the city from her foes and carried her sea-borne commerce. These works also resulted in marsh and lagoon formations which are now the sites for a large fish farming industry (Fig. 11, p. 183). 3. T i d a l conditions

Some movement of sea water, due to changes of level, is important in brackish-water fish farms. On non-tidal seas such as the Black Sea, there are seasonal changes of level due to evaporation, and both seasonal and longer term changes of level due t o the wind. These changes may exceed one metre in the Black Sea (Ilin, 1954), and be sufficient to cause currents to flow into and out of the limans through their natural or artificial channels t o the sea. I n the northern Adriatic there is a natural tide which may exceed 110 cm, though the tidal amplitude becomes much less in the more southerly Adriatic. Such small changes of level are not enough t o allow for a complete drainage of the ponds or limans, and this must be a factor in their modest rate of production per unit area. Where the estuary is truly tidal and has more constant and regular changes of water level, these can be used to fill fishponds ; to top them up as may be required in order to replace water lost by evaporation and seepage during the growth of the fish crop; to empty them as needed in order to sort out, count, or harvest the crop ; and to expose them to sun and wind and tillage. The inflowing water carries with it nutrients, silt, and detritus, which fertilize the pond and by frequent changes of water keeps the salinity under control. Therefore, it is of the first importance that estuarine fishponds should have an assured supply of sea water (Schuster, 1952; de Angelis, 1960), so care must be taken that they are planned with due consideration of tidal data at the site. Schuster

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(1952) considers that the most suitable level for the floor of a fishpond should be about sixteen inches above the level of mean high-water springs. It then becomes possible to fill the ponds during the hours in which sea level is higher than the floor level of the pond. Conversely, the ponds can be completely drained during the hours when sea level is below that of the floor of the pond. Schuster gives a table which shows that, in the years 1937-1941, the smallest number of hours in any month during which such ponds could be filled was two in September, 1937 (none in February, 1937), and the greatest number was 60 hours in May, 1938. He also shows that, where the level of the pond is too high (110-130 cm above mean sea level) the filling of the ponds can be done for only 11; hours per month, on average ; whereas where the level of the pond bottom is 80100 cm above mean sea level, the ponds can be filled for 32 hours per month, on average. Schuurman (1964) considers that the water of a brackish-water pond should be renewed a t least once every ten days. To maintain the ponds at the optimum depth of 40 cm, to change the water as required and to replace water lost by seepage and evaporation, the pond must be sited so that the tide regularly exceeds a height of 40 cm, above the level of the pond bottom. To get this result, it may be necessary to excavate the pond bottom so as t o adjust its level in relation to the tide. However, to lower an area of, say, 5 hectares by 10 cm involves moving some 5 000 cubic metres of soil. As this may have t o be done by hand labour, where the soil is too soft to bear earth-moving equipment, the cost will play a major part in determining whether the exploitation is practicable. I n fact, a height difference greater than 40 cm, would have to be allowed for. Except where the pond directly abuts on the sea, the sea water must be brought along a canal, which may also have to supply other ponds. Also, each pond will draw its water from the canal through one or more gates whose total area will be small in comparison with that of the pond. The loss of head ” on both these counts could be substantial, and would have to be allowed for in considering levels. A notable difficulty in the efficient working of large areas of brackishwater fishponds has been to keep the sea water supply canals clear, and their depth in correct relation with the tidal movements and so with the level of the pond bottoms. The inflowing estuarine water may carry with it a large load of silt, which may be deposited in the canal at times of slow flow, The bheris, or estuarine fishponds of West Bengal, are in danger of disuse through the siltation of the feeder canals (Pillay, 1954 ; Pakrasi et al. 1964) and clearance would be very ((

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costly. Entire pond systems may be jeopardized by siltation, and in Java it was necessary to introduce legislation to enforce the upkeep of the canal system and other waterways. As a result, says Schuster, great changes for the better were seen. Rabanal (1962) writing of conditions in the Philippines, advises sites which have an elevation between - 1 and +4.5 ft above mean low water as being most suitable for brackish-water fishponds. At greater elevations, between +4.5 and + 7 ft, ponds can only be made suitable by excavation, which is costly, because otherwise they will only be filled with sea water at extreme high tides and therefore at rare intervals. Conversely, sites on low levels between - 1 and -2 f t would become suitable only if filled in, while sites below -2 ft are unsuitable because they could never be completely drained by gravity. Lin (1968), writing of the brackish-water complexes in the south and west of Taiwan, thinks that the ideal site is one where an extensive tidal flat is covered at high tide to a depth of at least 60 cm, and is wholly exposed at low tide. Even after the building of embankments and feeder canals and sluices, this will still allow the optimum depth of 30-40 cm to be maintained in the ponds. So far, the situation of ponds has been considered in relation to irrigation by gravity. However, by the use of pumps, an artificial head of water can be created which would make the siting of ponds independant of tide levels and possible in tideless estuaries. Many fresh-water fish farms make use of pumps, and where the ponds are large and highyielding, pumping is economical or even cheap (Hickling, 1962).

Pumping Generally speaking, the yield of brackish-water fishponds is one half or less that of fresh-water ponds, so that in their case the economy of pumping is more doubtful. Lin (1968) considers that pumping would be uneconomic in Taiwan, even though the rate of fish production is the highest in the world’s brackish-water pond industries. Schuurman (1964) is also doubtful of the technical and economic aspects, since the equipment must be technically reliable for salt water, and must also be inexpensive to buy and operate. The pump would have to fulfil two requirements, namely, to fill the pond at the start of the exploitation period, which would call for a rapid rate of pumping, and thereafter to keep the pond topped up t o make good seepage and evaporation. Schuurman considers, as an example, a &hectare pond, to be filled to a depth of 40cm and kept at that depth with a pump which must work against a head of two metres. He finds that a 6 hp pump would satisfy both requirements, since it would fill the pond with 48 hours 4.

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of continuous pumping, yet also make good losses of 0.5 cm/day in only half an hour’s pumping. Over an assumed exploitation period of 180 days, expenses would be the cost of 276 litres of fuel, plus an allowance for depreciation. The fuel should be cheap, since many countries allow a drawback of duty on fuels used in agriculture. Certainly, just after the last War, the possibility of opening up new

FIG.2. Main sea water supply canal to a pond complex in Taiwan. Note prawn traps, ponds on the left with store house, ponds on the right with bamboo windbreak. Note the massive peripheral embankments on either side of the canal compared to the small embankments between the ponds on the left.

areas for brackish-water fish culture, based on large units supplied with sea water by pumping, was being seriously considered in Java. There is one special case where pumping is considered t o be economical. de Angelis (1960) states that none of the valli of the north Adriatic is in direct communication with the sea. All depend on a network of distributory canals. Yet the maximum tidal range is only 118 cm, so that there is no strong surge of sea water in the canals, but rather a slow drift, with the more saIine water running along the bottom. Sea water is considered essential to the fertility of the ponds ; t o allow this to reach some of the valli, pumping stations have been built which,

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at high tide, draw water from the bottom of the canal, where the salinity is highest, thus creating, as de Angelis says, an artificial tide. 5. Construction of the ponds

Most of the existing brackish-water ponds were put up in days gone by with cheap hand labour, or even, as in Hawaii, with forced labour. Nowadays, pond construction has become very expensive.

FIG.3. Embankment between two brackish- water Chanos rearing ponds in Taiwan. Note rice straw revetting on leeward side of the bank and the scum of detached blue-green algae.

Lin (1968) states that in Taiwan, where brackish-water fish culture is now most advanced, the first job t o be done is t o build a high and strong protective embankment around the entire site. It should be high enough to cope with any storm surge and strong enough to withstand any strain. Lin mentions a height of 3-5 m, with a slope of 1 :3 or 1 :4. The width at the top should be 3-4 m and carry a road or footpath. The width at the base should be 24-45 m. This storm dyke is therefore a very substantial structure, as this writer has seen for himself (Figs. 2 and 15). The slopes of the dyke may be protected with grass, or may be revetted with stone or brick (which is more costly). However, as some offset to the expense of the storm

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dyke, the dykes dividing the enclosed area can be very low, since they donot have to face large waves (Figs. 3 and 10). The small waves which are encountered are rendered harmless to the dykes by pegging rice straw on the leeward banks (Fig. 3). The level of water in the distributory canals, and therefore in the ponds, is controlled by sluices in the main storm dyke. Because the dykes are low, the productive area of the ponds is a high proportion of the area enclosed by the storm dyke. Lin sketches an ideal layout (Fig. 5 ) , showing that 94% of a pond area of 20 hectares could be allotted to productive ponds, and only 6% to canals, nursery and wintering ponds, passageways and refuges. The sluices in the storm dyke are substantial structures made of concrete or brick, and are important items in capital costs, but the sluices between the ponds can be cheap wooden slats sliding in grooves in small concrete or brick posts (Fig. 10). I n the Philippines, earth-moving machinery can be used in making the 3 000 hectares of new fishponds which are annually added to the country’s resources. I n Java, according to Schuster (1952), hand labour has been used for pond construction but this will have to be changed, since “ the costs of local labour do not permit profitable execution of such activities in the old-fashioned way ”. Mobile teams equipped with modern machinery will have t o carry out the work, and Schuster thinks that, in spite of many difficulties, the importance of this kind of work is too great to be indefinitely postponed. I n Java, the construction of a brackish-water fishpond begins with the excavation by hand of a ditch 3-5 yd wide to encircle the periphery of the future pond. The excavated soil is thrown on the outside so as to form a protective dyke (Fig. 4). At this stage, sluices are placed in position in gaps in the dyke; their dimensions may vary, and costs depend on whether they are made of wood, brick or, concrete. Moreover, in a soft soil, heavy sluices would have to be supported on piles, and though local mangrove wood could be used, this would be an additional cost. The soil moving may be done on contract by itinerant gangs of specialist workmen, but Schuster says that it is usual for the completion of a pond system to be extended over many years, as money becomes available to be ploughed back into the business. From a sample survey, Schuster estimated that only about 5 % of the total vast area of ponds on Java could be regarded as finally completed. No less than 8.7% was occupied by embankments, and 21% was “ high ground ” (that is, incompletely excavated so that it was not covered by water). Thus, Schuster estimated that the nominal area of some 200 000 acres occupied by the fishponds represented

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only some 145 000 acres of productive pond. By completing the construction of the existing ponds and deepening them, where necessary, to ensure a depth of water of at least 1-5ft, the ponds would give a far greater crop. Schuster thinks that this should, as a matter of common sense, take priority over the construction of new ponds. Schuurman (1964) gives a cross-section of a pond, showing that the height of the embankment must be at least one metre above the highest

FIG.4. The first stage in the building of a brackish-water fishpond in a mangrove forest in Borneo. Slabs of mud are heaped to make an embankment. There is a borrowpit full of water on the left.

normal flood level. The amount of soil needed for this can usually be provided from the soil excavated to level the pond bottom and from the perimeter ditch. I n Fig. 5 an “ improved Porong ” type of Javanese brackishwater fishpond is drawn (after Schuster) with a sketch of a pond system in Taiwan for comparison (after Lin). The more complicated layout of the Taiwanese ponds is partly due to the need for wintering ponds (not required in Java) and to ‘‘ passage ways ” in which the fish growing in the rearing ponds take refuge when the ponds are drained. I n the bheris of the Ganges Delta (Pillay, 1954),the main embank-

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ment which separates the ponds from the river branches may be 6-8 ft high, 10-12 ft wide a t the base, and 6-7 f t wide a t the top. The soil is obtained from the borrow pit on the inside of the embankment, which makes a deep canal 4-5ft below the level of the pond floor. There may be several compartments within the peripheral embankment. Pakrasi et al. (1964) state that there may be small nursery ponds where the young fish are kept for a period. The same ponds may, after

" 1 -I

0

A

B

FIG. 5. Plans of (A) a brackish-water fishpond system in Taiwan (after Lin), and (B) " improved Porong " type brackish-water fishponds on Java (after Schuster). (a) Rearing ponds, (b) nursery ponds (including small '' baby boxes "), (c) main distributing and collecting pond (Java), (d) wintering ponds (Taiwan), (e) passageways (Taiwan), (f) distributory canal (Taiwan), and (8)distributory and passageway (Taiwan).

harvest, be used as store ponds for the marketable fish awaiting transport to market. The bheris are impounded tidal mud flats and are generally shallow, from 60 cm t o 1.5 m, but about 1 m on average. The prawn ponds of Singapore (Hall, 1962) have a maximum depth of 7 ft where the dyke crosses the original channel, but elsewhere are about 4 f t deep a t high tide a t the deep seaward side, tapering off to a few inches at the landward side. These ponds are situated on lowlying flat tidal swamps, and though their main produce is prawns, fish are a useful by-product. The size of the ponds varies from 5 acres to 50 acres, and the banks are on average about 4 f t high, 3 f t wide a t the top, and 8 ft wide a t the base. There are several sluice gates, one or

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more of which may be used for fishing as well as for the exchange of water. Generally speaking, brackish-water fishponds are shallow, in recognition of the fact that in estuaries the benthos is the chief primary source of food and not the plankton ; therefore high and costly banks are not usually needed except for the perimeter flood dyke. The banks separating the brackish-water fishponds of Hong Kong are 8-10 f t high, but this is to enable as much rain water as possible to be collected during the season. These ponds are only very slightly brackish (Ti Chow, 1958), and do not normally exceed 1.4 chlorinity per thousand. They rely on rainfall, and this slight brackishness is due to salt in the soil since the ponds are on land reclaimed from salt marsh. The marine fishponds on the Biscay coast of France were put up two centuries ago and there seem to have been no additions since. As described by Arne (1938), the 300 hectares of ponds are surrounded by a strong perimeter dyke, 6 m wide at the top and carrying a roadway; the seaward slope of the bank is 11.5 m long and revetted with fascines. The inner banks are grassy. A deep ditch around the inner side of the banks is doubtless the original borrow pit, but is also the “ deep ” where the fish may shelter in cold weather or too hot weather. Apart from the “deep”, the pond is very shallow, only 40-50 cm, and Arne says these shallow areas warm up quickly and grow the maximum amount of useful food for the fish, which are chiefly grey mullet and eels. The Russian limans, though often of very large size, are not subdivided by embankments into ponds. Cobb (1901) writes that one of the largest of the original ponds on Hawaii was built by the forced labour of the people of a local king, who made them pass lava blocks from hand to hand to build the walls of the pond. These ponds stand on coral reef flats, so excavation seems unnecessary or impossible. In the upper deltaic parts of great estuaries such as that of the Pearl River in Kwangtung Province of China, there may still be a large rise and fall of tide even though the water is wholly fresh. These changes of level are used to operate huge fishpond systems which are of great antiquity, and which, covering 60% of the surface of a large delta, are probably the most extensive in the world. These ponds can be completely emptied at low tide and refilled at high tide to a depth of several feet. They are stocked with fresh-water fish, and may also be used alternately as ricefields. As the techniques of fish culture are those of intensive fresh-water fish farming, they will not be further considered here. Similar regions at the head of the deltas of great rivers such as the Niger might offer similar possibilities.

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6. The harsh estuarine physical environment

The estuarine environment has been described as “ harsh ”, especially in respect of rapid changesin physical factors such as temperature, salinity, and oxygen content. Only rather a narrow group of fish and other organisms can flourish there, and, of the fish, only a few species are also acceptable food fish, and so profitable for fish farming. Rapid changes of salinity are self-evident where sea water and fresh water are mixing, and where evaporation on the one hand and flooding on the other may cause extreme fluctuations. Rapid changes of temperature may be caused by the tide rising over flats heated by the sun or chilled by severe frosts or cold winds. Rapid changes of oxygen may be caused by water flushed out of reed beds or polluted with organic matter, or which has passed over beds of green vegetation actively photosynthesising in bright sunshine. When such waters are impounded in ponds, there will still be diurnal changes in temperature and oxygen content. If the impounded water is too deep and there is no wind, stratification may set in, leading to a deoxygenated layer of bottom water and the death of fish and other organisms. In the Italian valli, which are rich in nutrients, this stagnation and oxygen deficiency commonly accompany high productivity (d’Ancona, 1954). The control of salinity is achieved by having a system of freshwater canals, with branches to each pond, as well as sea water canals. Schuster advises that, in the Javanese ponds, salinity should be maintained between the limits of 10 to 35%, by regular replenishment with new water. Too high a salinity diminishes the quality of the food grown in the ponds as well as harming the fish. Salinity tolerances will be discussed later, but here it can be said that the most important fish able t o cope with these harsh conditions are the Chanos (Fig. 8), a silvery-white herring-like fish very popular as food throughout its range which is the tropical Indo-Pacific; the Grey Mullets (Fig. 8) (species of Mugil and Liza, but chiefly M . cephalus), fish of temperate as well as tropical and sub-tropical waters ; and eels, Anguilla japonica (Temminck and Schlegel) in the East, and A . anguilla L. in Europe. The penaeid prawns (Fig. 8) are also notably euryhaline and are a very important product of brackish-water fishponds in the tropics. 7. Intensive fish culture in cages

The sheltered conditions offered by estuaries have made possible the intensive culture of fish and prawns in open nets and cages. For example, the Hitsuishi fish farm in the Inland Sea of Japan makes use of a channel between two islands, one end of which is closed by a con-

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Crete wall equipped with a sluice gate, and the other by a net barrier which is no less than 350 m long, and is supported on concrete posts stayed to concrete anchors. I n this netting enclosure, young Yellowtail (Seriola quinqueradiata Temminck and Schlegel) are very densely stocked with a view to rearing them t o commercially saleable size in nine months. The naturally-produced food would be too scarce for even the maintenance of such a press of young fish, so chopped trash fish and shrimps caught by trawlers are fed to the growing yellowtail. I n this case, the water and benthos contribute little or nothing to the crop of fish, aside from providing living space and oxygen. The oxygen regime of this farm was studied by Inouye et al. (1966). The enclosed water area was 7.2 x 104 m2 at high water springs, and 6.0 x lo4 at low water neaps. The corresponding water volumes were 22.7 and 8.7 x lo4 m3. Evidently, at low tide the fish had at their disposal only one third of the volume of water at high tide ; and, because of the risk of suffocation at such a time, the rate of stocking recommended was only such as could be held safe at low tide. No advantage could be taken of the greatly increased volume of water at high tide. It was recognized that, if economical means could be found to aerate the water at low tide, the enclosed area could raise a much greater biomass of fish. The " kuruma prawn, Penaeus japonicus Bate, has been raised in the same way, and also fed on small shrimp and trash fish caught by commercial trawlers, and fed to the prawns t o the extent of 5-10% of the weight of prawns in the pond per day. But, as with the yellowtail, the reduced volume of water in the netted enclosure at low tide, limits the rate of stocking and so the profitability of the prawn raising (Hudinaga and Miyamura, 1962). Because of this difficulty of changing volumes of water as the tides rise and fall, very intensive cultivation of fish and prawns in floating cages moored to the sea bed is beginning. This technique has long been used in fresh water (Hickling, 1962) by the Japanese and is now being adopted by the Russians for growing fish in the cooling ponds of power stations. In sheltered situations in the Inland Sea of Japan, cages made of synthetic netting are supported on bamboo frames floated on oil drums. Lines from each of the bottom corners of the cage of netting are attached to weights on the sea bottom; these and the bamboo frames keep the cage in shape. The mesh of the netting must obviously be small enough to retain the fish when first stocked, and a single cage may have an area of 100 m2 and a depth 4-5 m, or say a volume of 400-500 m3. The fish most cultivated is the yellowtail, but the puffer fish, some parts of which are toxic, is also grown ))

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FIO.6. A raft of floating net-cages for fish culture on a n intensive scale. (Japan). (Photo : Professor Nakamura.)

FIG.7. Detail of floating net,-cage; note raised peripheral net to prevent the fish from escaping by jumping. (Japan). (Photo : Professor Nakamura.)

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intensively. The fish are fed on chopped trash fish, and because the cages are always well off the sea-bottom, the crop is less likely t o be lost through suffocation than in the enclosure. These fish-rearing cages are not operated singly but in batteries of 10 or more (Fig. 6) ; walkways along the framework between the two rows of cages allow service access, and the raft niay include a store and shelter. The entire outfit, though regarded as something of a novelty, seems much to resemble the very large wooden rafts in Brittany, where live lobsters and crawfish are stored in wells in free or pumped communication with the sea. Thousands of crustaceans can be held in good condition in these rafts. The present trend with these intensive fish rearing cages in Japan is to make the mesh of plastic or light metal. The high value and threatened scarcity of salmon and possibly sea trout has aroused interest in the possibility of intensive growth of these fish in captivity in sea water. This is not a new idea, as it has been tried for many years, (since 1912) with little success, but in the last few years a number of salt-water trout farms have been established. This revival is associated with the names of the Norwegian brothers Vik (Vik, 1963). Beginning in a small and amateur way, and using three small ponds filled respectively with fresh, brackish, and sea water, Vik was able t o acclimatize adult salmon from sea water to fresh water, where, as in nature, they matured. Their eggs were then stripped, artificially fertilized with milt from the males and placed in a hatchery, while the adults were passed back through brackish water t o seawater again. The spent fish, however, refused food during the winter and spring, and became very emaciated. But in May they suddenly began to feed very heavily on herring thrown into their pond. By July, when they stopped feeding again, they had fully recovered their best condition. For the second time, these mended fish were passed through the brackish-water pond to fresh water, and for the second time they spawned. So it was proved that the Atlantic salmon could be bred in captivity, and that the young so produced could be reared to full maturity without a period of free range in the ocean. A similar technique was evolved for the rainbow trout, which was also acclimatized to flourish in sea water. The fish grew fast on intensive feeding, and it was claimed that they need less food to grow faster t o a larger size than rainbow trout reared in fresh water and are also less liable to disease. But difficulties have arisen with trout reared in this way. One is that, when the trout have grown to a weight of 3 lb and more, a pro-

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portion become mature. As they are unable to shed their eggs in sea water, most become egg-bound and die, or have to be marketed at once without regard to the state of the market. As the fish are raised in cement ponds built at the water’s edge, sea water is easily available but has to be pumped. Surprisingly, the cost of pumping is given as 6-10% of production costs. On the other hand, the sea water remains warm in winter, so allowing growth to continue, whereas, in Norway, the fresh waters become very cold. Though this kind of trout farming is attractive to Norwegian operators because level ground for fishponds is so scarce, and though there has been some success, it seems that, at least as late as 1964, the industry had not got off the ground (Sedgwick, 1964). Now some Norwegian operators are rearing trout in small floating enclosures resembling, and probably inspired by, the cages in which yellowtail are raised in Japan. Control of the fish has proved difficult, and final success has been wanting. But their example has stimulated the international edible oil and animal food combine of Unilever to do some serious trials. They have established a base at Loch Ailort in the west of Scotland, and a popular account of this venture has been published by Frost (1968). Rainbow trout eggs from hatcheries in America and elsewhere were hatched out in conventional fresh-water hatcheries. The alevins were raised in the usual way in a series of concrete ponds fed by pure fresh water from the River Ailort, and given finely-minced liver as fodder. Pumped sea water was gradually admixed with the fresh water as the young trout grew, until they were fully acclimatized to life in sea water. Then they were transferred to cages floating in Loch Ailort, and intensively fed on chopped and minced white fish. The article claims growth of individual fish t o a weight of 54 Ib in slightly more than two years. The article also claims that the rate of production of fish p u l d be as high as 500 tons annually by the autumn of 1970 if the firm took the decision to go ahead. Unilever is in a stronger position than most firms to supply pelleted foods, and it seems that the success of this and other ventures, possibly such as the raising of sole (Cole, 1968), will depend on the production of a mass-produced and cheap high-protein fodder with high acceptance and digestibility. The present pelleted trout foods seem dear for the raising of table fish, and this country seems less fortunate than Japan in available supplies of abundant cheap trash fish. I n Sweden, pellets made with a protein basis of purified fish meal and casein, with kelp meal, fat, yeast and: vitamins, gave the very high rate of conversion of 1.5 :1, or even better (Carlin, 1966) when fed to young salmon, but they were expensive.

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The second condition for success will be the maximum amount of automation, in view of the very high cost of labour in this as in other countries. Carlin states that the feeding of the young salmon in Sweden is highly automated. But the intensive rearing of fish in cages, pounds or rafts makes no use of the natural fertility of the estuary, and their food represents the production of large areas external to the estuary. Rejected food, and the waste-products and excretions of the caged fish, will contribute to the fertility rather than draw from it.

B. The fertility of estuaries 1. Natural fertility

The great natural fertility of estuaries was emphasized in two symposia held in America in 1966 and 1968, by the American Fisheries Society (1966) and the American Association for the Advancement of Science (ed. G. H. Lauff, 1967) respectively. For example, Chesapeake Bay is estimated to produce at a rate of 80 lblacrelannum, and the Sea of Azov is equally productive. Zenkevitch (1963) quotes the very high figure of 100 kg/hectare/annum as the rate of commercial production of fish in the Siwash liman ; but this may refer to the liman used as a mullet farm. If the southern North Sea may be regarded as an estuary, as Korringa (1967) does, and as it was in very recent time, then in 1948 it gave a crop of fish of 52 kglhectare as compared with 26 kg/hectare for the rest of the North Sea (Kalle, 1953). Korringa (1967) states that in terms of crop per unit area the estuaries are much richer than the sea in food resources. 2. Benthic production

An interesting point about this estuarine fertility is that, unlike the open sea or lakes, where plankton is the prime producer, in estuaries the plankton plays a minor role, while the benthos is the dominant primary producer. Lackey (1967), for example, found that in estuaries benthic diatoms far outnumbered planktonic diatoms, and in most cases formed a large percentage of the organisms present. I n the Italian valli, de Angelis (1960) states that “ the physico-chemical characteristics of lagoon water and variations in these, produce a biological medium which is rich in benthos and which has an intense bottom life, yet is generally poor in plankton.” Ilin (1954) states that most of the natural fertility of the Black Sea limans is due to organogenic material accumulated on the bottom silt. To quote Hedgpeth (1967-8) “it is a functionof the comparatively shallow depth of estuaries

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and tidal flats, that the major control of the ecosystem should be that of the activity of processes on and in the bottom sediments.” I n a walled-off Hawaiian tidal fishpond, Malone (1969) found that gross primary productivity equalled 445 g C/m2/year, and of this 347 were contributed by the benthos, and only 98 by plankton. Pillay (1954) writes of the bheris of West Bengal, that the picture of biotic interaction in the ponds indicates a high demand on the benthic vegetation and a negligible one on surface plankton. It is common experience in fish culture that plankton and benthos are to a large extent antagonistic. If plankton develops and produces turbidity, the benthos is shaded out, while if the benthos is well established and flourishing, it leaves little nutrient material for the plankton. Plainly, shallow water will favour the benthos, and since the fish cultivated in brackish-water fishponds on estuaries are feeders on the benthos, the water of these ponds is shallow. When fertilizers are used, they are of the slow-acting kind which acts on the benthos : the more familiar soluble inorganic fertilizers now so successfully used in freshwater fishponds are ineffective in these shallow estuarine ponds. Estuarine fish farming is based on the exploitation of the great natural fertility of this environment by some control of the rate of stocking with fish, and some control of predators and competitors which would reduce the useful crop of fish. I n many cases, so little is done in the way of management that purists might object to the use of the expression “ fish farming ”. 3. Detritus

The fertility of estuaries is also associated with the presence of abundant detritus, and the detritus cycle plays a vital part. The estuarine ecosystem is “ a mixing region between sea and inland water of such shape and depth that the net resident time of suspended materials exceeds the flushing ” (Hedgpeth, 1967-8) “ Thus the system constitutes a nutrient trap ’,. d’Ancona (1954) ascribes the high rate of production in the brackish-waters of the north Italian lagoons to the mineralization of organic substances carried into the lagoon with the tidal current, which brings in more plankton than is removed by the outflow. Again, this is an accumulation of organic material. Detritus has been defined by Darnell (1967) as “ all types of organic material in various stages of microbial decomposition which represent potential energy sources for consumer organisms ”. For convenience, he recognizes two states of detritus, the particulate and the nonparticulate ; many forms of microbiota are associated with a decomposing substrate.

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Organic material entering the detrital system of an estuary " represents the total gross primary and secondary production of the community, exclusive of that material which is temporarily tied up in the protoplasm of producer, consumer, and decomposer species, and that material which has been oxidized to the low-energy state through respiration. Regardless of the form in which it enters the decomposition scheme, if it is not lost to the sediments it will be subsequently broken down t o smaller sizes until it reaches the end-molecule low-energy state " (Darnell, 1967-8). Brunelli (1937)points out that, in the brackishwaters of the Italian lagoons, stenohaline and stenothermal organisms die, and contribute to the fertility of the soil and that the flora and fauna of the soils of the valli are very rich in nutriment and supplement by their abundance, the poverty of the plankton. Those eurythermal and euryhaline organisms flourish best which feed on detritus a t first or second hand, such as the grey mullets among fish, mollusc-eaters such as the dorade, and eaters of small insectivorous fish and chironomid larvae, such as eels. Crustacea which feed on detritus and molluscs such as the suspension feeder Cardium, are found in great quantity. The soil abounds in shells of molluscs which assure its neutral reaction. Malone (1969) found that, in his Hawaiian fishpond ecosystem, organic matter had t o be imported, probably in the form of detritus, t o make good the deficiency of primary productivity over community respiration. The organic manure given to many fishpond systems must be effective due t o its contribution of detritus-forming material as much as t o its contribution of direct fertilizer. 4. Enrichment of detritus Odum and de la Cruz (1967-8) found that beds of Xpartina grass in the estuary they studied produced a rich supply of detritus. For example, the detritus content of the water varied from only 2 mgllitre at mid-flood tide t o 20 mg/litre a t mid-ebb ; detritus made up 90% t o 99% of the seston, plankton playing almost no part in the fertility of the estuarine water. They found, that as this detritus decayed into progressively smaller particles it became richer in protein. The fine particles had a rate of oxygen consumption seven times greater than the large particles. The small suspended particles of Spartina detritus contain 70~0-8070of ash, but of the remaining organic matter, 24% is protein reckoned on an ash-free basis, as compared with only 10% in living Spartina, and only 6% in newly-formed Spartina detritus. Thus, as the detritus breaks down into smaller particles, it becomes a progressively richer

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source of energy for bacteria, which in turn give the particles a high nutritive value. Another remarkable instance of how organic material may become enriched in an estuarine environment (in this case the estuary of the Thames) is supplied by Newell (1965). He found that the amount of nitrogen in the mud deposits shows a regular increase with decrease in particle size. Since the total surface area of a fine-grained deposit is far greater than that of an equal volume of coarse-grained deposit, the amount of nitrogen must be in some way influenced by the surface area of the deposit. Further, the ratio of carbon to nitrogen was highest ( 2 5 :1) in coarse-grained deposits, but approaches 7 :1 in finegrained deposits. The organic matter in fine-grained deposits supports a €ar richer bacterial flora and its associated micro-fauna than in coarse ones, even where the amount of organic matter as potential bacterial food is the same. Newell found that the percentage of carbon is high in the freshlydischarged faecal pellets of the snail Hydrobia ulvae (Pennant) (about 9.5% of dry weight), while the level of nitrogen is low (about 0.02% of dry weight). These pellets were cultured, and it was found that a population of non-photosynthetic micro-organisms developed, which oxidized the carbon in the faecal pellets to obtain energy for synthesizing proteins. The percentage of nitrogen in the cultured faecal pellets rose rapidly. These enriched pellets were fed back to Hydrobia, and during their passage through the gut the percentage of nitrogen again diminished. From this it could be concluded that the nitrogen in the pellets represents a population of bacteria and associated micro-organisms which fix atmospheric nitrogen at the expense of some of the carbon. Newell considered that the organic matter (detritus) had little nutritive value for the molluscs studied other than its content of bacteria and micro-organisms. He suggested that, since a population of microorganisms is attached to the surface of the fine soil particles, it might be just as profitable for a deposit feeder to ingest these as to ingest organic debris. It may be said in passing that many of the grains of soil present in the gut of the grey mullet, an estuarine fish, are found to have a coating of micro-organisms, including small naviculoid diatoms. Since blue-green algae, many of which are also nitrogen fixers, flourish in environments rich in organic matter, the presence of abundant detritus in estuarine soils must result in the fixation of much atmospheric nitrogen. Indeed, it is otherwise difficult to account for the production, year after year for decades, of fish which may have 20% protein in their flesh, as has, for instance, Chanos (Schuster, 1952),

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without the application of fertilizer other than organic matter such as leaf trash, or even with no fertilizer a t all. 5 . The further breakdown of detritus

Thus the detritus improves as a foodstuff as it is broken down by such agencies as mastication and digestion by animals, mechanical grinding by the soil which would release enzymes €or autolysis, and the chemical effects of saprophytic bacteria and fungi. Sub-particulate organic detritus includes colloids, aggregates of large molecules such as proteins, carbohydrates, fats etc. ; smaller molecules can exist, such as vitamins, amino-acids, sugars, urea, or as dissolved gases, methane, ammonia, H,S. All these represent some potential energy for species able to exploit them. It is worth noting that urea has proved t o be a successful fertilizer for blue-green algae. It can be seen therefore that detritus represents potential energy, originally accumulated by photosynthesis. It may have been formed in the estuary itself (autochthonous sources) or have been brought in from outside the estuary (allochthonous sources) (Darnell, 1967-8). 6. Autochthonous sources (a) Detritus derived from the death of phytoplankton which has flourished in the estuary. Ketchum (1967-8) cites the case of a very dense population of small Chlorophyceae produced by the discharge of duck manure into an estuary. The further growth of this population was inhibited by its own turbidity and by a lack of available nitrogen. These plants would die and add to the stock of detritus. (b) Detritus derived from submerged vegetation and from mud-$at diatoms and jilamentous algae. These may be very abundant ; whole areas may be carpeted with algae, which again may carry a coating of epiphytes. These algal pastures are the principal food for both Chams and grey mullet. I n fish culture one of the chief arts is the care and fostering of this algal pasture. Any surplus to current needs, with the faecal matter from fish and other organisms which have fed on this algal pasture, breaks down into detritus which still contains much of the original potential energy. (c) Periphyton growing on surfaces. Odum (1968) confirms the findings of Newel1 ( 1 965) that small particles of whatever origin “ are far from being poor inert bodies, but are flourishing micro-ecosystems containing bacteria, protozoa, and microalgae. To a great extent, the smaller the particle, the greater its relative food value.”

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7. Allochthonous Sources of detritus

(a) Marine seston, both plankton and detritus, carried into the estuary ; (b) marsh and swa,mp vegetation-the contribution of Spartina, for example, has already been mentioned; (c) water-side plants and forested slopes of estuaries, which in autumn drop large quantities of leaves into the water, and in the tropics, mangrove leaves, (the detritus in the stomachs of grey mullet taken in English estuaries shows the prevalence of material derived from the leaf-fall) ; (d) riverborne plankton and organic debris, including sewage. The problems posed by sewage disposal are too well-known to need discussion here ; they are an important source of organic material, and in excess create the serious problems of oxygen deficiency. The River Thames, in London, in the days of the first Queen Elizabeth, ran so clear that it was celebrated in poetry; in Queen Victoria’s reign it was so foul that Parliament once had to go into recess because of the unbearable stench of the river alongside. Only during the last decade have remedial measures re-introduced enough oxygen t o give a clean river. Rotting leaf mould washed into the rivers is another source of detritus. 8. The nutrient trap

Ketchum (1967-5) writes that water circulation in estuaries frequently has a two-layered flow. The surface layer diluted with river water escapes seaward, while salt water creeps upstream along the bottom. On contact with salt water, the fresh-water organisms will, in most cases, die and sink to counter-current depths in which they will be distributed around as detritus in various stages of break-down. Marine organisms carried into the estuary with the salt counter-current will also in most cases die on contact with fresh water, and so add to the supply of detritus. The inflowing current may add nutrients directly, since it may have come from depths below the zone of photosynthesis. I n these ways nutrients can become trapped in the estuary, and build up unusually high concentrations. Cooper and Steven (1948) suggested imitating this process to enrich marine fishponds made by the damming of a large tidal sea-loch, like the Loch Craiglin in Gross’s fertilizer trials (Orr, 1947). If such a barrier had two sluices-one a t the bottom to allow the entry of nutrient-rich bottom water on the rising tide, and one a t the top to allow of the discharge, on the falling tide of the spent surface waterthen the loch would become a nutrient trap in which fertility would accumulate without much risk of the formation of a deep de-oxygenated layer of water.

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Korringa ( 1967-8) showed vividly the importance of filter-feeding molluscs in the accumulation of nutrient material in estuaries. Each rising tide brings in organic matter from the sea, both dead, as detritus, and living as plankton. The filter-feeding molluscs are very efficient at straining off this material, which is thus trapped. After passage through the gut of the filter-feeders, this matter may be discharged as faecal pellets, which may become further enriched and be food material for other organisms, through whose food-chains it is distributed through the estuary. Korringa draws attention t o the immense number of benthic organisms per unit surface area in some estuarine situations (for example, as many as 1 000 cockles per m2in the Dutch Waddenzee). Such vast populations can only survive through the continuous accumulation of organic material brought in on flood tides. In such estuaries, the production of animal protein per square metre must rank among the highest in the world. Bottom-living algae, in particular, flourish on this rich material, and the two most important fish cultivated in estuarine fishponds, the Chanos and grey mullets, and many of the valuable penaeid prawns, feed directly on these algae, thus telescoping the food chain to get nutriment very economically from the base of the food pyramid. (Hiatt, 1944). 9. Particulate organic detritus

Particulate organic detritus is a direct source of food for many organisms. The striped grey mullet, Mugil cephalus, is believed to feed largely on this material (Odum, 1968))and so also is Mugil tade (Forsk.) in India (Pillay, 1953). It is also important in England for the thicklipped grey mullet, Crenimugil labrosus (Risso), (Hickling, 1970), and is a prime source of food for many prawns. Darnell (1967-8) was able t o show that areas of zooplankton abundance in estuaries were correlated with centres of detritus abundance rather than with phytoplankton abundance. 10. Colloidal and dissolved organic material

Darnell states that many invertebrate species of differing feeding habits are known t o be able to concentrate colloidal organic matter in the gut, and that even some fish may be able to use this material. Dissolved organic matter is common in sea water, and may be more abundant even than seston. Schuster (1952) states that the Java Sea contains 30-50 mg of organically combined phosphorus and about 50 mg of organic nitrogen per cubic metre. It is certain (Lackey, 1967-8) that dissolved organic matter is used directly as a nutrient both by

14i

ESTUARINE FISH FARMIPJQ

chlorophyll-containing organisms, and by colourless saprozoites, such as the large populations of colourless euglenoids in the sediment-water interface. Many kinds of bacteria also use these materials, which are thus brought back into circulation. 11. The microjlora

as food material

The great quantity of organic matter in all stages of degradation which accumulates in estuaries supports a correspondingly great flora of bacteria, which may become the direct food for a wide range of animals (Lackey, 1967-8). Enormous numbers of bacteria flourish on mud-flats, and their presence gives an important nutritional quality to fine sediment and suspended particles. They cover exposed surfaces of all kinds. It is certain that most groups of invertebrates and some fishes, especially small fishes, are able to flourish and grow on an exclusive diet of bacteria. 12. Some quantities of organic matter present

in estuarine soils

A simple way of estimating the organic matter in estuarine soils is to heat a sample to 580°C for several hours. The organic matter is burnt away, and the loss in weight represents the organic matter, subject to some errors which are not important for the present comparison. Some examples are given below, as percentages of the dried weight : Solway Firth, Scotland (Heather)* Dee Estuary, England, clean sand* Dee Estuary, England, dark mud and sand (Hoather)" Plover Cove, Hong Kong Java fishponds (Schuster) Algal pasture soils (Tang and Chen, 1966) Tamar estuary, England Menai Strait, Wales

yo

14-4-3 2.8% 5-10% 4.2-10.8y0 4.1% 0.39-4.17 8.4-12.0y0 7.2-11*3y0

yo

Tang and Chen (1966) show well, in their Table V (reproduced overleaf as Table 11),the close connection between the organic content of estuarine soils and the rate of production of algal pasture and thence of the fish which feed on that pasture. Table I1 shows how a rising amount of organic matter is accompanied by an increasing crop of algae, and hence with bigger fish crops. The table also shows that the conversion rate of algae into fish is about 11.3 t o 12-7 to 1. Schuster (1952) gives the figure of 25 to 35 to 1 as found in Java.

*

Data quoted by kind permission of Dr. R. C. Hoather.

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TABLEI1 Organic matter

%

Annual crop of Algae, kglhectare

Annual crop of Fish, kglhectare

0.39 1.23 2.41 3.27 4.17

-

-

15 000 18 750 25 000 28 250

1200 1500 2 000 2 500

Vatova (1962) gives data for the wet weight of the bottom fauna in the Italian ponds arranged in increasing order of salinity, as below.

Type of pond

Salinity %o

Oligohaline Mesohaline Polyhaline Hyperhaline

>5 5 to 20 20 to 35 < 35

Wet weight of bottom fauna, g/m2 6 to 81 to 185 to 282 t o

24 126 341 329

Table I11 shows that the greater the salinity, (which means the greater the access to seawater) the greater the mass of organic material and so the greater biomass of bottom animals. This is as would be expected if one of the main sources of fertility is derived from matter brought in by the tidal currents. 13. Other direct sources of fertility

Though the importance of organic matter in the fertility of estuaries is well established, there are other important sources of nutrients. Rivers bring down dissolved nutrients and also silt in suspension, and the fertility that these confer depends on the nature of the watershed. Where the pond soil is derived from youngivolcanic rock, it may be very fertile. As Schuster (1952) says, each eruption of one of the big volcanoes in East Java helps to maintain the productivity of the brackish-water pond systems of Surabaya and Sidoarjo. But, where the soil is derived from granite or quartz rock, it is poor in nutrients. MacNae (1967-8) found that the best development of mangroves occurred in the estuaries of rivers which drained areas of basaltic rock of comparatively recent lavas. Such rivers carry soils of high fertility which are deposited in the estuary.

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111. THE SPECIESCULTURED

A. Selection of organisms by salinity As Vatova (1962) said of the Adriatic lagoons, from the moment they enter the ponds, the organisms are selected for those forms which can stand the rigorous environment, not only of extreme and rapid changes of salinity, but also of temperature (0-31°C in Italy, 8-37°C in Taiwan) and dissolved oxygen (49-212% saturation in Italy). The fauna so selected are few in species but rich in individuals, as would be expected from fertile ponds. The fish which enter such ponds are either species which make true anadromous migrations, staying for one or more years (eels and to some extent grey mullets, sparids, and flounders) or temporary dwellers which enter in spring and summer for feeding, attracted by the warm water and plentiful food. All such fish must be euryhaline, and they are predominantly marine fish. Beadle has pointed out that most fresh-water animals are unable to maintain a blood hypotonic t o the external water and, with few exceptions, they ara restricted to salinities below lo%,. d’Ancona expresses the same thing by saying that the fish fauna of brackishwater is chiefly of marine origin, since many marine fish can support the dilution of sea water, while few fresh water species can tolerate an increase in salinity. Doroshev (1963) tested this in the brackish-waters of the Sea of Azov and the Aral Sea, using two species of fresh-water herbivorous fish, native to the rivers flowing eastward to the Pacific. There are vast stocks of vegetable food in these two seas which are used little or not a t all because the fish fauna of those waters do not include herbivorous fish. I n the hope that some of the unused plant production might support a fishery for herbivorous fish, Doroshev tested the salinity tolerance of two large and valuable members of the carp family-the Grass Carp or White Amur, (Ctenopharyngodon idella Val.) and the Silver Carp or- White Tolstolobik (Hyiophthalmichthys molitrix Val.). Doroshev found that the Grass Carp could survive without ill effects six weeks to two months in Sea of Azov water with salinities up to 9%,, if gradually acclimatized. I n Aral Sea water, grass carp would tolerate even 12%, after acclimatization. The silver carp (a phytoplankton feeder) would survive in Sea of Azov water of up to 7 . ~ 5 %after ~ acclimatization, and in Aral Sea water up t o 10-5%,. They did best when slowly acclimatized t o the change. Above these salinities, a breakdown of salt metabolism, illness, cessation of growth, and a high mortality were observed. Doroshev concluded that the salinity of the A.P.H.-8

n

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I?. HICKLINC

water in large areas of the northern Sea of Azov and of the Aral Sea need be no obstacle to the establishment and spread of these valuable plant-eating fish. I n the New Territories of Hong Kong, a large acreage of fishponds has been made in former salt marsh. They are described as brackish water, but their maximum salinity is of the order of 3%, (Chow, 1958)) and they grow the full range of Chinese carps (including the two mentioned above) with intensive fresh-water farming techniques. These ponds are fresh according to most definitions, and will not be further considered. Similar acclimatization trials have been made with the Indian major carps (Saha et al., 1969). The object is to find a cultivated fish to replace or supplement the brackish-water fish such as grey mullets which are taken into the bheris haphazardly as fry in the spring. By careful acclimatization experiments they found that these carp would tolerate salinities as high as 13%,. It seems doubtful if they would go much higher, and Pillay (1954) found that the salinity of the bheri he studied was 24-35%,. Schuster found that a carp, Puntius javanicus (Blkr) can stand for a short while a salinity of 22%,, but that for rational culture a salinity of S%, or less is needed. According to Djaingsastro (1956) the salinity limits for Chanos are 0-140%,, and for grey mullets, up to 70%,. I n the Black Sea, Ilin (1954) found that the principal grey mullet there cultivated, the golden grey mullet, Liza aurata, had a salinity range of 1-50%,. Ghazzawi (1933) referring to Egyption conditions, gives an upper limit of 40%, for Mugil cephalus, M . chelo, and M . capito. The most frequently cultivated M . cephalus grows well in fresh water but can also stand high salinities. Thomson (1966) writes that most members of the mullet family can live in some degree of brackishness, and quotes Brunelli’s observations from field work that the lower salinities tolerated by some species are:Liza ramada, 5%,, L. provensalis (Risso), lo%,, L. saliens (Risso), IS%,, L. aurata, 24%,. Acclimatization rates had not been studied. There is little knowledge of the upper limit of salinity tolerance, but Mugil cephalus tolerates 75%,. Ganpati and Alikhuri (1952) found that Mugil cephalus, Liza speigleri (Blkr), and Valarnugil seheli (Forsk.) fry can be transferred direct from sea to fresh water, particularly if well supplied with planktonic food. The 20-30% mortality which occurred, they ascribed to damage during handling. However, Devanesan and Chacko (1943) found that a gradual lowering of the salinity markedly reduced the mortality of the fry. The present writer has easily acclimatized Crenimugil labrosus (Risso) (referred t o above as Lizaprowensalis) to tap water, using one

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or more changes of water. As he writes, there are in front of him three small Crenimugil labrosus which have already spent eight months in tap water and are growing well. But this species can be transferred straight back from tap water to full sea water, showing that the grey mullets are true sea fish. Morovic and Sabioncello (1965) found the same result. However, grey mullet artificially transferred to fresh water seem more liable to parasitic infection than in sea water; Yashouv and BenSchachar (1967) found that keeping the Mugil cephalus in 1 part of sea water to 9 parts of fresh water protected them : Doroshev (1963) also found that placing his carp in diluted sea water rid them of infection. Grey mullet can obtain oxygen from water of low oxygen content and can survive for long periods in water containing less than 0.5 p.p.m. dissolved oxygen, but they have no accessory respiratory system and will die in water totally devoid of oxygen (Thomson, 1966). B. The natural history of the species The most important species cultivated in brackish-water f?&&&ms are :-Milkfish, Chanos chanos (Forsk.) ; Grey mullets, species of Nugil, Lixa, Crenimugil; Eels, Anguilla spp ; Salmon and Sea Trout, Salmonidae ; Tilapia, chiefly T . mossambica (Peters) ; Penaeid prawns. Chanos (Fig. 8) is an oceanic fish, which approaches the coasts to breed, so that the young are soon carried or swim into brackish-water lagoons, salt creeks, mangrove swamps, and open beaches. Lin (1968) believes that Chanos follow the Kuroshio Current in scattering schools north eastward from the Philippines to the coast of Taiwan, and to the coast of southern Japan, for feeding and spawning. There is no fishery for the adult Chanos, which can grow to a metre in length. Schuster (1952) says that no more than a hundred adult specimens are caught yearly along the coast of Java. He points out that there is some evidence that the spawning of Chanos takes place twice a year near the Spermonde Islands, south west of Celebes, among other places. The eggs and larvae are rarely found (Delsman was able to handle only 20 eggs in many years of work) ; but the fry, which are about 11-13 mm long appear in millions on the north coast of Java and Madura. After a stay of about 10 days in the coastal waters, the fry disappear, and adolescent Chaws are never observed in coastal waters even though there is an intensive fishery there. A few which enter the fresh water Temp6 Lake in Celebes grow to adolescence (at 28 inches) in 2-3 years. So there is still a gap in our knowledge of the natural history of this fish. Luckily, Chanos stay in coastal waters long enough for the capture of the fry needed for the important pond cultures of the Philippines, Taiwan,

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and Java. I n India, fingerlings of Chanos are caught in numbers large enough to be worth collecting and sending inland to stock fresh-water tanks and lakes-they are about 2-6 inches long, and can be placed immediately in fresh water, though they are more commonly acclimatized by several changes from sea water t o fresh water.

(c)

(4

FIG.8. Four of tho commonest animals reared in brackish-waterfishponds. (a) Milkfish, Chanos chanos Forsk. (b) Gray Mullet, Liza sp, (a) Tilapin mossainbica Pot)ers and (d) Penaeid prawn, such as Penaeus brevicornis (H. M. Edwards).

The most important of the grey mullets (Pig. 8) for fish culture is the striped grey mullet, Mugil cephalus L. This is a true marine fish, which has been seen spawning over deep water in the Gulf of Mexico (Arnold and Thompson, 1958). They also spawn in the Taiwan Channel (Tang, 1964), off Hong Kong (Bromhall, 1954) and over the deep water off the Mediterranean coasts (Ghazzawi, 1933). But as is the case with

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Chanos, the young soon seek shallow and less saline water, and generally tend to congregate where a stream of less saline or fresh water enters the sea. It is in such places that the fry are caught commercially. During their growth they can acclimatize completely to fresh water. As an extreme case, specimens were caught a t the Dennison Dam on the Red River in Texas, 500 miles upstream from the sea at the mouth of the Mississippi (Riggs, 1957). They enter many fresh-water lakes and rivers, and have been successfully transferred t o the Sea of Galilee. In Israel, they are cultivated with carp and Tilapia in fresh-water fish farms, and have become an important farm fish there. But not all grey mullets have this breeding pattern. The whereabouts of the breeding grounds of Crenimugil labrosus (Risso), the commonest English grey mullet, are still unknown, though in April, 1969, a newly-spawned female still releasing a few eggs on pressure of the abdomen, was caught in the Isles of Scilly. One species of grey mullet, a t first thought to be Mugil cephalus but now believed to be a different species, has been found spawning in the estuary of the Yung San River in Korea (Yang and Kim, 1962). The eggs of the grey mullet Liza macrolepis were found abundantly in the stomachs of the predatory fish Ambassis a t the entrance to the Chilka Lake on the east coast of India (Natarajan and Patnaik, 1967). Eels are cultivated in Japan and Taiwan (Anguilla japonica) and in the Mediterranean ( A .anguilla). I n both areas the young are caught as elvers or as young fish, several centimetres long. The astonishing life-history of these fish is well enough known, thanks t o Johs Schmidt. The elvers ascend the estuaries and rivers in great numbers, overcoming all obstacles. I n the estuary of the River Severn, in Gloucestershire, England, there is a fishery for the freshly ascending elvers, which are eaten as a delicacy, and there used t o be a fishery €or live elvers that were theii exported to Germany to stock the eastern fresh waters, which did not receive enough young eels naturally via the Baltic. The elvers acclimatize very easily to fresh water, and withstand a low oxygen tension, as also do the adults. Salmon and sea-trout acclimatize themselves t o sea water on their downstream migration as smolts or kelts, and in the reverse direction they spend enough time in the estuaries to acclimatize to fresh water before ascending the rivers. But the brothers Vik showed how they could be artificially acclimatized to fresh water from sea water and the reverse. The writer has amused himself by having in his cubicle two aquaria, one containing grey mullet, a marine fish. in tap water, and the other containing rainbow trout, a fresh-water fish, in sea water. According to Frost (1968) the acclimatization of rainbow trout to sea

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water is done very gradually on the commercial scale. The life-history of these salmonids is too well known to need repetition. The Tilapias are a successful group of fish, predominantly of Africa, though one genus, Etroplus, is found in India and Ceylon. Many of the species inhabit mangrove swamps, where they have to be adaptable t o rapid changes of salinity, and to tolerate a high salinity. One species, T . zillii, has been found living in the Red Sea, at salinities of 40%, (Bayoomi, 1969). By a series of odd chances, one species, Tilapia mossambica (Fig. 8 ) , has been spread round the world in tropical and sub-tropical countries. It has a lower temperature limit of about ll-l2"C, and such countries as Malta and Hong Kong are near this limit. Attempts to introduce them to Malta have failed, but they flourish in Israel, California, the southern states of the USA and the Caribbean. It has proved an embarrassing fish because of its extreme fecundity in fresh water ; but it grows better in brackish water, not perhaps unexpectedly since that seems to be its natural habitat, and it has proved to be a real blessing to Java. An account of the cultivation of Tilapia has been given by Hickling (1963). It is a firstclass food fish, giving lightly-fried fillets of delicate flavour. The yellow tail, Seriola quinqueradiata (Temminck and Schlegel), is intensively cultivated, as mentioned above, in cages in Japan. It is a purely marine fish, and the young are caught at sea among floating masses of seaweed (Anraku and Azeta, 1966). Milkfish (Chanos) and grey mullets have feeding habits so similar that they are in competition when grown together, but over most of their respective ranges they are separated by their temperature tolerances. According t o Lin (1968) Chanos becomes sluggish at 15-2OoC, and dies a t 12°C. On the other hand, grey mullet become torpid at about 5°C and die at prolonged exposure t o 1.5"C (Ilin, 1954 ; Zambribortch, 1962). The penaeid prawns (Fig. 8) are estuarine dwellers for a part of their distinctive life-history (Kutukuhn, 1966). Breeding is in the sea at varying distances from the mainland, and the eggs hatch into small planktonic nauplii. Rapid development follows through the larval stages, while the larval prawns are all the while moving in a still unexplained manner towards the mouths of rivers and estuaries and lagoons. The developing young quickly transform into juvenile prawns in estuarine conditions. They grow to commercially valuable size in a few months, and are usually caught in the estuaries on their way back to the sea to complete the life-cycle. As Kutukuhn says, there is appreciable variation among penaeids as to the use of estuaries during their life-history and to the distance out to sea from the estuarine en-

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vironment where they breed. I n pond culture, they are carried into the ponds with the water, and there is no control over their numbers (save that the more the better). Schuster can hardly imagine overstocking with prawn larvae, and mortality must be very heavy if of the millions which may enter a pond only enough survive to give a crop of 100-1 000 kg of well-grown adults. Management measures are designed to attract the maximum number of juveniles. OF YOUNGFISHAND PRAWNS IV. SOURCES A. Non-breeding and artificial breeding

1. Pish

It is a notable fact that none of the fish cultured in brackish-water ponds will breed in the ponds except Tilapia. The young of the salmonids must be bred in fresh water, those of the yellow tail are caught in the sea, those of Chanos, grey mullets and prawns in brackish-water creeks and lagoons. So a specialist fry fishery has arisen which will be described later. The industry’s needs for healthy living fry are very great, and a shortage and uncertainty of supply are one of its worst handicaps. Lin (1968) shows in a table that the availability of Chanos fry in Taiwan, as caught by the local fry fishermen, varied from 14 million in 1934 to 204 million in 1958. Requirements are about 160 million fry a year. It may be necessary to import fry from the Philippines, where there is always a surplus. I n the same way, there is a shortage of Chanos fry in Java, and the deficit has to be made good by importing fry the long distance from Madura. According t o Schuster, Java needs 190-200 million Chanos fry annually. The catch of Chanos fry in the Philippines exceeds 440 million (Bunag, 1957) but more are needed. As to grey mullet, Tang (1964) estimates the requirements of Taiwan at 10 million annually. Hong Kong requires some hundreds of thousands of mullet fry if the stocking rate is 3 000 per acre. I n Italy it is no longer possible to rely on local supplies of grey mullet fry for stocking the valli, and additional fry have to be imported from lagoons on the Tyrrhenian Sea on the west coast of Italy. The prosperity of brackish-water fish farming must remain precarious so long as it has to rely on naturally-spawned fry. Naturally, many attempts are being made to breed these fish. There is promise of success with the striped grey mullet, Mugil cephalus, but no success has been reported with Chanos as yet, though it will grow to full size in ponds. The gonads are said not t o ripen in ponds; however, the same was said of the major Chinese and Indian carps,

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which have since been bred very successfully. I n a matter so important, persistent effort may bring success. The striped grey mullet has been induced to spawn in captivity in Taiwan by Tang (1964). Live matura fish were collected at sea from purse seiners and placed in holding boxes. They were subjected to two hormone injections, 12 hours apart. Each injection consisted of one pituitary gland from a mature grey mullet of the same size, ground up in saline solution with 20 international units of a proprietary preparation of chorionic gonadotropin with hypophysial extract. The ambient sea temperature was 20-25'C. Tang had great difficulty due to the high mortality of the captive fish-they would not live longer than 48 hours. He found that the fertility of the eggs was low (32%) and that the hatching rate was less than 10%. But this fine pioneering effort has since been improved upon, with promising results in Hawaii and California and also in Israel where the pituitary glands of common carp were used. This fish seems t o be a universal donor but, at the time of writing, the young fish have not developed beyond the 21st day. So final success, though obviously very near, is still awaited. Success will mean that the grey mullet farms of the future must have hatcheries as a part of their layout but it is more probable that private firms or Government hatcheries will specialize in the breeding of fry, and sell the well-grown fry to the farmers. The writer tried Tang's technique with Crenimugil Zabrosus in February and March 1969, but had no success. The sea temperature was very low, at about 7-9"C close t o the beach. 2. Prawns

This may be the best place in which to describe the Japanese success with the rearing of the '' Kuruma " prawn, Penueus juponicus (Bate). It is not a genuine case of breeding, as with the grey mullet, because the female prawns will have already ovulated and been fertilized before being caught for the rearing of their eggs. The process is described by Hudinaga and Miyamura (1962). The females are placed in a shallow wooden tank (2 x 1 x 1 m) full of sea water at a temperature of about 28OC. The nauplius hatches out 13 hours after spawning and the larval prawn passes through the stages of the zoaea and mysis in about a week. On reaching the post-larval stage, they are transferred to a concrete pond of 5 m2 area and 30 em deep for about 20 days. Then follow the post-larval stages, leading to the attainment of a commercial size after about one year.

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The food given t o the larvae during the zoea t o post-larval stages is cultured diatoms, eggs, early-stage larvae of bivalves or early nauplii of Artemia. The food given to the post-larvae is small shrimps, bivalves, and trash fish caught commercially. Once more, Japan is lucky in its supply of trash fish, cheap enough t o feed to fish and prawns at a profit.

B. The Jish f r y and prawn f r y industry Lin ( 1 968) thinks that, until the breeding of Chanos is possible, the most desirable development would be an improvement in the eficiency of the fry trade. At present, the capture of the fry of both Chanos and grey mullet is mostly a small-scale peasant fishery, operated in season by part-time casual labour, including women and children. A simple triangular scoop net may be used and likely places t o try are where less saline or fresh water mixes with sea water, such as in creeks and lagoons or on open sandy beaches. I saw, in southern India, Chanos of fingerling size caught in a backwater among mangrove by dragging a rope, garnished with bunches of straw, rapidly along the surface. The fingerling Chanos leapt out of the water, and fell into cloths held by people following the rope. I n Java and Madura, as Schuster describes, simple lures are used, made of long ropes well garnished with strips of palm leaf or straw. Staked out a t right angles to the beach, these offer shelter to the Chanos fry moving along the shore ; all the operator has to do is to pass his net along the lure and collect the fry. I n a more elaborate manoeuvre, the operator may lay his lure in a circle, and then contract the circle until the fry are concentrated in the centre €or easy capture. More efficient methods are used in Taiwan and the Philippines. Not only scoop nets, but bag-nets and a kind of pelagic trawl are used in Taiwan (Chen, 1952) from motorized sampans or rafts. I n the Philippines, large hand seines and even a small trawl (Bunag, 1957) are used. But the call is still for a more effective detecting and catching method, since the full expansion and profitability of the industry depend on plentiful and reliable supplies of fry a t a cheap price. The fry of grey mullet are also caught in scoop nets ; usually, two fishermen using these nets work towards each other and so get more fry than either would alone. I n the Russian limans, lift-nets are commonly used to catch the fry but, more usually, the fry of grey mullet and eels are not caught, but induced to enter the ponds by allowing a slow current to flow out of the sluice. The fry respond t o this with accuracy, and collect in the sluice gate, where they may or may not be counted before admission t o the pond.

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I n English estuaries, grey mullet fry appear abundantly in the summer months from June and July to October (Hickling, 1970). At first, they tend to shelter among weeds, but later they move about with the tide, and tend to collect where a stream enters the sea. It is not difficult to take them in large numbers but there is no demand for them. Long-handled scoop nets are used for the capture of elvers. As the tide rises, for example in the River Severn below Gloucester, the elvers migrate upstream in dense shoals close t o the bank. They are easily scooped out into buckets. The fry of the yellowtail, Seriola quinqueradiata, shelter among masses of floating seaweed and are caught by scoop nets or by encircling the floating masses of seaweed with small seines (Anraku and Azeta, 1966). The seaweed also harbours arich population of crustaceans but the young yellowtail feed exclusively on zooplankton until they are 2.5 em in length, and after a length of 1 3 cm, exclusively on fish. The larvae of prawns are wholly caught in the sluices of the ponds where they will be raised. They are carried in with the water when the ponds are filled. Both Hall (1962) and Schuster (1952) give advice as t o how t o increase the intake of young prawn. Since it is inconceivable that a pond might be overstocked with prawns, everything possible is done to bring in as many larvae as possible. Insteadof relying on chance that good quantities of prawn fry will enter when the sluice is opened at high tide, Schuster advises that a head of water of about one foot should be allowed t o build up outside the pond. Then the opening of the sluice will result in a strong inrush of water which will carry in the prawn larvae, which are poor swimmers. A similar method is used to secure a good entry of young prawns into the paddy fields of south India. Hall (1962) makes a number of points, for example, that as many of the sluice gates of the pond as possible should be opened at high tide, especially during the months of March, June and November, when the prawn young are most plentiful in the Singapore area ; and that this should be done even if it means having to release some water later. As the young prawns, unlike the adults, are as abundant in the water by day as by night, every chance should be taken, and where a partial opening to the sluices is needed, this should be a t the bottom, rather than a t the top, since post-larvae, which might be settling outside the ponds, would then be swept in. Similarly, when taking the young of fish and prawns into the Indian bheris, Pillay ( 1 954) says that emergency extra gaps may be cut in the embankments to take in as many as possible. There appears t o be a specialist fishery for young prawn only in the

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Philippines, where the valuable " Sugpo or Penaeus monodon (Fbr.) is cultivated in ponds with Chanos or by itself (Caces-Borjaand Rasalan, ))

1967).

As with the young of the other penaeids used in farming, the creeks, lagoons and other shallow areas are the places where fishing for young takes place. Fish-lures are used, which take the usual form of bunches of grass tied along a rope which is moored in shallow water. One man may operate many of these ropes. The " sugpo " young are given to clinging to suitable substrates, and by lifting and shaking the lures over a net, the young prawns are easily taken. They may also be caught from canoes with hand-nets. During the peak season, as many as 1 000 young prawns per hour's work can be taken. Larvae are easily distinguished by a streak of dark-brown pigment running through their transparent bodies. When the young fish or prawns are caught, they are bought by dealers who resell them either to the farmers or to specialist fry cultwists. I n the hands of the ordinary fish-farmer the mortality among fish fry can be very high. Schuster (1952) says that a 30% survival of planted fry is a usual result in Java. Such low survival rates make the surviving fry costly and better care will clearly result in cheaper stocking material. For example, Djainsastro (1956) found that a very thorough screening of the water admitted to the fry-ponds, thus excluding predators, much improved the rate of survival of Chanos fry. Pillay (1966) says that little care is usually taken of grey mullet fry because they are so cheap, and the losses can be very high indeed. But Yashouv (1966) shows that when the very young mullet fry (151 8 m m long) are caught in the mouths of streams on the coast of Israel, and stored in small ponds where they have care and are fed to maintain their strength and growth, the mortality over so long a period as 4 months could be only 20-30%. A very sensible arrangement which seems to be increasing in the principal Chanos-growing countries is for certain dealers to specialize in the care and rearing of the tiny fry to strong fingerlings. Such specialists can reduce losses to 20-40%. With such a supply of well grown fingerlings available, progressive fish culturists can raise two or even four crops of fish in a year. Further, such a reserve of fingerlings is some insurance against a failure of the fry fishery (Mane et al., 1952). C. Care and rearing of fry 1. Chanos

These fry, when first obtained, are kept for a longer or shorter time in special very small ponds (with the delightful name of " baby boxes "),

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which may be as small as 6 ft by 6 ft in area (Figs. 9 and 16). These ponds are drained dry to kill predators and the bottom may be raked and puddled. Cover from the sun is provided by palm leaves stuck into the embankment or by an overhead shade (Fig. 9). In a fry pond Chanos may be stocked at a rate of 55 per square yard. At this stage there are two main dangers : from a wrong quality of the water or from harmful processes in the soil. Sudden changes of temperature are avoided by standing the containers, in which the fry

FIG.9. Chanos fry pond in Taiwan. Note the sunshade mounted on poles. The little temporary embankments are breached to allow the escape of the acclimatized fry into the main rearing pond.

arrive, in the water of the fry pond until the temperatures are equalized. Then the fry are carefully decanted out or the container is laid on its side so that the young can swim out at their leisure. The fry remain in this very small enclosure for only about 24 hours, while they have this extra protection to acclimatize them t o pond life. Then the temporary embankment of the " baby box " is breached so that the fry can make their way out into the fry pond proper. The water must be of the right salinity. High losses are suffered when the fry are placed in water with a salinity exceeding 40X0 and all fry die at salinities over SO%, (Schuster, 1952). As to soil conditions,

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if too much organic matter is present, sulphates may be reduced t o sulphides which would generate the very poisonous H2S. The tilling of the soil of the fry pond, following drying, which may be repeated several times (Mane et al., 1952),is intended t o reduce, by some mineralization, the organic matter. Wet places which cannot be dried are treated with lime. I n Taiwan, the Chanos fry are a t first placed in a nursery pond which has a small section only 10-20 m2 in area and filled to a depth of 20 cm

FIG.10. Brackish-water Ckanos ponds in Taiwan. Note low embankments between ponds and the high pcripheral embankment in the background. There is a small concrete sluice which is closed by wooden slats-the screen has been removed and is lying alongside. The sluice leads to the long narrow fry pond. Beyond is the big rearing pond.

with water of 20%, salinity (Lin, 1968) (Figs. 9 and 10). The fry spend enough time here to become so acclimatized that they will pass at will through an opening in the embankment into the much larger main nursery pond, of 500-1 000 m2 area, and with water of 30-45%, salinity. If this is done with care, says Lin, mortality should not exceed 3-4%. The treatment of the fry varies somewhat between the Philippines, Java and Taiwan because their seasonal availability varies. I n Indonesia. Chanos has two spawnings, one in each monsoon, and the young

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fry are thus available twice a year. But in both the Philippines and Taiwan, Chanos are available only once a year but over an extended period of time; that is, in Taiwan from April to September (Lin, 1968) and in the Philippines from March to September, with the peak season in May to June. In Taiwan, Chanos fry caught late in this long season cannot be grown to marketable size before the winter slows down growth and may even endanger the fish. Only in the south of the island can Chanos be overwintered in special wintering ponds. These are long and narrow, and always orientated in a n east-west direction so as not to be raked by the cold north winds. They are commonly 5 m wide and 100-200 m long, and 1.5-2 m deep. They are connected with the nursery pond by a narrow entrance. Unlike the similar ponds of Italy, trees do not seem to grow on the salty soil, so great wind breaks of bamboo are set up on which straw can be spread (Fig. 16). I n these wintering ponds the fish, which would not be normally very active, can be densely stocked during the 4 or 5 winter months, from November to March. The average temperature of the water must be kept above lS"C, and not be mixed with the outside water, which may fall to l2"C, a temperature fatal t o Chanos. Management of these wintering fish is tricky, because too long a period without water-renewal could lead to loss of fish through asphyxiation, especially since they may have to be fed occasionally to keep them in condition without serious loss of weight. Lin suggests that these overwintered fingerlings are valuable enough to justify the installation of air and water pumps to help maintain the stock, since these, when grown in the spring, are the first fish to be marketed and fetch a premium price. The food given is peanut cake. On warm days the fingerlings can emerge from a narrow entrance and browse in the adjacent nursery pond. 2. Grey mullet and eels

I n contrast to Chanos, grey mullet fry receive little care. This is strange, because the grown fish are as valuable as Chanos, even in Java (Schuster, 1952) and form an important part of the catch of miscellaneous fish from the fishponds. Usually, grey mullet fry are stocked directly into the growing ponds, as in Hong Kong and Taiwan. But grey mullet fry are in short supply in the Italian valli and more have to be brought from the west coast. They are valuable as well as delicate, and so are placed in special, well sheltered ponds, which are a series of parallel trenches called "seragio" arranged so that the cold winds of spring will not rake them, and which are supplied with fresh or

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brackish water (Fig. 11). The young fish stay long enough in the trenches to become accustomed to the climate of the valli. When strong enough, they are free (as in the Chanos wintering ponds) to swim out into the main growing pond. I n the Russian limans, the first grey mullet fry to ascend the channels from the sea to the lagoon are those of the golden grey mullet, Liza aurata, and these may be caught by lift-nets or seines to be counted. Any surplus may be sold while, if there is a deficit, more fry may have to be bought (Zambribortch, 1962; Ilin, 1954). Later in the season, the ascending fry include a proportion of Mugil cephalus and M . saliens, and these late migrants will not have had time to grow to a commercially acceptable size by winter. Zambribortch thinks that inadequate stocking with fry is one of the chief reasons for the poor performance of the limans as fish farms, and he describes wintering ponds in which these late arrivals can be kept alive, and so be available to supplement the spring influx of new fry. Like the other wintering ponds already described, these are a series of trenches and ponds, totalling 4 500 m2 in area in the Shabolatsk liman. These can be covered over against the cold, and are warmed by underground water which has a constant temperature of 10°C. At temperatures above 8"C, the fry can even be given some food such as bloodworms, Daphnia, Cyclops, and dried Daphnia. I n Israel, grey mullet fry are caught in the mouths of streams at the beginning of winter, and are stocked in the fishponds to grow t o marketable size. They therefore have to be wintered in special ponds where they may be crowded a t a rate of 25-30 per m2 of pond area. They are fed, and are able to put on some weight in the winter storage period (Yashouv, 1966). I n India, the fry admitted into the ponds in spring may be held in small ponds within the larger ones until they have grown strong enough to hold their own in the main ponds. The small fish, both Chanos and grey mullet, are manipulated about the ponds by using their strong instinct to swim against a current. I n the culture of the " sugpo )'prawn in the Philippines, the use of fresh water in which to grow the young has been found more favourable during the earlier stages, but in the later stages brackish or salt water gives the better rate of growth (Caces-Borja and Rasalan, 1967). " Sugpo '' fry, when newly stocked in a pond, tend to remain where they are liberated, no doubt as a feature of their known habit of clinging to a substrate. So in practice, the fry are widely and evenly distributed in the pond, so as to be less vulnerable to predators than if they remain crowded together.

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V. THE FOODOF CULTIVATEDFISHAND PRAWNS A. Chanos, grey mullet, eels, Tilapia and prawns I n their very early stages, both Chanos and the grey mullet tend to feed on plankton and even zooplankton, but by the time they have grown to the size at which they are stocked in ponds, namely, at about 1-5-2.5 em, they feed on an algal felt of blue-green algae with its associated epiphytic flora and fauna. Though artificial foods are expensive, they can be economical in certain circumstances, as when valuable young have to be overwintered or when a crop of fish has exhausted the natural food supply. Zambribortch (1962) states that the small grey mullet in the Russian wintering ponds may be fed on bloodworm (presumably chironomid larvae) and Daphnia; Lin (1968) mentions peanut cake as supplementary food in the wintering ponds for Chanos on Taiwan ; Yashouv and Ben-Shachar (1969) used food pellets (wheat, fish meal, and soya flour, with a 21% protein content) successfully with young grey mullet ; and Schuster mentions yolk of egg and rice flour as supplementary foods for Chanos fry. Ronquillo et al. (1957) tried rice bran and corn meal, enriched with Terramycin and a proprietary product “Vigofac”. But Lin quotes Yamamoto, who found that Chanos fry of 1.5-2.3 cm absolutely require blue-green algae and diatoms as food. There was a high rate of mortality when artificial foods such as flour, soybean meal, rice bran, and peanut meal were used. Schuster (1952) gives analyses of bluegreen and green algae from ponds in the region of Djakarta. TABLESV. COMPOSITIONOF ALGAEPER 1000 G

Water Raw protein Fat Nitrogen-free matter Ash Raw Fibre

Blue-greens

Chaetomorpha

Enteromorpha

829.0 16.5 3.9 13.7 122.3 14.6

951.2 22.8 9.6 2.7 9.1 4.6

937.3 12.7 2.4 13.3 21.4 6.9

The high proportion of ash in blue-greens, as compared with the green algae, is explained by the fact that the ash contains 32.9% of silica. Since the blue-greens contain very little, the analysis reveals the presence of a large diatom epiflora. I n spite of their very dissimilar appearance and distant relationship (Fig. 8), Chanos and grey mullet have a gut of very similar structure.

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These two fish share the following features, (i) small and toothless mouth, (ii) shovel-like lower jaw, (iii) absence of all masticating teeth, (iv) a pharyngeal sieving mechanism, including gill rakers, (v) an anterior thin-walled stomach for food storage, (vi) a very muscular bird-like gizzard of rather uncertain function and (vii) a very long intestine, relatively shorter in juveniles. Several different accounts have been given of the food and feeding of Chanos and grey mullet but the food in fact is so similar that Hiatt (1944) could say, of the Hawaiian fishponds where both fish occur together, that competition for food was greater than had been supposed. Schuster agrees, but adds that if the competing grey mullet are of a species which grows t o a large size, the fish farmer has nothing to worry about, since the mullet grow as fast, as the Chanos and fetch the same price. I n fact, however, the two fish have different geographical distributions so that competition is limited. For example, the southern coast of Taiwan is warm enough for the culture of Chanos, but the west coast is too cold so that grey mullet are cultivated in the ponds instead, and by the same methods. There is some difference of opinion about the food of the growing Chanos. Fish have been found feeding on different materials in the same pond. There is general agreement that blue-green algae and diatoms represent a high proportion of the food, and that they are preferred to green algae. Thus Schuster found that Chanos grown in a pond with a dense growth of green algae had eaten proportionately more blue-greens and less green algae than would be expected. Comparing two populations of Chanos, one in a pond well-grown with bluegreens, and one in a green-alga pond, it was found that in the latter 49 out of 66 stomachs were empty, whereas, in the former, only 20 out of 75 were empty. It would seem that many Chanos would rather go hungry than feed on green algae. Even so, there was a higher proportion of blue-green than green algae and a much higher proportion of detritus in the stomachs of Chanos from the green alga pond (Schuster, 1952).

Larger Chanos, however, seem able t o flourish on green algae, especially when it has begun to decay. Even parts of higher plants, such as the leaves of Ruppia, are eaten, though the statement that Chanos, transplanted t o fresh-water reservoirs in India, controlled the vegetation, must await confirmation, as the fish has no provision for masticating higher plants. As Schuster (1952) writes, Chanos is morphologically adapted t o consume great quantities of soft and smallgrained food, and to digest it quickly. The same is true of grey mullet. I n the Philippines, " lumut " or filamentous green algae are considered suitable food for larger Chanos, and are cultivated for the

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purpose as will be shown later. But in Taiwan, experiments done by Tang and Huang (Lin, 1968) on the digestibility of crude protein, crude fat, nitrogen-free extract, and fibre of four groups of algae, namely Chaetomorpha, phytoflagellates, diatoms, and fresh blue-green algae, showed that fresh diatoms had the highest coefficient of digestion of protein (87%), next came phytoflagellates (81%), then blue-green algae (69%) and finally, decayed Chaetomorpha (66%). However, fresh Chaetomorpha had a digestion coe%cient for crude protein of only 6%) and the fresh filaments have a tough and wiry impenetrable cell wall. According to Villadolid and Villaluz, quoted by Lin (1968), Chanos, feeding on filamentous algae, have a poor rate of food conversion, namely, 33 to 87 parts of Enteromorpha or Cladophora, to make one part of fish. This compares with a conversion rate of 12.5 to 1 in algal pasture consisting mainly of blue-greens (Tang and Chen, 1966), and Schuster (1952) gives an approximate conversion rate of 25-35 lb wet weight of algae to produce 1 lb of fish. These views are criticized by Schuurman (1956), who carried out three experiments to test the food preferences of Chanos. He quotes the results of Markus, who showed that the rate of production of Chanos was only 14-24 kglhectare in two ponds with very few filamentous algae, was 80-108 kglhectare where filamentous algae were moderately abundant ; but as high as 170-270 kglhectare in four ponds in which filamentous algae were abundant. The species of algae are not given, but presumably were filamentous green algae. Schuurman divided a single rectangular pond into 24 compartments by low dykes, all compartments irrigated by water taken from the same canal. As this pond had been in use for seven years previously, it would have a reasonably homogeneous bottom soil. The salinity of the 24 small ponds, each having an area of about 800 m2, did not vary significantly from 30x0 throughout the experiment. He randomized three treatments among the 24 ponds as follows: (i) Undisturbed growth of filamentous algae. (ii) Filamentous algae growing in the pond raked together and heaped into mounds, so as to compost slowly and act as green manure, and (iii) Filamentous algae removed repeatedly from the pond. The ponds were each stocked with 25 fingerlings of Chanos of 14 g weight. After 95 growing days, it was found that though the rate of survival was not affected, the fish in treatment (i) had grown by 226 g, those in (ii) by 163 g, and those in (iii) by 152 g. I n the second and third experiments, which were run simultaneously, the 24 small ponds were divided into two lots of 12 ponds each. I n one

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series, small Chanos of 1 4 g weight were stocked and in the other, larger Chanos of 200 g. The biomass of fish stocked in the one series was 350 g, and in the other 4 000 g. The results were the same as in the first experiment. Schuurman sums them up by saying that they give no evidence that filamentous algae are only of value as food for Chanos when in a decaying state, and that average growth was best in the ponds where the filamentous algae grew undisturbed and therefore in a living condition. Another point which seems t o come out of these instructive experiments is the good growth shown by Chanos, both large and small, in the ponds from which the growing filamentous algae were repeatedly removed. The growth observed is hardly inferior to that in which the algae were raked together, and better than half that in the undisturbed ponds. Evidently, a substantial part of the observed growth was at the expense of organisms not directly associated with the green algaeeven the very high biomass of the third experiment (20 g/m2) increased by 12 g/m2. It would have been interesting if Schuurman had examined the stomach contents of these fish. I n Hawaii, Hiatt (1944) found that, while the small Chanos ate mostly blue-green algae and benthic diatoms, larger fingerlings of 1140 cm ate up t o 20% of green algae, 25% of detritus and 43% of diatoms. However there seems to be agreement that the blue-green algal felt, with its associated flora and fauna, is the best food for the young fry of Chanos. This gelatinous mixture is called lab-lab in the Philippines, and tai-ayer in Indonesia. It is carefully cultivated in the fry ponds and success in the rearing of the fry is proportional to success in raising an algal felt which will sustain the growth of the fry to fingerling size. There are many species of grey mullet, but they all seem t o have the same feeding habits. By far the most important is the circumtropical striped grey mullet, Mugil cephalus L. Grey mullet have a filtering mechanism (Gunther, 1861 ; Pillay, 1953), which can reject large particles through the mouth, while filtering off small particles on the gill-rakers. I n those species studied, detritus plays a large part in the composition of the food, together with plant and small animal material. Accounts of the gut contents of Chanos do not mention the presence of abundant soil and grit, but this is always present in the gut of the grey mullets. Because these fish have no masticating organs, the soil ingested may act as a grinding paste (Odum, 1968). When forced along the gut by the very muscular gizzard, this soil helps to triturate the food and so expose it to the action of the digestive enzymes. Ilin (1954) states that in the Black Sea limans, singil (Liza aurata),

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when very young fry, feed wholly on plankton when they first enter the limans in April. I n May, they begin to take zoobenthos, and in June, when the fry are growing into fingerlings, zooplankton drops to 27% while zoobenthos rises to 51% of their food. I n July, zoobenthos falls t o 3y0,while 97% consists of microbenthos. Yashouv and BenShachar (1967) found that the young fry of Mugil cephalus feed freely on copepods, chironomid larvae and cladocerans. Microcystis and various diatoms were found whole and undigested in the rectum. Pillay (1954) found that Mugil tade (Forsk.) is an " iliophage ", because decayed organic matter, filamentous algae and diatoms form its main food, apart from inorganic soil. But very small M . tade feed mainly on blue-green algae, and fry of 2.1 to 4.6 cm begin to feed on detritus and also on important numbers of small crustacea such as copepods, cladocerans and mysids. At this stage, sand or mud is not eaten, so it would seem that the relatively short gut, like that of a carnivore, which the fish has when very small, has an enzyme system able to cope with this kind of food. Odum (1968), working on M . cephalus in Georgia, found that the fish takes its food by sucking up the surface layer of the mud or by grazing on submerged surfaces such as Zostera leaves or stones. He found that the major constituents of the stomach contents were (i) microalgae, including epiphytic and benthic diatoms, dinoflagellates and green and blue-green algae, (ii) decaying plant detritus, and (iii) inorganic sediment particles. He regards the microalgae as the main source of nutrition, though plant debris, no doubt much enriched by bacteria, also appears to be important. Ghazzawi (1933) found that, even when he examined fish from water where planktonic diatoms were abundant, they were not feeding on these but on littoral diatoms and algae with epiphytic diatoms. Sand grains were always present in the gut. Hickling (1970) found that the gut contents of Crenimugil labrosus in English waters included only 5-20y0 of organic matter, the rest being soil. Of this small proportion of organic matter, detritus was always an important part, but equally important were benthic diatoms such as the naviculoids, blue-green algae and small animals such as harpacticoid copepods and nematodes. The very long gut present in this species increases in length relative to the total length of the fish, from 3 times in fish of 20 cm to 5 times in fish of 50 cm. This, and the fast rate of passage of food through the gut, are probably adaptations for the digestion of food of very poor quality, and not an adaptation to a herbivorous habit. Tilapia mossambica also feeds on the algal pasture. There are many

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differing accounts of the food of this fish, but they indicate an omnivorous habit with the exception of larger animals, since this fish does not have the short gut and carnivorous teeth of a carnivore. The gut contents are generally green in colour, which means that the food most usually available is of vegetable origin. Schuster (1952) describes how the introduction of T . mossambica into the Javanese fishponds led to control of the filamentous green algae which had always been a health hazard, and the same has proved true of Indian bheris (Pakrasi et al., 1964). The feeding habits of this fish resulted in a good level of fish production in the Javanese fishponds a t the end of the last war, when Chanos was not available. I n Japan and Taiwan eels are raised very intensively in ponds (Fig. 14). Onodera (1963) states that yields unsurpassed by any other fish culture can be obtained here. However, these are fish which are wholly fed from outside-the analogy is with the broiler house and not the farm. Giving as an example a group of five ponds, Onodera calculates that an initial biomass of 16 110 kg grew in 230 days to one of 32 980. This is equivalent to a stocking density of 0.51-0.71 kg/m2, and an increment in weight of 1.36-2-63 kg/m2 per annum, or 13 600 to 26 300 kg/hectare/year. This certainly is high, but intensive trout ponds regularly give a crop a t the rate of 10 000 kg/hectare/year, and intensive carp rearing in running water can give a crop of 161 kg/m2 or a notional fish crop of 1.5 million kg/hectare/year (Hickling, 1962). The unit rearing pond for eels is 1 000 m2, and the most productive depth, 4 ft. The fodder which is so intensively fed is cheap trash fish such as sardine, skipjack heads, akta mackerel, and silkworm pupae. The food conversion rate varies from 7.6-19.9 per pound of eel (Fig. 14). I n Taiwan, where the culture of eels flourishes, the conversion rate is roughly 13 to 1. Clearly, large amounts of fresh food must be always available, and this could be a serious problem. However, Onodera says that, in spite of the great quantities of fodder necessary, the culture pays. Certainly, in Taiwan, eels are very well-priced, and can stand high production costs. I n Japan and Taiwan, the eel which is cultured is Anguillajaponica, but in the Italian valli it is Anguilla anguilla. The eel comprises 80% of the fish caught in the valli of Commachio, but there is no intensive culture. The elvers or young eels enter in the spring, spend some years in the valli, and are caught when, a t approaching maturity, they seek to return to the sea. They are given no supplementary food, but grow well on the rich food available t o them. This again is the result of the natural fertility of the estuarine environment in which the valli are constructed. Brunelli (1937) points out that decomposing organic

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matter, or detritus, nourishes directly or indirectly a rich fauna including fish, such as the small species of Cyprinodon and Atherina, which are good food for the eels. I n such rich muds, chironomid larvae, which are also good food for the eels, would abound, and no doubt a proportion of the grey mullet young are also taken by the eels. The food of prawns, according to Schuster, is partly animal matter found on the bottom of the ponds, and partly unicellular algae of different kinds, as well as detritus. They feed mainly at night and burrow in the mud by day. Hall (1962) shows that penaeid prawns, while generally omnivorous, show preferences for polychaetes, crustaceans, or a general carnivorous diet, or for vegetable matter. The three species of Penaeidae which are of the greatest importance in the Singapore prawn ponds do not compete for food. Penueus indicus (H. Milne Edwards) feeds mainly on large crustaceans, Metupenueus ensis (de Haan) is chiefly vegetarian and so is the fourth most important, Metapenaeus brevicornis (H. Milne Edwards). M . mastersii (Haswell) is omnivorous, but with a preference for the appendages of large crustaceans. The “ sugpo ” of the Philippine prawn ponds Penaeus monodon (Fabr.), feeds on the blue-green algal felt so important as a fish food. But supplementary foods are also given (Caces-Borja and Rasalan, 1967). The fry are given rice bran and care is taken to see that filamentous algae which would entangle the fry do not develop in the fry ponds. The older ‘‘ sugpo ” are given, as supplementary food, fish, meat and small crabs, which may be ground up and piled in a corner of the pond or some fish is lightly boiled and placed along the shores of the pond, where the prawns can start feeding in the evening.

B. Culture of algal pasture Clearly, success in brackish-water fish farming must lie in encouraging and enhancing the production of useful benthic plants, and their associated animals and detritus, in shallow water. In Italy and Arcachon and in the Russian limans, no measures seem t o be taken. The ponds are too big for such measures in Italy and Russia, and they cannot be drained out completely. So the operators must rely on natural fertility and stock the optimum number of fish, and try to eliminate predators and competitors. Hiatt (1944) and Malone (1969) studied the Hawaiian fishponds, where, according to Cobb (1901), no culture takes place, with a view to suggesting ways of improving the productivity of these ponds, and so of halting the decline of the fishpond industry in Hawaii. Both authors agreed that turbidity was a restricting factor in the productivity

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of the ponds, so Hiatt suggested that the shallow areas of the ponds should be increased, and that inorganic fertilizer might increase the growth of the algal foods on which both the Chanos and grey mullet mainly subsist. Malone, however, found that dissolved inorganic nutrients were not a limiting factor to production, but turbidity was definitely so in limiting the growth of microbenthos. So his results indicated the need for a search for a means of reducing turbidity and thus increasing primary production. As this turbidity is due t o depth and wind stress, it might be overcome by placing rows of wattles or hurdles which would both check water movements and provide a large additional area of surface on which the microbenthos could grow. I n the Indian bheris (Pakrasi et al., 1964) the ponds are dried out in winter and tilled t o expose the soil, thus promoting mineralization and securing some fixation of atmospheric nitrogen by the algae and bacteria present. Fertilizer is not generally used, but quantities of sewage from Calcutta find their way into the creeks which supply the bheris with water and may give rise to excessive growths of algae. Sewage in controlled quantities can be a potent fertilizer, and it has been responsible for some high rates of fish production. Pillay (1954) pointed out that the bheris were on short leases only, since they are a stage in the reclamation of the land, so that there was no incentive to cultivate the ponds. Since the best natural food for the small fish is the jelly-like growth of blue-green algae and their associated plant and animal epiphytes, the technique for producing the " lab-lab " or " tai-ayer " is specialized. Shallow water favours the growth of blue-greens over green algae, as does a high organic content of the soil. For these reasons the fry ponds are always very shallow, organic matter such as rice bran is given a t a rate of 400-1 000 kg/hectare in Taiwan (or several times that amount in the Philippines) and the ponds are repeatedly flushed with the fertile estuarine water, which is then allowed to evaporate and so deposit its nutrients. When dry, the soil may be tilled and levelled, and poisons such as teaseed cake or tobacco waste may be used to eliminate predators and competitors. The teaseed cake also acts as a fertilizer, for the nitrogen content is as high as 2%. The rice bran will also ferment and cause temporary toxicity of the water. I n the Philippines, the depth of the water in the fry pond does not exceed 3-5 cm, and the fry must be stocked within three weeks to have the full advantage of the freshly-grown " lab-lab ". Some success has been claimed by Sulit et al. (1957) in the use of compound inorganic fertilizer of formula N :P :K : : 8 :18 :4. They claimed such an increase in " lab-lab ", that the rate of stocking with

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Chanos fry could be increased from 20 to 50 fish per m2, and mortality was reduced from 60% to zero. I n Java, the cultural measures used to increase the growth of the algal pasture are chiefly draining, and the addition of organic fertilizer. The production ponds are drained in any case two to four times a year for the sorting, counting or harvesting of the fish crop. While the fish shelter in the deep ditches on the inner periphery of the pond, the shallow parts of the pond dry out until the mud cracks open, admitting air to the top few centimetres of the soil. This leads to some mineralization of the organic matter and releases some of the nutrients, and the result is a good cover of blue-green algae on which the fish can resume feeding when the pond is refilled. However, as Schuster says, each removal of water by the emptying of the pond must entail loss of nutrients, and this loss must be balanced against the advantages which can be expected if there is plenty of organic matter present already partially mineralized in the anaerobic environment in the subsurface mud. Then, when drying is carried out, this mineralization continues and more than replaces the loss of nutrients by drainage. Bose (1959) found that the optimum salinity for the growth of the blue-green Oscillatoria in India was 5-17%, during the summer months and Schuster and Lin find that at high salinities the green algae may become indigestible. Lin (1968) writes that the productivity in algal pasture of the Chanos ponds of Taiwan can be increased and maintained by tilling, levelling, and working in fertilizer, according to the condition of the pond and the means of the farmer. The purpose of this work is (i) t o provide a firm and well-levelled top layer of soil rich in organic matter upon which benthic algae will grow, and which should last throughout the period of growth of the Chanos ; (ii),to liberate nutrients from the soil by mineralization; and (iii), t o destroy predators and pests by the use of teaseed or tobacco wastes or modern insecticides. As Taiwan has a winter period when the growth of Chanos ceases and the ponds lie fallow, these essential measures are taken then. A crisis may come in early summer when the fast-growing overwintered Chams begin to crop down the algal beds at a rate faster than they can regenerate. The fish may then even need t o be given supplementary food (see below). A shortage may be much aggravated if the algal beds are infested with chironomid midge larvae. Cerithiid snails may also be very troublesome in both Taiwan and Java. These snails can only flourish wherethe pond topsoil has not yet acquired, or has lost, the firm texture needed for a flourishing algal bed. Measures to ensure the

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growth of a firm algal bed diminish the snail nuisance. The snails can also be controlled in newly-constructed ponds by poisoning with teaseed cake or tobacco waste a t the rate of 200 kglhectare, or by the use of 3 p.p.m. of “ Baylixscide ”. More recently, Djaingsastro (1956)found that cerithiid snails could be controlled by manuring with rice straw. However, the competition of the chironomid larvae for the algal pasture is serious. Lin says that, especially in July and August, when a good supply of benthic algae is most needed to feed the fast-growing Chanos, the chironomids may be consuming 60 to 90 kg/hectare/day of algae, which is almost as much as the Chanos themselves need. A total rate of production of 190 kg/hectare/day which would be needed to satisfy both the fish and the chironomid larvae, is beyond the productive capacity of most ponds, so that the production of fish suffers. Though splendid food for carp and trout in fresh water, these midge larvae are of no use as food for Chanos. Moraover, the burrows they make loosen and destroy algal beds, leading to further loss of fodder for the fish. Using pesticides such as gamma-BHC, Tang and Chen (1959) have claimed control of these cliironomid infestations, with a resulting increase in fish production. Tang (1967) summarizes these measures to increase the algal pasture in terms of the resulting fish production, as follows : Treatment Chanos production, kglhectare 200 Untreated control 800 Use of fertilizers 1000 Use of fertilizers and pest control The euryhaline fish, Tilapia rnossambica, when they occur in the ponds, also disturb the algal beds by scooping out their bowl-shaped nests, and they also compete with the Chanos for food. Lin knows of no selective remedy. However, as in Java, Tilapia make a contribution to the output of the ponds since the statistics quoted by Lin suggest that Tilapia is an important part of the 1 401 tons of ‘‘ other ” production of the brackish-water ponds. But though a first-class food fish, Tilapia is less prized than Chanos. I n the Philippines the green algae or “ lumut ” are considered the preferred food for the Chanos, once they are past the nursery stage. Measures taken t o cultivate the “ lumut ” are much the same as those for “ lab-lab ” ; repeated floodings are followed by a two-week dry period. A thin crust of “ lab-lab ” appears, and this is scraped off. Plates of soil inoculated with “ lumut ” are then planted a t two-metre intervals. These soon grow out t o spread and cover the soil (Esguerra,

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1951) which is flooded to a greater depth than that for the cultivation of “ lab-lab ”. It will be recollected that Schuurman found the green algae good food for Chanos. Rabanal et al. (1951) found that the sown “ lumut ” showed a very rapid growth during the first few weeks, but that later growth almost ceased. I n an experimental culture, the average monthly growth of “ lumut ” in these poiids was 202 g/m2 after one month, 474g/m2 after two months, 491 g/m2 after three months, and 580 after four months. I n terms of kglhectare, the weight of “ lumut ” after four months was 5 800, which compares with 28 250 kg/hectare in very productive ponds on Taiwan (Tang and Chen, 1966), where, however, the production was mainly of blue-greens and diatoms. But Rabanal et al. say that first-class Chanos ponds with a luxuriant growth of “lumut ” may give figures in excess of the above. The maximum growth attained in these experimental ponds was at a rate of 10 930 kg/hectare, a low figure in comparison with those from Taiwan, though it is not certain that like is being compared with like. The alga Gracilaria confervoides (Abagon et al., 1951) in the Philippines crops at a rate of 35 000 kg/hectare/year. From their trials, Rabanal et al. deduce that a prolonged culture of “ lumut ” in a pond may reach its maximum in 2-3 months, so that a culture for a longer period is a waste of time. Fertilizers are used to increase the growth of the algal pasture and so of the fish. The best results have been obtained with organic fertilizers. Even in Java where fertilizer is scarce and expensive, it was found that the growth of the blue-greens could be stimulated by relatively small amounts of green manure, such as cut grass and weeds, and mangrove leaves. The organic fertilizer is applied in the form of heaps at intervals over the pond bottom, each heap being ballasted by a topping of soil. As the vegetable matter composts and rots down to detritus, blue-greens begin to grow at the foot of the heaps and soon spread over the pond bottom; Schuurman (1956) realized that the ponds in which he had heaped up his cut algae might benefit from such a manurial effect. Schuster (1952) says that even ponds exhausted by over-cropping could be restored by 2-3 applications of about 1 500 kg/ hectare each at 3-monthly intervals. The heaped organic manure exposes only a small area t o the water, so that its decomposition proceeds slowly, releasing nutrients without at the same time causing deoxygenation of the water so that the fish suffer. This practice is still followed, for Saanin and Tati Ramelan (1966) give recent data. They say that in the area of Surabaya the effects of manuring with Avicennia leaves were (i) no significant difference in temperature, salinity, pH, nor alkalinity, but (ii) dissolved oxygen distinctly lower at night, and

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carbon dioxide higher than in the unfertilized controls, and (iii), a sevenfold increase of blue-greens, a fourfold increase of diatoms, and a 3.5-fold increase of green algae over the unfertilized control. There was no significant increase in the production of zooplankton. Saanin and Tati Ramelan say that stable manure gives similar results, but high transport costs make the use of city wastes (presumably night soil) and stable manure from outside the pond area, uneconomical. Copra-slime, the residue left after the extraction of the oil, was a successful fertilizer. This easily decomposable by-product was tested at dosages of 400-800 lblacre, and gave rise t o a very good growth of blue-greens. Schuster gives a graph which shows that 80 days after the treatment with copra slime a t the rate of 700-1 000 kglhectare, the crop of algae so increased that the Chanos grew in weight from 20250 g, while in the unfertilized control pond Chanos, stocked a t the same rate, grew from 20 g to only 160 g. Less encouraging results were obtained by the use of molasses, which were chiefly for the control of cerithiid snails. Favourable results were got a t first, but prolonged use quickly led t o the exhaustion of the soil. I n Taiwan, organic fertilizers, such as various oilcakes, rice bran, or pig and chicken manure, may be added to Chanos production ponds at a time when the good growth of blue-greens, with which the season began, starts to be cropped down. Some experimental work has been done in Taiwan on the effectiveness of organic fertilizers in stimulating algal growth. Lin (1968) quotes Yamamura’s tests with benthic algae, chiefly Lyngbya spp. He applied fertilizer a t a standard rate of 1 800 kglhectare, and each trial lasted 60-80 days. No fish were stocked. Soybean cake gave the best results, producing 192g/day wet weight of alga. Then followed a group of fertilizers including fish waste, coconut cake, rice bran, castor-oil cake, night soil, and pig manure, all of which gave about the same amount of algal growth, namely, 162172 g/m2 dry weight. Far behind came pineapple waste (115 g) and potash (105 g/m2/day). This last result could have been expected, for there is ample potash in brackish and sea water. I n some commercial Chanos ponds the effect of organic fertilizers was studied over a period of nine years (1957-1966). The highest fish crop (1 900 kglhectare), was obtained by fertilizing with 1 000 kg/ hectare of rice bran, 970 of legume seed, and 250 kglhectare of peanut meal. The next best results (1 700 kglhectare of fish each) were obtained by fertilizing with 2 000 kg/hectare of rice bran, 800 of legume seed, 100 of peanut meal and 2 000 kglhectare of night soil; and by 1 700 kglhectare of rice bran and 900 kglhectare of night soil, respectively. The poorest result was obtained ( 1 200 kglhectare of fish) with 970 kg/

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hectare of rice bran, 780 of legume seed, 15 of peanut meal and 81 kg/ hectare of oilcake. Not much can be learnt from this, except that rice bran seemed the most effective, as is already well known. On the other hand, inorganic fertilizers gave poor results. I n most cases, ready-mixed N :P :K fertilizers were used even in cases where there was known to be enough K and enough P. For example, Sulit et al. (1957) added an N : K : P fertilizer to a fry pond though they found sufficient K present. An excess of potassium may be toxic (Mortimer and Hickling, 1954). I n the circumstances it is not surprising that there was no notable gain in fish production, but rather losses, after using these fertilizers. Lin was right in considering that inorganic nutrients may have a depressing effect on the growth of plankton and bottom algae of brackish-water ponds. The results given, however, would have been more convincing if the experimental ponds had included untreated controls, and ponds treated with organic fertilizer only. Urea is now a mass-produced fertilizer which can be regarded as lying between organic and inorganic fertilizer, since it contains combustible matter, and could be regarded as detritus under Lackey’s classification (1968). I n some experiments with urea, Djahjadiredja (1966) found that benthic algae (blue-greens) showed a luxurious growth, estimated a t 15-26 tons wet weight per hectare, as a result of a dosage of urea of 2.5-7 qt per hectare. The urea was found to be toxic to fish, so it should be applied a fortnight before stocking with the desired species of fish, and in the meantime the urea will have killed off unwanted competitors or predators. Supplementary foods are not given in brackish-water ponds to the same extent as in freshwater fish culture, but are often used in special conditions. For example, Chanos fry can be fed with rice bran and yolk of egg (Schuster, 1952), or with powdered milk, rice bran, and cornmeal enriched with terramycin and a proprietary product “ Vigofac ” (Ronquillo et ab., 1957). But Lin (1968) quotes the results of Yamamoto, which were that young Chanos fry absolutely need bluegreen algae and diatoms as food, and suffer a high rate of mortality when fed on artificial foods such as flour, soybean meal, rice bran and peanut meal. Lin (1968) thinks that much of the rice bran and oilcake, applied t o the growing ponds in summer when the fish crop is threatened by the exhaustion of the algal pasture, is used directly as food by the fish, rather than indirectly as fertilizer. Tang (1967) goes further in advising the feeding of pelleted foods to forestall overgrazing of the algal pasture.

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These foods contain 20-25y0 protein, 4-8% of fat, 40-50y0 of nitrogenfree extract, 10-1470 of fibre, and 2-5% of yeast. I n the culture of Chanos in the Philippines, Mane et al. (1952) state that there also, when the fast growth of the fish exhausts the algal pasture, other foods, or algae from outside sources, may be given as supplementary food. Abagon et al. (1951) name, as such supplementary foods, rice bran, rice straw, and " digman )' (Naias and Ruppia) or " lumut " (filamentous green algae). But the best supplementary food is " gulaman dagat )', Gracilaria confervoides. This alga grows in great abundance in Manila Bay from November to June. It flourishes in water of salinities between 5 and 30%,, with 10-15%, as the optimum. The alga is abundant enough to cover great areas of flats exposed at low tide and also in water as deep as 8 ft, but it seems to flourish best in waist-deep water. It is easily collected by wading and collecting the weed with the feet, and photographs show boatloads of Gracilaria being delivered to the sshponds. The nutritive value of this Gracilaria is high, so that very heavy applications are not needed. These may be given to the fish in several lots, or in a single application, which may vary from 200-500 kg (presumably per hectare). One big application is favoured because labour is saved, and also because the alga not only remains edible for a long time but may even grow. Two or even three crops of Chanos a year become possible when Gracilaria is freely available. For instance, the ponds may be filled with Gracilaria in December to January and stocked with Chanos fingerlings of 4-6 inches ; these fish can be harvested in May or June. The pond is then fallowed for two months, to allow the natural growth of green algae, or " lumut ". This algal crop would benefit from the excess organic matter and nutrients left over from the surplus Gracilaria and the faeces of the fish which had fed on it. Then the pond can be restocked for a harvest in December to January when fish prices are high. So beneficial is the use of Gracilaria that the rate of stocking of the pond can be increased to three times that of an untreated pond in which green algae are the natural food available. As the cost of the Gracilaria is low, the gross return in the value of the fish crop may be 15 times that of the cost of the algae. It is the general view, say Abagon et al., that the income of a fish farm can be doubled by the use of Gracilaria as a supplementary food, and they would even like to see it dried for use in the off-season and where it is not naturally available. Various supplementary foods may also be given to grey mullets.

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Blanco and Acosta (1958) say that the supplementary foods for grey mullet in the small subsistence ponds on Luzon consist of boiled " camote )', rice bran, and corn meal, on which the fish grow fast. In the Russian limans, the overwintering grey mullet are fed with bloodworms, Daphnia, etc. and in Israel, where the grey mullet are grown in ponds (in this case, fresh water or very slightly brackish water) in company with common carp and species of Tilapia, they share with these other fish the supplementary foods such as oilcakes and grains which are given on a large scale t o achieve the very high rates of fish production now customary in Israel. I n Japan, where grey mullets are grown together with carp or eels, they share the supplementary foods given to these other fishes, but probably feed mainly on the residues and faeces which fall to the pond bottom (Asia Kyokai, 1957). With the intensive rearing of the yellowtail and the Kuruma prawn in Japan, the whole of the food supplied is supplementary food, since the fish and prawns being cultivated are far too densely stocked for natural foods to play any part in their growth. Success must depend on finding a reliable source of food a t a price, delivered and dispensed to the fish, which will enable the finished fish to be sold at a profit. I n Taiwan, I was told that suitable trash fish could be bought in the market for $2 per Ib, that the conversion rate when fed t o eels was 13 to 1, and that the eels sold a t the luxury price of $80 per lb. At such prices, there is a margin of profit, especially as the ponds also contain fish, such as grey mullet, which feed on the food residues, and add to earnings without adding to the cost. VI. MANAGEMENT OF BRACKISH-WATER FISHPONDS A. Tilapia Tilapia, is the only fish cultivated in brackish-water fishponds which will breed naturally there. I n fresh water it is a disappointing subject for fish culture because in captivity it runts down to a small and commercially valueless size. Various stratagems have to be applied to avoid this runting and get marketable fish (Hickling, 1963). However, in brackish water, maturity seems to be delayed somewhat, so that Tilapia grown there include a larger proportion of saleable fish. Schuster (1952) describes the first appearance of this East African fish in Javanese waters in 1939, and by the end of World War I1 it was found t o be firmly established in the Javanese fishponds. It proved a blessing in those distressful days when the customary cultivation of Chanos was almost at a standstill. Because there could be no maintenance of the pond systems during the war, they had largely reverted to the appear-

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ance of the salt marsh, from which they were made, by the end of the war. Though conditions had prevented any of the usual measures of pond maintenance, the Tilapia found suitable conditions, so that they gave rise t o a productive fishery, chiefly with cast nets a t monthly intervals. Nevertheless, the pond soil showed no sign of exhaustion, the production of blue-greens and diatoms was abundant. The green algae which also flourished were kept in check by the Tilapia, which thus also helped to solve a health problem, for malarial mosquitoes bred dangerously among the floating masses of green algae. Schuster found that, in brackish water, Tilapia could grow t o a weight of a pound or more in eight months-a far better performance than in fresh water ; but commercially the best results were obtained by marketing at about 3-5 ounces weight, which would be at lengths of about 17-22 cm. It proved possible, in fertile shore ponds, t o cultivate prawns and Tilapia together, the Tilapia breeding naturally, and the prawns entering the ponds as larvae with the filling water. Schuster quotes statistics of the fishpond system, " Heemrad ", near Djakarta where, in 1947-8, prawns were produced a t the rate of 60-85 lb per acre per annum, as well as 170-260 lb of Tilapia. Tilapia has established itself in the Singapore prawn ponds, and some reasonably well-grown specimens (up to 270g in weight) can be found when required. Le Mare (1950) showed convincingly the value of T . mossambica as a fish for brackish-water fish culture. He empoldered an area of saline swamp in Singapore, on which were eight Malay houses, built, as is customary, on stilts over the water, and therefore whose household wastes fertilized the area. No other fertilizer was used, and the salinity was maintained at 20%,. The shrimp Acetes, penaeid prawns, and fish, especially grey mullet, entered the pond with the water, and the filled pond was stocked with 5 cm Tilapia rnossambica. These fish grew very rapidly and reached a maximum size of 36 cm in eight months. They were fished by cast-net and by draining and gave a crop of fish a t the impressive rate of 1 500 lblacrel annum. Pakrasi et al. (1964) state that Tilapia and carp do well in the brackish-water impounded paddy fields in the delta area of West Bengal where they play a part in the high rate of fish production ( 3 600 kglhectarelannum). Schuster found that Tilapia could be grown together with Chanos. In two ponds of total area 240 acres, there was a fish crop of 99 lb of Chanos, 227 lb of Tilapia, 31 lb of other fish, and 114 lb of prawns.

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When I was in Djakarta (then Batavia) in March, 1947, I was told that the " Heemrad " ponds had produced 4 254 kg of Tilapia and 1 682 kg of grey mullet and prawns in February to March 1947. B. Russian limans I n the Russian limans there is hardly any pond management. The very large size of the limans, often several thousand acres in area, would make most measures impracticable. As they are mostly shallow, they warm up early in the spring, and the naturally-spawned fry, chiefly of the golden grey mullet, Lixa aurata, approach the coasts in spring a t sea temperatures of 5-6"C, and seek to enter the limans, where the water is slightly warmer. They are able to react to temperature differences of less than 1°C. As they ascend the channels leading from the sea to the limans, they may be caught and counted, so that there may be come control over the rate of stocking. If such counts show that there are insufficient fry, these may be supplemented with fry bought elsewhere. Other fish also enter, notably the flounder and atherines. Some small gobies are permanent inhabitants. At first the young mullet fry, which have their maximum migration in the latter half of May, scatter along the shores of the liman, especially where there is a good growth of Zostera and Ruppia. By day, they browse in these shallow areas, but a t night they go into deeper water. By July, when the fry have grown to small fingerlings, they quit the shallows and feed on the detritus and microbenthos of the deeper silty bottom of the liman. Towards autumn, when the temperature of the liman begins to fall, and when evaporation has lowered the level of the liman below that of the sea, a current flows down the channel from the sea into the liman, and the now well-grown fingerlings, or " chulari ", react t o this current by swimming against it up the channel towards the sea. They then have a maximum weight of about 200 g, though in limans with poor feeding conditions they may be much smaller ; however, the " chulari " are marketable a t these sizes. Meanwhile, during the summer, fences with more or less elaborate traps will have been put up across the channels, and in these the migrating fish are caught. Because these fish are still far from maturity when caught, fears have been expressed for over a century that the main mullet fishery in the Black Sea may be adversely affected by the capture of these fish from the limans before they have had the chance to breed. But Babaian et al. (1967) show that natural fluctuations in the abundance of the year-classes of grey mullet in the Black Sea far exceed any

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possible effect of withdrawing from the potential spawning stock those fry reared in the limans. One would have thought that the fact that the grey mullet fishery in the Black Sea still flourishes after 100 years of doubt would have settled the matter. Clearly, mullet rearing in the Russian limans depends on succesful stocking and, when fry are few, the considerable expense of keeping the channels open and fitting up the fences and traps is not worth while. Therefore, when the golden grey mullet are scarce in the spring, Zambribortch (1962) suggested that more use might be made of the other species of grey mullet, notably Mugil cephalus and M . saliens. Though in the spring immigration of fry, the L. aurata are by far the dominant (70-95%), M . saliens may occasionally comprise 25%. But in the later stages of the fry immigration (July to September) the immigrants include a substantial proportion of both species, which, because of their late arrival, cannot attain commercial size before the winter. If overwintered, these late fry would grow to marketable fish during the next summer. Because of this, wintering ponds warmed by underground springs which have a year-round temperature of about 10°C, have been put up in the Shabolat liman, into which the fry are guided from October to December. Here they are sheltered from the fierce winter by screens and covers until, in March and April, they return t o the open liman to resume their growth. This closely resembles the overwintering of small fish in the Italian valli. An effect of this overwintering is that the harvest of fish from the Shabolat liman may consist largely of M . saliens and M . cephalus. Of course, the ideal remedy would be for the golden grey mullet to be bred artificially so as t o make the liman operators independent of the natural supply of fry, and there can be no doubt that this is being attempted.

C . Hawaiian jishponds I n the Hawaiian fishponds (according t o Cobb, 1901) there is practically no attempt a t fish culture, a statement which was also true of the barrachois of Mauritius which are so similar. I n Hawaii, Chanos and grey mullet are the chief fish raised. The young of these, and other fish, may be induced t o enter the ponds on the rising tide through the opened gates. If not enough fish enter, the pond owner or manager may hire fishermen, a t the right season, t o seine for young Chanos and grey mullet and place them in the ponds t o grow to a marketable size. I n the pond itself there may be some fishing with seines and gillnets, which is easy because of the shallowness of the ponds which may be only 10 cm deep a t low tides, and 100 cm a t high tides, the tidal rise and fall being small in these oceanic islands. But A M I3 - 8

7

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most of the fish are caught in the sluice gates, into which they are attracted by an inflow of water. Cobb does not say how long the fish remain in the ponds to grow to a commercial size. D. Brackish-water ponds at Arcachon There was also no management of the 300 hectares of brackishwater ponds a t Arcachon. Even the shallow “ jas ” were not tilled, or a t least no mention of tilling is made by Am6 (1938) or le Dantec (1955). The ponds were stocked haphazardly by enticing the young mullet and eels into the sluices, by allowing a slow current to flow out of them in the spring (as in the Russian limans), and there seems to have been no control of the rate of stocking. Harvesting was done by beating the fish into trammel nets or, if only a few fish were needed, they could be lured into the sluices by allowing a slow current to flow in from the sea. I n the winter, the fish too small for market would shelter in the deep peripheral ditches, though le Dantec says that there could be severe mortality during very cold weather. Fontaine (1968) speaks of this industry as in disuse, and hoped for its future revival using a more complete system of fish culture, especially the artificial breeding of grey mullet for the controlled stocking of the ponds.

E. North Italian lagoons Even in the great 100000 hectare pond complexes in the north Italian lagoons there seems t o be no cultivation, or none is mentioned by Beadle (1946), Vatova (1962), d’Ancona (1954), or de Angelis (1960). The pond management consists chiefly in the maintenance of the sluice gates and deep peripheral channels, which is done during winter. Probably, the very large size of the ponds (300-500 hectares) makes cultivation impracticable, even though, a t times of low water level, there may be very large areas of the pond bottoms uncovered (Fig. 11). I n the early spring the sluice gates, and also the smaller subsidiary gates called ‘‘ cogolere ”, remain permanently open so as to attract the maximum number of fry of grey mullet and elvers, though considerable quantities of other useful fish, such as Sparus, Chrysophrys, atherines, and bass, also enter. From about the second week in May, the sluice gates are opened only on the high tides, so as to take in the maximum amount of sea water. So long as the immigration of young fish into the ponds continues, the smaller fish are guided t o sheltered separate ponds called “ sergei ”. I n these small and sheltered ponds, the young fry brought from elsewhere to supplement the naturally immigrating young fish are also placed. When these fish have become acclimatized t o the pond conditions, they can swim out into the main pond.

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FIG.11. View across an Italian brackish-water fish farm (valle). Over-wintering ponds sheltered by trees, in foreground; main pond in background. Note low water-level in main pond due to summer evaporation. (Photo : Professor L. 8. Beadle.)

During the rest of May and June, the sluice gates are kept closed, and are only opened a t high water if the water-level within the pond falls too much through evaporation. I n July and August, when evaporation is intense, sea water may be admitted, or fresh water from the canals, until the water temperature begins t o fall in September. The water in the ponds should now have a high salinity, and its IeveI be low through evaporation (Fig. 11, taken in August). This ensures that when fishing begins, a strong flow of water will enter the pond through the main sluice, in which are placed the fishing traps.

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I n autumn and until the end of December, as the temperature falls, the fish in the valli endeavour t o return t o the sea ; a t high tide the main sluice gate is opened, and the fish press seawards against the inflowing current. This migration is especially strong on stormy nights. The eels tend t o migrate most on moonless nights, but the grey mullet at full moon (de Angelis, 1960). It will be noticed that the device of guiding the fish into the traps by using a flow of water is world-wide. The catching and sorting traps, which tend t o become ever more elaborate, are placed in the sluices. Metal grids of different mesh sizes sort out the marketable fish, while the smaller fish are guided to groups of small sheltered ponds called " conserve ". These are well protected from the cold winds by trees. The smaller fish are overwintered here (Fig. l l ) , (being fed in the meantime as required) to resume their growth in the spring. Thus there is, in these valli, a succession of fish crops in autumn and winter. A few fishing operations may also be done in the ponds with nets in the summer.

F. Bheris of West Bengal Descriptions of the bheris, or brackish-water fish farms of West Bengal, have been given by Pillay (1954) and by Pakrasi et a2. (1964). Pillay wrote rather pessimistically of their present position and future, of the lack of incentive t o do culture operations, of silting up, and neglect. Pakrasi et al. painted a better picture, though they listed many serious problems, of which floods, drought, and silting were three, together with a lack of exact information on the best means of operation, and adverse socio-economic factors. Saha et al. (1969) wrote as though the best years of this industry were in the past. The decline, they think, is due t o over fishing in the rivers and creeks, leading to a scarcity of fish fry for stocking, so that the operation of the ponds scarcely pays. However, much is being done to improve the situation by research into the occurrence of fry, and the supply of fry which enter the ponds can be supplemented by seining the nearby areas of shallow brackish water, where many fry are found. From the end of February, brackish water is admitted to the ponds on spring tides. During the full moon and new moon quarters, the fry of the commercially valuable fish are generally plentiful, and in order t o obtain a good stock of these for the ponds, not only are the main sluice gates opened, but additional gaps may be cut through the embankments. To avoid excessive pressure on these embankments, excess water may be let out at low tide. Provision is made t o prevent the escape of the fish fry caught on the rising tide. When the pond

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operator considers that the pond is sufficiently stocked, the gates are closed, and the supplementary gaps in the embankments are also stopped up. From April to September, the work consists of maintaining a working depth of water, repair and maintenance work, and guarding against thieves. Where a bheri has several compartments, as in the one studied by Pillay (1954),the water is distributed equally between them, and where there are nursery ponds, the small fry are guided to them by the water flow. The salinities of the bheris vary from 24.5-35.0%, (Pillay) or even 36%, and above in the summer (Pakrasi et al.). The principal fish whose fry are swept into the ponds with the inflowing water are two species of grey mullet (Mugil parsia [Blkr] and M . tade), two predatory fish, Lates calcarifer (Blkr) and Mystus gulio (Hamilton), Pristiopoma hasta (Blkr), and prawns, which are among the most valuable of the products of the ponds. With the presence of powerful predators such as Lates, a considerable proportion of the other small fish and prawns must be sacrificed as food. Schuster estimates that each lb of Lates is gained a t the expense of 8Ib of other fish, but as Lates is a highly-priced fish some sacrifice is justified. During the summer months, there is some subsistence fishing in the ponds, but the serious fishing begins in September. Additional fishermen may be taken on, and the ponds are gradually drained. During draining, fishing may be done with seines and gillnets into which the fish are beaten, but as the ponds empty the remaining fish collect in the deeper ditches and are induced to enter non-return traps by a current of water. Marketing and transport are a problem, and the deep ditches used as nursery ponds in the spring may be pressed into service as storage tanks in which the fish can be kept alive until transport and markets are available. I n a hot climate this is a matter of urgency. One interesting way of catching the fish in these ponds is used in one form or another the world over. Cut brushwood is heaped up in the pond and the fish take shelter in these, partly for protection, and partly for food, since the brushwood will be a good substrate for the growth of the algal felts on which fish depend directly or indirectly. When fishing is to take place, the heaps of brushwood are surrounded by nets and the brushwood removed. During the winter the ponds lie dry, and may also be tilled. This is known to encourage the growth of blue-green algae and to assist in the fixation of atmospheric nitrogen and to mineralize the organic material in the pond soil.

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G. Prawn ponds of Singapore The prawn ponds of Singapore have been described by le Mare (1949), Hall (1962), and Tham (1967). Le Mare describes the ponds as having been introduced t o Singapore in the early 1900s by Hokkien Chinese immigrants. The best sites are on low-lying tidal swamps in muddy river basins where the catchments are so small that there is no great risk of an excessive fall in salinity even after heavy rains.

FIG. 12. A prawn pond in Singapore. The main sluice is seen from the inside. Note the screens in the gate, the turn buckles to the left and tho nets drying in the sun. There is an embankment of mud slabs revetted with mangrove stakes.

Hall points to the commercial value to which these swamps have been put by the simple expedient of clearing the mangrove growth, including the felling of the mangroves, and putting up rough mud embankments to enclose prawn ponds of an area varying from 5-50 acres. The pond in which Hall did his observations was one of 24 acres, with three sluices in use, and one sluice filled in. Le Mare wrote of a pond of 30 acres with 10 sluice gates. No cultivation is done in these ponds nor is fertilizer used except in the form of the tea-seed cake, which is usually strewn in the ponds twice a year to kill off unwanted fish, and composted mangrove leaves. But clearly the considerable fertility of these ponds is due to the regular and frequent floodings with the silty estuarine water.

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Le Mare says that success with a well-sited prawn pond is largely dependent on the correct use of the sluicegates (Figs. 12 and 13). The tides permit fishing on about, 20 days per month, and during the day water is let into the pond through all the sluice gates as the tide rises. A head of water may be built up by keeping the sluices shut. On opening them, there will be a rush of water which will carry into the pond the fry of the prawns, which are feeble swimmers. Then, still in daylight, water is allowed to escape from the pond so as to equalize the

FIG.13. The main sluice seen from the outside. When the gate is opened water rushes out through the fine meshed net which is supported by 8 wooden trough. The prawns are filtered off.

pressure on both sides of the embankments ; there need be no loss of prawns because they remain buried in the mud of the pond by daylight. However, le Mare says that, after heavy rain, some prawns may swim to the surface during the day, and a net may be put into the sluices to catch them as the flood waters escape. Normally, fishing is done a t night. As much water as possible having been taken into the pond during the rising tide, a t the turn of the tide a long bagnet of fine mesh, mounted on a frame, is placed in the sluice. As the water rushes out of the sluice, the larger prawns, swimming freely in the water in the darkness, will be swept

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into the net (Fig. 13). After a couple of hours of fishing, or according to the state of market demand, the sluices are closed, the catch emptied out of the net, sorted, and iced for the morrow’s market. The capture of the fry of the “ Sugpo ” prawn, Penaeus monodon, in the Philippines has already been described. The fry may be cultivated in company with Chanos, as is more usual, or as a monoculture, as is now being done by a few large-scale fishpond operators. CacesBorja and Rasalan (1967) show that a more valuable crop is obtained by the monoculture. I n both cases, the fry are first reared in nursery ponds a t a high density, namely, 30-50 per m2, and fed on the “ lab-lab ” for about 14-2 months. They are then transplanted to the growing or rearing ponds at a much lower rate of stocking, namely 1 per m2 where the prawn is raised alone, or 1 per 2 m2 where the prawns are being raised together with Chanos. Thus there must be a very low rate of survival, and one of the reasons is the difficulty of managing the prawns. Traps are used to catch the young for transplantation t o the rearing ponds or the young may be driven from one pond to the other by disturbing the pond. The prawns burrow readily and have no schooling habit. There is the same difficulty and loss on harvesting, which may be done by means of traps or by the same method as used in Singapore, namely, t o fish at night with a net in the main sluice after the water in the pond has been raised to the maximum level a t high tide. Supplementary foods are given, as described earlier, and the giving of some animal food not only greatly increases the rate of growth, but also the rate of survival. The prawns reach commercial size at 5 months to one year of age, and production is about 250 kg/hectare/annum in monoculture, or 100 kg/hectare/annum when grown with Chanos.

H. Fish and prawn culture in paddy Jields Pakrasi et a2. (1964) also describe fish and prawn culture in impounded paddy fields in the northern and less saline parts of the delta of the Ganges. Here, in summer, the inflow of inland drainage water brings the salinity down to as low as 0.3%,, and the intake of saline water is restricted to the months of July and August. The fish which enter the fields with the flood water take refuge in the deep peripheral ditches, which are also the borrow-pits from which the spoil was taken to make the embankments. When the salt-resistant varieties of paddy are planted and the fields are flooded for the growth of the crop, the fish, which include Tilapia as well as grey mullet and carp species,

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find good feeding conditions, and so also do the very abundant prawns. When the fields are drained t o take the paddy harvest, the fishing rights are leased out t o skilled fishermen who use traps and cast nets. These fisheries are very productive, cropping a t the high rate of 3 600 lb/acre/annum (Pakrasi et al., 1964). I n Kerala State in south western India, paddy fields border the brackish-water lagoons, which form a system which extends for many miles behind the coast. These fields grow a crop of paddy during the rainy season, which ends in September, when inland drainage water freshens the lagoons. This crop is harvested in October. Then, with the dry season, the salinity of the lagoons increases, and preparations are made to take a crop of prawns by raising and strengthening the low earth embankments which surround the paddy fields and installing simple sluice gates in them (Menon, 1955). These sluice gates are used, as has been described for Singapore, to carry in on a rush of water as many prawn fry as possible. This process is repeated several times t o ensure the greatest possible number of fry in the fields. The fry grow so fast in the fertile paddy-fields that fishing for those grown to commercial size is soon begun, as in Singapore, by emptying the fields through long nets set in the sluices. This fishery is repeated four to five days after full and new moon throughout the winter, during which the salinity of the lagoons can reach 33%,. At the end of winter, the rains flush out the salt from the fields and a new crop of paddy is sown. Thus these fields give two crops a year, one of rice and one of prawns. About 11 000 acres give a prawn crop which, after local requirements, still allows for the export of 3 800 tons of high-priced dry prawn meat. As with the bheris of West Bengal, the owners of the paddy fields usually lease out the fields for the prawn crop and they may thereby derive, as rent, an additional income of Rs 100-300 per acre.

I. Chanos culture in Java I n Java the traditional method of raising Chanos is t o take one crop a year from the less brackish inland ponds and two crops a year from the more marine and saline ponds. The success of the latter is to have two overlapping groups of Chanos growing in the same pond. I n the inland ponds the calendar of operations is much as follows (Schuster, 1952). I n October, about 1 000 Chanos fry per acre of pond surface are placed in the fry ponds, and in November the grown survivors are admitted to the rearing ponds. I n December, following the clearance of vegetation, the growing fish are admitted to the deeper parts of the ponds and by February to all sections of the ponds.

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In March and April, the cutting of the pond vegetation and its disposal for use as fertilizer is followed, in dry years, in May, by the beginning of the cropping of those fish which have grown to commercial size of 8-12 ounces. In June and July cropping continues by driving the fish successively into the deep ditches and thence t o the sluice gates where

they are fished out with d;pnets. In August all the remaining Chams are cropped by bailing out the water from the ponds, and September is devoted to the preparation of the nursery pond for the next crop and the restoration of the ditches, embankments, and sluices. In these inland, almost fresh water, ponds, the year is an almost constant battle to control the aquatic vegetation. I n the more saline shore ponds, where the sea water has direct access, a more continuous raising of marketable fish is possible. The fry of Chanos are available twice a year in Java, once from a spawning during the west or south-west monsoon, and once from a spawning during the east or north-east monsoon. The former prevails from about June to September, and the latter from about October to March or April. Again taking the month of October as the arbitrary start of the Chums calendar, about 1 000 fry per acre from the west monsoon crop are placed in the nursery ponds ; meanwhile, the east monsoon fish, now about four months old, are growing in the deeper parts of the rearing ponds. I n November, the survivors of the October west monsoon fry will have grown large enough to be released into the rearing ponds. The east monsoon crop of fish is now counted. Those of marketable size are culled out for sale and extraneous fish are also removed and sold. In December, the capture and sale of the east monsoon crop is continued, and now the well-grown fingerlings of the west monsoon crop are admitted to the deeper parts of the rearing ponds and mixed with the remainder of the east monsoon crop. Thus two generations of Chanos are growing together in the ponds, a cultural practice which has proved of great value, for instance, in the culture of carp in Israel. In January and February the capture and sale of the east monsoon crop continues, but the west monsoon crop is still too small to be sold and if caught is released, Repair work on gates and embankments is done at about this time. I n March, the rest of the east monsoon crop is culled out and sold, and the west monsoon crop, now nearing marketable size, are counted and extraneous fish removed and sold. In April and May the capture and sale of the west monsoon crop begins and, at the same time, the fry ponds are prepared for the current

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east monsoon crop, which is stocked a t a rate equal t o 250-300 fry per acre of pond surface. I n June, July, and August, the east monsoon crop is admitted to the rearing ponds and is then mixed with the remainder of the west monsoon crop, which continues to be culled out and sold. A few specimens of the west monsoon crop are retained to be grown to very large fish of 2-8 lb weight, for which there is a limited demand. I n September, the Chanos calendar ends with preparations for the reception of the new west monsoon fry, and general maintenance work. I n most of the months of this calendar there is an important sale of prawns, which are usually caught in traps placed along and at right angles to the pond banks. At night the well-grown prawns emerge from their hiding places in the mud and swim about the ponds parallel with the banks. Thus they are caught in the traps, which are made even more effective by lamps placed a t their entrances. Unlike the " sugpo " prawn of the Philippines, there is no culture of the prawns in the Javanese ponds. The young larval and post-larval stages of these penaeid prawns are carried into the ponds with the filling water, and the only cultural measure is t o try to take in as many prawn fry as possible, using the methods already described in the case of the Singapore prawn ponds. As prawns sell well and are cropped continuously, the pond operator has a steady income to bridge intervals in the sale of Chanos and, in consequence, says Schuster, they are usually wealthy people. Their resilience was well shown during the depression years of the 1930s, when they were able to find the capital to improve and extend their ponds using the cheap labour then available. As in the Singapore prawn ponds, the best catches take place a t night when the prawns are active, for during the day they burrow in the mud, Schuster says that millions of young prawns must enter a pond to give a normal yield of marketable prawns, so that overstocking with fry is hardly possible. The mortality of the young prawns must be exceedingly high. The above is the usual procedure where the pond operator handles Chanos from the fry to the market, but a more efficient trend is apparent in both Java and the Philippines, namely, the rearing of fingerlings for sale t o the farmers by specialist fry dealers. I n the usual way, a farmer can only expect a 30% rate of survival of the planted fry, but these specialists may achieve 70%. The progressive fish farmers buy these fingerlings, which are past the dangers of infancy, and rear a succession of them for market, with only a lO-12% loss. Three or four successive crops can be raised in a year, so that a well-managed pond can be

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intensively used. The dealers bring the fingerlings to the ponds by livewell boat or barge. No doubt these fingerlings are expensive, but so also must be the few survivors of the fry bought by the non-specialist farmers. The fast growth and intensive rearing of the bought fingerlings must give a good margin of profit. Chanos fry can be raised to fingerlings in the Philippines and may be kept on a subsistence ration for as long as two years, so as t o be available for sale a t times when the supply of fry is short. Such specialist fry dealers must play a most useful part in the industry. A variation of this type of continuous cropping is to be found in East Java, according to Schuster (1952). Some of the pond operators keep a large stock of fingerlings which they transfer to the rearing ponds a t a rate of stocking per acre carefully calculated to give a succession of marketable Chanos all the year round.

J. Chanos culture in the Philippines I n the Philippines, Chanos fry are available for capture from March to September with the peak in May t o June. Specialization in rearing Chanos has gone far, and though the common practice is still for each farmer to rear his own fry to marketable size, the rearing of the fry to the fingerling stage has become an industry in itself, (Mane et nl., 1952). A brief account of the management of the fry ponds has already been given, and the management of the rearing ponds is similar, except that the object is to grow " lumut " or green algae rather than bluegreen algae. There are repeated flushings of the pond bottom followed by a dry period. A thin crust of " lab-lab " forms, which must be removed (Esguerra, 1951). Then water is allowed to enter, and pieces of soil infected with green algae are planted to give the new crop of green algae a good start. Frey (1947) also states that the rearing ponds are flushed out and sun-dried before the Chanos fingerlings are stocked. The ponds are then flooded with saline water to a depth of 10-15 cm, because this greater initial depth of water will favour the growth of the green filamentous algae, or " lumut ", rather than the complex of blue-green algae or " lab-lab ". After the growth of " lumut " has well started, the depth of the water is increased to a depth of 30-50 cm. Mane et al. (1952) state that, in the Philippines, there are big holdings of brackish-water fishpond areas, some as large as 1 0 0 0 hectares. They agree that shallow water (3-5 cm) favours the strong growth of " lab-lab " and deeper water that of " lumut ". After the fingerlings have been stocked, a t a rate of 1000-1 500 per hectare,

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they need little attention so long as abundant food is present, except for the frequent renewal of the water. But should this natural food become exhausted, other foods such as digman (several species of Hydrocharitaceae) or gulaman dagat, (Gracilaria sp.) may be given. Mane et al. (1952) state that each pond system includes a catching pond, about 20-30m square, and in this the marketable fish are collected for sale when the ponds are drained. Blanco and Acosta (1958) describe a rural-industrial farming of grey mullet and other fish in Luzon, in small brackish-water enclosures of about $ hectare area, fitted with wooden or bamboo gates. These ponds are stocked haphazardly, as are those of the Indian bheris, by opening the gates on the rising tides and closing them when the tide falls. The fish are held in these ponds for 6-8 months and then used or sold. The fish chiefly depend on the natural food available in the pond but supplementary food may be given. Grey mullet, which are among the most important of the fish reared in these ponds, grow fast on these foods. Blanco and Acosta point out that at this subsistence level, operational expenses for the ponds are very low. K . Fishpond management in Japan Accounts of fishpond management in Japan are hard to come by, but, in their article, Blanco and Acosta (1958) briefly describe the culture of grey mullet in Japan. I n March and April, young Mugil cephalus about 3-6 cm long, swarm in the estuaries of the rivers, where they are caught and transplanted to rearing ponds in brackish water or salt fields. The rate of stocking is 1-3 individuals per m2. The fish grow t o a commercial size of 200g by the end of October or November. The Japanese fish farmers do not grow the grey mullet alone, but together with carp or eels or both, in the same pond, and sharing the same foods such as rice bran and flour. This is confirmed in Asia Kyokai (1957) where it is stated that the young grey mullet migrating up the rivers are caught and placed in ponds where they are grown together with other fish, chiefly eels. This culture takes place in brackish, more frequently than in fresh water. No artificial foods are given t o the grey mullets, which feed on the residues of foods given to the other fish. There is no need t o doubt that these grey mullet would be feeding on bottom soil enriched by the faeces and food fragments left by the other fish. The writer saw the culture of eels in Taiwan, but this time in a fresh-water pond. The fish were fed on trash fish bought from the fish market in Taipeh, the capital, for 2 local dollars per kg (Fig. 14). The conversion ratio was said to be about 13 t o 1, so that crude costs per

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kg of eel would be about 26 local dollars. As the eel is a highly-priced fish, selling a t 80 local dollars per kg, there is a margin in hand for the other expenses of culture and for a profit. More than that, the pond develops a rich plankton and bottom fauna and flora, so that it is also stocked with plankton-eating silver carp, common carp, and grey mullet, all of which would add t o the income of the pond without adding t o expenses. The technique, like that of the culture of the ‘‘ ayu ”, is a relic of the days when the island was under Japanese rule, and is the Japanese technique transported abroad.

FIG.14. The culture of eel (Anguilln japonica) in Taiwan. A double basket load of trash fish from the fish market has been offered and is covered with feeding eels.

L. Fish culture in Taiwan I n Taiwan, brackish-water fish culture reaches its highest technical level. Grey mullet are grown in the brackish-water ponds on the west coast (Tang, 1964) but the writer has seen no description of their culture and management. This neglect of grey mullet in favour of Chanos is the more peculiar, in that the former grow as fast (Schuster, 1952, Blanco and Acosta, 1958) and fetch the same price (Schuster, 1952). Their young are caught in brackish water in the same way, and their food is so much the same that they are competitors (Hiatt, 1944).

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I n Taiwan, Chanos are cultivated on the warm soutli-west coast, but farther north on the west coast the winter temperature falls too low, so the more temperature tolerant Mugil cephalus takes its place. A further advantage of grey mullet over Chanos is that the former will soon be bred in captivity, whereas the latter cannot, as yet. Lin (1968) gives an up-to-date account of the farming of Chanos in Taiwan, which has frequently been quoted in this chapter. He

FIG.15. The main sea water supply canal t o a pond complex in Taiwan. On it there is a bamboo raft with piled traps to catch ScyZZa serrata, the valuable mangrove crab. Note control sluice across the canal and the sluice on the left for admitting sea water to the farm.

makes no mention of the culture, in the same ponds, of prawns and crabs, nor of extraneous fish, which make up a high proportion of the earnings of the brackish-water ponds of Java. The statistics published by Lin show only 921 metric tons of prawns and crabs (Figs. 1 and 2), and only 1 401 tons of " other " fish, as against 29 093 tons of Chanos. I n the Javanese ponds there is a very different ratio, namely, 6.5 million lb of prawns, 3-3 million lb of other fish, as against 20 million lb of Chanos. Yet both crab and prawn traps are to be seen in the sea water supply canals in Taiwan (Figs. 2 and 15). Taiwan, has a winter during which the temperature falls below that

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tolerated by Chanos. Growth ceases in winter and the Chanos have t o be overwintered in specially protected ponds. Because of this, the technique in Taiwan differs from that in Java and the Philippines, where there is no winter, and where the growth of the fish is continuous all year round. But in spite of there being only eight growing months in the year in Taiwan, the rate of production is high for three reasons. Firstly, care is taken to ensure a good algal pasture throughout the growing period, secondly, the fish are given a supply of supplementary food, especially if there is a threat of overgrazing of the algal pasture, and thirdly, the method of mixed stocking. The overwintering of Chanos has been described. To get the best results when the fertilized ponds are stocked in April, when the water temperature rises above 22OC, the rate of stocking with overwintered fingerlings is 4 000-5 000 fish of 10-100 g per hectare. I n addition 5 000-8 000 new fry of the year are stocked over the period May t o September as and when they become available. The larger overwintered fish will grow fast to give a crop in July of about 1 300 kglhectare, at the time of year when prices are high. They are selectively fished for sale as they grow, so that increased space and food become available to speed the growth of the remaining smaller fish. The best-grown of the new fry of the year will be of marketable size by autumn, and can add 800 kg/ hectare of fish of an average weight of 200 g . Thus, the total weight of Chanos for sale will be about 2 100 kglhectare, plus enough fry of the year, not large enough to be marketable, to provide the stock to restart the next year's production. Lin sums up as follows: with a n average water temperature of 25°C in April, 31OC in May to August, and 27OC from September to early November, the overwintered fingerlings, stocked in the rearing ponds in April, will grow to a weight of 350g in 50-70 days at a survival rate of 95%. The smaller overwintered fingerlings will grow t o 300-450 g in 90-120 days, also with a 95% survival. The new fry of the year stocked in May and June will grow to 200 g or more in 120-150 days, with an 85% survival; and of the late new fry of the season, stocked June, one half can be expected to grow to 150-200 g by October and November at a survival rate of 80%. The remainder of the years' fry go t o the overwintering ponds, where, a t weights from 10-lOOg, they are confined in small ponds in very congested conditions for four months, during which, in spite of careful feeding, they may lose 10-17~0of their weight, and have a survival rate of 60-95y0 depending on the condition of the fish and the oxygen supply. Tang (1967) adapted these methods to the Philippines, where there is no winter cessation of growth, so that Tang allows for a daily rate

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FIG.16. Large Chanos pond in Taiwan. On the left and right there arc the bamboo frames of the windbreak. There is a stack of rice straw a t the far end of the pond, a fry pond in the right corner of the large pond and a canal in the foreground.

of producbion of 10 kglhectare during the period from March to November and a lesser rate of 5 kglhectare during the rest of the year. Tang recommended fertilizer to stimulate the algal pasture, including a mixture of organic and inorganic fertilizer, based on an analysis of the soils, and a system of pest control t o decrease loss of algal pasture. He recommends as follows : General pest control of the bottom soils : 12-15 kg/hectare of nicotine, or 15-18 kglhectare of saponin, or 1 000 kg/hectare of quicklime (the last seems a very drastic remedy). To kill undesirable fish use 3 p.p.m. saponin, or 5 p.p.m. rotenone before the ponds are re-stocked. To control chironomid larvae: 0.75 p.p.m. of gamma-BHC, or 0.5 p.p.m. of Diazinon, or 0.75 p.p.m. of Sumithion in pond water. To control polychaete worms : 2 p.p.m. nicotine or 3p.p.m. of “Bayluscide ”. To control snails : 12-15 kg/hectare of nicotine, or 15-18 kg/hectare of saponin before the pond is filled with water, or 3 p.p.m. of “Bayluscide ” in the water.

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To kill fish lice: 3 p.p.m. of Dipterex in the pond water. To control flagellates : 2 p.p.m. copper sulphate.

As supplementary food Tang recommends pelleted food t o be given daily a t the rate of 1-2% of the biomass of fish. Finally, as t o the manipulation of the stocking, Tang recommends a start with 7 000 fish per hectare, of which 2 000 will be large fingerlings of 100 g, 2 000 small fingerlings of 40 g, and 3 000 very small fingerlings of 3 g. This will give a succession of fish to market, and production can be continued by maintaining the biomass of the fingerlings a t 300-800 kglhectare. Tang estimates that by these measures a natural rate of production of 200 kglhectarelannum can be increased to 800 by fertilization, to 1 000 by fertilization and pest control, and to 2 000 by stock manipulation. VII. THE RATEOF FISHPRODUCTION The rate of production of fish in brackish-water fishponds will depend on many factors, such as the natural fertility of the soil, the effect of added fertilizer, of tilling, and of a dry period, on the culture of the algal felt which is the basis of primary production. It will also depend on the rate and manner of stocking in relation t o the fertility of the pond, and the rate of survival of the fish stocked. Finally, it will depend on the amount and composition of the supplementary feeding, if any. I n intensive systems of fish culture, the whole production of fish depends on supplementary feeding-the natural production of food by the environment (even so rich as that of an estuary) playing no part. I n these cases it is no more justifiable t o speak in terms of rate of production per hectare or per acre per annum than to use these terms for hens raised intensively in multi-tiered batteries, or swine in intensive fattening pens. Yet they are so used and cause much confusion. To get a fair figure for production per acre and per annum in such cases, one would have to calculate the number of acres on which the food fed intensively was grown, and this would be difficult. Two examples of intensive fish culture may be given, both from Japan. I n the culture of the eel, Anguilla japonica, the rate of production, scaled up t o terms of per hectare and per annum, is about 13 60026 300 kglhectare. I n the case of the yellowtail, fed intensively on trash fish, the rate of production is 3 250-7 750 kglhectarelannum. Onodera (1963) claims that the rate of production of the eel in the instance quoted is one of the highest recorded, but it is the production

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of the broiler-house, not of the farm. The limit is set only by the availability of dissolved oxygen, the removal of the waste products of the fish, freedom from disease, and plentiful cheap fodder. I n Table V below, the rates of production quoted are those for fish raised on the resources of the pond itself, improved by husbandry, and with the minimum of supplementary feeding. TABLEV Country &tang de Biguglia Russian limans

Hawaii India Italy Singapore Philippines Java Taiwan

Author

Fish crop, kglhectare or lblacre

130 kg/hectare About 50 kg/hectare ; but Pokrovski liman, 60 acres, 33-750 kg/hectare ; Shabolatsky, 3 000 acres, 2-54 kg/ hectare; Sasik, 19 500 hectare, 0.811.6 kg/hectare Cobb, 1901 176 lb/acre Pillay, 1954 100-150 Ib/acre Pakrasi et al., 1964 858-1 244 kg/hectare 90-170 kg/hectare de Angelis, 1960 Beadle, 1946 60-100 kg/hectare d’dncona, 1954 150 kg/hectare le Mare, 1950 Tilapia, 1 500 lb/acre le Mare, 1949 Prawns 505, fish 250, total 755 Ib/acre Rabanal, 1961 470 kg/hoctare Frey, 1947 500-1 000 kg/hectare Tang, 1967 500 kg/hectare Schuster, 1952 147-627 kglhectare 940 kg/hectare in 1947 to 1 863 in 1966, Lin. 1968 maximum 2 500 kg/hectare

Belloc, 1938 Ilin, 1954

VIII. PROFITABILITY It is a very difficult matter to obtain information on profitability. The fact that fish farming is carried out shows that it must pay. Schuster (1952) relates how attempts to assess profitability through questionnaires failed through the canniness of the people. But, as he says, the prosperity of the operators of the brackish-water fishponds of Indonesia made a reasonable profit very probable. The ponds give many products, other than fish and prawns, which, though hardly assessable on a cash basis, contribute t o the welfare of the operators, and make high cash returns less essential than to a western-style business. Schuster operated a number of test ponds, the results of which he summarized. These data have been used by Hofstede et al. (1953). They calculate that the rate of return on invested capital, in

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three examples of fishponds in Java, is 63%, 7.7%, and 11.7%. This seems only a moderate return on risk capital. Answering the question, how many acres of brackish-water fishponds are needed to provide a living for a family, these authors calculate that 4 acres will give as good a living as a man would get as a labourer, but that the man would be self-employed, and not a hired labourer, which would be a matter of importance t o him. Moreover, he could undertake some other work, and have perquisites such as firewood and crabs, nipa palm leaves for sale as roofing material, and he could keep a couple of goats. All these add up to a better life than the bare cash figures would suggest. Schuster emphasizes that the ponds do not want for takers, when, as sometimes happens, they become available. A. Need foi-a large pond area Lin (1968) gives an account of the finance of brackish-water fish farming per hectare in Taiwan, which, as the preceding section shows, has the highest rate of production, with a maximum of 2 500 kg/ hectarelannum. Per hectare, he estimates income a t 33 300 and costs a t 27 300 Taiwan dollars, showing a net profit on production of 21%. This may sound good, but when the salary of the operator is added, there is little left for profit or for reserves. If, in English terms, we assume 2s. per lb for these well-priced fish, and a pond giving 2 000 Ib/acre, then the pond earns $200 gross, and the net profit will be sE42 per annum. Obviously, no one could live on the earnings of one acre of ponds on this rate of production. Lin considers that any pond unit of less than 10 hectares must be regarded as a part-time or subsistence occupation, and that only units of more than 50 hectares are fully viable. However, for these bigger units considerable capital outlay and working capital are needed. Caces-Borja and Rasalan (1967) give data as to the rate of production of ponds in the Philippines. One hectare of pond will gross 599 pesos when growing Chanos alone, 896 when growing Chanos and " sugpo " prawns, and 1 250 pesos when growing " sugpo ') alone. (1 U.S. dollar = 3.85 pesos.) The Division of Fisheries of Singapore operated a 14-acrz prawn pond during the four years 1954-58, in order t o get some data on the probable profitability of the prawn-farming industry there. They found that the average monthly gross income was just over Malayan dollars 750. The capital cost of embankments, sluices, nets, huts and sheds, etc. was Malayandollars 12 840, and the sale of produce amounted t o 42 921 lb of prawns, fish, and crabs, sold for Malayan dollars 35 963.

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The capital costs were recouped in two years. The rate of cropping was 766 lbiacreiannum. Plainly, where the rate of cropping is low, as it is in brackish-water fishponds generally, only large acreages will make a viable industry, able to amortize invested capital, pay a good rate of interest, and set aside reserves for contingencies and expansion. The rate of production of the Italian valli, for example, at, say 100 kgihectare, would not be enough t o support a small-scale enterprise, but on the existing pond areas of, say 500 hectares, income becomes 50 000 kg or more of wellpriced fish, which can, moreover, be sold under favourable conditions. And as with the Javanese ponds, there are extras such as the sale of wild duck in season, shooting rights, etc. I n his account of the Russian limans, Ilin (1954)makes the same point. The larger the acreage of ponds, the lower the prime cost of fish production. One xentner of " chulari ", the marketable grey mullet which is the chief produce of the limans, decreases in prime cost from 640 roubles in a 250 hectare liman, to 169 roubles in a 2 000 hectare liman. I n a liman of 250 hectares, the cost of exploitation is covered by earnings by only l a times, but in a liman of 2 000 hectares by 42 times. As some of the limans exceed 10 000 hectares in area, there seems to be scope for profitable working even on a low or very low rate of fish production per hectare. B. The state of the industry-progress,

stagnation and decline

Big units need big investment, and the provision of capital seems to be the chief obstacle to the continued prosperity and expansion of the brackish-water fish farming industry. I n the case of the Singapore prawn ponds, for example, the capital needed was Malayan dollars 12 840, in addition t o working capital. As Schuster says, these are large sums in comparison with those needed in other rural industries, and further, a pond operator needs more ready money for working expenses than the villager usually possesses. The recent history of the industry is mainly one of stagnation or even decline. Cobb (1901)wrote that, in Hawaii, there were at that time not more than half of the number of ponds in use that there had been thirty years previously, and Hiatt (1944)repeated that the industry was in decline in his day. The chief reasons were the decline in population and the conversion of the ponds for land development. Fish farms which occupy desirable waterside sites in the developed countries are bound t o attract the interest of land development agencies. Though the income from a well-managed fishpond may exceed that of agri-

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cultural land of the same acreage, the capital value of the land as industrial or residential sites would be far higher. According to Fontaine (1968), the brackish-water ponds at Arcachon, in use for some 200 years, are now in disuse, and Pillay (1954) and Saha et al. (1969a) were not hopeful as to the future of the Indian bheris. Although a better view was taken by Pakrasi et al. (1964), who also gave some impressive data on their productivity, they agreed with Pillay that the restoration of the feeder channels and the excavation of the silted ponds to their original depth needed a lot of capital. I n Java, according to a graph in Schuster’s book (1952))the acreage of fishponds increased until 1949, but he says that the future progress of the industry is greatly dependent on technical improvements. Largescale excavation, he says, and digging out of the canals and strengthening of the embankments would much increase the productivity and value of the ponds. Since 1920, the large-scale construction of ponds has ceased, and what has been done is a rounding-off of the existing pond-complexes, rather than an extension of their area. The costs of pond-construction have always been high and it is unlikely that, under present conditions, work will be undertaken by the pond proprietors themselves, since labour costs in 1952, when Schuster wrote, made even the upkeep of ditches and embankments a heavy burden on the proprietors. Tang (1967) gives the total area of ponds in Indonesia as 160 000 hectares, or about twice that given by Schuster in 1952, but probably Tang includes large acreages of less complete ponds on Celebes and other Indonesian islands. Lin (1968) gives a table showing the expansion of the area of brackish-water fishponds in Taiwan. From 8 700 hectares in 1947, the area increased to 13 100 in 1951. Since then, however, there has been only a slow and irregular increase, with no net change in area from 1962 to 1966, the last year given in the table, and this in spite of a well-maintained level of productivity. However, in the Philippines the industry continues to expand. From an area of some 60 000 hectares before the last war (Frey, 1947) the acreage grew to 100 097 in 1954, 119 582 in 1959 (Rabanal, 1961) and 131 850 in 1964. The average annual increase in acreage has been 3 000 hectares. Fertile foreshore and deltaic areas have attracted the interest of fishpond operators. However, the reclamation of land for fishpond purposes is not only confined to foreshore areas, but also to low swampy ground along the fringe of the rice fields. It has been found that fishponds are more profitable than rice fields in marginally

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suitable sites. Many operators are combining fish farming with the manufacture of salt. The greater part of the acreage of brackish-water fishponds was built in earlier years, in the days of cheap labour. Since the war, however, labour costs seem t o have risen faster than the value oi the fish obtained from the ponds, so efforts are being made towards an intensification of culture, to give larger crops in the present ponds, and so make investment in fishponds more profitable. I n Hawaii, for instance, research is being done into means of increasing the productivity of the algal pasture which is the basis of the primary production of the ponds. Hiatt (1944) suggested measures to eliminate predatory fish, a t present able to enter the ponds almost a t will (Malone, 1969). Means to reduce the turbidity of the ponds would increase algal production. I n all countries concerned, this increase of algal production is being sought by the use of fertilizer. For instance while the recorded production of algal pasture at Taiwan, namely, 28 000 kglhectare wet weight is nearly equal to that of " nori " (Porphyra) in Japan, itself claimed to be equal t o the highest land production of plants, the experiments with Chlorella show how much further the culture of algae as pasture can be taken. With this alga, a rate of production of 8-17 tons dry weight of alga per acre per year has been achieved ; or if we assume that the alga contains 85% of water, the rate of production of wet weight would be 45-96 tons per acre per annum. While it is not suggested that these results, obtained under aquarium conditions, could be equalled in the field and on the commercial scale, they do make the point that there is still great room for increases in the productivity of algal biomass, and thence of the fish which feed on algae and their associated organisms. This is one of the most worth-while lines of research waiting to be done. I n India, Pillay (1954) suggested better arrangements for the stocking of the ponds. Selective stocking would give fewer predators in the crop, and fishing in the shallows near the bheris would provide subsidiary fish and prawn fry. Pakrasi et al. (1964) also had in mind the lack of a trade in fish fry, through which the ponds could be stocked with controlled numbers of the desired kinds of fish. Saha et al. (1969) hoped t o replace naturally spawned fish fry with those of the valuable Indian major carps, provided these could be acclimatized t o live in the saline ponds. Saha et al. (1969) worked out the occurrence and abundance of the fry of fish valuable for pond stocking. They found, for instance, that fry of the most popular species, Mugil parsia, was available in the drains leading t o the ponds a t almost all times of the year.

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Trials with fertilizers are giving results with varying degrees of success; especially notable is the promise of urea as a fertilizer for algae. Tang (1967) has shown that the methods of multiple stocking, so successful in Taiwan, give equally notable increases of fish crops in the Philippines. The intensive use of the ponds in Java and the Philippines by rearing successive crops of fingerlings bought from specialist fry farmers is a forward-looking development. The ultimate in the intensive use of ponds or enclosures is in the eel, yellowtail and Kuruma prawn raising industries. Development along such lines is the most likely outcome for the future, at least in the industrial countries. But the problems of expansion of this industry are not small, for example the search for an economic fodder, and the transport requirements of a large-scale outfit. C. Need for long-term credits Schuster (1952) says that short-term loans are willingly taken up and given by the banks, and that such loans give much relief in matters such as the purchase of fry. The ponds are taken as security for these short-term loans. But Schuster also considers that the most urgent need is for long-term credits, with which improvements t o the ponds can be made. He thinks that the loans could easily be serviced on the increased rate of production which the loans would make possible, provided expert control is kept over the transactions. The rapid and successful expansion of the fishpond industry in the Philippines, mentioned earlier, is undoubtedly due to the loans policy of the Development Bank of the Philippines. This bank employs technically trained staff who can advise and assist prospective as well as existing fishpond operators (Rabanal, 1961). The same Bank makes loans for the prawn-farming industry (Caces-Borja and Rasalan, 1967), and their technical staff advises on husbandry procedures and on sources of fry. No doubt the matter of security for these long-term loans is made easier by these technical officers who can closely supervise the recipients. Another aspect of subsidy to the Philippine pond operators is their sensible classification as farmers, whereby they can procure subsidized fertilizers for their ponds. (foodsell (1959) found that credits or financial assistance to pond operators are inadequate, and, even when available, more expensive than credit for agricultural enterprises. Rural financing is very expensive in the under-developed countries, and even when some kind of organized credit is available, interest rates are seldom less than

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14-15% per annum. Schuster writes of the money-lenders who take a good part of the daily revenues of the fishponds in reduction of a never-cleared principal. The economic weakness of a rural cash economy may justify these onerous loan terms ; however, apart from cases of social injustice, such terms give no incentive to expansion and improvement. Where this state of affairs prevails, Goodsell considers that Government action is needed to establish a sound credit system. Schuster also concludes that if long-term credits cannot be provided by the banks, then Government itself should find the money. Where there are established banks, the crucial matter is security for the long-term loans needed. If, in Java, where the fishpond industry has been established for more than 200 years, banks “with long experience of rural affairs are unable to judge the terms of redemption, or to estimate the value of securities ” (Schuster), how much more difficult it must be for a bank t o judge the terms of loans where the technique of fish culture is new and unfamiliar, and where they have no technical advisers? The expansion of the fish farming industry and its establishment in new countries is attracting more attention as the wild fisheries continue to show diminishing returns, and the prices of the best sea foods increases. It seems certain that the raising of the finance is likely to be a more serious problem than any biological difficulties, until some pioneers are able to make a success of the technique, and so give the banks the data they need.

I X . Is

THERE A

FUTURE FOR ESTUARINE FISHFARMING?

To some extent, the future of estuarine fish farming is linked with that of the estuaries themselves. Schmidt (1966) shows that the tidal marshes from Maine to Delaware have lost 47 000 acres since 1954. Dumping of spoil accounted for %yo,housing developments accounted for 27 yo, construction of racreational facilities t’ook 15%, bridges, roads, airports, and parking facilities took loyo,and development of industrial sites and trash dumps took 13%. The amount distributed between schools, agricultural cropland, drainage, and beach erosion control was 1%. Most great conurbations are based on estuaries, and the estuaries are the ‘‘ septic tanks of Megalopolis ”. I n Britain, we are planning to abolish the Wash, Morecame Bay, the estuary of the Dee, and even the estuary of the Thames. Only those inlets far from present or likely future development seem possibilities for fish farming. Even there, as Ryther and Matthiessen (1969) point out, private efforts

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to start aqua-cultural projects may be thwarted by local statutes and by public resentment. In the developed countries, therefore, it seems most likely that future fish culture will be of the intensive kind as in Japan. The success of Shelbourne (1964) in breeding plaice, soles and other valuable flatfish in captivity opens the way t o broiler-house techniques of fish raising. Kennedy (1969) is making similar trials with the culture of the sablefish in Canada. The trials of commercial salmon and sea-trout raising by Unilever have been mentioned. But, so far as is known, none of these projects has as yet got off the ground. Cheap fodder, mechanized handling, and first-class transport facilities are all needed. The increase in the numbers and power of thermal and nuclear power stations, many of which are placed on estuaries, has made available large quantities of flowing water heated to many degrees above that of the environment. The possibility of using this heat has attracted much interest, and one of the possibilities canvassed is that of growing fish intensively in the warmed water (see, for example, Nash, 1968 ; Cole, 1968). The growth of fish is accelerated (within limits) by higher temperatures, and may be continued during at least some of the winter months when the ambient water becomes too cold for rapid growth, or indeed for any growth a t all. I n cultures in which fish have to be overwintered, the use of warmed water would allow of survival and even of some useful growth. It seems likely that the use of this heat on the full scale is more of an engineering than a farming problem. The engineer wants to get the heated water away as quickly as possible since the efficiency of his condensers, and therefore of his turbines, depends on this. But the farmer wants the heat t o be available in an accessible form, which means either a slow passage or an efficient heat-exchanger. Agreement will have to be sought between engineers and farmers on such matters as ducting off at least some of the warmed water from the discharge pipes, and the future design of power stations may incorporate systems of cooling water disposal which make the warmed water available without increasing the cost of power generation. For example, it might be possible to discharge the heated water into a reservoir from which it would flow away down a number of channels, each of which could include many fish-rearing units. I n a marine setting, the Japanese are understood to have had the encouraging results that would be expected, in accelerating the growth of fish (yellowtail) in water warmed by waste power-station heat. The Russians have also been experimenting for some years with the warmed

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water from inland power stations. There is still enough land available in Russia for the creation of large reservoirs from which cooling water is drawn for the power station, and to which the heated water is returned to give up its heat to the atmosphere. Thus there is a thermal gradient between the point of discharge of the hot water and the point of intake of the cooled water. The heated water may be 10-15°C higher than that of the ambient, and may be 20°C even in the winter. Gribanov et al. (1968) report on the results of rearing common carp intensively in cages in this warmed water. The technique is the same as that of the raising of yellowtail and prawns in Japan, but in this case the experimental cages were small, (about 2 m3 in volume). The fish were fed on an artificial food consisting of sunflower, flax, and peanut seed meals, with silkworm pupae and food yeast. As an example, at a population density of 200 fish per m2 (or m3, since the cages were about one metre deep), each fish about 40g weight, they got fish yields of 80 kg/m2, with a food-conversion rate of 5.4. This yield is equivalent to a notional yield of 800,000 kg/hectare, and compares with a notional figure of 26 300 kglhectare for intensive eel raising in Japan (Onodera, 1963). Though the fish would take their own weight of food daily if offered, the food-conversion rate was very poor and wasteful, that is over 14 ; whereas the best conversion rates (of between 5 and 6) were obtained a t much lower rates of feeding. Gribanov et al. (1968) found that giving the food 12 times daily gave twice as good a food conversion-rate as when the same weight of food was given once daily; that it was a waste t o give more than 15% animal protein in the food mixture, and that both terramycin and food yeasts improved the food-conversion rate. Even sea-trout may benefit from being reared in warmed water, for Lavrovsky (1964) shows that rainbow trout continue to feed a t temperatures as high as 24OC though the optimum was 16-18°C. The British White Fish Authority (1968-9) are experimenting with fish rearing in floating cages in sea water, a t stock densities of up to 5 fish per foot2 (about 45 fish/m2). This is a much lower density of stocking than in the Russian trials, but they have had " rather better results than those obtained in much larger enclosures on natural bottoms ". The situation is different in the still under-developed countries. There, the estuaries are likely t o be available for development for many decades t o come. Tang (1967) estimated that there are still 6 million hectares of lands suitable for brackish-water fish farming in Indonesia, 500 000 in the Philippines, and even in Taiwan, a further 10 000 hectares. Pillay (1968) thinks that there are 1.8 million acres

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available for brackish-water fish farming in the Niger delta and, that if they can be made to produce the modest crop of 400 lb/acre/annum, they will repay their capital costs in four years, A demonstration unit has started work, and this may give the banks enough information t o finance extension, but government-sponsored pilot schemes have an unfortunate way of losing money. The scope is still considerable, and can be linked with reclamation schemes for rice cultivation, etc. Not only the knowledge which can be provided, but the aptitude and willingness of the local people, their flair for animal husbandry, and the willingness of the local banks or investors to invest, are needed for the fuller development of estuarine fish farming.

X. REFERENCES Abagon, M. A., Bunag, D. M. and de Vera, A. M. (1951). “ Gulaman dagat ” as supplementary feed for Bangos. Bull. Fish. SOC.Philipp. 2, 41-49. American Fisheries Society. (1966). A Symposium on Estuarine Fisheries. Special Publication 3, Supplement to Trans. Amer. Fish. SOC.9(4), 5. d’Ancona, U. (1954). Fishing and fish culture in brackish-water lagoons. Fish. Bull. F.A.O. 7(4), 147-172. de Angelis, R. (1960). Brackish-water lagoons and their exploitation. Stud. Rev. gen. Fish. Coun. Mediterr. 12, 1960. Anraku, M. and Azeta, M. (1966). The feeding habits of larvae and juveniles of Yellowtail associated with floating seaweeds. Abstracts of papers to 2nd Int. Oceanogr. Congr. Moscow, 8--9. Antipa, 0. (1937). Les bonifications hydrologiques des deltas. Rapp. P.-v. Rdun. Commn. int. Explor. scient. Mer. Mdditerr. 10, 99-120. Arn6, P. (1938). Contribution a 1’6tude de la biologie des Muges du Golfe de Gascogne. Rapp. P.-v. Rdun. Commn int. Explor. scient. Mer. Mdditerr. 11, 77-113. Arnold, E. and Thompson J. (1958). Offshore spawning of the Striped Mullet, Mugil cephalus L. in the Gulf of Mexico. Copeia, 1958, 130-132. Asia Kyokai. (1957). Japanese fisheries, their development and present status. Tokyo. 1957. Babaian, K. E., Kromov, A. V. and Staruschenko, I. L. (1967). The effect of mullet rearing farms on the state of the reserves of grey mullet in the sea. Vop. Ikhtiol. 7(44), 463-473. (In Russian.) Bayoomi, A. R. (1969). Notes on the occurrence of Tilapia zillii (Pisces) in Suez Bay. Mar. Biol. 4(3). 255. Beadle, L. C. (1946). The Venetian Lagoon. Scient. Prog. 34, 734-750. Belloc, G. (1938). L’fitang de Biguglia. Rapp. P.-v. Rdun. Commn. int. Explor. scient. Mer. Mdditerr. 11, 433-473. Blanco, G. J. and d’Acosta, P. A. (1958). The propagation of Grey Mullet in northern Luzon brackish-water fishponds. Philipp. J . Fish. 6( l ) , 1-15. Bose, B. B. (1959). An experimental study of the optimum salinity for the growth of the benthic blue-green alga Oscillatoria splendida Greville of brackishwater ponds. Proc. nut. Inst. Sci. India, 26 B ( l ) , 19-21.

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Bromhall, J. D. (1954). A note on t)he reproduction of the Grey Mullet, Mugil cephalus L. Hong Kong Univ. Fish. J . 1, 19-34. Brunelli, G. (1937). La valliculture et la bonification des deltes fluviaux. Rapp. P.-v. Rhun. Commn. int. Explor. scient. Mer. Mhditerr. 10, 99-120. Bunag, D. M. (1957). The “ Bangos ” fry trawl. Spec. Publs Indo-Z’acif. Fish. Coun. 7(2--3),77-81. Caces-Borja, P. and Rasalan, S. B. (1967). A review of the culture of the sugpo, Penaeus monodon Fabr., in the Philippines. F.A.O. World Conf. on the Biology and Culture of Shrimps and Prawns. Mexico City, 1967. Carlin, B. (1966). Salmon rearing in Sweden. Swedish Salmon Research Institute. Rept. L. F.I. medd. 5/1966. Chen, T. (1952). Milkfish culture in Taiwan. Fishery Ser. Chin.-Am. j t Comm. rur. Reconstr. 1. Chow, T. (1958). A study of water quality in the fish ponds of Hong Kong. Hong Kong Univ. Fish. J . 2, 7-21. Cobb, J. (1901). Commercial fisheries of the Hawaiian Islands. Rep. U.S. Commnr Fish. 427-433. Cole, H. A. (1968). The scientific cultivation of sea fish and shellfish. J . R. SOC. Arts, 590-603. Cooper, L. H. N. and Steven, G. A. (1948). An experiment in marine fish farming. Nature, Lond. 161, 631-633. Darnell, R . M. (1967-8). Organic detritus in relation to the estuarine ecosystem. I n “ Estuaries ”, vol. 2 (Lauff, G., Ed.) pp. 376-382. American Association for the Advancement of Science, Washington, D.C. Davis, F. M. (1923). An account of the fishing gear of England and Wales. Fishery Invest., Lond., Sor. 2. 5, no 4. Day, J. (1967). The biology of Knysna estuary, South Africa. I n “ Estuaries ”, vol. 2 (Lauff, G. ed.,) pp. 397-407. American Association for the Advancement of Science, Washington, D.C. Devanesan, D. W. and Chacko, P. I. (1943). On the possibility of culture of certain marine mullets in fresh-water tanks. Proc. natn. Ilwt. Sci. India. 9, 249-250. Djaingsastro, A. S. (1956). Experimentations in the brackish-water ponds a t Polgan (Madura, East Java). Proc. Indo-Pacif. Fish. Coun. 6(2-3), 202-209. Djahjadiredja, R . (1966). The use of urea as fertilizer and stimulant for the production of Benthic algae in brackish-water ponds. Proc. 11th Pa@. Sci. Congr., Tokyo, 1966, pp. 15-16. Doroshev, S. I. (1963). The survival of White Amur and Tolstolobik fry in Sea of Azov and A d Sea water of varying salinity. Symposium on the fisheries exploitation of plant-eating fishes in the water-bodies of U.S.S.R. Turkmen S.S.R. Ashlrhabad. (In Russian.) Esguerra, R. S. (1951). Enumeration of Algae in Philippine Bangos ponds and in the digestive tract of the fish, with notes on conditions favourable for their growth. Philipp. J . Fish. 1(2), 171-192. Fontaine, M. (1968). L’agriculture marine. Bull. Cent. Etud. Rech. scient., Biarritz. 7( l ) , 7-25. Frey, D. (1947). The pond fisheries of the Philippines. J . mar. Res. 4(3), 247258. Frost, A. (1968). Unilever fish farms-arainbow profits haul. I n “Sunday Times”, London. June 9, 1968.

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Ganpati, S. V. and Alikhuri, K. H. (1952). Experiments on the acclimatization of salt water fish seed to fresh watjer. Proc. Indian Acad. Sci. (B) 35, 93109. Ghazzawi, F. (1933). The pharynx and int>est,inaltract of the Egypt,ian mullets, Mugil cephalus and M . capito. Part 1. On the food of mullet from Egyptian waters. Notes Mdm. Dir. Rech. Pgch., L e Caire. 5. Ghazzawi, F. (1935). Ibid. Part, 11. Notes M6m. Dir.Rech. Pgch., L e Caire. 6. Gianotto, F. (1965). Conditions of fishing in Lake Trasiimen during the years 1956-1963. Proc. tech. Pap. gen. Fish. Coun. Mediterr. 8, 147-159. Goodsell, W. (1959). Some economic aspects of fish pond operations. Fish. Pap. F.A.O. 14. Gribanov, L. V., Korneev, A. N. and Korneeva, L. A. (1968). Use of thermal waters for commercial production of carps in floats in the U.S.S.R. Proceedings of the World Symposium on warm-water pond fish culture. Vol. 5, pp. 218-226. Gunther, A. C. L. (1861). Catalogue of Acanthopterygian fishes in the British Museum, London. Vol. 3. Hall, D. N. F. (1962). Observations on the taxonomy and biology of some IndoWest Pacific Penaeidae (Crustacca, Decapoda). Colonial Office Fisheries Publication, No. 17. Hardenberg, J. D. F. (1950). Estuarine problems in South-east Asia. Proc. Indo-Pacij. Fish. Coun. 2(2-3), 175-180. Hedgpeth, J. W. (1967-8). The Sense of the meeting. I n ‘‘ Estuaries ”, vol. 2 (Lauff, G., ed.) pp. 707-710. American Association for the Advancement of Science, Washington, D.C. Hiatt, R. W. (1944). Food chains and the food cycle in Hawaiian fishponds. Part I. The Food and feeding habits of Mullet (Mzcgil cephalus), Milkfish (Chanos chanos) and Ten-Pounder (Elops machnata). Trans. A m . Fish. SOC. 74, 250-261. Hickling, C. F. (1960). “ Tropical Inland Fisheries.” Longmans Green, London. Hickling, C. F. (1962). ‘‘Fish Culture.” Faber and Faber, London. Hickling, C. F. (1963). The cultivation of Tilapia. Scient. Am. 208(5), 143-152. Hickling, C. F. (1970). The Natural History of the English Grey Mullets. J . Mar. Biol. Ass. U.K. (In press.) Hofstede, A., Ardiwinata, R. and Botke, F. (1953). Fish culture in Indonesia. Spec. Publs. Indo-Pacif. Fish. Coun. 2. Hornell, J. (1926). Report on the Fishery Resources of Mauritius. Port Louis, Mauritius. Hornell, J. (1950). Fishing in many waters. Cambridge Univcrsity Press, Cambridge. Hudinaga, M. and Miyamura, M. (1962). Breeding of the “ Kuruma ” prawn (Penaeus japonicus). J . oceanogr. SOC.Japan, 20th Anniversary Vol., 694706. (In Japanese with English summary.) Ilin, B. (1954). “ Mullet Farming.” 81 pp. Krimizdat. (In Russian.) Inouye, H., Yoshiaki, T. and Saito, M. (1966). On the water exchange in the shallow marine fish farm of Hamachi. BUZZ. Jap. SOC.scient. Pish. 32(5), 384-392. Kalle, K. (1953). Der Einfluss des englischeri Kiistenwassers auf den Chemismus der Wasserkorper in den siidlichen Nordsee. Ber. dt. wiss. Kommn Meeres~ O T S C 13(2), ~ . 130-135.

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Kennedy, W. A. (1969). Sablefish culture-a preliminary Report. Tech. Rep. Fish. Res. B d Canada, 107. Ketchum, B. H. (1967-8). Phytoplankton nutrients in estuaries. I n “Estuaries ”, vol. 2 (Lauff, G., ed.) pp. 329-335. American Association for the Advancement of Science, Washington, D.C. Korririga, P. (1967-8). Estuarine fisheries in Europe as affected by man’s multiple activities. In ‘‘ Estuaries ”, vol. 2 (Lauff, G., ed.) pp. 658-663. American Association for the Advancement of Science, Washington, D.C. Kntukuhn, J. H. (1966). The role of estuaries in the development and perpetuation of commercial shrimp resources. Trans. Amer. Fish. SOC.Sp. Pubn. 3, Suppl. to 95(4), 16-36. Lackey, J.B. (1967-8). The microbiotaof estuaries arid their role. I n “Estuaries ”, vol. 2 (Lauff, G., ed.) pp. 291-302. American Association for the Advancement of Science, Washington, D.C. Lavrovsky, V. (1964). Raising of rainbow trout (Salmo gairdneri) together with carp (Cyprinus carpio) and other fishes. F.A.O. World Symposium on Warm-Water Fish Culture. Rome, 1966. le Dantec, J. (1955). Quelques observations sin la biologie des Muges des reservoirs de Certes B Audenge. Rev. Trav. Off. (Scient. tech.) Pdch. Marit. 19(I), 33. le Mare, D. W. (1949). The prawn pond industry of Singapore. Ann. Rep. Fish. Fed. Malaya and Singapore. 121-124. le Mare, D. W. (1950). The application of the principles of fish culture to estuarine conditions in Singapore. Proc. Indo-Pacif. Fish. Coun. 2(2-3), 175-180. Lin, S. Y. (1968). Milkfish farming in Taiwan. Fish Culture, Report 3. Taiwan E‘ish. Res. Inst. MacNae, W. (1967-8). Zonation within mangroves associated with estuaries in North Queensland. I n “ Estuaries ”, vol. 2 (Lauff, G. ed.) pp. 432-441. American Association for the Advancement of Science, Washington, D.C. Malone, T. C. (1969). Primary productivity in a Hawaiian fishpond and its relationship to selected environmental factors. Pacif. Sci. 23, 26-34. Mane, A., Villaluz, D. and Rabanal, H. (1952). Cultivation of fish in brackish and estuarine waters in the Philippines. Philippine Fisheries, Manila. Menon, M. K. (1955). On the paddy-field prawn fishery of Travancore-Cochin. Proc. Indo-Pacif. Fish. Coun. 5(2-3). Morovic, D. and Sabioncello, I. (1965). Snr les possibilities de survivance des Mugilides dam l’eau douce et lour transport de la mer en eau douce. Rapp. P.-v. Riun. Commn int. Explor. scient. Mer. Mkditerr. 18(3), 701-704. Mortimer, C. H. and Hickling, C. F. (1954). “Fertilizers in Fishponds.” Colonial Fisheries Research Publication, 5, H.M.S.O. London. Nash, C. (1968). Power stations as sea farms. New Scientist, 40, 367-369. Natarajan, A. V. and Patnaik, S. (1967). Occurrence of mullet eggs in the gut contents of Ambassis gymnocephalus (Lacep). J . Mar. Biol. Assn India, 9, 192-194. 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.,Lond. 144, 25-45. Odum, W. E. (1968). The ecological significance of fine particle selection by the St,riped Mullet, Mugil cephalus. Limnol. Oceanogr. 13(I), 92-98.

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Odum, E. P. and de la Cruz, A. (1967-8). Particulate organic detritus in a Georgian salt marsh estuarine ecosystem. In “Estiiaries vol. 2 (Lauff, G., ed.) pp. 383-388. American Association for the AdvancementJof Science, Washington, D.C. Onodera. K. (1963). Some data on eel culture in Japan. Occ. pap. 62/6 IndoPacif. Fish. C0un.c. Orr, A. P. (1947). An experiment in marine fish cultmivation.I1 Some physical and chemical conditions in a fertilized sea loch (Loch Craiglin, Argyll). Proc. R. SOC.Edinb. (B) 63, 3-20. Pakrasi, B. B., Das, P. R . and Thakurta. S. C. (1964). Culture of brackish-water fishes in impoundments in West Bcngal. Indo-Pacif. Fish. Coun. 11. Pillay, T . V. R. (1953). Studies o n the food, feeding habits, and alimentary tract of Grey Mullet, Mugil tade Forsk. Proc. natn,. Inst. Sei. India, 19(6), 777-827. Pillay, T. V. R. (1954). The ecology of a brackish-water Bheri with special reference to the fish-cultural practices and tho biotic int,eraction. Proc. natn. Inst. Sci. India, 20(4), 399-427. Pillay, T. V. R. (1966a). A Bibliography of brackish-water fish culture. F.A.O. Fisheries Division, Rome, (Mimeographed). Pillay, T. V. R . (1966b). Brackish-water culture of Grey Miillet in the Pacific region. Proc. 11th Pacijk Science Congress, Tokyo, 1966, pp. 16-17. Pillay, T. V. R. (1968). Estuarine fisheries of West, Africa. In “ Estuaries ”, (Lauff, G., ed.) pp. 639-646. American Association for the Advancement of Science, Washington, D.C. Rabanal, H. R. (1961). Status and progress of Chanos Fisheries in the Philippines. Occasional Papers 61/8, Indo-Pacific Fisheries Council. Rabanal H. R. (1962). The elevation of a swamp land based on the tidal datum, and its importance in selecting sites for Chanos fishponds projects. Proc. Indo-Pacif. Fish. COWL.10(2), 138-140. Rabanal, H. R., Esguerra, R. S., Lopez, J. V., Adana, A. M., Ramos, V. and Felix, S. S. (1951). The rate of algal (lumut) production in the Dagatdagataii salt water fishponds. Philipp. J . Fish. 1(2), 155-169. Riggs, C. (1957). Mugil cephalus in Oklahoma and Texas. Copeia, 158. Ronquillo, I. A., Villamater, E. and Angeles, H. (1957). Observations on the us0 of Terramycin and “ Vigofac ’’ enriche,d diet on Bangos fry Chanos chanos Forsk. Proc. Indo-Z’acif. Fish. Coun. 7(2-3), 44. Ronquillo, I. A. and de Jesus, A. (1957). Note on growing lab-lab in Bangos nursery ponds. Proc. Indo-I’aciif. Fish. C o u n ~7(2-3). 43. Round, F. (1965). “ The Biology of t,he Algae.” Edward Arnold, London. Ryther, J. and Mat>thiessen,G. (1969). Aqiiaculturc, its status arid potential. Oceanus, 14(4), 2-14. Saanin, H. and Tati Ramelan. (1966). Fert>ilizationand its effect of the hydrology of brackish-water ponds. Proc. 1l t h Pacific Science Congrcss, Tokyo,

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Saha, K., Chakraborty, D., De, B. and Chakraborty, S. Jr. (1969). Studies on the salinity tolerance of fry of major Indian carps in captivity. Indian J . Fish. A. 11, 247-248. Schuster, W. (1952). Fish culture in the brackish-water ponds of Java. Spec. Publs. Inndo-Pacif. Fish. Coun. Special 1, 1-143. Schmidt, R. (1966). Needed-A coastwise comprehensive program for development of estuaries. Supplement, to Truns. A,mer. Fish,. Soc. 95(4), 102--109.

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Schuurman, J. J. (1956). The value of filamentous algae for the growth of Ch,anos chams Forsk. Inrlones. J . nat. Sci. 112(1), 65-72. Schuurman, J. J. (1964). A method for the determination of the sriitjahilitJyof coastal regions for the construction of brackish-water ponds. Proc. In,doPacif. Fish. Coun. 11(38), 1-4. Sedgwick, S . D. (1964). ‘‘ Rainbow trout farming in Denmark and Norway ”. Roneotype Report, Scottish Home Dept., Edinburgh. Shelbourne, J . D. (1964). The artificial propagation of marine fish. I n “ Advances in Marine Biology, Vol. 2.” (F. s. Russell, ed.) Academic Press, London. Singapore Fisheries Division. (1958). Ann. Rep. Fish. Div., Singapore. Smith, R. F. (1966). Foreword to A Symposium on Estuarine Fisheries. Special Publication 3, Supplement to Trans. Amer. Fish. SOC.9(4), 1966. Sulit, J. I., Esguerra, R . S., and Rabanal, H. R. (1957). Fertilization of Bangos nursery ponds with commercial chemical fertilizers. Proc. Indo-Pacif. Fish. C O U ~7(2-3), . 44. Tang, Y. A. (1964). Induced spawning of striped grey mullet by hormone injection. Jap. J . Ichthyol. 12(1-2), 23-30. Tang, Y. A. (1967). Improvement of Milkfish culture in the Philippines. Curr. Aff. Bull. Indo-Pacif. Fish. Coun. 49. Tang, Y. A. and Chen, T. P. (1959). Control of Chironomid larvae in Milkfish ponds. Fishery Ser. Chin.-Am. j t Comm. rur. Reconstr. 4. Tang, Y. A. and Chen, S. (1966). A survey of the algal pastures of Milkfish ponds in Taiwan. F.A.O. World Symposium on warm-water fish culture. Rome, 1966. Tham, A. K. (1967). Prawn Culture in Singapore. Review Paper F R :BCSP/ 67/R/2. F.A.O. World Symposium on the biology arid culture of Shrimps and Prawns. Mexico City, 1967. Thomson, J. (1966). The Grey Mullets. Ocean. Mar. Biol. Rev. 4, 301-335. Vatova, A. (1962). Salt water fish farms of the north Adriatic. J . Cons. perm. int. Explor. Mer. 27(1), 109-115. Vik, K. 0 . (1963). Fish Cultivation. Balm. Trout Mag. 169, 203-208. Villadolid, D. and Villaluz, D. (1950). A preliminary study on Bangos cultivation and its relation to alga culture in the Philippines. Pop. Bull, Dep. Agric. nat. Resour. Philipp. I d . 30. Yang, W. T. and Kim, U. B. (1962). A preliminary report on the artificial culture of grey mullet in Korea. Proc. Indo-Pacif. Fish. Counc., 9, 62-70. Yashouv, A. (1966). Breeding and growth of Grey Mullet Mugil cephalus L. Bamidgeh 18(1), 3-13. Yashouv, A. and Ben-Shachar, A. (1967). Breeding and growth of Mugilidae. Feeding experiments under laboratory conditions with Mugil cephalus L. and M. Capito Cuv. Bamidgeh. 19(2-3), 50-66. Zambribortch, F. S. (1962). Biology of the over wintering of young Grey Mullet. Vop. Ikhtiol. 2, 4(25), 615-625. (In Russian.) Zenkevitch, L. V. (1963). “ Biology of the Seas of the U.S.S.R.” George Allen and Unwin, London.

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THE PROBLEM OF OIL POLLUTION OF THE SEA A. NELSON-SMITH Department of Zoology, University College of Xwansea, Swansea, Wales

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I. Introduction . .. .. .. .. .. *. 11. Sources and Control .. .. .. .. .. .. A. Tanker Operation and General-cargo Shipping . €3. Harbours and Marine Terminals .. .. .. C. Coastal Industry and Other Sources . . .. .. 111. Properties of Petroleum Oils .. .. .. .. A. Physico-chemical Characteristics .. .. .. .. .. B. I3ehaviour of Spilt Oil on Sea and Shore C. Detection and Identification . . .. ,. *. IV. Effects of Oil Pollution .. .. .. . . .. A. Mode of Action and Toxicity of Oils . . .. .. B. Effects on Marine Comrnunities .. .. .. C. Carcinogenesis . . .. .. .. .. .. D. Rehabilitation of Oiled Birds . . . . .. .. E. Public Amenity and the Tourist Industry . . .. V. Removal of Spilt Oil . . .. .. .. .. .. A. Bacterial Degradation and Other Biological Processes B. Dispersal, Sinking and Recovery at Sea .. C. Problems in Cleansing Shores . . .. . . .. D. Mode of Action and Toxicity of Solvcnt-emulsifiers VI. Conclusions and Prospects . .. . . .. .. VII. References .. .. .. . .

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I . INTRODUCTION The Report from the Select Committee on Science and Technology (1968) points out that oil pollution is referred to (as " slime ") in the Book of Genesis and by Herodotus. Such natural seepages still occur in petroleum-producing areas, but elsewhere, oil pollution of the sea results mainly from its transport or use as a fuel by shipping. Possibly the first account of this was by Jonas Hanway who in 1754 complained of leakages from wooden petroleum-barges in the Caspian Sea (Hawkes, 1961); a century later, these barges were still creating a pollution problem on the Volga. The first widespread use for petroleum products was in lamps, where mineral oil began t o replace vegetable or whale oil in the mid215

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nineteenth century. It was shipped in barrels carried in the hold, like whale oil or any other liquid cargo, but even so was liable to spillage as with the schooner " Thomas W. Lawson )', wrecked on the Isles of Scilly in 1907 with the loss of her cargo of two million gallons of crude oil (Parslow, 1967a). Steamers did not at first engage in the petroleum trade for fear of fire, so the first true tankers were sailing vessels fitted out with wing tanks. The Anglo-American Oil Company's " Daylight )', one of the most successful, sailed on into 1921, although the steamtankers " Gluckauf " and " Bakuin " entered the Batoum oil-service in 1886. At much the same time, the internal-combustion engine and the steam-turbine were invented. The Royal Navy turned t o oil-firing for the turbine-driven Tribal-class destroyers in 1908, while the first seagoing motor-ship '' Vulcanus was launched in 1910. Much of the early pollution of European coasts was by fuel from the bilges and bunker-tanks of oil-fired or motor ships, whose numbers were increasing rapidly. Crude oil was mostly processed in petroleumproducing regions and tankers carried the refined products, many of which were clean light oils. The shipping lanes converging on the English Channel are the busiest in the world, so that the degree of pollution already became sufficient to prompt the passage in 1922 of the Oil in Navigable Waters Act, which prohibited the discharge of oil or oily water in British territorial waters. The United States followed with the Oil Pollution Act of 1924. I n 1926 an international conference in Washington recommended the establishment of coastal zones 50-150 miles wide in which the discharge of oil should be prohibited ; agreement could not be reached, but the zones were recognized voluntarily by the shipowners' associations of many Western nations. The scheme formed the basis of a Convention drawn up by the League of Nations in 1935 but after the withdrawal of Germany, Italy and Japan from the League, this Convention could not be ratified and the outbreak of war in 1939 prevented further action. I n 1938, world petroleum production was 278 million tons ; western Europe consumed 36 million tons of oil, of which the British share was 11 million tons. Rate of consumption was enormously accelerated by the 1939-45 war and subsequent industrial expansion, until by 1967 world production had reached 1 828 million tons and Britain alone consumed 85 millions tons (Select Committee, 1968 ; British Petroleum CO., 1968). During this period, the contribution made to world production by Middle East oilfields grew from nearly 4% to over 27% (Fig. 1). By 1960, the growth of the European market and the political instability of the Middle East and other oil-producing regions made it economically and politically prudent to build refineries at the point of )'

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FIG.1. Main oil shipments t o western Europe-A, from 1963 t o early 1967 ; R, in late 1967. The width of tho arrows is proportional t o the tonnage carried. Compare with similar maps by the Ministry of Transport (1953) and IMCO (1964); after British Petroleum Review-( 1967).

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consumption. Thus not only was there a great increase in the seatransport of oil ; there was a basic change in its nature. Large tankers entering European waters now carry crude oil, while refined products (whose spillage creates less of a pollution problem) are carried overland or in small coastal tankers. Recent governmental efforts to control oil pollution of the sea have been reviewed in a US. State Deyt. Report (1959) and by BarclaySmith (1958, 1967). Various meetings of naturalists and wildfowlers in 1952 were followed by the appointment of the Faulkner Committee, which reported the next year (Ministry of Transport, 1953). I n 1954 an international conference in London drew up a Convention which, like that of 1935, prohibited the discharge of oil within specified coastal zones. The United Kingdom was the first to ratify the Convention, passing the Oil in Navigable Waters Act of 1955; by 1958, having been ratified by ten nations, the Convention came into force. I t s administration passed t o the Intergovernmental Maritime Consultative Organization (IMCO) when that body was formed by the United Nations in 1959. The United States ratified the Convention in 1961, after a further international conference in Copenhagen. Amendments to the 1958 Convention extending the prohibited zones (to include, for example, the entire Baltic and North Seas) and regulating further classes of vessel were proposed a t an IMCO conference in 1962 and eventually came into force in 1967 (IMCO, 1962, 1967) ; but by this time " Torrey Canyon " had been stranded off the coast of Cornwall, bringing to a head the apprehension felt in many quarters about the operation of increasingly large tankers. Proposals discussed a t subsequent IMCO meetings include regulations governing the construction, navigation and routeing of tankers as well as measures directly concerned with pollution prevention and control (Goad, 1968). Legal problems arising from the " Torrey Canyon " incident, summarized by Marshall (1967; see also Edwards, 1968) were discussed at, an International Legal Conference on Marine Pollution Damage convened by IMCO in Brussels during November 1969. Procedures were laid down by which a coastal nation might act if a casualty on the high seas threatened to cause severe pollution. A Convention was drafted placing strict liability for compensation upon the owners of an oilcarrying ship from which the cargo escapes or is discharged. As an interim arrangement, nearly 60% of the world tanker fleet had already subscribed to the TOVALOP plan, which from October 1969 provided for much of the cost of cleaning up an oil spill to be covered by the owners, encouraging them to take quick action in minimizing the resultant damage.

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11. SOURCES AND CONTROL A. Tanker operation and general-cargo shipping The largest and most dramatic spillages of oil a t sea have resulted from the collision or stranding of tankers. It has been argued that the current trend towards very large bulk carriers should reduce this risk, because fewer voyages are necessary to keep any one refinery or tankfarm supplied. Nevertheless, in the three years ending with April 1967, 91 tankers went aground and 238 were involved in collision. 19% of the groundings and 9% of the collisions resulted in cargo spillage-a total of 39 incidents. I n the first five months of 1968, a further 39 tankers were involved in various accidents, not all resulting in oil-spills (Brockis, 1967; Select Committee, 1968). When a large tanker is damaged, it is obvious that she is potentially capable of losing a great deal of oil ; modern design trends do little to minimize this possibility. Before the 1939-45 war, typical tankers carried 10 000-12 500 tons of cargo a t speeds up to 12 knots. To meet wartime demands, American shipyards went into mass-production of the T2 tanker, carrying some 16 500 tons a t a sustained speed of 144 knots. For some years after the war, this type formed the backbone of tanker fleets before it was ousted by " supertankers " (as they were called in the early 1950s) of about 24 000 tons. Tankers are constructed on a basic plan of three longitudinal series of tanks ; in the T2 and related designs, these were about 36 ft long. After the closure of the Suez Canal in 1956, even larger and faster tankers became economically desirable ; the implications of their deviation from earlier designs are reviewed in the Batelle-Northwest Report (1967). To reduce hull weight and simplify the plumbing, alternate wing-tank divisions became swash bulkheads (incomplete divisions which merely reduce cargo movement) ; in later designs this practice was extended to the centre tanks. Many recently-built vessels of 40 000-60 000 tons have tanks which are effectively 80-100 ft long. A greater capacity (and larger tanks) can be incorporated in older tankers by the process of " jumboizing ", in which a new and larger centre-section is inserted between the original bows and stern, which contain expensive machinery, crew-quarters, etc. Many T2 tankers were enlarged in this way, although the best-known example is now Torrey Canyon ", which " grew " from 67 000 to 118 000 tons. The capacity of today's '( supertankers "in the 100 000-500 000 tons range is obtained by increasing draught and breadth rather than length, so that a tank only three times as long as those in the T2 design may contain fifty times as much oil-the entire cargo of a pre-war tanker. Some ((

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dry-cargo bulk carriers of over 100 000 tons, designed for alternative oil-carrying service, lack even the longitudinal bulkheads. Doubt has been cast on the seaworthiness of some such designs if more than one compartment should be damaged. I n these circumstances, the simplification of pumping arrangements reduces flexibility in the control of cargo, while the development of better anti-corrosion treatments permits the use of thinner plating, which is less resistant to violent impacts. Although they are capable of high speeds, all but the very largest of modern tankers still have a single screw for reasons of economy. Their manceuvrability in narrow waterways is necessarily restricted. For example, “ Torrey Canyon ” was making about 16 knots when she struck Pollard Rock and would otherwise have required a t least 2 miles to come to a dead stop; other supertankers require as much as 7 miles (Wiebe, following Edwards, 1968). The turning circle of such tankers ranges from one-half to over 2 miles. Of course, modern navigation aids should compensate for this (see Kluss, 196813). Although she lacked a Decca Navigator, “ Torrey Canyon’s ” radar had a range of 40 miles. Had she been following a prescribed course, as all civil aircraft are required to do, she would have avoided disaster. Traffic separation is already observed, on a voluntary basis, in the Strait of Dover and other regions of high traffic density; its operation is discussed by Dilling (1968). However, the 40 000-ton tanker “ Anne Mildred Brravig ” was rammed by a small coaster in fog off the Elbe estuary in 1966 when proceeding on a faultless course. The collision was entirely the responsibility of the coaster, yet such small craft would not be subject to the proposed controls (see Brockis, 1967). Further preventive and remedial measures are discussed in a U.S. Congress Committee Report (1967). Measures which can be taken t o control pollution after accidental damage has occurred depend, of course, on the severity of the accident. A tanker still having her own power may be able to move off towards repair facilities or the open sea and might well have surplus tank capacity into which she could pump oil from the damaged compartment. Even when a stranded vessel is stuck fast, it is rarely necessary to jettison oil overboard in order to avoid immediate disaster. Unfortunately, the value of the ship is invariably much greater than that of the cargo and current salvage contracts provide no reward for the avoidance of pollution. The possibilities of pumping the cargo into an empty tanker standing off the wreck were well demonstrated when the “ Esso Margarita ” successfully received over 15 000 tons of the 18 000 tons of fuel-oil carried by the “ General Colocotronis ”, which ran onto a

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reef in the Bahamas in March 1968 (Spooner and Spooner, 1968; Fig. 2). However, it is often impossible for vessels of suficient capacity to approach as close as this ; transfer of cargo becomes unacceptably slow, especially if the stricken tanker has lost the use of her pumps. Holdsworth (1968) and Kluss (1968b) discuss the equipment and methods

FIG. 2. “ Esso Margarita ” (foreground; 1 1 000 dwt) unloading fuel-oil from the *‘ General Colocotronis ” (18 000 dwt), stranded on a reef off Eleuthera (Bahamas). Three-quarters of her cargo was safely removed, after which she was hauled off and sunk in deep water (photo : Frederic Maura).

available for salvaging the cargo in these circumstances, but weather conditions may, in any case, make such lightening impossible. Alternatives listed by Holdsworth include gelling, freezing and burning. Gelling is now feasible ; the material of choice is slow setting and thus does not require mixing. The process is expensive, but may be cheaper than clearing up the spill. Freezing would require a vast amount of energy and might lead to the brittle fracture of an already weakened

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hull. Burning is considered to be a last resort, since it renders the ship worthless ; experience with “ Torrey Canyon ” shows that it is possible, but requires the addition of much additional inflammable material and frequent reignition. The compartmental construction of tankers may permit salvage of an undamaged portion by “ explosive surgery ”, using shaped plastic charges, if the fire risk can be minimized. The after half of the “Anne Mildred Brovig ” was saved in this way and, in general, it is more useful after a collision than a stranding. Once a tanker has sunk in fairly deep water, it appears that oil remaining in her is released slowly but steadily through deck vents. The U S . Coast Guard (1959) estimated that, a t the end of the Second World War, a t least 61 tankers still containing 210 million gal of oil lay along the Atlantic and Pacific coasts of the United States; but recent dives on carefully selected wrecks off the north-east Atlantic coast failed t o produce even a small sample for analysis (U.S. Coast Guard, 1968). The fuel-tanks of other ships may retain their contents for longer ; the German cruiser “ Blucher ”, sunk in Oslo Fjord during April 1940, began to leak oil in June 1969. A source of pollution from tank-shipping which is less obvious but, until recently, was much more important than accidental damage, is the need for a tanker to carry sea-water ballast on her return journey. This is usually accommodated in the oil tanks and occupies up to one-third of the cargo space. The ballast has to be discharged a t the loading port as oil is taken on. Each tank contains the residues of its previous cargo ; in all 0.3-0*5% of the cargo is left behind-about 200 tons in a 50 000ton tanker. The discharge of even a third of this amount of oil in the ballast water would not be permitted at the loading port, nor would it be practical to build shore separating facilities capable of dealing with such large volumes ; so it was normal practice t o wash the tanks a t sea, pumping the washings overboard and then taking ballast into the clean tanks. From recent shipping figures, this would result today in the discharge into the sea of some 6 000 tons of crude oil per day-nearly 2+ million tons per year. Fortunately, the major tanker operators introduced the “ load-on-top ” system in 1964. This is described in detail by Kluss (1968a) ; in brief, the washings are pumped to one tank (acting as a slop-tank) where the oil is separated, often by the use of demulsifying chemicals or heating coils. When separation is as nearly complete as possible, the water is pumped from below the oil and discharged into the ship’s wake. At the destination port, a fresh cargo is loaded on top of the recovered oil. This procedure requires care, since only a little excess salt water can be dangerous in some refining processes; it also takes time and t,rouble, although this is balanced on

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average by the value of the oil saved (Brummage et al., 1967 ; Brummage, 1968). The 1958 Convention set an upper limit of 100 p.p.m. oil in water discharged a t sea, whereas the last of the slop-tank water reaches a concentration of 400-1 000 p.p.m. ; but the turbulence of the wake is such that in the immediately surrounding water this is reduced to 0.17 p.p.m. IMCO amended the Convention in October 1969, setting a new limit in terms of distance travelled. Sixty litres of oil per nautical mile will now be permitted which, in trials, produces no detectable slick. I n some of the latest large tankers (" Universe Ireland " and " Universe Kuwait ", for example), two wing-tanks function exclusively as ballast-tanks ; in those which will still require washing, special coatings and redesigned internal structures reduce the amount of " clingage " (see Davis, 1968). It is probable that as many as half a million tons of persistent oils are nevertheless discharged into the sea each year (Dudley, 1969). Their source is partly tanker-operators who still do not observe proper precautions and partly shipping other than tankers. Most generalcargo ships, when sailing only partially loaded, require extra weight low down in the hull. This is usually provided by filling empty bunkertanks in the double bottom with water which thereby becomes contaminated with fuel oil (in addition to any other pollutants or disease organisms present in the waters of the port of origin). A typical freighter carries about 1 000 tons of ballast, which may contain up to 10 tons of oil; in 1964, 16 000 such vessels discharged their ballast water in U.S. ports alone (U.S. Department of Interior Report, 1967). Some countries require ships ballasted in this way to carry oil-water separators but this does not guarantee that they will be used and many designs are very inefficient (see Shackleton et al., 1960; Permutit Co. Report, 1966). Many depend on gravity separation, even though the density of fuel oils is often very near that of the sea in European waters and may exceed that of tropical or fresh waters (Blade, 1966). I n any mechanically-powered vessel, particularly oil-fired or motor ships, the engine-room bilges will also become oily and may exceed the 100 p.p.m. limit. Ideally, such oily water, as well as recovered oil from separators, sludge filtered from fuel lines, and other oily wastes should be discharged to special reception facilities a t the destination port. I n most European and North American ports these exist and may even include mobile separator- or tank-barges, but in many others, facilities are inadequate or lacking (IMCO, 1964). The Faulkner Report (Ministry of Transport, 1953) points out that 1-2% of the total oil consumed escapes unburnt through the funnel of an oil-burning ship. A large vessel on the transatlantic service may burn 6 000 tons in it

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single crossing, so appreciable quantities must be deposited on the surface. Even outboard motors contribute a quantity of waste oil which in open waters is insignificant but can accumulate appreciably in enclosed bays, harbours and inland waters (English et al., 1963a, 196313; Dietrich, 1964).

B. Harbours and rnarine terminals Many of the sources of oil spillage a t sea, enumerated above, occur equally in port. Collisions happen with the greatest frequency in harbour approaches where the traffic is densest and other accidents may be associated with docking activities-an unusual example is the tanker ‘‘ Fina Norvege ”, which holed her forward fuel tanks with her own anchor in Plymouth Sound (see Holme and Spooner, 1968). Coastal tankers do not normally clean tanks a t sea before taking on ballast, but after a short period of separation in port much of the water can nevertheless safely be discharged overboard and the small volume of oily residues remaining can usually be accepted by shore facilities. It is worth noting that in very enclosed docks, where the water is more or less static, a series of small discharges containing 100p.p.m. of oil or less can still lead t o an appreciable concentration of oil in the receiving water. Under still conditions this may trap silt and other suspended matter and sink to the bottom, from which it is released to rise to the surface again after the slightest disturbance (as, for instance, in the Queen’s Dock, Swansea-Naylor, 1966). Perhaps the commonest source of oil pollution from dry-cargo ships in port is the process of bunkering with fuel oil. This is pumped through flexible hoses which are liable t o damage through wear or ship movement; an overlong one may fall between hull and jetty, becoming kinked or crushed, whereas too short a hose may be snatched from its couplings by sudden movements following the close passage of another vessel. Precautions which should be taken are listed by the American Merchant Marine Institute (1953). Unless each end of the hose is blanked off as soon as it is disconnected, its remaining contents are liable to drain out when it is hoisted ashore. Leakages can occur from inlets and vents, especially if the tank overflows ; any deck spills will reach the sea unless the scuppers are plugged. When the bunker-tank has been used for water ballast, the sea-cock may have been left open ; it is then possible for oil t o be forced out beneath the hull, appearing as a surface slick only a t some distance from the ship. A good look-out and efficient communication between pump and deck crews will avoid or minimize the more obvious forms of spillage. At oil terminals the same comments apply. With more pipes and

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valves to handle and a far greater pumping rate, there is a considerably increased danger of pollution; on the other hand, oil-jetty and tanker crews have the advantage of training and experience. An American Petroleum Institute manual (1964) deals with all pollution-control aspects of tanker loading and unloading operations. Dudley (1968, 1969) concludes that the major cause of oil-port pollution is human error-partly through poor communication and partly because of inattention or carelessness. I n Milford Haven, where development as a major oil port has taken place very rapidly, it is observable that each terminal suffers a rash of incidents (most of them fortunately minor) during its first few weeks of operation, until its jetty crew gains experience. It occasionally happens that a tanker enters her unloading port with hull damage sustained en route. If her tanks were ruptured below the waterline, oil will have escaped to be replaced by water, but as she is unloaded and her buoyancy increases, this water will flow out and will eventually be followed by the remaining oil. Kluss (1968b) describes the similar situation of a tanker stranded on a falling tide. Damage of this sort caused an overnight leakage of 250-500 tons of crude oil from the " Chryssi P. Goulandris ') into Milford Haven in January 1967 (see Nelson-Smith, 1968a, b). I n 1962 the " Benjamin Coates )' was holed in several places along the bottom of her hull when she hit rocks in the mouth of the Haven, but in this case oil escaped only immediately after the impact. Sea water was pumped into the damaged tanks to raise the level of the remaining oil, which was then unloaded from above by portable pumps (Dudley, 1968). In still waters, a leaking tanker can be surrounded by a floating spillboom, which contains the oil until it is pumped off or soaked up. Some booms are themselves made of, or stuffed with, absorptive materials such as fibrous polypropylene. Commercial booms consist basically of a floating barrier supporting a weighted skirt. Experience has shown that although they are little affected by a slight swell, choppy waves exceeding 6 inches slop oil over the barrier, while a current greater than 1+-2 knots lifts the skirt or carries oil beneath it (Hydraulics Research Station, 1967 ; Mayo, 1968 ; Dudley, 1969). A disadvantage for more routine use in oil docks is that a continuous boom blocks the passage of traffic. Most designs are made in jointed sections which can be dismantled, while one air-filled type sinks to the bottom when deflated (Anon., 1962). I n harbour mouths (or, equally, t o prevent an offshore slick from penetrating an estuary) the Hydraulics Research Station suggests a '' chicane of two curved booms, overlapping but staggered. A more promising alternative seems to be the )'

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FIG.3. A pneumatic boom (" bubble barrier ") retaining burning oil in the harbour at Ghent (Belgium); note that the wind is blowing the oil towards but not across the barrier, which is partly obscured by reflected sunlight at lower right (photo: Rudolf Harmstorf Lt,d.).

pneumatic barrier " (Stehr, 1959, 1964; Abbott, 1961 ; Sorrentino, 1963) in which a perforated pipe remains permanently on the bottom.

"

When required, compressed air is fed into it, producing bubbles which lift a current of water to form a standing wave on the surface. This entrained water, flowing away on each side of the line of bubbles, prevents the drift of oil and other floating debris quite effectively without hindering the passage of shipping (Fig. 3). I n a dock where oil is spilt regularly and can be boomed, it is usually

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feasible to provide a mechanical collector of some sort. If the area is small, a floating separator is often used, pumping its harvest ashore ; it may merely remove the surface Sayer, create a cyclone-separation vortex or concentrate the oil with rotating cylinders (the " Earle system "). I n larger docks and waterways a variety of special vessels has been used. They include barges with weir intakes and gravity separation such as " Norfolk Skimmer " (U.S. Navy Yard-see Schneider and Beduhn, 1967) or " Waferwisser " (Shell, Holland) whose outriggers hinge on each side to form a " vee-boom " collector, and those which use rotating cylinders or an endless belt to exploit the greater surface-adhesion of oil, such as " Port Service " (Baltimore -see the Batelle-Northwest Report, 1967) or " Sea Sweeper '' (BP/ Harmstorf-see Lane, 1967). Skimmers using weirs or ramps t o draw off the surface layer cannot operate in waves and are not very manceuvrable ; those with adhesion collectors have overcome these difficulties but the oil-water mixture which they pick up will not separate properly in rough-water conditions. I n more open harbours it will therefore be impossible t o contain spilt oil or t o recover it from the water by mechanical means. For economy of effort and materials, as well as the conservation of amenity and shore life, the oil should nevertheless be dealt with while still afloat whenever this is possible. I n estuaries there is often a problem of responsibility ; it may take months to identify and prosecute the culprit, while the body which is in the best position to deal promptly with the spill may lack the authority to allocate funds for treatment. For example, during the " Tank Duchess " incident in the Tay Estuary (February-March 1968, when about 90 tons of heavy crude oil leaked from a damaged tanker) it was found that Dundee Corporation could not finance the cleansing of waters beyond their beaches. The Harbour Trust was responsible only if the oil were a hazard t o navigation, which it was said not t o be, while the River Board had no jurisdiction over tidal waters and in any case was empowered to prosecute, but not to clean up. The result of this administrative stalemate was that after 3-4 days all the oil was stranded over many miles of shore, some of which proved extremely difficult and expensive to clean (Dundee Corporation Report, 1968 ; Greenwood and Keddie, 1968). I n contrast, oil pollution incidents in Milford Haven are investigated, treated and prosecuted by one authority, the Harbour Conservancy Board. Because of the great tidal volume and strong currents (see Nelson-Smith, 1965) solvent-emulsifiers are specially equipped launchroutinely used, but '' Seaspray "-a applies them t o the slick as soon as a spill is reported. Only after the worst incidents or in the mostt extreme conditions does oil reach the

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shore. The cost of dispersal is borne by the offending party; the oil companies operating there have agreed to accept the harbour-master’s assignment of responsibility for this purpose, even when there is no legal proof, sharing between them the cost of treating unassignable pollution (Dudley, 1968). The general position of responsibility for pollution of the sea or shore under British law is summarized by Elliott (1969). It is becoming an increasingly common practice to load or tranship oil at terminals or moorings which are some considerable distance off shore, where many of these remarks do not apply. Shell International pioneered the use of single-buoy moorings 10-15 miles (16-24 km) off the coast, where the cost of providing conventional shore facilities was prohibitive. The first was laid off Sarawak in 1960 and they are now in use at many terminals. Off the Libyan coast, a similar mooring system utilizes a pylon built on the sea-bed. A submarine pipeline carries oil to a manifold beneath the buoy (attached by a swivelling connection) or pylon ; valves below this connection are under remote control from the shore. The loading tanker may tie up directly to the buoy or, at a terminal in the Persian Gulf which acts as the wellhead of an offshore oilfield, t o a tanker permanently moored and adapted to store the oil produced. Loading takes place through flexible floating hoses. These operations seem hazardous, but strains are less than at multi-buoy moorings or conventional jettyheads because the tanker is free to swing and thus offers the least resistance to winds and currents (Howe, 1968 ; Anon., 1969). Off-shore terminals have also been made necessary by recent great increases in tanker size ; for example, in 1968 an island jettyhead was built 10 miles (16 km) off Kuwait to accommodate the present Gulf Oil 312 000-ton tankers of 79 ft (24.1 m) draught and projected vessels up to 450 000 tons. The only European facilities capable of receiving these tankers were opened at the same time, at Bantry Bay in south-west Ireland, solely for transhipment (see Davis, 1968). The oil is transported to refineries in Milford Haven, Europoort (Rotterdam), Denmark and Spain by tankers up to 100 000 tons. Milford Haven can now accept tankers up to 220 000 tons and 63 f t (19.2 m) draught. Shell, lacking a refinery in the Haven, found that it was economical to use 200 000-ton tankers drawing 62 f t (18.9 m) from 1968 even though Europoort would not be deep enough for them until 1970. The fully-loaded tanker is met in the English Channel, the southern North Sea or the Irish Sea by one of two specially equipped 70 000-ton tankers which is tied up alongside t o lighten the larger vessel either at anchor or while steaming gently ahead (Fig. 4). To

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FIG.4. '' Megara " (200 000 dwt) transferring 65 000 tons of crude oil to the specially equipped " Drupa " (70 000 clwt) off Lyme Bay (photo : Shell International Marine Ltd.).

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enter Europoort it is sufficient to pump off 30000 tons, which takes 10 h. Before the large tanker could dock at Thames Haven or Tranmere (on the Mersey), she must be lightened by the full 70 000 tons in order to reduce her draught to 45 f t (13.7 m) ; this takes 16 h (Anon., 1968a). There is as yet no record of a serious spill during this procedure. Kirby (1969) discusses possible sources and Shell refer to their experience of transhipnient in the Persian Gulf, pointing out that the Royal Navy refuels warships at sea as a matter of routine. Wiebe (in discussion following a paper by Edwards, 1968) advocates the off-shore unloading of tankers exceeding 100000 tons as a safety measure, to avoid the risks attending the navigation of these large vessels in constricted waterways. Nevertheless, since most spillages occur during transfer operations, the risk must necessarily be increased when multiplying the number of these operations per voyage. It has already been noted that many of the possible methods for containing and recovering oil spilt during such operations cannot be carried out under open-sea conditions.

C. Coastal industry and other sources A coastal refinery represents the most obvious risk for oil pollution, considering the millions of gallons of crude oil and its fractions which are processed or stored there. However, refineries are planned with the possibility of spillage in mind, and, provided that the relevant codes of practice (American Petroleum Institute, 1960, 1963 ; Institute of Petroleum, 1965) are properly observed, serious pollution incidents occur only as a result of rare accidents. I n a refinery, crude oil is purified and processed to produced a variety of fuels, lubricants and solvents as well as feedstocks for petrochemical plants. During these operations, continuous small-scale pollution occurs through leaking connections and glands, spills, breakages, sampling operations and the emptying of traps or settlement tanks. Larger volumes of oil may be released during emergency or routine shut-down of plant, cleaning and start-up operations. Water is used in some processes and inevitably becomes contaminated with the product. All drainage from the refinery site is carried to separators, usually of the API gravity type, although process-water may need special treatment first. The effluent may be held in a further settlement pond after passing through the separator. Most coastal refineries discharge to an estuary, creek or stream rather than across the open coast, so quality standards will be demanded for the effluent by some pollution-control authority, which may place the maximum permissible oil content anywhere between 5 p.p.m. and 100

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p.p.m. I n Milford Haven, the limit is 50 p.p.m. and, by adopting aircooling instead of the more normal water-cooling of plant, effluent flows are relatively small. However, there is still an appreciable effect on the vegetation and sedentary animal life of the shore in the vicinity of one refinery outfall (G. B. Crapp, personal communication, 1969). At Fawley in Southampton Water, the oil concentration in a refinery effluent is as low as 10-20p.p.m. but the rate of discharge is over 100 000 gal (455 000 litres) per minute, so a t least 1 500 gal (6 825 litres) of oil are discharged daily. The result is that in the area of saltmarsh surrounding the outfall, all vegetation is dead and even normal bacterial decomposition of the remains appears t o have been arrested (Baker, 1969). As a result, erosion of the mud-flats is taking place. Petrochemical works are often sited within or adjoining refineries and, as far as oil is concerned, the sources and control of pollution are much the same. The range of products is much wider, so the variety of compounds which might occur in waste waters is enormous ; their origins, removal from effluents and effects in receiving waters have been considered by Huntress (1953), Montes et al. (1956) and Gloyna and Malina (1963). Oil wells, loading and unloading terminals, refineries and bulk users of oil are often interconnected by pipeline. Nation-wide or international systems have been used in North America and the Near East for many years and are now being extended throughout Europe. I n many instances they connect with marine installations or cross waterways near the coast. The volumes and distances involved render a large pipeline an important potential source of pollution. One of the largest, the 30 inch (760 mm) Trans Arabia pipeline, carried an average of 10 million gal (nearly 50 million litres) per day in the early 1960s but is potentially capable of twice that performance. The 18 inch (460mm) pipe from Angle Bay (Milford Haven) to Swansea carries 250 000 gal (about one million litres) per hour a t an initial pressure of 800 p.s.i. (56 atmos) (OECD, 1961 ; B.P. Llandarcy, personal communication, 1969). Standards for construction and operation have been laid down by the Institute of Petroleum (1964, 1967) and their significance to possible pollution is discussed by Henderson (1967). The Ohio River Valley Water Sanitation Commission (ORSANCO) guidebook (1950) and Meyer (1967) consider the causes, detection and control of pollution from pipelines. Leak-detection techniques have an accuracy of 0.03% of the flow ; in the example given by Meyer, a 30 gal (140 litre)/h leak in the 100000gal (450 000litre)/h flow of a 12 inch (300mm) pipe would be detectable by discrepancy after 24 h pumping or by pressuredrop within 2 h of shutdown. Even such a small leak should be located

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in an underground pipe within 24 h and probably sooner in an underwater situation-although repairs in such a situation might take longer. The points where pipelines pass under waterways and shipping channels are the most liable to mechanical damage, from such natural causes as bank erosion or a shifting bed as well as from dragging anchors or dredging operations (Scherer, 1964). Such mechanical damage represents the greatest danger of a pipeline. Many thousands of gallons could be lost in a few minutes through a breakage (more than 175 000 gal-SO0 000 litres-were lost after sabotage of the Trans Arabia line in November 19691, whereas it would take 28 days for a 30 gal/h leak to lose 20 000 gal (about 100 000 litres). This sudden loss should be immediately detectable and could be minimized by stopping the pumps and isolating the damaged section. The BE' pipeline has twelve isolating valves ; its shortest section is one mile (1.6 km) long and contains about 57 000 gal (250 000 litres). When a pipeline crosses a waterway from which domestic supplies are drawn, it has been arranged that the water authority has control of these valves (see Cunningham, 1954). It is also possible to place the operation under automatic control-although a serious spill in Milford Haven resulted from the failure of automatic shut-off equipment in the Waterston refinery pipeline. Pipelines are none the less much more free from accident than tankers and limitations on their wider use are largely economic. The pollution hazards associated with bulk oil storage are considered in a paper by Samson (1967) and in subsequent discussion. I n Europe, covered tanks are used, often enclosed by an earthwork (bund) sufficient to contain temporarily the entire tank contents. I n Venezuela, non-volatile fuel-oil has been stored successfully in open earthbanked reservoirs, the largest containing nearly 400 million gal (1 750 litres). Their cost is only 15% of conventional tanks, so it is possible that in a highly competitive industry their use may spread. The risk of pollution by seepage from a badly sited reservoir is obvious ; a less obvious danger is indicated by North American experience with smaller open sumps in which many waterfowl died, mistaking the oil surface for water (King, 1952). The bulk distribution and storage of oil is usually controlled by skilled and responsible specialists. A much higher pollution rate, even though on a smaller scale, results from oil-transfer operations a t engineering factories, garages, oil-fired heating installations, etc. by personnel who have little knowledge of the proper procedures (Hogg et al., 1947 ; McKee, 1956). I n waterside areas, surface drains empty directly to the river, harbour or sea-shore ; waste cutting, lubricating

THE PROBLEM OF OIL POLLUTION O F THE SEA

233

and sump oils are all too likely to be jettisoned down the nearest drain, together with the results of spills, leakages and overflows. All industries use petroleum oils in some form or another ; in some branches of the steel industry, in which plants are almost all sited along sea or lake shores, large quantities of oil are used in quenching baths. I n petroleum-producing regions, but not a t present in European waters, off-shore oilfields are a significant source of pollution. Natural seepages are so well known off Southern California that a coastal feature is named Coal Oil Point and two are marked on the official Hydrographic Charts (see Merz, 1959) ; they also commonly occur in the Gulf of Mexico (Dennis, 1959), the Caribbean and the Persian Gulf. Oily material reaching beaches from this source usually has a composition which clearly distinguishes it from oil spilt during commercial activities (Rosen et al., 1959; Ludwig and Rich, 1964). Geologically, oil and natural-gas stocks are associated with salt deposits. I n many fields, particularly the older ones, large volumes of brine are produced with the oil. The Lake Barre field was recently discharging up to 320 000 gal (1 440 000 litres) per day of this (‘bleedwater ”, containing 5-35 p.p.m. of oil, into shallow Louisiana coastal waters (Mackin and Hopkins, 1962). Oily residues were found in bottom deposits around the bleedwater outlets (about 2 p.p.m. a t Lake Barre and up to 15 p.p.m. elsewhere) but were very local, attenuating rapidly with distance. During the process of drilling and tapping the well, carelessness, ignorance or poor communication can be as serious a cause of pollution as a t a tanker terminal. Their effects can be minimized by the observation of proper precautions as laid down, for example, by the Institute of Petroleum (1964). However, towards the end of the drilling operation, a sudden uncontrollable discharge may occur, resulting in a “ wild well ” (Mackin and Sparks, 1962). This is not infrequent in off-shore oilfields-Tarzwell (1967) places it a t the head of his list of serious oilpollution sources and the Batelle-Northwest Report (1967) notes that there are about 3 000 active wells off the U.S. coast-but such events are rarely recorded in the literature. A serious (‘blow-out ” occurred off the Texas coast in 1941, but the oil drifted to sea causing no damage (Bourne, 1968a). The leakage from the Union Oil Company well A-21 off Santa Barbara, California, received much greater publicity and its effects are still being documented. An initial blow-out a t the end of January 1969 was successfully contained by normal emergency procedures, but oil and gas under pressure were then forced through a porous layer outcropping to one side of the drilling platform. After ten days, during which the magnitude of the leakage averaged 21 000

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gal (95 000 litres) per day, this fissure was also plugged, whereupon a further leak appeared flowing a t up to 4 000 gal (18 000 litres) per day. The problems of dealing with a leakage under pressure in 190 f t (57 m) of water are considerable; 100 days after the blow-out it was estimated that a total of 3: million gal (nearly 15 million litres) had been losta much over a tenth of the cargo of the '' Torrey Canyon"-within smaller area (Smithsonian Institution, 1969a, b ; Jones et ab., 1969; Standley et al., 1969). Oil was still flowing a t the end of July 1969 and fresh leaks were reported in January 1970. I n a recent American study quoted by Batelle-Northwest (1967) it was estimated that a minimum of 300 000 gal (1 300 000 litres) might be lost during the six weeks required t o regain control of a typical GuIf Coast off-shore well. The upper limit of the estimate was, however, set a t nearly four times the volume of " Torrey Canyon's " cargo.

111. PROPERTIES OF PETROLEUM OILS

A. Physico-chemical characteristics Serious problems of pollution are caused by the crude oils, residual fuel-oils, lubricating oils and miscellaneous tank washings, sludges and tars-known collectively as " persistent oils " (Ministry of Transport, 1953) t o distinguish them from light fuel oils such as gasoline (motor spirit), kerosine and gas oil which spread and evaporate very rapidly when spilt. Crude oils are by far the most complex and variable of these persistent oils. A general review of their composition and properties is given by McKee (1956) and some typical values of important characteristics of crude oils entering European waters are listed by Berridge et al. (1968a) and Brunnock et al. (1968). When fresh, they have relative densities in the range 0.829-0-896, although evaporation of the lowboiling " light ends " quickly increases this to 0.921-0.975 for an " atmospheric residue " boiling above 370"C, or t o 1.023-1.027 for a Middle East crude residue boiling above 1000°C (the density of sea water being 1.025). Smith (1968) gives a table showing the loss of bulk and gain in density of Kuwait crude oil as progressively higher-boiling fractions evaporate from it, reproduced as Table I . The '' pour-point "-an imprecise value giving some indication of whether an oil will spread or solidify on a cold surface-varies from 7°C (Brega, Libya) t o minus 34OC (Tiajuana, Venezuela). The Libyan oil has 11.4% wax against 4.8% in the Venezuelan; Middle East crudes contain 5.5-7.0y0 wax and their pour-points are also intermediate. Kinematic viscosity (measured a t 38OC) is fairly uniform for these

THE PROBLEM O F OIL POLLUTION O F THE SEA

235

TABLEI Loss

of

fraction

up t o 100°C up t o 200°C up t o 300°C up t o 400°C

Loss of wt :h 9.0 13.0 38.1 53.1

Loss voi

of

l/o

11.8 27.7 43.6 58.5

Relative density of residue (at 15.5'17) 0.895 0.926 0.955 0.983

crudes a t 4.13-9.6 cRt except €or Tiajuana, which is much thicker at 25 cSt. Fuel and lubricating oils lack volatile components and are thus not subject to loss or thickening by evaporation. Some lubricating oils are fairly thin (McKee quotes a viscosity of 250 cSt a t 20°C for an S.A.E 30 oil) whereas residual fuel-oils are essentially crude oils from which the lighter fractions have been distilled, and are thus very thick and heavy a t sea temperature (see, for example, Blade, 1966). Sludges settle out from crude oils during transit and may have a wax content as high as 37% (Brunnock et al., 1968). The solubility of hydrocarbons in water is proverbially very low, but is appreciable in straight-chain paraffins up to C, and in several of the liquid aromatics-for example, a t sea-water temperatures : benzene, 820 p.p.m. ; toluene, 470 p.p.m. ; pentane, 360 p.p.ni. ; hexane, 138 p.p.m.; heptane, 52 p.p.m. (McKee, 1956; Hodgman et al., 1960). McKay (in discussion following paper by Wardley Smith, 1968b) quoted a solubility of 1Op.p.m. for nonane, pointing out that the solubility reduces by a power of ten for every three carbon atoms added. He therefore suggested that a ton of dodecane might be dissolved in each 100 mile2 (256 km2) of the English Channel, although the entire Channel would be required to dissolve a ton of octadecane. Freegarde (during the same discussion) reported that increases in the oil content of sea water in the Western Approaches had been detected at the time of the " Torrey Canyon " incident, using spectrofluorimetry, from a normal 3 parts to over 20 parts per 1 000 million. The chemical composition of crude oils has a bearing on both their toxicity and the changes which they undergo when spilt a t sea. Apart from the water-soluble phenolic compounds, the most toxic elements are the more volatile aromatic hydrocarbons. During the early stages of a spill, an aromatic crude such as Kuwait (whose high sulphur content of 2.5 yo tends t o inhibit oxidative processes) will be more toxic than the highly paraffinic Libyan, with 0.21% sulphur. Oxidation may

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be catalysed by sunlight or by trace metals, such as vanadium, which are present in the oil. The products may be water-soluble or surface active and may thus reduce the bulk of the slick or contribute to its emulsification. Compounds originally present in crude oil may also contribute to the formation or stability of emulsions, for example resinous “ asphaltic ” particles and sulphonic acids (Pilpel, 1954, 1968). B. Behaviour of spilt oil on sea and shore When a thin oil is spilt on a clean water surface it will rapidly spread until, at least under theoretically perfect conditions, it has become a monomolecular layer. Crude oils on natural waters probably never achieve this, but the typical iridescence of a small slick indicates mm, which represents about 150that its thickness is 1-5-10 x 1 000 litres/kmz. Quantities less than this produce a silvery sheen, colours begin to appear at the lower limit and become dull a t the upper limit. A thicker slick is dark, without interference colours (Stroop, 1930; American Petroleum Institute, 1963). As the oil spreads, its more volatile constituents evaporate and the water-soluble materials are leached out. The remaining residue will have an increased viscosity and pour-point, thus a lessening tendency to spread further, so that spreading is a self-retarding phenomenon. Blokker (1964, 1966) has given equations for the spread of an oil-slick which are elaborated €or various crude oils by Berridge et al. (1968a) in an account of their field experiments. Evaporation plays a considerable part in reducing the bulk of a crude-oil slick; i t is estimated that about one-third of the “ Torrey Canyon’s ” cargo of Kuwait crude was lost by evaporation following the spill (Brunnock et al., 1968), equivalent in effect to the removal of all fractions boiling below about 300°C (see Table I, p. 235). McKay (in discussion following Brunnock’s paper) pointed out that this quantity of hydrocarbons equals the average total amounts of sulphur dioxide and smoke in the atmosphere over Great Britain, so that the “ Torrey Canyon ” stranding contributed substantially to air as well as water pollution. Although oil traditionally calms rough waters, appreciable amounts are still carried away by wind from the tops of breakers at sea or from waves as they strike the shore (ZoBell, 1964). Considerable damage was caused to lichens and flowering plants on Cornish cliff tops by wind-blown oil-spray from below (Ranwell, 1968a, b). Very large amounts may also disappear by the sinking of heavy residues, often aided by the incorporation of water during the formation

237

THE PROBLEM O F OIL POLLUTION OF THE SEA

of emulsions. Some 20 000 tons of crude oil were lost from the “ Anne Mildred B r ~ v i g” but never appeared on the nearby beaches of NW Germany, it is thought because they sank a t sea (Stehr, 1967). The reverse process has been recorded on a t least one occasion when about 6 400 tons of heavy fuel-oil were spilt in icy seas, sinking to the bottom but reappearing later under warmer conditions (Dennis, 1959). Crude oil emulsifies very readily a t sea, forming stable water-in-oil emulsions which can contain up t o 80% water (Berridge et al., 1968b). Such emulsions are stiff, yellowish-brown in colour and, since the “ Torrey Canyon ” incident, have become widely known as “ chocolate mousse ”. The process of emulsification slows down the tendency of a slick t o spread. The viscosity of “ mousse ” is in excess of 1 000 cSt (Canevari, discussion following paper by Moore, 1968) and it is more likely to break into ragged patches or “naps ”. However, by the incorporation of so much water, the total amount of material which might eventually require removal from a beach is considerably increased. Where there are large quantities of suspended matter, for example in tidal estuaries, this also becomes incorporated into the oil, increasing its tendency to break up and sink (Poirier and Thiel, 1941). Chipman and Galtsoff (1949), observing this, carried out a n investigation on the intentional removal of oil by sinking with specially-treated sand. Hartung and Klingler (1968) report several observations on the occurrence of sunken oil in aquatic sediments. Their experiments agree with those of Chipman and Galtsoff, that increasing salinity reduces the ease with which oil is sedimented-sinking was most effective in fresh water. Masses of sunken oil, rolled along the bottom by waves and currents, accumulatz larger particles of sand, shells and small stones ; appearing on the beach as hard tarry balls, they are described as coquina ” (Dennis, 1959; see also Stander and Venter, 1968). The formation of these discrete masses of oil probably assists in processes of biological degradation, which takes place largely a t the oil-water interface (see, for example, Orton, 1925; comments by Gunkel following paper by Ramsdale and Wilkinson, 1968 ; Langston, 1969). I n experiments on the rate of spread of small samples of crude oil on calm waters, Berridge et al. (1968a) found that 9 gal ( 2 $ litres) produced a slick of 7 ft (220 cm) radius in 30-60 s, but in winds exceeding 3 mile/h (1.35 ms - l ) the slicks moved bodily faster than their rate of spread. Over the long term, the pattern of oil pollution along some coastlines corresponds predictably with seasonal changes in the strength and direction of ocean currents (Dennis, 1961). Observations on the movement of individual slicks a t sea suggest that the wind has more effect than water movements although, in making predictions, due ( (

238

A. NELSON-SMITH

allowance should be given for strong ocean or tidal currents. Calculations made when plotting the drift of " Torrey Canyon " oil showed it to move in the direction of the wind a t about 3.4% of its speed (Smith, 1968). This agrees well with measurements of surface drift in the Atlantic made by Hughes ( I 956), using floating plastic envelopes which travelled with the wind at 3.3% of its velocity. An oil-slick released experimentally in Japanese waters travelled a t 4% wind speed (reported by Brockis following Berridge et al., 1968a) while the German Hydrographic Institute, plotting the movement of oil from the " Gerd Maersk " after her accident in the North Sea in 1955, showed that it moved a t about 4.2% wind speed (Tomczak, 1964). Earlier experiments at sea off the United States in 1926-27 and off the British Isles in 1952 are referred to in the Faulkner Report (Ministry of Transport, 1953). Slicks were followed for 90 miles over 72 h during the American experiment, when it was concluded that most persistent oils will form an invisible film and thus " disappear " within 100 h of discharge; the British experimenters tracked a slick for 20 miles over eight days. Evidence from the Department of the Government Chemist, appended t o the Report, suggests that even very thin films can build up o n a windward shore to cause appreciable pollution. Berridge et nl. (1968b) report that emulsions containing less than 50% water appear, on casual inspection, t o be undiluted oil. These emulsions probably form thin films and ultimately disappear, whereas " mousses " containing 5 0 4 0 % water remain as a film over I mm thick. The 30 000 toils of oil which were converted into " mousse " and polluted the north coast of Brittany on 1 1 April 1967 were spilt from the " Torrey Canyon " on 18-20 March and followed an irregular course eastwards for about 140 miles, touching Guernsey on 7 April before drifting south over the remaining 40 miles. A further 40 000-50 000 tons, released on 26-30 March, moved southwards from about 2 April for nearly 200 miles, passing Ushant on 1 7 April and penetrating well into the Bay of Biscay by 1-3 May. After apparently successful sinking operations, a small quantity eventually reached the south coast of Brittany on 1920 May (Smith, 1968). When the slick reaches the coast, its behaviour depends on the nature both of oil and shore. In all but the heaviest pollution, much of the oil will be carried to the strandline along high-water mark by successive tides. Well-weathered or heavy oils become mixed with mineral or vegetabIe particles during this process, forming the oil-cakes mentioned above. Those which are thin, because freshly spilt or by the action of hot sun, may cause greater trouble by sinking into sand and shingle or clinging to seaweeds. The most troublesome beach to

THE PROBLEM OF OIL P O L L U T I O N O F THE SEA

239

clean is one of large pebbles, between which oil may sink t o a depth of 0.5-1 m (see Wardley Smith, 1968a). Oil does not sink so readily into wet sand, but breakers may throw fresh sand over it, burying it in layers like geological strata (Fig. 13, p. 276). I n this way a badlypolluted beach may appear clean shortly after the stranding of the oil, which is revealed later by the removal of surface layers during storms or in seasonal sand-movements (ZoBell, 1959, 1964; Smith, 1968; Kolpack, 1969). Oil may also persist on dry rock surfaces or amongst weed, barnacles and mussels, where in addition to the biological agencies discussed below it is slowly removed by drying, hardening and the incorporation of sand particles, finally eroding or flaking off. Although they fail to wet the mucous body surfaces of animals or the mucilaginous surface of lower-shore algae, some oils cling t o the byssus-threads of mussels, the horny outer layer of shells and upper-shore weeds which have a naturally oily surface. At the head of the shore, oil also has an affinity for some maritime grasses and flowering plants, which have been used in the mopping-up of localized spills. Tide-pools become covered with a thick film of oil, but this has a surprisingly small influence on gas-exchange across the surface. Roberts (1926) showed that during a 24-h test period, water depleted of oxygen by boiling reached 99% saturation below a film of diesel oil 0.002 mm thick and 60% saturation below an 0.03 mm layer. Boswell (1950) found that a layer of crude oil 0.5 mm thick reduced the rate a t which boiled sea water absorbed oxygen to 85% of his uncovered control during a six-day test. Brown and Reid (1951), in similar experiments over a two-day period, found that in some tests a 1.4mm layer had no detectable effect; a t worst, the amount of oxygen absorbed through the oil was 75% of that taken up by the control sample. Water beneath a 17 mm layer absorbed 73% as much as the control. During the pollution of the Santa Barbara Channel by a ieaking off-shore oil-well, the oxygen saturation beneath a " heavy slick " (thickness not specified) was 98.5% of that in clear water nearby. However, light intensities beneath the oil, measured on two occasions, were generally 1% of surface intensity and a t best 5-10% (Smithsonian Institution, 1969b). This attenuation is likely to be unimportant beneath a moving oil-slick a t sea but may have greater effects in rockpools which, on a sunny day, are normally supersaturated with oxygen from the photosynthetic activity of the algae growing in them. It seems probable that a layer of dark-coloured oil would also raise the water temperature by its absorption of solar energy and by blanketing the surface of the pool, but measurements or estimates of the magnitude

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A . NELSON-SMITH

of this effect are not to be found in the literature. Spencer (1967) found that mud in an Essex estuary was warmed through 5-6°C during tidal exposure in late summer, raising the temperature of the returning sea water by about 1°C. C. Detection and identi$cation liuman senses can detect surprisingly low concentrations of petroleum oils. Melpolder et al. (1953) found that a very sensitive nose can detect 0.005 p.p.m. of gasoline (motor spirit) in cold water, receiving a " strong odour " from 0-01 p.p.m. Ineson and Packham (1967) quote the even higher sensitivities of 0.00005 p.p.m. for motor spirit (with additives) and 0.0005 p.p.m. for diesel oil, although heavier fuel and crude oils are detected only at 0.2-25.0 p.p.m. Oily taint in fish and other sea-foods or in drinking water can presumably also be detected at these levels. An oil-film 4 x 10-5 mm thick (corresponding to about 0.04 ml/m2) is just visible in the most favourable of normal lighting conditions (Stroop, 1930 ; American Petroleum Institute, 1963). Dangl and Nietsch (1952) claim that 0.01 p.p.m. of mineral oil can be detected by blue fluorescence at the meniscus of a sample under ultra-violet light, although the specificity of this test has been questioned (see Ineson and Packham, 1967). I n the field, oil-slicks invisible to the eye can be recorded from the air by infra-red colour photography (Cowell, 1969a). It is also possible to distinguish an oil-film from the effects of wind, fish-shoals or floating debris which sometimes resemble a slick. The necessity for processing the film involves a delay, but the technique may prove useful for the enforcement of antipollution legislation. A simple field-test was reported by Weir (1964), who discovered that kerosine contaminating a drinking-water supply stopped the active movement of a small piece of camphor dropped on the water surface. Camphor also moves actively on clean sea water and is completely arrested by a film of crude oil at the lower limits of visibility. A rapid method which can determine less than 0.1 p.p.m. of petroleum oils in water is the combustion of a small water sample in oxygen (van Hall et al., 1963). Inorganic carbon is first removed by acidifying the sample. The gases evolved are passed over heated cupric oxide and carbon dioxide is determined in the gas-stream, using an infra-red analyser. It should be remembered that the technique determines all organic carbon and is not specific to hydrocarbons. Webber and Burks (1952) stripped light hydrocarbons (C, and below) from water in a stream of carbon dioxide. Melpolder et al. (1953) were able to include all those boiling below 200°C by passing hydrogen through a water

THE PROBLEM OF OIL

romwIoN

OF THE SEA

141

sample heated to boiling. The vapour was trapped in liquid nitrogen and then dissolved in carbon tetrachloride for analysis by mass spectrometry. Such low-boiling fractions are, however, not characteristic of oil spilt a t sea and the concentration of samples is more usually achieved by filtering the water through a column of active charcoalsee, for example, Rosen and Middleton (1955) and Greenberg et al. (1965)-or by liquid/liquid extraction with benzene, chloroform, carbon tetrachloride or hexanes. Kirschman and Pomeroy ( 1 949) discuss the merits of various solvents and extraction methods. Most are unreliable where the original concentration lies below 10 p.p.m. Merz (1959) found chloroform to be the best solvent for extracting oily material from beach deposits. Hartung (1963) used carbon tetrachloride to extract oil from the plumage of ducks killed in a pollution incident. Standard laboratory methods for the sampling, determination, and analysis of oils in water are given by the American Petroleum Institute (1957) and the American Public Health Association ( I 960) ; techniques for the quantitative determination of mineral oil arc briefly reviewed by Blokker, discussing a paper by Ineson and Packham (1967). The main problem with such determinations is that petroleum, being a complex mixture, has no outstanding overall characteristics. Various methods may, by their nature, exclude certain components or include extraneous organic materials in the result : for many analytical purposes, ‘‘ oil ” and “ grease ” are terms defined on the basis of the extraction or analysis recommended (see, for example, Ludwig et al., 1965).

Gravimetric or volumetric methods involve the measurement of a solvent extract after evaporation under standard conditions. The detection limit is about 5 p.p.m. and up t o 30% losses are to be expected. The extract may be purified by chromatographic separation on alumina before evaporation and weighing, which increases the sensitivity to 0.1 p.p.m. and also increases the accuracy. Alternatively, the density of the extract may be obtained in a pycnometer (see, for example, Levine et al., 1953) and compared with that of the pure solvent ; the density of the oil, if unknown, has to be assumed. Using carbon tetrachloride, the method is accurate only down to 10p.p.m. but this sensitivity is increased t o 0.3 p.p.m. by substituting the much denser tetrabromoethane. Optical methods may be applied to the partially evaporated extract, for example, measurements of infra-red absorption a t 3.3-3.5 p are sensitive t o about 0.1 p.p.m. and are fairly accurate unless there is a high proportion of low-boiling aromatics, whose i-r absorption is weak (Simard et al., 1951). Ultra-violet light at 2 700-4 000 A is strongly absorbed by petroleum oils, permitting a

242

A . NELYON-SMITIL

high sensitivity, but the absorption is due only to aromatic rings and similar structures. Thus the precise nature of the polluting oil must be known and the error can be quite large (Harva and Somersalo, 1958). Ultra-violet fluorescence is an extremely sensitive measure for oils rich in aromatics, although interference may be experienced from naturally-occurring polynuclear aromatic hydrocarbons. A detection limit of 0.001 p.p.ni. is claimed and reference has been made above to determinations of 0.003 p.p.m. in coastal Atlantic Ocean water. Oil adsorbed onto active charcoal can be extracted in acetone and suspended in water with the aid of a detergent, when the turbidity of the sample is measured (Sherratt, 1956; 1962). The detection limit is about 1.0 p.p.m. ; the method will not determine water-miscible fractions and assumes a constant particle-size in the suspension, although it may vary from component to component. Marine oil pollution is often heavy enough not to require confirmation in the laboratory ; the problem is then to determine the probable nature and source of the oil. This involves either comparisons with suspected sources, if samples can be obtained from them, or an analysis sufficiently detailed to characterize the polluting sample. A simple comparative method utilizes the patterns revealed under ultra-violet light after a crude form of paper chromatography. Schuldiner (1951) allowed spots to spread in concentric circles, whereas Herd (1953) suspended a paper strip overnight, dipping into an ether solution of the oil, to obtain bands of varying width and density. These papers can be stored for several years and have been used in successful prosecutions. Johannesson ( 1955) made similar comparisons, using the vanadium and nickel content of ashed fuel-oils to determine the source of harbour spillages. Brunnock et al. (1968) investigated the usefulness of vanadium, nickel, sulphur, wax and asphaltene content in identifying beach pollution. They also give distillation curves and n-paraffin profiles of crude oils, their residues and beach deposits, concluding that these data make it possible t o determine which crude is responsible for the pollution, a t least amongst those normally entering European waters. It is pointed out that tank sludges accumulate over a number of voyages, whilst fuel-oils are usually blended from several different crudes, so that pollution from these sources poses problems of analysis and interpretation. Rosen and Middleton (1955) adsorbed samples of polluting oil on silica gel, eluting aliphatics with iso-octane and aromatics with benzene. The infra-red absorption spectrum given by each fraction between 5 and 1611 proved sufficiently distinctive to match samples from the known source of the oil. Their later work (Rosen et al., 1959) showed

THE PROBLEM OF OIL POLLUTION OF THE SEA

243

that such spectra were, in general, useful more for confirming the nature of the pollution than for identifying its source. Meinschein and Kenny (1957) used a similar method, eluting successively with n-heptane, carbon tetrachloride, benzene and methanol. They analysed the eluates by infra-red and mass spectrometry for the higher-boiling hydrocarbons occurring in soils. According to Melpolder et al. (1953), mass spectrometry permits easy calculation of hydrocarbon typeanalysis from a sample containing 0.1 p.p.m. oil. Paper chromatography is a simple, rapid method of analysis which has been applied to the identification of crude oils by Bhattacharya (1961). As a technique, it has t o some extent been replaced by separation on thin layers of silica gel, alumina or porous synthetic polymers. Thin-layer chromatography has been used mostly for aromatic or heterocyclic hydrocarbons (Kucharczyk et al., 1963 ; Sawicki et al., 1964; Janak and Kubecova, 1968), but Snyder (1968) has developed a solvent suitable for the separation of saturated hydrocarbons and olefins. Gas-liquid chromatography is also rapid and very sensitive, but until recently it was restricted to hydrocarbons of C, or less, at best, those boiling below about 350°C (Halasz and Wegner, 1961). Ramsdale and Wilkinson (1968), using a dual-column GLC apparatus in a programmed temperature-gradient, have since produced curves with peaks corresponding to paraffins of C,, or higher, boiling at about 5OOOC. The chromatogram of a fuel-oil has a general shape which distinguishes it from that of a crude. Weathered oil from beach pollution produced a curve generally resembling that from tank residues. Evidence of blending can be seen in some fuel-oil chromatograms and a peak near C,, seems typical of Kuwait crude. As well as their use in making direct comparisons of the pollution and its possible source, it seems that a reference collection of the gas-liquid chromatograms of typical oils could be slowly accumulated.

IV. EFFECTS OF OIL POLLUTION A. Mode of action and toxicity of oils 1: Birds

Most marine animals are protected from oil to some extent by the fact that it fails to wet their exposed flesh, which is usually covered by a film of mucus. The plumage of sea-birds is water-repellent but oleophilic, so they lack this basic protection. Ducks, auks (razorbills A k a torda L., puffins Pratercuka arctica L., Uria spp.-guillemots in Europe or murres in N. America), divers Gavia spp. and penguins are particularly at risk because they and the oil both normally occur on the

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water surface; gulls (Larus spp.), gannets (Sula spp.) and their relatives are far more aerial, whereas waders feed on slioras and mudbanks. Auks and divers swim for some distance underwater and if they surface in an oil-slick their backs and wings become covered. Bourne (1968b) observed that their immediate raaction to oil was to dive again, but in any large-scale pollution this would almost certainly rasult in further oiling. Gulls, swimming into oil on the surface, flew off. I n contrast, long-tailed duck CZanguEa hyemdis (L.) in the Baltic are reported to settle preferentially in oil patches (International Committee for Bird Preservation, 1960 ; Lemmetyinen, 1966). The primary effect of oil on sea-birds is t o penetrate or cling t o their plumage, which mats the feather structura. I n a lightly-oiled bird, water can then fill the spaces in which air is usually trapped, eliminating heat-insulation and reducing buoyancy (Portier and Raffy, 1934 ; T h i n g , 1952; Hartung, 1967; Goethe, 1968). A mora heavily oiled bird is physically weighted down so that its swimrniiig movements are impeded and flight becomes impossible (Figs. 5 and 6). It has been stated repeatedly (Dennis, 1959; Tuck, 1960; Hawkes, 1961) that a spot of oil 2-3 cm in diameter on the breast of a bird is enough t o bring about death, a t least in the colder seas. On the other hand, Erickson (1962) reports that up t o one-half the coastal ducks shot by hunters in the north-eastern United States showed “ oil-burn ” and many had tainted flesh, although they were otherwise healthy. Even a light oiling causes birds to come ashore if possible, whera they preen incessantly. This further damages their feather structure. They are disinclined to feed, but are certain to ingest quantities of the oil (Hawkes, 1961 ; Goethe, 1968). Hartung (1963) extracted an average of 3.6 g oil from the plumage of medium-sized scaup (Aythya sp.) found dead and ‘‘ moderately ” oiled. His experiments showed that a single dose of one-third this quantity had marked effects on mobility, although it was not fatal. A later sample (Hartung, 1965a) had plumage soaked with an average of 7 g oil. Ducks preen approximately half the polluting oil from their feathers within a week, most of it on the first day of oiling. The oils fed to ducks (Anas pzatyrhynchos L. and A . rubripes Brewster) by Hartung and Hunt (1966) caused lipid pnedmonia, severe intestinal irritation, fatty changes in the liver, necrosis and adrenal enlargement. Nervous abnormalities, suggesting inhibition of anti-cholinesterase activity, also reported, were probably due to organic phosphate additives in the samples of diesel and cutting oils. Amongst birds kept in optimal conditions, the amounts fed were relatively non-toxic ; all survived doses of up t o 20 ml/kg body-weight of lubricating and 24 ml/kg of diesel oil. The toxicity was greatly

FIG.5. A guillemot (Uria aalge) struggling to keep afloat after oil has destroyed the buoyancy provided by its plumage (photo : Carl Stockton).

FIG.6. Another guillemot which died in crude oil emulsion from the ’‘ Torrey Canyon ”, washed ashore in Sennen Cove (photo : Anthony Clay). A.I.B.-S

9

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enhanced amongst a group kept a t low temperatures in crowded conditions, when an LD,, of 4 ml/kg was found for the diesel oil (i.e. about 2 ml per duck). Hartung (1967) found that an oiled duck was under the same temperature stress a t plus 15°C as a normal duck at minus 20°C; however, even heavily oiled ducks survived a t minus 26°C for as long as 36 h, provided they had sufficient fat reserves t o keep up the high metabolic activity needed t o maintain their body temperature. Mallard ( A .platyrhynchos) in poor condition survived this temperature for only 4 h after being covered with 7 g diesel oil. Adequate food is thus essential to survival, but in a coastal oil-spill the feeding-grounds are likely also to be affected by oil. Harrison and Buck (1967) reported that, although a high sea-bird mortality attended an overnight spill in the Medway Estuary during the autumn of 1966, the greatest effect was on the food supply. Surviving birds were forced to leave the area for the whole of the following winter. Oil is known t o affect the viability of bird eggs. Fuel-oil has been sprayed onto their eggs in successful attempts to control populations of gulls Larus spp. and cormorants Phalacrocorax carbo (L.) (Gross, 1950). I n experiments by Hartung (1965b), duck eggs treated with 236 mg medicinal oil (presumably non-toxic) showed a hatchability of 20y0 as against 90% in controls ; only one egg treated with more than 12 mg subsequently hatched. The undersides of ducks were then smeared with 4-5 ml of the oil before setting them to incubate fresh fertile eggs; of 19 eggs, none hatched. Rittinghaus (1956) reported an incident in which the eggs of numerous terns (Sterna sandvicensis Latham) and other shore birds failed t o hatch after the parents had become contaminated with stranded oil, and Jouanin (1967) observed that gannets Sula bassana (L.) (which are normally unaffected by floating oil, since they dive only on prey that they can see) were fouling themselves and their eggs by collecting oiled seaweed as material for building nest-mounds. Hartung (1965b) further found that a single dose of lubricating oil, fed a t 2g/kg, immediately halted laying and suppressed reproductive behaviour. 2. Mammals Aquatic mammals are in somewhat the same situation as diving birds. They return to the surface a t intervals to breathe and most of them have fur which readily traps oil, thereby losing its property of heat-insulation. Fewer accounts have been published, but Peller (1963) records the oiling of muskrats (Ondatra sp.), beavers (Castor Jiber L.) and even deer, while Wragg (1954) observed that fuel-oil used as a

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medium for spraying insecticide destroys the water-proofing of muskrat fur. Amongst marine mammals, damage t o seals has been reported from the Antarctic by Lillie (1954), from Cornwall during the “ Torrey Canyon ” incident by Spooner (1967), and during the Santa Barbara Channel spillage in California (Smithsonian Institution, 1969b ; California Department of Fish and Game, 1969). The latter incident occurred during the seasonal migration of the grey whale Eschrichtius glaucus Cope, but it was observed that the whales took pains to avoid the oil. Five whales and four porpoises (Phocaena sp.) were found dead, a rather high mortality. Oil was not proved t o be the cause, but the corpse of a bottle-nosed dolphin Tursiops truncatus (Montagu) had the blow-hole plugged with oil. Heavy slicks surrounded island colonies of sea-lions Zalophus californianus Lesson and sea-elephants Mirounga angustirostris Gill, amongst which further unexplained mortalities were observed. Oil damage in seals is frequently said to include severe eye irritation; a blind female now in a Cornish seal sanctuary was rescued during a fuel-oil spillage some years ago. 3. Fish

The outer surfaces of fish, their mouths and gill-chambers, are coated with a slimy oil-repellent mucus. Rushton and Jee (1923) painted the gills of trout (Xalrno trutta L.) with fuel-oil and immersed others completely in it, but commented that within a half-minute of returning them t o clean water, the oil had completely floated off. They observed no harmful after-effects, but Thomas (quoted by Gutsell, 1921) found that a petroleum residue and a light fuel-oil, applied as emulsions, coated the gills of his experimental fish and rapidly killed them by suffocation. Presumably, pelagic eggs and young fish might become trapped in slicks which have begun to form a mousse ”, but evideiice from California during the wreck of the “ Tampico Maru ” (North et al., 1964) and the Santa Barbara Channel spill (Smithsonian :Cnstitution, 196913) suggests that adult fish avoid areas of heavy oil contamination. The situation in Cornwall after the wreck of the “ Torrey Canyon ” is complicated by the use of toxic emulsifiers on doatiiig oil a t sea ; 50-90% of the eggs of pilchard Sardina pilchardus (Walbaum) were dead and young fish were few or absent in plankton samples (Smith, 1968) but adult food-fish caught in the vicinity of oilslicks and spraying operations were numerous and in good condition (Simpson, 1968a). However, Tendron (1968) reported a decrease in numbers of such fish off Ushant. He also observed oily nodules in the gut of ‘(whiting ”, probably Micromesistius poutassou (Risso), which he attributed to their feeding on oil-impregnated detritus. Tainting of

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the flesh, resulting from contact with oil which has had little effect on the fish, is nevertheless damaging to fisheries and has been recorded on many occasions (Surber et al., 1962 ; Reichenbach-Klinke, 1962 ; Zahner, 1962; Mann, 1964; Nitta et al., 1965). Tagatz (1961) tested the toxicity of petroleum products to juvenile shad Alosa sapidissima (Wilson). Gasoline (motor spirit) had the greatest effect while a heavy fuel-oil had the least : TABLEI1 Median tolerance limit (p.p.m.) 24 h 48 h 96 h Gasoline Diesel oil Bunker oil

91 204

-

91 167 2 417

1952

Turnbull et al. (1954) found comparable values of 2 820-2 990 p.p.m. for kerosine, using sunfish Lepomis macrochirus Raf. Chipman and Galtsoff (1949) determined the toxicity of oils adsorbed onto carbonized sand. The survival of embryos of the toadfish Opsanus tau L. ranged from one day in 100p.p.m. to ten days in 5p.p.m., using crude oil; diesel oil was less toxic and lubricating oil had no apparent effect. They refer to Veselov (1948), who found a " marked toxicity " of crude oil at 0.4 p.p.m. and of its aqueous extract at 15 p.p.m. to small carp Carassius carassius (L.). Chemical rather than mechanical effects are, of course, exerted only by water-soluble components and these are of significance to large mobile animals mainly in restricted surroundings such as tide-pools or some fresh-water habitats, where appreciable concentrations can occur. Toxicities reported in the literature are almost all for fresh-water fish. Cole (1941) considers the effects of pollutants in general, discussing variations in toxicity due to the environment or condition of the fish. Fish usually choose an optimum value for normal environmental variables, but they may be indifferent to an unfamiliar harmful substance or even attracted t o it, as Shelford (1917) found for phenol in gas-works wastes. Phenol itself may occur in oil-refinery effluents, It irritates the gills, causing heavy secretion and erosion of the mucous membrane, and also affects the central nervous and endocrine systems (Reichenbach-Klinke, 1962 ; M&licea et al., 1964). Toxicities of 17 p.p.m. for minnows Phoxinus phoxinus (L.) (Schaut, 1939) and 19 p.p.m. for sunfish (Turnbull et al., 1954) seem to be representative for most fish. Mosquito fish Gambusia afJinis

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(Baird & Girard) are particularly resistant with a median toxic limit of 72 p.p.m. (Wallen, unpublished but quoted in McKee, 1956). Naphthenic acids occur in crude oils a t 0.05-2.5y0 generally and exceptionally a t 4.5% (MBlbcea et al., 1964). These authors reported median toxic limits of 29-36 p.p.m. for minnows and 92-118 p.p.m. for bitterling Rhodeus sericeus (Bloch) in 24 h and 48 h tests. Cairns and Scheier (1962) found a value of 5.6-7-2 p.p.m. over 96 h for sunfish and a U.S. Public Health Service guide (1939) reported that naphthenic acids killed minnows in 72 h a t 5 p.p.m. As with phenol, the poisoning effect is irreversible. ‘‘ Naphthenic acids ” are carboxylic acids with one or more alicyclic rings. Russian work report3d by Gutsell (1921) and Galtsoff (1936) identified “ hexahydrobenzoic acid ” (cyclohexane carboxylic acid) as the toxic principle of Baku petroleum. It killed test perch (Perca sp.) and minnows a t 4-16 p.p.m. The lower hydrocarbons themselves have similar high toxicities, perhaps relating to their anaesthetic properties, but their effects a t low concentrations may be reversible (Schaut, 1939). Shelford (1917) exposed sunfish for 1 h and found the following concentrations to be lethal : ethylene, 22-25 p.p.m. ; benzene, 35-37 p.p.m. ; toluene, 61-65 p.p.m. and xylene, 47-48 p.p.m. I n experiments by Hubault (1936), 10 p.p.m. cyclohexane, 10 p.p.m. benzene or 50 p.p.m. methylcyclohexane killed roach (Rutilus sp.) in 3-4 h. Turnbull et al. (1954) also found that 20 p.p.m. benzene was the median toxic limit for sunfish in 24 h and 48 h tests, although in the tests of Toman and StGta (1959), trout (Salnzo gairdneri Richardson) survived for one day in 100 p.p.m. and almost indefinitely in 10 p.p.m. benzene. Mosquito fish were again very resistant in Wallen’s tests, with median toxicities of 386-395 p.p.m. benzene, 4 924 p.p.m. heptane and 15 500 p.p.m. cyclohexane. 4, Molluscs

I n a catastrophic coastal oil spill, molluscs-usually attached to rocks or buried in sand and, a t best, literally sluggish-may suffer heavy mortalities. Diesel oil from the “ Tampico Maru ” wreck in 1957 (North et al., 1964) killed enormous numbers of Pismo clams Tivela stultorum (Mawe) and abalones (Haliotis spp.), with long-lasting ecological consequences (see below, p. 259). I n 1963 a tank-barge was stranded on the NW coast of the United States and its cargo of various fuel-oils was pumped overboard against the protests of the state Department of Fisheries. 300 000 dead razor clams Siliqua patula (Dixon) were carefully counted during the first week of pollution but were only a small fraction of the total mortality. The commercial

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fishery based on them closed after gathering only 9% of the normal catch (Tegelberg, 1964). Commercial shell-fisheries suffered very little during the “ Torrey Canyon ” wreck (Simpson, 1968a) largely because the oil failed to reach the major oyster-layings. Shore molluscs suffered very heavily from emulsifier spraying but survived where the oil was left untreated (Nelson-Smith, 1968b). Most toxicity studies have been on bivalves of commercial importance, particularly oysters (species of Ostrea and Crassostren). At the beginning of adult life, these become permanently fixed to the bottom and are thus subject t o smothering by oil sinking en masse. Almost all bivalves are filter-feeders; droplets of oil carried in the inhalent current may collect within the mantle cavity and, if the oil is emulsified or adsorbed onto silt particles, it may also cling to the gills or pass into the gut (see Spooner, 1968a, b). Gowanloch (1835) and Galtsoff et nl. (1935) investigated oyster beds near Louisiana coastal oil wells and found no evidence that continuous slight oil pollution caused mortality. They felt that it had a definite deleterious effect, but this might have been due to the salinity of the “bleedwater ” from the wells or to a fungus disease which was not detected until 1950 (see Mackin, 1962). Hawkes (1961) reported that quahogs Mercenaria mercenaria L. seem to be “practically immune to oil pollution . . . in Narragansett Bay (Rhode Island) where the bottom is literally paved with oil ”. Oysters subjected to crude oil from a “ wild well ” actually showed a lower mortality than those in clean adjacent waters, perhaps because of its effect on their predators (Mackin and Sparks, 1962). However, Gilet (1959) observed that the previously abundant Chiton polii Marion was not t o be found on quaysides in Marseilles which had become coated with oil around the waterline (although there is evidence that chitons can graze away oil without harm-see below, p. 268). Leenhardt ( I 925) showed that O . l - l . O ~ o fuel-oil has an appreciable effect on oysters (Ostrea edulis L. and Crassostrea angulnta Lam.) and mussels (Mytilus galloprovincialis Lam.) ; 34% killed his specimens in less than a week. I n a variety of experiments (Galtsoff et al., 1935; Chipman and Galtsoff, 1949; Lunz, 1950) the water soluble equivalent of 5-10y0 crude oil slowed down the pumping rate of oysters Crassostrea virginica Gmelin, probably by anaesthesia of the ciliated gill epithelium. Such oysters feed poorly and lose condition. Where mobile molluscs such as shore gastropods become anaesthetized, they are very vulnerable to predators-as was observed during an unusually cold winter by Moyse and Nelson-Smith (1 964)but may be washed away to deeper water, reappearing on the shore later as shown for some gastropods in Fig. 18.

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Field experiments with an " atmospheric residue " of crude oil (approximating to a naturally weathered oil) showed reductions of 2040% in the population of the mobile winkles Littorina obtusata (L.)and L. saxatilis (Olivi). The shells, encrusted with heavy oil, were carried away by wave action on an exposed rocky shore. I n the laboratory, this residue is non-toxic although a 6 h exposure to fresh crude oil, followed by washing in clean water, caused mortalities of 34-44y0 in L. obfusata and L. littorea (Crapp, 1969a). Mironov (1967) found rather lower mortalities from Russian crude oils tested on the gastropods Bittium reticulatum (da Costa), Rissoa euxinica Mil. and Gibbula divaricafa L. ; kerosine was less toxic and a heavy fuel-oil had virtually no effect. Limpets Patella vulgata L. survived for several months in aquaria on rocks covered with weathered oil but died rapidly upon contact with fresh crude in preliminary tests by Nelson-Smith (1968a). They normally close down the shell to exclude noxious liquids, but apparently fail to recognize the danger of the unfamiliar oil. Cockles (Cardium edule L.) in aerated aquaria also quickly succumbed to 0.05% fresh Kuwait crude. Simpson (unpublished, 1961) found that cockles exposed t o toluene or a commercial aromatic solvent for up to 4 h and then washed in clean water suffered 25-30y0 mortalities in the following week. The toxicity of naphthenic acids has not been reported for marine molluscs, but with a pond snail (Physa heterostropha Say), Cairns and Scheier (1962) obtained a 50% mortality in 96 h with concentrations between 6.6 and 15.6 p.p.m. A comparable effect on cockles requires over 500 p.p.m. phenol (Portmann, 1968). Edible molluscs are frequently unsaleable because of oily taints. Quahogs from some beds off Providence, R.I., have become quite inedible (Hawkes, 1961) ; as little as 0.01 p.p.m. oil can give rise t o a marked taste in Crassostrea virginica and, after heavier doses, it may persist for six months (Menzel, 1948). Mackin and Sparks (1962) observed the similar persistence of taint for two months and the Faulkner Report (Ministry of Transport, 1953) refers to Morecambe Bay mussels (Mytilus edulis L.) which retained the oily taste for several months after a spillage there. 5 . Other animals: plankton

Amongst the larger bottom-living animals, the echinoderms are notoriously sensitive to any reduction in water quality, although as the majority live slightly off shore they may escape the effects of floating oil. Oily slurries have been used to form a barrier around oyster beds to protect them from predatory molluscs and sea-stars. During the " Tampico Maru " wreck, powerful surf filled the affected bay with an

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emulsion of diesel oil (North et al., 1964) which eliminated sea-stars of the genus Pisaster for five years and caused sufficient mortalities amongst sea-urchins (Strongylocentrotus spp.) t o alter the entire ecology of the area (see below). Laboratory tests showed that an 0.1% emulsion of the oil inactivates the tube-feet of these urchins. If exposed t o the oil for more than 1 h they do not recover. Even weathered tank sludge reduced the success of artificial fertilizations of sea-urchins Echinus esculentus L. and sea-stars Asterias rubens L. in experiments by Elmhirst (1922) and caused abnormalities in the resulting larvae. North and his co-authors noted that the sea-anemone Anthopleura xanthogrammia (Brandt) was very resistant, surviving high concentrations or direct contact with the oil in tide-pools. They recalled that it was the only animal surviving in sea-water effluent ponds of a large oil refinery farther up the coast. Similarly, the jelly-fish Aurelia aurita (L). is seasonally very abundant in Swansea docks and appears undeterred by floating slicks and oily scum. I n contrast, the hybroid Tubularia crocea (Agassiz) suffered 20% mortality from 0.1% crude oil in tests by Chipman and Galtsoff (1949) and all were killed within 24 h at 5%. Of the annelids known to tolerate polluted conditions, McCauley (1966) recorded the survival of species of the oligochaete Tubifex in oily river-bottom sludges. Reish (1964) utilized the polychaete Capitella capitata (Fabricius) as an indicator of heavy pollution from oil refineries in Los Angeles harbour and Gilet (1959) report,ed it as one of the few animals to occur in large numbers on the bottom of the heavily oilpolluted port of Marseilles. Orton (1925) observed large numbers of Ophryotrocha puerilis Claparitde and Mecznikow burrowing into and feeding around a lump of weathered oil. Lobsters Panulirus interruptus (Randall) and shore crabs Pachygrapsus crassipes Randall were also numerous amongst the " Tampico Maru " casualties, although in chronically oil-polluted waters, the European shore crab Carcinus maenas (L.) survives well (see, e.g., Naylor, 1965) and also has a high resistance t o phenol. Its 48 h median toxicity is 56 p.p.m. according to Portmann (1968). The American freshwater crayfish (Cambarus sp.) is eliminated from irrigation channels by weed-killing treatments with aromatic hydrocarbons at about 300p.p.m. (Shaw and Timmons, 1949). McCauley (1966) observed that amphipods of the genus Gammarus disappeared from an oil-polluted river whereas copepods (Cyclops sp.) survived. Rushton and Jee (1923) also found that Gammarus pulex L. was badly affected, becoming narcotized by fresh fuel-oil but also coated and trapped in weathered residues. Orton (1925) observed that the marine copepod

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Calanus finmarchicus (Gunnerus) was undamaged by engine oil leaking from a wreck and, in aquarium tests by Nelson-Smith (1968a), brown shrimps Crangon crangon L. and prawns Leander serratus Pennant survived 0.1% fresh crude oil (the highest concentration used). For comparison Portmann (1968) determined 48 h median toxic limits of 23.5 p.p.m. phenol for Crangon crangon and 17.5 p.p.m. phenol for

FIG.7. A lump of hardened oil which has been adopted as a float by three of the oceanic goose-barnacles Lepas fascicularis (photo : John Moyse).

pink shrimps Pandalus montaqui Leach. MBlBcea et al. (1964) found phenol toxic in 30-60 h a t 10-65 p.p.m. for the freshwater cladoceran Daphnia magna Straus but did not extend their tests of naphthenic acids to this organism. Barnacles are insensitive to weathered oil, so long as it does not entirely smother them. Amongst goose-barnacles stranded in South Wales, Lepas fascicularis Ellis & Solander has been found using a lump of hardened fuel-oil as its float (Fig. 7). Smith includes a photo-

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graph (1968 ; pl. 19B) of acorn-barnacles Chthamalus stellatus (Poli) covered with crude oil “ mousse ” to the level of the shell-apertures, but apparently healthy, and Crapp (1969a) has treated experimental areas of C . stellatus and Balanus balanoides (L.)with numerous monthly, 6 h, exposures to fresh and weathered crude with no evidence of damage. However, fresh crude a t Santa Barbara (Abbott and Straughan, 1969) and diesel oil from the “ Tampico Maru ” (North et al., 1964) had marked effects on Chthamalus ,fissus Darwin and Balanus glandula Darwin. Chipman and Galtsoff (1949) reported slowing of the cirral beat in B. balanoides, followed by failure t o close and death in three days, from 2% crude oil. Abbott and Straughan (1969) observed that in the areas of heaviest pollution, barnacles were not breeding nor were larvae settling. I n Spooner’s tests (1968a), 100 p.p.m. fresh crude killed 50% of the larvae of Elminius modestus Darwin in less than 1 h. I n the field, marine plankton seems surprisingly little affected by catastrophic pollution. During the “ Torrey Canyon ” spill, slight mortalities were observed amongst phytoplankton organisms netted and cultured, but zooplankton was as abundant and varied as usual (Smith, 1968). Preliminary reports from the Santa Barbara Channel (Smithsonian Institution, 1969b) showed plankton there, too, t o be normal although detailed analyses are still in progress (see Abbott and Straughan, 1969). Belikhov (1963, quoted in the Batelle-Northwest Report, 1967) and McCauley (1966) both found many Protozoa surviving oil pollution in rivers, but believed that the more sensitive species had been eliminated. Minter (1965) reported that the speciesdiversity of freshwater plankton in a series of refinery effluent holdingponds increased as toxicity decreased ; pollutants included phenol a t about 1 p.p.m. The diatoms Ditylum brightwelli (West)Grun.)Coscinodiscus granii Gough and Chaetoceros curvisetus C1. are very sensitive t o kerosine and fuel-oil, which are toxic after 24 h at 100 p.p.m. or less. Melosira moniliformis (0. Mull.) Ag. and Grammatophora marina (Lyngb.) Kutz. tolerate concentrations up to 1% although lower levels suppress the growth of the cultures (Mironov and Lanskaja, 1967). Galtsoff et al. (1935)found that growth of cultures of Nitzschia closterium E. is also retarded, but only at concentrations of oil over 25% ; lower levels have a slight stimulating effect. Elmhirst (1922) kept cultures of marine Protozoa (Oxyrrhis marina Duj. ; species of Amoeba, Diophrys and Bodo) in contact with weathered tank sludge with no ill effects. Any experimenter who has kept suspensions of fresh oil in sea water will soon observe large numbers of ciliates feeding on or around the droplets-see, for example, Spooner (1968a, b). Marsland (1933) investigated the action of a series of paraffins on Amoeba dubia

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(Schaeffer). Larger molecules have a greater anaesthetic effect whe inhaled by mammals, but they are less soluble in water ; C , X I 4 paraffins were narcotic, but above C,, they were iiisufficiently soluble to have an effect. Goldacre (1968) extended these experiments to include cycloparaffins and aromatic hydrocarbons, which in low concentrations have the same effects. With rising concentration, these are increased irritability followed by anaesthesia, swelling of the plasma membrane, contraction of the granular cytoplasm, bursting of the membrane and death. Even after considerable swelling of the membrane, the process is reversible; the action seems to be due t o solubility of the hydrocarbons in the lipid phase of the membrane. 6. Larger plants Unlike all but the simplest animals, a considerable portion of most marine plants can be damaged without necessarily destroying their capacity t o recover. Thus the algae affected by a large oil spill are likely to show less long-term damage, even without the advantageous elimination of grazing animals which usually follows such an incident and will be discussed below. The larger brown algae are covered with a coat of mucilage which is not readily wetted by fresh oils. Topshore forms which have been emersed for long enough to dry out (for example, during neap tides) are more readily oiled, especially Pelvetia canaliculata (L.) Decne. & Thur., which occurs a t the highest intertidal levels. Emulsified oils or " mousses " will cling more readily still and may cause the overweighted plants to be torn off by waves. On Santa Cruz Island in the Santa Barbara Channel, spilt crude oil covering the surface canopy of the kelp Macrocystis pyrifera (L.) Ag. was easily washed of€ by water movement, whereas the heavily oiled smaller alga Hesperophycus harveyanus (Decne.) Setchell & Gardner quickly disappeared from the rocks (California Department of Fish and Game, 196913, c). Macrocystis was more seriously affected in the " Tampico Maru " wreck and toxicity studies carried out with the diesel oil concerned (North et al., 1964) showed that a 0.1% emulsion almost completely inhibited photosynthesis in young blades. The effect appeared in three days, although irreversible damage is caused by exposure to the oil for 6-12 h. A 0.01% emulsion inhibited photosynthesis after a delay of seven days. Fuel-oil was even more toxic. I n another study, Clendenning and North (1960) showed that 10-100 p.p.m. caused 50% inactivation of photosynthesis in four days, compared with 5-10 p.p.m. cresol and 10 p.p.ni. phenol. Crosby et al. (1954) investigated the growths of bacteria, fungi and lower algae in a brackish oil-refinery effluent. They found that 25-50 p.p.m. naphthenic acid, introduced in an attempt to

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control the slime, stimulated its growth by about 15% although “ shock doses ” of 300 p.p.m. phenol killed it. Further data on algae are anecdotal rather than quantitative. Extensive algal damage has been reported, for example, by DiazPiferrer (1962) after the wreck of the “ Argea Prima ”. “ Torrey Canyon ” oil appeared t o cling particularly tenaciously t o the laverweed Porphyra umbilicalis (L.) Xutz. (Rhodophyceae), which subsequently became discoloured, whilst North and his colleagues noted that red algae (especially corallines in rock pools) also suffered a discharge of pigment and are thus perhaps particularly sensitive to oil. Shaw and Timmons (1949) recommended the use of aromatic hydrocarbons (their mixture contained a high proportion of xylene) t o clear irrigation channels. An initial concentration of 300 p.p.m., declining t o 150-250 p.p.m. downstream of the treatment point, completely eliminated submerged freshwater plants although it had little effect on those with aerial leaves. Currier and Peoples (1954) found that 740 p.p.m benzene killed the pondweed Anacharis (Elodea) canadensis Michx. within 1 h, although a saturated solution of the less soluble (and non-aromatic) hexane was not lethal. Mackin (1950a-c) tested the effects of crude oil on salt-marsh plants. Saltgrass Distychlis spicata (L,),glasswort (Salicornia spp.), cordgrass (Spartina sp.) and young mangroves (Rhizophora sp.) were more sensitive than oysters. I n one series of experiments they were damaged by 25 ml oil per square ft of water surface (about 280 ml/m2). Some plants were rapidly killed but there was a complete repopulation later. DiazPiferrer (1962) also found that stranded oil killed mangrove plants. Cowell and Baker (1969) described the effects of pollution of a saltmarsh by fresh crude oil spilt in Milford Haven from the tanker, ‘‘ Chryssi P. Goulandris ”. The grasses Pestuca rubra L., Puccinellia maritima (Hds.) Parl. and Spartina townsendii H. & J. Groves recovered readily; Suaeda maritima (L.) Dun. and Salicornia spp. recovered only slowly, while Triglochin maritima L., Nalimione portujacoides (L.) Aell. and Armeria maritima (Mill.) Willd. a t its seaward end showed no recovery in the first year. Cowell (196gb) studied salt-marshes in Cornwall affected by weathered Oil from the Tomey Canyon ”. Experiments by Baker (1969) confirm his observation that fresh oil is more toxic (i.e. the phytotoxic components are volatile) ; she found that weathered oil has a growth-stimulating effect and discusses unpublished Russian work suggesting that naPhthenic acid might act as a phytohormone. In her greenhouse experiments, a 10% solution ofnaphthenic acid applied a t about 170 ml/m2 Was toxic to P,uccinellia whereas lower concentrations had no obvious effects, 6‘

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either damaging or stimulating. Flowering of several species was inhibited by oiling, probably because it kills the leaves and thus interferes with photoinduction. Subsequent growth stimulation probably results from this inhibition, more nutrients being available for vegetative growth. Chronic pollution, for example by large volumes of effluent containing a low proportion of oil, can eliminate all salt-marsh plants, as would a single catastrophic oiling. Such damage denies their normal feeding-grounds t o birds and other animals (see Harrison and Buck, 1967) and may also seriously accelerate coastal erosion or alter the pattern of silt deposition in an estuary. The maritime vegetation of the cliffs and strand-line, often containing salt-marsh species or their relatives, is equally sensitive t o heavy oil pollution, which it receives most often as droplets carried on windblown spray (see p. 236 above; Ranwell, 1968b). Most lichens are known to be sensitive indicators of air pollution and only a few species can survive in large towns (see, e.g., Fenton, 1964). The phytotoxic action of hydrocarbons has, however, been studied in most detail using terrestrial plants. I n agriculture, they have been used both as weedkillers and as carriers for insecticides. Currier and Peoples (1954) and van Overbeek and Blondeau (1954) review previous work before reporting their own experiments on phytotoxic oils. Minshall and Helson (1949) also discuss earlier studies. Spraying a series of pure hydrocarbons on plants showed that their toxicity increases in the order: straight-chain paraffins, olefins, cycloparaffins, aromatics. Within each series, smaller molecules are more toxic than the larger ones ; octane and decane were toxic when tested by van Overbeek and Blondeau, whereas dodecane and higher paraffins had scarcely any effect. However, C,, olefins showed marked effects and C,, aromatics were quite toxic. According to Currier and Peoples, benzene is narcotic. in low concentrations, depressing some cellular functions ; in high concentrations, low-boiling hydrocarbons in general are cytolytic and cause an irreversible increase in permeability. As the concentration rises, the cell contents leak out, the plant wilts and finally dies. van Overbeek and Blondeau found that low-viscosity oils can penetrate stomata (which aqueous solutions cannot do) and readily spread through the intercellular spaces. They suggested that hydrocarbons become incorporated in the lipoid portion of the plasma membrane, disrupting its structure and thus rendering it permeable. Similar disturbance of the fine structure of chloroplasts would account for the recorded disturbances in photosynthesis following oil pollution and perhaps also for the discharge of pigments which has often been observed. The selective action of herbicidal oils may be due to differences of mem-

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brane structure in some families, e.g. the Umbelliferae, which are very resistant to oils (see also Baker, 1969).

B. Eflects on marine communities A very large number of sea-birds die as a result of oil pollution; chronic pollution probably kills each year as many as die in a single catastrophic spill. Tanis and Morzer Bruijns (1968) calculated that total annual losses due t o oil in the North Sea and North Atlantic amount t o 150-450 thousand birds. Amongst losses quoted for specific areas, Lemmetyinen (1966) estimated an annual 10 000-40 000 (mostly long-tailed duck) in the Baltic, 1952-62; along the Dutch coast, about 11 000 (Tanis and Morzer Bruijns, 1962) and on British coasts, somewhere between 50 000 and 250 000 (Barclay-Smith, 1958, reporting the results of a nationwide survey in 1951-52). Further annual surveys, utilizing many observers, have been organized for British shores since 1966-67 (see Bourne and Devlin, 1969). Estimates can never be more than very approximate, especially where numbers collected over a mile or two of coast are multiplied by several hundreds to give a " total " for a lengthy seaboard (see Tuck, 1959; Gillespie, 1968; Cowell, 1968). Furthermore, it is clear that the corpses stranded on shore represent a fraction of the total mortality a t sea, variously assumed to lie between 5% and 15%; it factor of 10 is probably the most reliable estimate (Tanis and Morzer Bruijns, 1968; Clark, 1968). As examples of mortality following a major tanker spill, the wreck of the " Frank H. Buck " in San Francisco Bay in 1937 killed 10 000 or more birds, of which 6 600 were guillemots (Aldrich, 1938; Moffitt and Orr, 1938); the collision of the " Fort Mercer " and " Pendleton " off Chatham, Mass., in 1952 reduced the wintering population of eiders from 500 000 to 150 000 (Burnett and Snyder, 1954) and the stranding of the " Gerd Maersk " in the Elbe estuary in 1955 affected 250 000-500 000 birds, mainly common scoter (Goethe, 1968). From a humanitarian point of view, each of these mortalities is very regrettable; from that of a zoologist, the significance of the figures depends entirely on the bird species concerned. The gulls (Larus spp.), cormorants (Phalacrocorax spp.), gannets (Sula bassana) and petrels (fulmars Pulmarus glacialis (L.); Manx shearwaters Pufinus pufinus (Briinnich) ; storm-petrels Hydrobates pelagicus (L.) and others, although often oiled, are increasing in numbers. Divers (Gavia spp.) form only a small percentage in lists of oiled birds, but the total world population is small and their reproductive rate is low, so any additional losses may be serious. Populations of sea ducks are already showing a downward trend ; the Baltic is the major wintering-ground for the long-

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tailed duck Clangula hyemalis of NW Europe, but as early as 1960 the number of migrants there was only one-tenth that recorded in 193740 (Bergman, 1961). Eider Somateria mollissima (L.) and shelduck Tadorna tadorna (L.) also congregate over-winter or for moulting in areas subject to pollution incidents (see Bourne, 1968a; Clark, 1968). The auks are, however, probably the most seriously affected. They are long-lived with few natural predators, and have an extremely low reproductive rate. Guillemots, Uria aalge (Pont.), do not breed until they are three years old and then produce one brood per year, usually of only one egg. According to Tuck (1960) and Southern et al. (1965),in several species of this genus only 20% of the eggs laid produce chicks which safely reach the sea and many of these drown or are taken by gulls in their first days on the water. Clark (1968) estimates that if an oil spill halved a guillemot colony, it would take more than half a century for it to recover. Most auk colonies on each side of the North Atlantic are situated in regions particularly subject to oil pollution. Puffins, Fratercula arctica, which numbered 100 000 on Annet (Isles of Scilly) in 1907 have been reduced to 100 in 1967 (Parslow, 1967a, b) and similar declines have been recorded a t other colonies. The process is an accelerating one, since smaller colonies have proportionally less reproductive success and suffer greater losses of eggs and young (Clark, 1968). It is a commonplace that areas subjected t o chronic pollution, whether industrial, domestic or natural (e.g. of sea water by fresh water and silt from a river), usually support a less diverse population than similar unpolluted sites, although the numbers of the few resistant species may be very large. I n this respect, oil is little different from other pollutants (see, for example, Gilet, 1959; Reish, 1964). A catastrophic pollution incident results in a similar selection of resistant species, but the system has no time in which to reach a new balance. The " Tampico Maru" wreck (North et al., 1964) provides a good example of the ecological effects of a serious oil spill. One of the main factors restricting the spread of the giant kelp Macrocystis pyrifera is the grazing of young plants by species of sea-urchins Strongylocentrotus and of abalones Haliotis. Although the kelp itself suffered immediate damage from the diesel oil spilt from the wreck and emulsified by wave-action, juvenile plants began to appear within 2-3 months. North and his colleagues suggested that their settlement was assisted by severe reductions in the population of filter-feeding mussels and scallops, which did not therefore take their customary toll of the swimming kelp spores ; but the major biological factor which made possible the great development of the kelp canopy over the next five

JUL 1958

7w7 OIbf' O C T 1959

FIG.8. Variations in the canopy of the giant kelp Macrocystis pyyifera (solid black) in a cove in Lower California after heavy diesel oil pollution following the wreck of the small tanker " Tampico Maru " in March 1957. The position of the wreck, until she broke up in the winter of 1957, is also shown; redrawn from North ct al., 1964.

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years (Fig. 8) was undoubtedly the virtual elimination of the grazing sea-urchins and abalones. The wrecked tanker did, indeed, provide a breakwater t o protect the initial growth of the young plants, but it broke up and was dispersed during the first winter, after which the Macrocystis climax passed through a t least two growth cycles. No similar catastrophe on the shores of north-west Europe has yet created such an effect on the North Atlantic equivalents of this kelp, but observations have been made on the ecological effects of the " Torrey Canyon " wreck and of several spills in Milford Haven upon the intertidal zone (Bellamy et al., 1967; Nelson-Smith, 1968a, b ; Smith, 1968; Crapp, 1969a, b). These effects cannot be ascribed to oil alone, as in every case solvent-emulsifiers used to clean the shores probably caused more damage than the oil (although their most toxic components are themselves aromatic hydrocarbons-see below, p. 284). On these shores the most obvious seaweeds are three species of FUCUS, Ascophyllum nodosum (L.) le Jol. and Pelvetia canaliculata ; in large pools and a t the lowest tidal levels, other brown algae such as Halidrys siliquosa (L.) Lyngb., Himanthalia elongata (L.) S . F. Gray, Laminaria spp., Xaccorhiza polyschides (Lightf.) Batt. or Alaria esculenta (L.)Grev. may make a significant contribution. Beneath these there is a '' turf '' of many species of smaller brown, red and occasionally green algae. The main grazers on the algae are the limpets Patella vulgata and the less widespread P. depressa (Pennant)or P . aspera (Lam.) (distantly related t o Haliotis spp., the abalones and ormers), winkles of the genus Littorina and topshells (Gibbula spp. and Monodonta lineata (da Costa)). Factors influencing the balance between the seaweeds, their grazers and such competitors for space as the acorn-barnacles and mussels are considered by Southward (1956) and Lewis (1964). On the most heavily polluted and vigorously cleaned shores in Cornwall, which are also exposed t o strong wave-action, all the limpets were killed; within two or three months they became clothed with the green algae Enteromorpha intestinalis (L.) Link., E . compressa (L.) Grev., Ulva lactuca L. and Colpomenia peregrina Sauv., which are normally confined t o sheltered shores and estuaries. During the following year, a vigorous new growth of fucoids appeared t o replace the " green phase ". Young limpets also began to reappear within a year of the incident, but these graze sporelings rather than mature plants. A small cove in Pembrokeshire which showed the same succession of events after a pollution incident in 1962 still had an unusually dense cover of seaweeds three years later. During experiments in the Isle of Man in which limpets were systematically removed, a strip of shore also passed through a " green phase " and produced a dense growth of fucoid algae which persisted for about

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four years. Peculiarities developed in the zonation of Fucus species and in the form of some plants of 3’. vesiculosus L. (Lodge, 1948 ; Southward, 1956). I n Cornwall it was observed that on an exposed shore where F . vesiculosus was previously represented only by its bladderless form linearis Powell (evesiculosus Cotton), the increased weed cover permitted the development of scattered plants of the more usual F . vesiculosus vesiculosus. Such dense algal growth occupies space otherwise available for barnacle settlement, and moving fronds of the weed brush away prospecting larvae. Settlement of Balanus balanoides, a northern form already a t a competitive disadvantzge with Chtham,alus stellatus in south-west Britain, might well be discouraged by a pollution incident occurring a t the time its larvae would be seeking settlement sites. Most available rock surfaces inspected after the wreck of the “ Torrey Canyon ” were occupied only by spat of Chtham,alus, which breeds later in the year. Similar zoogeographical differences affect the survival of the topshell Monodonta lineata which is near its northern limit in Milford Haven and was thus badly affected by the cold winter of 1962-63 (Moyse and Nelson-Smith, 1964). Its recovery was checked early in 1967 and again late in 1968 by serious pollution incidents (Fig. 18, p. 286), although farther south in Cornwall it appears to be more resistant t o oil and emulsifiers than the winkles (Spooner, 1967 ; Smith, 1968).

C. Carcinogenesis Russian work quoted in the Batelle-Northwest report ( 1967) associated papillomatous tumours in Baltic eels with deposits containing fuel-oil, and Russell and Kotin (1956) reported carcinomas and papillomas on the lips of bottom-feeding fish caught near an oil refinery. However, no direct evidence is to be found in the literature that spilt oil can produce malignant growths either in marine animals or those who feed on them, although Goldacre (1968) points out that changes in the cell-membrane brought about by hydrocarbons could lead t o a breakdown in cell-to-cell communication and thus to cancer. Carcinogenesis associated with oily industrial effluents or motor exhausts is usually due to benz(a)pyrene (3, 4-benzpyrene) and related polycyclic hydrocarbons. These have been detected in marine sediments off the coast of north-west France a t concentrations up to 1.76 p.p.m. by Perdriau (1964) and Mallet and Priou (1967), and in the Mediterranean up to an exceptional value of over 3 p.p.m. (Bourcart and Mallet, 1965). The maximum concentration found in edible molluscs by Mallet and Priou was one hundred times less than this, although they found 0.16 p.p.m. in the viscera of a food-fish. Shimkin et al. (1951) detected 0.05-

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0.20 p p m . benz(a)pyrene in barnacles on the coast of California ; an extract injected into mice produced subcutaneous sarcomas. Plankton contained up to 0.40 p.p.m. off French coasts but only 0.006 p.p.m. off Greenland (Mallet and Sardou, 1964), suggesting that benz(a)pyrene is created during industrial activities, and it is known that to obtain it experimentally from naturally-occurring hydrocarbons they must be heated to over 400°C. However, Shabad (1967) reported Russian work on the accumulation of polycyclic carcinogens by micro-organisms and Mallet et al. ( 1 967) have demonstrated that they can be synthesized by marine bacteria from the lipids of plankton. Thus, although the major source of carcinogenic hydrocarbons in the marine environment is the relatively small amount of heated waste oils reaching the sea from industry and shipping, it is a t least possible that marine micro-organisms could manufacture them from the crude or other oils which are or&sionally spilt in much larger quantities.

D. Rehabilitation of oiled birds Most people show an understandable desire to help birds which come ashore oiled, although from a coldly scientific point of view this assistance is not necessary to maintain the numbers of such species as the herring gull Larus argentatus Pont. or greater black-backed gull L. marinus L. On the other hand (as shown above) a vigorous conservation policy which includes the rehabilitation of oiled specimens will soon become the only way to protect many auks, a t least of the North Atlantic region, from complete extinction. Existing methods of rehabilitation have little success. Of 5 71 1 oiled birds (mostly guillemots Uria aalge) collected during the “ Torrey Canyon ” incident, about 150 were returned to the sea and 25-30% of these are known to have died within a month of release (Conder, in discussion following Clark’s 1968 paper ; Clark, 1969). This suggests that a great deal of trouble and resources were, in effect, being devoted to prolonging the suffering of over ninetenths of the stranded birds. Most ornithologists advise that quick humane killing is at present the best treatment. Beer (1968a, b) gave an account of the methods used on oiled auks after the “ Torrey Canyon ” wreck; Clark (1968) and Clark and Kennedy (1968) reviewed the wider problems of rehabilitation and conservation. Because these birds rarely come ashore until very badly affected, stranded auks will be starving, chilled, exhausted and with secondary complications in addition t o oiling even before they can be collected. They must be prevented from preening or overcrowding each other and kept as warm and clean as possible before treatment.

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Most cleansing processes remove natural as well as polluting oils and do further damage to the plumage, so the birds have to be kept a t least until they are again naturally oily and usually until they have moulted (a new but relatively untried treatment coats the plumage with wax as it removes the contaminating oil). Auks are very difficult to keep in captivity even when healthy. They eat only fresh fish (preferably taking it from the water themselves), require sea water and are very subject to fungal infections or other diseases and deficiencies. When the survivors are finally released they are often too tame to resume independent life. It seems possible that they never resume breeding, so they do not contribute to the recovery of the colony. Nevertheless, breeding (as yet unsuccessful) has been reported in a pair of captive guillemots (Marsault, 1969) and it seems possible that jackass penguins Spheniscus demersus (Linn.) can be rehabilitated successfully in South Africa (Westphal, 1969). Bourne (196th) and Clark (1968, 1969) suggest that more research ought to be devoted to the improvement of failing auk colonies, for example by providing artificial ledges from which eggs would not be lost, or to methods of scaring birds from known slicks. Some form of acoustic buoy, drifting with the slick, would also assist in tracking the oil or relocating it if lost.

E. Public amenity and the tourist industry Sea shores and coastal waters are used by commercial or amateur fishermen and sailors as well as other sportsmen, naturalists, and holidaymakers in general. I n harbours and enclosed waters, fresh oil is a direct danger when it constitutes a fire risk. It is also a hazard to coastal power stations, which usually draw sea water for cooling from docks or estuaries. Oil in the water may cause an explosion in the condensers and after a serious spill they have t o be shut down (as a t Hayle, Cornwall, in 1967). It is now generally accepted that floating oil has little direct effect on commercial fisheries (see, for example, Simpson, 1968), although sunken oil may smother or taint shellfish and foul nets or other gear. Indirect effects on the planktonic young stages and on organisms providing food or shelter can be guessed at from the data assembled above. Korringa (1968) has called attention to an additional indirect effect. After the much-publicized " Torrey Canyon " spill, fish sales in Paris dropped dramatically regardless of the origin of the fish. Amateur fishermen are more likely to experience direct effects, as they operate close in shore if not from the beach itself, seeking coastal fish with bait taken from the shore. Marine pursuits of all kinds have become increasingly popular and

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costly along the coasts of industrially affluent nations. The paintwork of a speedboat or sails of a yacht are easily spoiled by oil ; the oil is equally easily transferred t o boat-trailers, towing vehicles, caravans and clothing. I n Milford Haven and elsewhere, yachtsmen in need of a repaint have been observed to sail deliberately into a slick of known origin, when they could be certain of compensation, but these are few compared with the numbers who are forced to spend time and money on cleaning and touching-up operations. Underwater swimming, surfing and water-skiing are further sports of increasing popularity which require expensive equipment-for example, neoprene-foam " wet suits " which can be ruined by contact with oil. On almost any shore in western Europe, stranded oil is to be found in rock crevices, in lumps along high-water mark or in patches beneath the sand. Even if the swimmer, sunbather or walker avoids all obvious traces of its presence, the warmth of his body as he sits on an apparently clean area is likely to melt a hardened deposit, causing it to smear his skin or stain his clothes. Many resorts in the south of England now operate " detergent stations ') in addition to first-aid huts and lifeguards, where the worst of the oil may be removed. Nevertheless, oil is carried or trodden into hotels, boarding-houses, caravans, cafhs and places of entertainment, ruining their carpets and upholstery. The total cost of cleaning, repainting or repair to the individuals affected, together with the cost to the public of beach cleaning and other services, cannot be determined but must be large. The loss of seasonal income from holidaymakers is potentially even greater. Many countries today depend heavily on tourism (see Ricci, 1968) and it is economically the fourth most important of British industries, earning as much as the total of machinery exports. Cornwall alone has more than two million visitors per year, spending between them nearly E40 million (Croft, 1959, and in discussion after Ricci's paper ; Cowa.n, 1968). The adverse effect of a widely publicized disaster like the " Torrey Canyon )' wreck can be countered by reassurances from government ministers and agencies (which were not entirely founded on fact). After a slow start, the Cornish holiday season in 1967 was a profitable one (Grieve, in discussion after Ricci, 1968). Holiday areas can, however, acquire a reputation for chronic pollution which increasingly keeps visitors away, though they usually prefer not to admit to such a reputation, even in the form of a denial. In any final analysis, to these economic considerations must be added the sheer unpleasantness and frustration of finding the enjoyment of carefully chosen surroundings in hard-won leisure time marred by defiling and unnecessary jetsam of the industrial society from which most users of the sea-shore are seeking temporary escape.

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V. REMOVALOF SPILTOIL A. Bacterial degradation and other biological processes Orton recognized in 1925 that bacteria play an important part in removing oil from the sea. Although Adam (1936) later ignored biodegradation in his otherwise full discussion of the dispersal of oil a t sea, Pilpel (1968) concluded from the work of Dzyuban ( I 958) and others that bacterial oxidation could proceed as much as ten times as fast as auto-oxidation. There is no doubt that bacteria can utilize a variety of hydrocarbons under field conditions. Their activities in industrial cutting and fuel-oils are frequently troublesome (see Birkholz et al., 1961-62). Ludzack et al. (1957) observed that the amount of oil in a stretch of river receiving a refinery effluent diminished by 40-80y0 below the discharge point, according to the season, and in laboratory experiments a t summer temperatures 50-80y0 of the oil in their water samples underwent biological degradation within a week. ZoBell and Prokop (1966) found that, although oil was continually polluting bays and creeks on the Louisiana coast, its concentration in bottom deposits was generally low (see above), reaching 1% only in localized areas of recent pollution and persisting there only for a few weeks. Oil-oxidizing bacteria were detected in 94% of their mud samples. Prokop (1950) concluded that the presence of acclimated cultures was essential to the degradation of crude oil and McKee (1956) gave values for the biochemical oxygen demand of various organic compounds in cultures seeded with sewage organisms in which pure hydrocarbons gave low figures (no BOD from toluene, xylene or benzene over five days ; 1-20 g BOD/g benzene over ten days ; 0.53 g from kerosine and 0.078 g from gasoline over five days), although those containing oxygen or nitrogen had much higher demands. ZoBell ( 1 964) obtained higher figures (1.4-4.0 mg oxygen/mg sample) using mixed cultures of hydrocarbon oxidizers. I n a 35-day test a t 25"C, the samples were 4785% oxidized. Comparable BOD values for other substances are 1.07 (glucose), 1.18 (starch, cellulose), 1.5-1.8 (protein), 2.5-2.9 (vegetable and animal oils). However, Stone et ab. (1942) used ordinary soil " seeds " on a selection of light oils, crudes and residues to obtain after a few days cultures capable of attacking all the samples they tested. The American Petroleum Institute's manual on biological treatment for oil refinery wastes (McKinney, 1963) says, of recommended sources, " The engineer need only look under his feet to find suitable organisms." ZoBell (1946) and Voroshilova and Dianova (1950) have shown that over 100 organisms can decompose pure hydrocarbons. Pseudomonas is thc outstanding type for crudes and is represented by several marine

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species (Stone et al., 1942 ; ZoBell, 1964). There is thus little necessity t o " seed " a coastal spill with cultures of specially selected organisms, nor is there any case for supposing that marine bacteria will show a lack of enthusiasm for polluting oil, as available carbon is scarce in the sea (usually less than 2 mg per litre-see Berridge et al., 1968a, and subsequent comments by Gunkel). Experiments by Gunkel (1967) showed that, under suitable conditions, normal marine bacteria decomposed nearly 60% of added fuel-oil in 8 weeks. Light oils are oxidized more rapidly than heavier ones and paraffinic (aliphatic) hydrocarbons more rapidly than aromatics, according to Stone and his colleagues. However, Ludzack and Ettinger (1959) observed that aromatic hydrocarbons disappear from polluted streams more rapidly than aliphatics. This conflict is considered in a review by ZoBell (1950) as being due mainly to differences in the environment and the types of microorganisms originally present there. Gunkel (1968 and in Smith, 1968) sampled oiled beaches in Cornwall after the " Torrey Canyon " disaster and found very high numbers of oil decomposers, especially in well-aerated situations. The greatest density (over 400 million organisms per ml of wet sediment) was higher than any he had recorded in previous oil spills and approached the maximum which could be obtained with pure cultures on artificial media in the laboratory. The average numbers of oil decomposers a t his Cornish stations varied from one-half to three times the total numbers of other aerobes. Even where there was no oil, he obtained 50 000 oil decomposers per ml. Earlier, ZoBell (1964) had calculated that after two days' presence of oil in sea water, the population of bacteria capable of degrading it might reach 8 million per ml. This population would oxidize about 1 mg oil per litre per day a t 25"C, 0.3 mg at 15OC and less than 0.1 mg a t 5 O C . Nitrogen and phosphorus might be limiting in the water but would probably be adequate in shore sediments. Oxygen is also potentially limiting, but degradation takes place only at the surface of the oil. The formation of " mousse "-like emulsions may aid the process by increasing the oil-water interface (see Berridge et al., 1968b and subsequent discussion, also Gunkel discussing Ramsdale and Wilkinson, 1968). Smith (1968) reported the occurrence of grey sulphide layers, unusual in Cornish sands, after the " Torrey Canyon " spill, taking them to be evidence of considerable decomposition of the oil (as might be expected by scaling ZoBell's figures up t o Gunkel's population counts). Anaerobic degradation was occurring a t a much slower rate; this process also depends on the availability of nitrates, phosphates or sulphates which here provide a source of oxygen. For example, complete oxidation of 1 mg of a typical mineral oil

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under anaerobic conditions requires about 4 mg nitrate ; sea water may contain as little as 0.1 mg per litre and rarely has more than 2 mg (Pilpel, 1968). Izyurova (1952) has achieved four- to ten-fold increases in the rate of anaerobic degradation by the addition of nitrate. Crosby et al. (1954) reported the periodical abundance of sulphur bacteria in a refinery effluent holding-pond and ZoBell and Prokop (1966) concluded that bacteria of the genus Desulfovibrio or Desu&muculum can definitely degrade mineral oil under anaerobic conditions. Davies and Hughes (1968) disagree, but only over the precise definition of anaerobiosis. These authors reviewed the basic pathways of crude oil degradation. Treccani (1965) gives a concise account of the bacterial metabolism of individual pure hydrocarbons, on which there is a large and specialized literature. The final products of aerobic oxidation are carbon dioxide and water. Many of the intermediate products are water-soluble and almost all are readily susceptible to further attack by micro-organisms commonly present in coastal waters (Brown et al., 1951).

Intermediate products of degradation, as well as the bacteria themselves, provide support for many higher micro-organisms. Protozoa, fungi and lower algae contribute to the slime in a brackish refinery effluent described by Crosby et al. (1954). Spooner (1968a, b) reported many ciliates amongst oil droplets, some with oil in food-vacuoles, and Voroshilova and Dianova (1950) refer t o an increase in the numbers of protozoans following that of oil-degrading bacteria in polluted waters. Orton (1925) observed numbers of the small polychaete Ophryotrochu burrowing into weathered oil, he assumed t o feed on bacteria. Larger animals can contribute directly to the removal of oil, although probably not actually digesting it. George (1961) reported that limpets Putella. were capable of scraping weathered oil from the rocks in the normal process of browsing. Oil appeared in the faeces, mixed with rock fragments and plant debris, while the limpets apparently remained unharmed. Some months after a fairly severe spill, he found the shore cleared of oil except for a band deposited above the highest level which limpets could reach. On the worst-affected shores in Cornwall after the " Torrey Canyon " wreck, all limpets were killed by emulsifier spraying (see below), but it was seen that Patella and the topshell Xonodonta had been grazing oil from the few unsprayed reefs (Holme, 1967 ; Spooner, 1967; Smith, 1968) and in Brittany (Fig. 9). Spooner and Spooner (1968) observed that chitons-which occupy a similar ecological niche to limpets but are there nearly twice as large-removed from coral rock in the Bahamas much of the fuel-oil spilt from the stranded " General Colocotronis " (Figs. 10, 11).

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Aljakrinskaya (1966) showed that the filtering activities of mussels Mytilus from the Black Sea were not slowed by crude oil in suspensions up to 1%. The oil was accumulated in mucous strings and discharged as pseudofaeces. Spooner (1968a, b) found that 0.4% suspensions of

FIG. 9. Tracks made by the radula of & limpet (Patella vuZga,ta)in grazing oil from rocks at St. Jean du Doigt (FinistBre); an idea of scale is given by the acorn-barnacles at the edge (photo : N. A. Holme).

weathered Kuwait crude and of bunker C oil wer2 filtemd by mussels, which rejected some of the oil as pseudofaeces but ingested a proportion. The oil tended t o " pond " in the gut but was eventually expelled in true faeces. It seems unlikely that such globules could be digested by the mollusc, but the incorporation of oil into faeces apparently made it more readily available t o micro-organisms.

Fro. 10. A chiton (A4canthopleurayranulafa Gmelin) in the area of coral rock which it has rleared of oil, following the stranding of tho " General Colocot,ronis " off Eleuthera (Bahamas). The anim.al is abont 2 inches (5 rm) long (photo : C. M. Spooner).

FIG.11. The chiton, removed to a dish. with faeces (right) which clparly contain 011 (photo : Marine Riological Association. Plymouth).

TIIE PROBLEM OH’ OIL POLLUTION OF THE SEA

27 1

B. Dispersal, sinking and recovery at sea

It is always preferable to deal with spilt oil on the water, before it reaches the shore. I n reasonable weather conditions it is usually easy to transport and apply dispersing or sinking agents by ship. When these are toxic, their rapid dilution and the relative scarcity of plants and animals in the open sea makes for far less biological damage than their application directly onto the densely-populated intertidal zone. I n treating oil spillages in European waters, the method most used so far has been to spray with solvent-emulsifiers. The more effective of these, such as B P 1002, Gamlen, Fina-Unisol or Essolvene, contain 8-30% non-ionic surfactant and 60-80% hydrocarbon solvent (usually of high aromatic content) with additional emulsifiers and stabilizers (some formulations are given by Smith, 1968). They are designed to be laid on the oil in a fine but powerful spray without dilution. Under laboratory conditions as little as 10% of the oil volume produces a stable milky emulsion after shaking, although in the field any quantity from 25% to twice the oil volume may be needed. The mixture must tht JI be agitated vigorously t o disperse it as an oil-in-water emulsion. This can be accomplished by making a faster return journey through the slick (or using a following vessel) to break it up by propeller action, or with high-pressure water hoses. Some surfactant mixtures are effective without the addition of hydrocarbon solvents and can be applied in polar liquids (water or alcohols). Examples of these are the American Corexit (see Moore, 1968) and Polycomplex-A (Spooner, 196th) or the British Dispersol 0s. Crop-spraying aircraft might appear to be suitable for applying dispersants, but the payload is very small if they have to fly over any distance (Wardley Smith, 1968b). A Canadian aircraft used for fighting forest fires carries a payload of ten tons of water and could be modified to deliver dispersants. The mixture could not be agitated from fixed-wing aircraft, although Moore suggested that the rotor-wash from a helicopter might be adequate. Oil can be sunk by the addition of any fine, dense material-for example, dry sand-as often happens naturally ; unfortunately, it then coagulates on the bottom into large globules which rise at the slightest disturbance. Because of this, and due to fears that sunken oil might smother shellfish beds, interfere with fish feeding or breeding grounds and foul nets or pots, British official policy seemed until very recently to be opposed to sinking oil. I n America, Carbosand (sand coated with heavy oil and then heated sufficiently to char the coatingsee Hofmann, 1949) has been in use for some years, but it is not an effective oil-binder (Schneider and Beduhn, 1967) and is rather toxic

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(Chipman and Galtsoff, 1949). During the “ Torrey Canyon ” affair the French used “ craie de Champagne ”, which is ground calcium carbonate treated with about 1yo sodium stearate, apparently with some success (Bone and Holme, 1968 ; Smith, 1968). Stearated whiting has been advocated in Britain. Various absorbent waste materials such as crushed cinders, brick-dust or pulverized fuel-ash can be rendered hydrophobic but oleophilic by treatment with chloro-silane vapour a t about 0.2% by weight (Anon., 1967a; Wardley Smith, 196813, c). Wardley Smith also refers to a gypsum residue called “ Stucco ” which is a by-product of the manufacture of phosphoric acid. It sets hard in sea water and should thus bind the oil in a firm mass on the bottom. Early attempts a t applying these materials were made by spreading the dry powder over the oil slick in about a 1 : 1 ratio. After a pause, the mixture was sunk by agitation with propellers or water-jets. This is successful in harbours, for which most products were originally intended. The French, operating in Channel and Biscay waters, had t o withdraw naval vessels because chalk-dust carried by the wind was ruining military equipment (Wyllie and Taylor, 1967). It has been proposed more recently that hydrophobic sinking agents could be applied as a slurry in water (see, for example, Holdsworth, 1968). Another technical objection is that the nearest port a t which a sufficient quantity of the material could be loaded might be quite distant from the slick. Stocks of the agent of choice might similarly be stored a t a distance from that port. The costs of transport, as well as of raw materials and storage, could be minimized by a further suggestion from Holdsworth that provision should be made for fitting suction-dredgers with spray-booms. I n dealing with an off-shore spill, such a dredger could be loaded with sand from the nearest shoal and her cargo could be treated with a water-repellent agent while still wet in the hoppers and then distributed through the spray-booms as a slurry while she steamed through the floating oil. Oil adsorbed onto inert particles is in a state favourable to bacterial degradation and a sinking agent could even be seeded with the nutrients likely t o be limiting on the sea-bottom, or with oil-degrading bacteria themselves (Anon., 1967a; Davies and Hughes, 1968). The fine droplets produced by dispersants may also be favourable to biodegradation, but many emulsifiers are toxic t o oil-degrading organisms as well as t o plankton in general. As neither sinking nor dispersing actually destroys oil, methods which permit its collection and disposal seem attractive. Natural materials such as straw (McKay, 1967 ; Roberts, 1967), pine-bark (Anon., 196810) or maritime vegetation (gorse and dune grasses) have been used in emergencies by drawing them across the

THE PROBLEM OF OIL POLLUTION

OF THE SEA

273

slick in some form of net. Straw, for example, can remove up to thirty times its own weight of oil and is readily burnt afterwards. Siliconized sawdust or peat, india-rubber dust (Saugolit), expanded mica or vermiculite and volcanic glass (Ekoperl) have been used in Europe and are relatively inert (Sturz and Klein, 1964; Mann, 1966). They are also light and finely divided, presenting problems in spreading and recovery in open-sea conditions. Although it has the same limitations,

FIG.12. A patch of oily emulsion from the ‘‘ Torrey Canyon ” lies on the bottom of a shallow sandy pool in Watergate Bay. Although some globules are rising to the surface, waves have already begun to cover the patch with sand (photo: A. Nelson-Smith).

an ingenious scheme for oil recovery minimizes problems of space and storage by utilizing shredded polyurethane foam. This can be manufactured in a small boat by the reaction of two liquids. I n about 1 min, the mixture undergoes a hundred-fold expansion. 50 cu ft (28 litres) of foam, when shredded into approximately 1 in (2 cm) cubes and spread on the slick, absorb up t o one ton of oil but remain afloat. Collected in a fine drag-net, 80% of the oil can be squeezed out between rollers after which the foam is used again (Anon., 196713; Mayo, 1968). Solidification is another technique permitting the recovery of oil

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spilt in calm conditions. Castellanos (1968) advocated the use of paraffin waxes or waste wax residues, sprayed a t a temperature of 70°C. The addition of 15-20% wax will solidify crudes, although as much as 50-60% is needed for thinner oils. Similarly, spraying the slick with polyvinyl plastic in a volatile solvent covers the oil with a web of fine fibres; the necessary 15% ratio of plastic to oil is expensive, but the cost can be reduced by incorporating cheaper material such as waste textile fibre into the oil befors spraying it (Department of Scientific and Industrial Research, 1963b). During experimental use of this “ plastic moss ” in France, much of the spray blew away. Agglomeration was very efficient but difficulty was experienced in collecting the resultant raft (Rocquement, 1968). Such methods seem better suited to use on inland or drinking waters than a t sea. Mechanical collection a t sea has been discussed in an earlier section (p. 227), but it should be mentioned that the French collected an appreciable amount of “ Torrey Canyon ” ‘‘ mousse ” by aligning a coastal tanker (the ‘‘ Petrobourg ”) at the downwind end of a V-boom. The emulsion accumulated in a layer about 2 f t (60 cm) thick along the ship’s side and was pumped aboard from a floating weir device (Holdsworth, 1968, and Spooner in the following discussion). A similar method of collection was tried in the Santa Barbara Channel early in 1969.

C. Problem8 in cleansing shores One of the main lessons of the “ Torrey Canyon ” disaster is the value of advance planning. Although British government laboratories had been investigating methods of dealing with coastal oil spills for years before this (Department of Scientific and Industrial Research, 1961, 1963a; Zuckerman, 1968) the necessity of cleaning so much oil from so many miles of coast had never previously arisen. I n retrospect, it can be seen that some inaccessible coves need never have been treated. On most shores, far less of the solvent-emulsifiers could have been used and on others, mechanical methods would have been more effective. Since that event, local authorities throughout, Britain have been instructed t o prepare oil-pollution plans (Beaumont, 1968 ; Ministry of Housing and Local Government, 1968). That other governments have need of similar contingency plans is revealed, for example, by statements of U.S. Senator Muskie (1968) on the “ Ocean Eagle ” spill in Puerto Rico. Rocquement (1968) has referred to the French “ Plan Offset ”. British coastal laboratories and marine stations have been selected to act as emergency scientific or technical bases and maps have been drawn up defining those sections of coast which are of special value t o biologists, fishermen or holidaymakers (Natural

THE PROBLEM O F OIL POLLUTIOS OF THE SEA

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Environment Research Council, 1969). An analysis of this sort was made before deciding how t o deal with a small spill of bunker oil near Plymouth (Holme and Spooner, 1968) which polluted a popular swimming beach, rocks which are visited by fair numbers of people and an extensive reef which is little used and supports a rich fauna and flora. It was decided t o leave the latter area untreated, although there is still much controversy about the fate of such pollution. Those in charge of clearance operations are understandably concerned about the possibility of untreated oil floating off to re-pollute amenity beaches (see, e.g., Dudley, 1969). Observations on areas polluted but left untreated are not very informative; the deposits of oil removed by grazing molluscs i n Milford Haven (George, 1961) and at Marazion, Cornwall (Smith, 1968),were fairly light. At Eleuthera in the Bahamas (Spooner and Spooner, 1968) i t had soaked into the porous coral rock, while in Lower California (North et al., 1964) the polluted cove is so isolated that the ultimate fate of the oil went unreported. " Torrey Canyon ') pollution was heavy enough to cause raasonable apprehension about re-pollution. On some untreated beaches in Brittany, oil deposits were still visible a year or more later (Zuckerman, 1968) and much of the oil from others was later carried to beaches previously cleaned. However, according to some French authorities, " mousse "-type emulsions float off a polluted beach more readily than crude oil which has not been emulsified. Where removal of the oil is necessary, a working guide has been provided by the Ministry of Technology (Wardley Smith, 1968a). Additional comments on the methods available have been made by Beynon (1968) and Mayo (1968). Wherever good access permits, mechanical collection is the method of first choice, using bulldozers, scrapers, powered or manual shovels and rakes for solidified material. Liquid oil in large quantities can be collected into pits or troughs and carted by gully-emptiers or sewage tankers. There are often backshore regions where trenches can be dug t o receive this material, but the possibility of contaminating water supplies should always be borne in mind. Much of it could be burned in incinerators supplied with a compressed-air draught. Many of the absorbents used a t sea can also be spread on a polluted beach, gathering the oily straw and other fibrous materials for burning but leaving deposits dusted with stearated rockdust or siliconized ash to erode naturally or hosing them into the sea. Thick deposits of fresh oil can be burned in situ, using flamethrowers or igniting either with " oxygen tiles ') or magnesium flares, but it is a slow process and may require the addition of extra fuel or oxidizing agents. Water-in-oil emulsions or oil floating on rock pools

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will not burn readily. Portable oxy-propane burners will clean seawalls and breakwaters, but only by causing the stone or concrete surface t o flake. Steam-cleaning was attempted on some rocky shores in Brittany (Holme, 1 9 6 7 ; Smith, 1968). The softened oil was carried away with water-jets, using a small quantity of surfactant or emulsifier. This is also slow and requires reasonable access for the portable boilers.

FIG.13. ‘‘ Ploughing ” oily sand a t Sennen Cove with bulldozers. “ Strata ” of oil are exposed in the foreground. As the tide rises, emulsifier will be sprayed onto the disturbed area (photo : A. Nelson-Smith).

Where it has been decided to accept the adverse biological consequences, solvent-emulsifiers are very effective in cleaning rocks. Ideally, the emulsifier mixture should be adjusted to suit the type of pollution. Thin fresh oil can readily be emulsified by the sparing use of one of the less toxic aliphatic solvents, whereas thick hardened deposits may require several applications of a highly aromatic solvent. I n each case, proper application involves the use of a fine high-pressure jet t o ensure thorough mixing, followed by vigorous washing with water (either by hosing or the incoming tide) within half an hour. Greater delay or inadequate agitation results in the separation of a thin toxic

277

T H E PROBLEM OB OIL POLLUTION O F T H E SEA

oil which will probably pollute an adjacent area (Figs. 14 and 15). Even under the best of circumstances, the operation can result in a whitish plume of concentrated emulsion (Fig. 16) which may penetrate t o a depth of 8-9 fm (17-18 m) and drift along the shoreline for several krn, affecting communities which had not experienced direct pollution

FIG.14. A coralline pool near Porthleven, Cornwall. The encrusting species of Lithothamnion and the tufts of Corallina officinalis have been bleached by the action of emulsifier, which also killed all the limpets; a dozen or more of their " homes " are visible as dark, roughly oval patches (photo : A. Nelson-Smith).

(Drew et al., 1967 ; Potts et al., 1967 ; Smith, 1968). Solvent-emulsifiers of the standard type are intended to be applied undiluted, although unsuccessful attempts to apply them in a water-jet through a foam eductor have been reported by Wardley Smith (I968b) and Crapp (1969a). Dispersants which can be applied in this way are ineffective in cleaning beaches (Moore, 1968). The fire-fighting services which normally provide the pumps used in hosing off the emulsion prefer to A.M.R.-S

10

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A. NELSON-SMITH

FIG.15. A rock-pool a t Sennen Cove during cleansing operations ; note the algae (delicate red and brown) emerging from the milky emulsion. The tide did not flush this pool for several hours, during which time all its inhabitants were exposed to toxic concentrations of emulsifier. I n the absence of agitation, the emulsion has begun to break up, producing a thin black oil (background) which could float off to pollute other pools (photo : A. Nelson-Smith).

use fresh water in their equipment, thus imposing an additional stress on the shore fauna and flora. Sandy beaches present special problems which have already been touched on (p. 239). Oil usually remains on the surface and is frequently concentrated towards the head of the beach by successive tides, when its mechanical removal is fairly simple, but heavy oil, " mousse ", or

FIG.16. The tide, rising over an emulsifier-cleansed shore on the north coast of Cornwall near St. Ives, carries away a plume of emulsion and a thick crust of partly-separated oil (photo : A. Nelson-Smith).

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partly sedimented oil are all liable to burial by wave-action. Spraying with emulsifier also tends to cause the oil t o penetrate deeper and may create a quicksand. British practice is to spray emulsifier while ploughing or " rotavating " the sand, preferably only just ahead of the rising tide (Fig. 13), or to bulldoze the treated sand into the sea. I n Brittany, the French used the " German Machine " (Wyllie and Taylor, 1967 ; Wyllie, discussing Mayo, 1968) in which oily sand is roasted at a high temperature. The product, although dark grey in colour, is clean and does not stain. If there is advance warning of an approaching slick, it is possible to bulldoze a stockpile of surface sand to the head of the beach, providing clean material with which to cover any slight deposits remaining after treatment. Absorbents might also be spread in advance. Shingle and cobbles are more likely to trap oil and are less easy to '' cultivate ". The best that can be done is probably to spray emulsifier as vigorously as possible, just in advance of the tide. It will probably be necessary to apply many treatments. Sait-marshes are unlikely to be much used by the public, but as they are frequented by many birds the worst of the oil should be removed ; it is often sufficient t o cut and burn the emergent parts of reeds and grasses.

D. Mode of action and toxicity of solvent-emulsij2ers A certain amount of confusion has arisen from misuse of the term '' detergent ". Silsby (1968) pointed out that although this word applies to any agent which aids in cleaning, it has become restricted in popular usage to synthetic household washing agents, excluding soap. It is therefore particularly unfortunate that solvent-emulsifiers, so unlike domestic washing-up liquid, were referred to as " detergents " by the press and in some scientific reports during the " Torrey Canyon )' affair. Synthetic household detergents came into widespread use after the Second World War and numerous investigations were made of their effects and toxicity, mostly upon fish and almost all in fresh water. Reports of these studies have been reviewed by Matulovh (1964), Prat and Giraud (1964) and Marchetti (1965a) and many are listed in a recent bibliography (Nelson-Smith, 196%). The surfactants which form the major part of these detergents are anionic (for example, alkyl or aryl sulphonates) and many are now " soft ", i.e. more or less biodegradable. Those used in solvent-emulsifiers are non-ionic (for example, alkyl phenol-ethylene oxide condensates) and are mostly " hard ') or not readily degraded, According to Jones (1964) and Marchetti, non-ionics are slightly less toxic than anionics, for which toxicities to a variety of fish species fall within the range 1-100 p.p.m. The

THE PROBLEM OF OIL POLLUTION OF THE SEA

281

constitution of the surfactant molecule is important ; the lethal concentration of a nonyl-phenol polyoxyethylene condensate to goldfish Carassius auratus (L.) after 6 h exposure ranges from 5 p.p.m. t o 2 500 p.p.m. according to the ratio of ethylene oxide to nonyl phenol units (Marchetti, 1964, 1965a). Sublethal effects observed from anionic surfactants a t 0.5-10 p.p.m. include erosion of gill epithelia and destruction of mucous cells (Schmid and Mann, 1961; Scheier and Cairns, 1966) or damage to the chemical senses (Bardach et al., 1965). These result in loss of equilibrium, convulsions and respiratory difficulties (Maldura, 1961) or an inability t o detect food (Foster et al., 1966). Mann and Schmid (1961) found that a t 5-10 p.p.m., anionic surfactants immobilize the sperm of trout Salmo trutta, reduce the fertilization rate and kill fertile eggs. According to Marchetti (1965b), the fry of rainbow trout S. gairdneri are most resistant t o nonyl-phenol polyoxyethylenes when newly hatched (42 p.p.m. is toxic in a 6 h exposure). Their maximum sensitivity (to 2 p.p.m.) is reached as the yolk-sac is exhausted, but is slightly reduced in older (fingerling) stages to just over 5 p.p.m. The larvae of marine clams Mercenaria mercenaria and oysters Crassostrea virginica are more sensitive than adults, showing developmental defects a t 0.14-3.0 p.p.m. of anionic and 1-0-5.0 p.p.m. of nonionic surfactants (Hidu, 1965). Matulov8 (1964, 1966) has tested a variety of surfactants on species of the micro-algae Chlamydomonas, Scenedesmus and Chlorella. A non-ionic compound showed unfavourabie effects on growth a t 5 p.p.m. and was lethal a t 200 p.p.m., but had a slight stimulating effect a t concentrations below 2 p.p.m. Surfactants form only one part of mixtures for dispersing oil spills and are often the least toxic component (see pp. 284, 287). Chadwick (1960) tested the toxicity of an American solvent-emulsifier (Tricon) to striped bass Roccus saxatilis (Walbaum) and found it lethal in 5-10 h at 10 p.p.m. George (1961) reported the drastic effects of emulsifier cleansing after a spill in Milford Haven a t about the same time as the Ministry of Agriculture, Fisheries and Food shellfisheries laboratory a t Burnham-on-Crouch was investigating the toxicity of a number of cleansers to molluscs and crustaceans of commercial importance (Department of Scientific and Industrial Research, 1961 ;Portmann and Connor, 1968 ; Simpson, 1968b). Preliminary tests intended to simulate conditions during the cleansing of a shellfish bed showed that a brief immersion in 25% suspensions of four emulsifiers caused unacceptable mortalities (up to 96% in cockles Cardium edule) ; this led to an official recommendation not to spray oyster layings or cockle beds. The edible winkle Littorina littorea (L.) appears to be extremely resistant, as was confirmed by Crapp (1969a) ; the winkle showed a mortality of only

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5% after one hour’s immersion in undiluted B P 1002, while that of topshells and other winkles lay between 75% and 100%. Mortality of the topshell Monodonta lineata was less than 20% after treatment with 80% B P 1002. Littorina obtusata and Gibbula umbilicalis (da Costa) were the most sensitive in these tests, with L. saxatilis, G. cineraria (L.) and the dog-whelk Nucella lapillus (L.) showing an intermediate response. Simpson offered as a partial explanation of differences in bivalve sensitivity the “ persistent gape ” of cockles, which do not close completely as do oysters (Ostrea edulis) and mussels (Mytilus edulis). Crapp applied the emulsifier to actively crawling gastropods, but noted that mortalities are much lower if they are first shaken to make them close tightly. Spooner (1968a) suggested that a heavy dose of emulsifier might have less effect than a light one, because it stimulates those animals which can to close up quickly. Crapp also reported marked seasonal changes ; for example, L. obtusata collected a t the end of the winter were exceptionally sensitive. Perkins (1968a) also studied the effect of brief exposure to a high concentration (25%) of various emulsifiers which only some winkles and whelks survived. He found that the median lethal concentration of B P 1002 over 24 h is greater than 3 000 p.p.m. for Littorina saxatilis, greater than 2 000 p.p.m. for L. littorea, 1 000 p.p.m. for Nucella and 250 p.p.m. for L. obtusata. Mytilus is fairly resistant a t 90 p.p.m. over 24 h, but in a 96 h test its LC,, dropped to 2.5 p.p.m. ; the sea-star Asterias rubens survived 40 p.p.m. and the shore-crab Carcinus maenas, about 30 p.p.m. The other common shore animals which he tested are even less resistant. Portmann and Connor showed much the same results. Hermit crabs Eupagurus bernhardus (L.), brown shrimps Crangon crangon and pink shrimps Pandalus montagui are particularly sensitive (LC,, about 5 p.p.m.). Tests a t the Plymouth laboratory (Smith, 1968) revealed that a variety of sublittoral crabs are killed by B P 1002 a t 5-25 p.p.m., bpt molluscs failed to survive one-tenth these concentrations. Wilson (1968a) found that larvae of the tubeworm Sabellaria spinulosa Leuckart were killed within a day or two by 2.5 p.p.m. of this emulsifier. Although irritated by 0.5-1.0 p.p.m. they apparently survived, but later became unhealthy and died in 4-6 weeks. Corner et al. (1968) found that adults of the barnacle Elminius modestus are killed by 10-100 p.p.m., although 5-10 p.p.m. slows down their feeding; 3p.p.m. slows down the swimming of the settling (cypris) larvae but, again, only 0.5-1.0 p.p.m. inhibits the development of younger (nauplius) larvae. Developing his earlier work, Perkins (1968b) showed that whelks Buccinum undatum, which had apparently recovered from brief immersion in 25% emulsifier, died as much as four

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months later without making further growth. The growth of Littorina littorea is detectably limited at 7.5 p.p.m. (one-four-hundredth of the LC,,) and significantly inhibited a t 30 p.p.m. (one-hundredth of the LC,,). At a cellular level, Manwell and Baker (1967) have demonstrated powerful effects on enzymes and other proteins (e.g. it binds the haemoglobin of soles Solea solea (L.))but used only high concentrations. Corner and his colleagues also made preliminary experiments with tissue extracts from Mytilus edulis, Patella vulgata and Chlamys opercularis (L.). They found that emulsifiers kill these molluscs at 10100 p.p.m., but concentrations around 1 000 p.p.m. were needed to inactivate their enzymes by more than 50%. They suggested that physical effects must therefore also be involved in the toxicity. Hicks and Chaplin (unpublished, 1969) also found that 6 000 p.p.m. of BP 1002 inactivated various enzymes of Carcinus by only about 60%. Fewer laboratory studies have been reported on the sensitivity of plants t o emulsifiers. George (1960; unpublished but quoted by Nelson-Smith, 1968a) added Polyclens to rock pools at 0*2%,killing most of the algae, but observed that the corallines eventually recovered from an addition of 1%. Boney (1968) found that the reproductive bodies of Ascophyllum nodosum (typical of the large fucoids) are killed only at high concentrations of emulsifiers (25% or more) although free spermatozoids are inactivated in 9-150 p.p.m. The green algae Cladophora rupestris (L.) Kiitz. and Bryopsis hypnoides Lamour., together with the microscopical form Prasinocladus m r i n u s (Cienk.) Waern and the small filamentous red alga Acrochaetium infestans Howe & Hoyt are damaged or killed at 25-50 p.p.m. Boney was unable t o demonstrate that undiluted emulsifiers did any harm to Polysiphonia lanosa (L.) Tandy or the laver-weed Porphyra umbilicalis. Rather more anecdotal evidence from O’Sullivan and Richardson (1967a, b), Spooner (1967) and Nelson-Smith (1968a) of decolorized and flaccid plants of Porphyra, as well as of the large brown alga Himanthalia elongata, species of Cladophora, Ulva and Enteromorpha, and corallines (Corallina oficinalis L. and Lithothamnion spp.) suggests that damaging concentrations were none the less attained during ‘‘ Torrey Canyon ” cleansing operations. 0.25-0.5y0 B P 1002 altered the colour of pigment extracts from the red alga Calliblepharis jubata (= C. lanceolata (Stackh.) Batt.) in experiments by Manwell and Baker (1967). The sublittoral Delesseria sanguinea (Hds.) Lamour was killed by as little as 0.001 yo (10 p.p.m.) in tests reported by Smith (1968) and showed unusual colours at some depth and distance from the shore (Drew et al., 1967; Potts et al., 1967). Phytosocial analyses by Bellamy et al. (1067) have also demonstrated damage to sublittoral as well as intertidal algae. Unlike the plants

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observed by George, the coralline algae lining rock-pools which were whitened by emulsifier treatment on many Cornish shores (Fig. 14) showed little sign of recovery (Nelson-Smith, 1968b); the gradual return of pink and purple colours to these pools was more probably due to recolonization. Damage t o lichens and maritime plants on the strandline or cliff ledges after the " Torrey Canyon " spill was probably due mainly to emulsifier spraying (Ranwell, 1968b). Clifftop and bacltshore vegetation was certainly killed by the spillage of undiluted cleansers, sometimes over a large area (Ranwell, 1968a). Tests on turves of Puccinellia maritima (Baker, 1968) show that 10% BP 1002 is damaging, but only the undiluted emulsifier kills it completely. Not only are non-ionic surfactants bacteriologically " hard " ; the type used in B P 1002 is actually recommended for use in mixtures to suppress bacterial decomposition of stored oils (Davis, 1967). It is thus not surprising that the emulsifiers used in Cornwall kill most oil-degrading bacteria at 10 p.p.m. Nevertheless, some survive 100 p.p.m. or more. These multiply rapidly, utilizing the emulsifier solvent and probably also the oil dissolved by it. Samples treated with 1 000 p.p.m., however, became sterile and remained so (Gunkel, 1968 ; Smith, 1968). The aromatic solvent used in BP 1002 and similar cleansers is more toxic than the surfactants or other components, as reported by Smith, Crapp (1969a) and other authors. A scattered literature on the toxicity of aromatic hydrocarbons has already been reviewed above (see pp. 249-256). Corner et al. (1968) found that BP 1002 solvent is very nearly as toxic to barnacle larvae as the mixture, other components having markedly less effect. However, although Wilson (1968b) demonstrated that some material, toxic to polychaete larvae, remains on sand grains for some days after their treatment with emulsifier and subsequent thorough washing, experiments described by Smith (1968) show that the solvent is readily volatile. Solutions of emulsifier from which it is free to evaporate become increasingly less toxic. Small soles (Xolea solea) suffer lOOyo mortality after 24 h in water containing 50 p.p.m B P 1002, but if their introduction t o the tank is delayed by 24 h this mortality drops to 30%. After 48 h it is 10% and after 72 h the water has become non-toxic (Portmann and Connor, 1968 ; Simpson, 1968). It is now generally recognized that cleansing with solvent-emulsifiers inflicts more biological damage than the original pollution. George (unpublished ; see Nelson-Smith, 1967a) estimated that after a 1960 spill in Milford Haven, approximately 30% of shore life was damaged by the oil alone whereas 90% was killed after emulsifier cleansing. Cowell (1969b ; see also Crapp, 1969) found that 38% of the cordgrass

THE PROBLEM OF OIL POLLUTION O F THE SEA

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FIG.17. The distribution of common animals and plants on two shores in west Cornwdl, resurveyed six months after '' Torrey Canyon " pollution and cleansing. Open (white) histograms show the situation just after the disaster ; black histograms superimposed on thess indicate survival. Many of the animals previously present had been killed and washed away before the original survey, leaving no record. Stippled histograms show settlement since the first snrvey-mainly barnacle spat and green algae (from Nelson-Smith, 1068b).

286

A. NELSON-SMITH

27r

25

l J a n 67

,

I

1

-

23 21 19

-

17 -

15 13 I1

Littorina neritoides

Littarina saxatills feet above chart datum

occasional

Littorina littorpo

Jan67-

-MHWN

.M T L 9-

- MLWN

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FIG.18. The distribution and abundance of some common winkles and topshells on a shore a t Hazelbeach. Milford Haven. Repeated surveys by Nelson-Smith (1967b, 1968a, 1968b) and Crapp (1969a) show the effects of oil-spills from the " Chryssi P.

Goulandris '' (Jan. 67) and the Gulf refinery (Nov. 68). Redrawn from Crapp.

Spaytinu townsendii was killed by a spill of fresh crude oil, but the mortality rose to 55% where emulsifiers were also applied. Many reports based on " Torrey Canyon " experience make the same point -for example, O'Sullivan and Richardson (1967a, b), Nelson-Smith (1968a, b), Ranwell (1968a), Smith (1968) and Wardley Smith (1968ac). Apart from their immediate toxic effects, emulsifiers spread the pollution to the crevices and landward or leeward surfaces which all but the heaviest oil pollution fails to reach. They also distribute the oil in fine droplets throughout the depth of rock pools and coastal

THE PROBLEM O F OIL POLLUTION OF THE SEA

287

shallows (Figs. 15 and 16). Such droplets are readily taken into the food-stream by filter-feeders (see, for example, Spooner, 1968a) and may be better able t o " wet " exposed animal tissues. On the worstaffected sites in Cornwall, solvent-emulsifiers applied liberally, in conjunction with heavy oil pollution, killed every limpet on the shore, bringing about the changes in algal cover described above (p. 261 and in Fig. 17). Perkins (1968a) offered the opinion that an oil emulsion containing B P 1002 is more toxic than the emulsifier alone. This is probably true where the surfactants help the oil t o penetrate-the oil then carries in with it the toxic elements in the emulsifier. Portmann and Connor (1968) found that the addition of twice its volume of oil to Polyclens almost doubles its toxicity t o cockles Cardium edule and renders it slightly more toxic t o brown shrimps Crangon crangon, although B P 1002 and Gamlen become less toxic when treated in this way. Van de Wiele (1968) discovered that emulsions of Finasol possess the same toxicity to the brine-shrimp Artemia salina (L.) and the guppy Lebistes reticulatus (Peters) whether or not crude oil (which by itself had little effect in her tests) is added. Preliminary experiments a t Swansea using yeast in a microrespirometer indicate that the addition of an equal amount of fresh crude oil to B P 1002 approximately halves its toxicity, which is here exerted a t the surface of the test organism. Presumably the oil binds some of the toxic elements, effectively removing them from the culture solution. Since the " Torrey Canyon " disaster, manufacturers have striven to reduce the toxicity of their emulsifiers, either by diminishing the proportion of aromatics in the solvent or by eliminating hydrocarbon solvents altogether. Test blends of B P 1002 in which the solvent contains a high proportion of aliphatic compounds are considerably less toxic to gastropod molluscs (Crapp, 1969a) and yeast cultures (unpublished; Fig. 19). Finasol is a similar reformulation of Fina Unisol. Tests by Capart (1968) show that it is highly toxic a t 0.1% and a t 100 p.p.m. it is still somewhat toxic to guppies, brine-shrimps, a freshwater snail Planorbis sp. and Daphnia pulex Degeer, but not to protozoans or other micro-organisms. At 10 p.p.m. it is entirely nontoxic. The water-soluble dispersants Polycomplex-A and Corexit 7664 have been compared with various more conventional emulsifiers by Spooner and Spooner (1968) and Spooner (1968a). Polycomplex-A appears to be approximately one-fifth as toxic as B P 1002 t o a selection of marine organisms. Corner (quoted by the Spooners) found it twelve times less toxic in similar tests on barnacle larvae. Corexit, however, is less toxic

288

A . NELSON-SMITH

by several orders of magnitude. Spooner (1968a) found that concentrations at least up t o 1 000 p.p.m. are safe for mussels Mytilus edulis. Griffith (1969) reported that the median toxicity for limpets Patella vulgata is 1 000 p.p.m, while for the winkles Littorina littorea and L. obtusata it lies between 1000 and 10 000 p.p.m. (0-1-1.0%). I n its sublethal effects on yeast cultures, Dispersol 0s appears to be about 500 times less toxic than B P 1002. Corexit or Dispersol are obviously the dispersants of choice for use at sea, but comparisons with B P 1002 a're informative rather than practical, since they are both ineffective HIGH-AROMATIC EMULSIFIER

LOW-AROMATIC EMULSIFIER

-Q~e

4 0 0 p g Oxygen

4 0 0 p g . Oxygen

consumed

consumed

200

0

,/

,

20

~

4,O

~

6Prnin.

0

20

40

60min.

FIG. 19. Respiration of standard yeast cultures in vnrious concentrations of BP 1002 (left) and a test-blend containing a much more aliphatic solvent-mixture. Individual curves have been superimposed so that the points a t which the sample wns introduced coincide; the axes are calibrated from that point (unpublished, Dunn and Nelson-Smith, 1969).

against oil stranded on the beach. The new B P 1100 appears to be useful in both situations and to have the same very low toxicity.

VI. CONCLUSIONS AND PROSPECTS I n summary, the increased use of petroleum products (in the synthetic chemical industry even if internal-combustion engines eventually become obsolete) will continue to demand the large-scale transport of crude oil, much of it a t sea in even larger bulk carriers, with an attendant degree of unavoidable spillage. Sturmey (1967) has predicted a doubling of world oil consumption every ten years at least until the end of this century. Pressures from responsible operators within the oil industry, as well as from official and unofficial bodies outside it, must ultimately bring about the universal adoption of every possible

THE PROBLEM OF OIL POLLUTION OF THE SEA

289

method of reducing such spillages. An important aspect of this is the development of efficient methods for apprehending vessels which deliberately discharge oily wastes and the successful prosecution of their owners or operators. It is also important that international agreement be reached on the rights and responsibilities both of ship operators and those countries whose coastal waters are threatened by the wreck of a vessel carrying heavy oils-or, indeed, even more hazardous cargoes. The probable path of a slick can now be predicted with reasonable accuracy, provided that proper observations are kept and accurate meteorological data are speedily provided. With equipment now available for military intelligence, it should be possible to maintain continuous surveillance of quite small slicks far out at sea from high-flying aircraft or satellites (see Cronin (1965) and more recent NASA press releases). It is now accepted policy to treat the oil at sea wherever possible. The means to do this efficiently and with little damage to marine life by sinking, dispersing or mechanical removal (where weather conditions permit) are now known and require only the organization t o get them t o the right place in time and in sufficient quantities. The drastic effects of ‘‘ first-generation ” emulsifiers effective on stranded oil have been well documented. As Sennen Cove’s Rural District Councillor said (having done his share in cleansing Whitesand Bay from “ Torrey Canyon ” oil) “ no one in his right mind would use detergent . . . if any other effective method was available ” (see Cowan, 1968). Unfortunately, many thousands of gallons of these emulsifiers are now stockpiled against an emergency spill by local authorities throughout Britain. To replace these with newer, more expensive formulations would be very costly although, in emergency, it is with the earlier mixtures that enthusiastic but uninstructed volunteers can do great if unwitting damage. The responses of shore biota t o catastrophic pollution in Milford Haven and Cornwall show that partial recovery occurs quite quickly in regions where populations are both plentiful and varied (Fig. 18). Like any other abnormal stress, oil pollution has a particularly marked effect on organisms near the limits of their geographical range. Zoogeographical and seasonal differences account for some of the discrepancies which exist between the various accounts of mortalities observed on affected shores or recorded in laboratory experiments. A good example is the topshell Monodonta lineata, which was found to be very resistant in Cornwall but, farther north in Milford Haven, serves as a sensitive indicator of shore damage and showed marked seasonal variations in susceptibility during an extended series of toxicity tests. The disproportionate effects that oil pollution and its cleansing have

290

A. NELSON-SMITH

on grazing molluscs and the algal cover which they normally control indicate that in regions where this is repeated too often, rocky shores might become permanently covered with a slippery and unsightly growth of seaweeds, while adjacent sandy shores could lose the services of those scavengers which usually remove unpleasant debris. Thus the amenities which repeated (‘cleansing ” is intended t o preserve might, in the long term, suffer ever1 greater damage. Outstanding problems in the purely biological and technical fields of oil pollution have been summed up by Arthur (1968). Concluding his account of the part played by the Plymouth laboratory in the ‘( Torrey Canyon ” affair, Smith (1968) called for a higher degree of co-ordination between government agencies, the oil and shipping industries, and biological interests ; Lord Geddes, summing up the scientific deliberations of the Rome Conference (1968), extended this plea to the international field. Administrative and legislative action, although always lagging well behind scientific discovery, is nevertheless essential to its practical application and control and there are significant advances t o be rnade in this area, too. Dr. Giovanni Spagnolli said, in closing that Conference, “ technical progress threatens t o upset the normal balance of nature and the adoption of legal, technical and administrative measures to prevent and check pollution is a matter of urgency ”.

VII. REFERENCES Abhott, B. C. and Straughan, D. M. (1969). Biological and oceanographic effects of oil spillage in the Santa Barbara Channel following the 1969 blowout. Mar. Pollut. Bull., Newcastle, no. 13,4-9. Abhott, M. B. (1961). Containing oil spills with a pneumatic barrier. Dock Harb. Auth. 42(12), 259-260. Adam, N. K. (1936). The pollution of the sea and shore by oil. Report to Council, Royal Society, London. Aldrich, E. C. (1938). A recent oil pollution and its effects on the waterbirds in the San Francisco Bay area. Bird Lore, 40, 110-1 14. Aljakrinskaya, I. 0. (1966). On the behaviour and filtering abilitty of the Black Sea Mytilus galloprovin,cialis in oil-polluted waters (in Russian). Zool. Z h . 45, 998-1003. American Merchant Marine Institnte (1953). Oil pollution manual. (Jointly with American Petroleum Institute, Pacific American Steamship Ass. and Pacific American Tankship Ass.). American Petroleum Institute (1957). Manual on disposal of refinery wastes. 4. Sampling and analysis of waste water. New York (2nd edn.). American Petroleum Institute (1960). Manual on disposal of refinery wastes. 3. Chemical wastes. New York (4th edn.). American Petroleum Institute (1963). Manual on disposal of refinery wastes. 1 . Waste water containing oil. New York (7th edn.).

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American Petroleum Institute (1964). Manual for the prevention of water pollution during marine oil terminal transfer operations. Washington, D.C. American Public Health Association (1960). Standard methods for the examination of water and waste-water. New York ( 1 l t h edn.). Anon. (1962). Floating oil spill booms. Dock Harb. Auth. 42(4), 401-404. Anon. (1967a). A way to tackle the oil menace. NewScient. 35,424. Anon. (196713). Shredded polyurethane absorbs oil spilled on oceans. Chem. Engng News, 45(41), 12-13. Anon. (1968a). Transfer of oil cargo a t sea. ShipbZdg int. 11(3), 28-32. Anon. (1968b). Using bark to mop up spilt oil. NewScient. 38,216. Anon. (1969). Single buoy mooring systems. Ports Dredg. 62,20-21. Arthur, D. R. (1968). The biological problems of littoral pollution by oil and emulsifiers-a summing up. Fld Stud. 2(snppl.), 159-164. Baker, J. M. (1968). The effects of oil pollution on salt-marsh communities. Oil Pollution Research Unit, Orielton. Baker, J. M. (1969). The effects of oil pollution on salt-marsh communities. Annual Report of the Oil Pollution Research Unit, 1968, Bl-B11. Field Studies Council, Orielton. Barclay-Smith, P. (1958). Oil pollution of the sea. Rapp. P.-v. Rkun. Commn int. Explor. scient. Mer Mdditerr. 14, 553-556. Barclay-Smith, P. (1967). Oil pollution-an historical survey. J . Dewon Trust Nut. Conserv. (suppl.), 3-7. Bardach, J. E., Fujiya, M. and Holl, A. (1965). Detergents: effects on the chemical senses of the fish Ictalurus natalis (le Sueur). Science, N . Y . 148, 1605-1 607. Batelle-Northwest Institute (1967). Oil spillage study : research report to U.S. Coast Guard. Pacific Northwest Laboratories, Richland, Washington, D.C. Beaumont, F. N. (1968). Pollution prevention (pp. 149-160). Institute of Petroleum, London. Beer, J. V. (1968a). Post-mortem findings in oiled auks dying during attempted rehabilitation. FZd Stud. P(suppl.), 123-129. Beer, J. V. (196813). The attempted rehabilitation of oiled sea birds. Wildfowl. 19, 120-124. Bellamy, D. J., Clarke, P., John, D. M., Jones, D., Whittick, A. and Darke, T. (1967). Some effects of pollution from the " Torrey Canyon " disaster on littoral and sublittoral ecosystem8 dominated by attached macrophytes. Nature, L a n d . 216, 1170-1173. Bergman, G. (1961). The migrating populations of the longtailed duck (Clangula hyemalis) and the common scoter (Melanitta nigro) in the spring, 1960 (in Finnish). Suom. Riista, 14,69-74. Berridge, S. A., Dean, R. A,, Fallows, R. G. and Fish, A. (1968a). Scientific aspects of pollution of the sea by oil (pp. 2-9). Institute of Petroleum, London. Berridge, S. A., Thew, M. T. and Loriston-Clarke, A. G. (196813). Scientific aspects of pollution of the sea by oil (pp. 35-57). Institute of Petroleum, London. Beynon, L. R. (1968). Cleaning up. Hydrospace, 1(2), 17-27. Bhattacharya, S. N. (1961). Identification of crude oils by paper chromatography. J . Inst. Petrol. 47, 291-294.

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Birkholz, D. O., Rogers, M. R. and Kaplan, A. M. (1961-62). The microbial deterioration of hydrocarbons and the related deterioration of equipment used for the storage, distribution and handling of petroleum products. A selected bibliography. Res. engng Cmd Project Y-65-01-003, ser. Rep. 5 , 1-19; suppl., 1 , l - 1 6 . Blade, 0. C. (1966). Petroleum products survey no. 46 : Burner fuel oils. U.S. Bureau of Mines, Washington (pp. 28-30). Blokker, P. C. (1964). Spreading and evaporation of petroleum products on water. (Paper read to 4th International Harbour Conf., Antwerp, June). Blokker, P. C. (1966). Die Ausbreitnng v o ~ 0i 1 auf Wasser. Dt. gewasserk. Mitt. 10, 112-114. Bone, Q. and Holme, N. A. (1968). Oil pollution-another point of view. New Scient. 37, 365-366. Boney, A. D. (1968). Experiments with some detergents and certain intertidal algae. Fld Stud. 2(suppl.), 55-72. Boswell, J. L. (1950). Experiments to determine the effect of a surface film of crude oil on the absorption of atmospheric oxygen by water. Texa*sA & M Research Foundation. Bourcart, J. and Mallet, L. (1965). Pollution marine des rives de la region centrale de la mer Tyrrhenienne (baie de Naples) par les hydrocarbures polybenzeniques du type benzo-3,4 pyrhne. C.r. hebd. Skanc. A c a d . Sci., Paris, 260, 3729-3734. Bourne, W. R. P. (1968a). Oil pollution and bird populations. Fld Stud. ~ ( s u P P ~99-121. .), Bourne, W. R. P. (1968b). Observation of an encounter between birds and floating oil. Nature, Lond. 219, 632. Bourne, W. R. P. and Devlin, T. R. E. (1969). Birds and oil. Birds, 2, 176178. British Petroleum Company (1968). Statistical review of the world oil indust.ry, 1967. London. Brockis, G. J. (1967). Preventing oil pollution of the sea. Helgolander wiss. Meeresunters. 16, 296-305. Brown, S. 0. and Reid, B. L. (1951). Experiments to test the diffusion of oxygen through a surface layer of oil. Texas A & M Research Foundation. Brown, S. O., Van Horn, Virginia and Reid, B. L. (1951). Decomposition of organic compounds by marine micro-organisms. (Mimeo. 1 1 pp.). Texas A & M Research Foundation. Brummage, K. G. (1968). The consequences of load-on-topin petroleum refining. Proc. Int. Conf. Oil Pollut. Sea, Rome, 183-189. Brummage, K. G., Maybourn, R. and Sawyer, M. F. (1967). How LOT affects refinery costs. Petrol. Reflner. 46, 116-120. Brunnock, J. V., Duckworth, D. F. and Stephens, G. G. (1968). Scientific aspects of pollution of the sea by oil (pp. 12-27). Institute of Petroleum, London. Burnett, F. L. and Snyder, D. E. (1954). Blue crab as a starvation food of oiled American eiders. Auk, 71, 315-316. Cairns. J. and Scheier, A. (1962). The effects of teniperature and water hardness upon the toxicity of naphthenic acids to the common bluegill sunfish Lepomis macrochirus Raf. and the pond snail Physa heterostropha Say. Notul. Nat. 353. 1-12.

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California Department of Fish and Game (1969a). Summary of progress report on wildlife affected by the Santa Barbara Channel oil spill. Mar. Pollut. Bull., Newcastle, no. 13, 3. California Department of Fish and Game (1969b). Cruise Report 69A2 : Inshore survey of Santa Barbara oil spill. State Fisheries Lab., Terminal Island. California Department of Fish and Game (1969~).Special cruise report : Inshore survey of Santa Barbara oil spill. State Fisheries Lab., Terminal Island. Capart, A. (1968). Toxicite des detergents et des p6troles. Institut Royal des Sciences Naturelles de Belgique. Castellanos, E. (1968). Paraffin for oil pollution of the sea. Proc. Int. Conf. Oil Pollut. Sea. Rome, 239-241. Chadwick, H. K. (1960). Toxicity of Tricon oil spill eradicator to striped bass. Calif. Fish Game, 46,373-374. Chipman, W. A. and Galtsoff, P. S. (1949). Effects of oil mixed with carbonized sand on aquatic animals. Spec. scient. Rep. U.S. Fish Wildl. Serv. 1, 1-53. Clark, R. B. (1968). Oil pollution and the conservation of seabirds. Proc. Int. Conf. Oil Pollut. Sea, Rome, 76-112. Clark, R. B. (1969).Paper read a t joint American Society of Zoologists/Canadian Society of Zoologists Symposium on Coastal Oil Pollution, Burlington, Vermont, U.S.A. Clark, R. B. and Kennedy, R. J. (1968). The rehabilitation of oiled seabirds. University of Newcastle-upon-Tyne. Clendenning, K. A. and North, W. J. (1960). Effects of wastes on the giant kelp Macrocystis pyrqera. Proc. I n t . Conf. Waste Dispos. mar. Envir. 1, 82-91. Cole, A. E. (1941). Effects of pollutional wastes on fish life. Symp. Hydrobiol., Wisconsin, 241-259. Corner, E . D. S., Southward, A. J. and Southward, Eve C. (1968). Toxicity of oil-spill removers (“ detergents ”) to marine life; an assessment using the barnacle Elminius modeetus. J . mar. biol. Ass. U.K. 48, 29-47. Cowa.n, E. (1968). ‘‘ Oil and water : the Torrey Canyon disaster.” Lippincott, Philadelphia. Cowell, E. B. (1968). “ Report on visit to Newfoundland.” Oil Pollution Research Unit, Orielton. Cowell, E . B. (1969a). Introduction to first annual report. Annual Report of Oil Pollution Research Unit, 1968, 1-4. Field Studies Council, Orielton. Cowell, E . B. (1969b). Effects of oil pollution on salt marsh communities in Pembrokeshire and Cornwall. J . appl. Ecol. 6, 133-142. Cowell, E. B. and Baker, J. M. (1969). The recovery of a salt-marsh in Pembrokeshire, South Wales, from pollution by crude oil. J . biol. Conserv. 1, 291295. Crapp, G. B. (1969a). Second report by zoologist. Annual Report of Oil Pollution Research Unit, 1968, Z 1-224. Field Studies Council, Orielton. Crapp, G. B. (196913). Oil pollution in Milford Haven. Nature in Wales, 11, 131-137. Croft, E. D. (1959). Contamination of beaches in Great Britainand itseffects on +,ourism. Proc. I n t . Conf. Oil Pollut. Sea, Copenhagen, 69-70. Cronin, J. F. (1965). Oceanography from space (pp. 63-72). (Ed. G. C . Ewing), Woods Hole Oceanographic Institution, Mass. Crosby, E. S., Rudolfs, W. and Heukelekian, H. (1954). Biological growths in petroleum refinery waste waters. Ind. Engng Chern. i n d . Edn, 46, 296-300.

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Cunningham, M. B. (1954). Panel discussion on oil pipeline crossings. W a t . Sewage W k s , 101,392. Currier, H. B. and Peoples, S. A. (1954). Phytotoxicity of hydrocarbons. Hilgurdiu, 23, 155-173. Dangl, F. and Nietsch, B. (1952). Zum Nachweis von Erdolprodukten im Brunnerwassern durch Fluoreszenz. Mikrochemie mikrochem. Actu, 39, 333-335. Davies, J. A. and Hughes, D. E . (1968). The biochemistry and microbiology of crude oil degradation. Fld Stud. %(suppl.),139-144. Davis, J. A. (ed.) (1968). Kuwait to Bantry. Oil Gas int. 8(11), 69-100. Davis, J. R. (1967). “ Petroleum microbiology.” Elsevier, Amsterdam. Dennis, J. V. (1959). Oil pollution survey of the United St,ates Atlantic coast,. American Petroleum Institute, Washington, D.C. Dennis, J. V. (1961). The relationship of ocean currents to oil pollution off the southeastern coast of New England. American Petroleum Institute, Washington. Department of Scientific and Industrial Research (1961). Oil pollution of beaches. The use of emulsifier/solvent mixtures for the removal of liquid oil pollution. Warren Spring Laboratory, rep. RR/ES/17, Stevenage. Department of Scientific and Industrial Research (1963a). The removal of oil from contaminated beaches. Warren Spring Laboratory, rep. RR/ES/39, Stevenage. Department of Scientific arid Industrial Research (1963b). The treatment and disposalof floating oil. Warren Spring Laboratory, rep. RR/ES/40, Stevenage. Diaz-Piferrer, M. (1962). The effects of an oil on the shore of Guanica, Puerto Rico. Association Island Marine Laboratories, 4th Meeting, Curapao, 12-13. Dietrich, K. R. (1964). Der Verschmutzunganteil der Auspuffgase von ZweitaktAussenbordmotoren in Gewassern. Wasserwirtsch. 54, 196-200. Dilling, T. (1968). Separation of traffic a t sea. Proc. Int. Conf. Oil Pollut. Sea, Rome, 191-198. Drew, E. A., Forster, G. R., Gage, J., Harwood, G., Larkum, A. W. D., Lythgoe, J. N. and Potts, G. W. (1967). “ Torrey Canyon ” report. Report of the Underwater Association, 1966-67, 53-60. Dudley, G. (1968). The problem of oil pollution in a major oil port. Pld Stud. ~ ( s u P P ~ 2. )1-29. , Dudley, G. (1969). Oil pollution and methods of dealing with it. (Paper read at 6th Meet. Harbourmasters NW Europe, Antwerp, May.) Dundee Corporation (1968). Report of the technical advisory committee on oil pollution in the Tay Estuary. Dundee, Scotland. Dzyuban, I. (1958). The spontaneous removal of petroleum contamination from Volga water in storage reservoirs (in Russian). Byull. Inst. Biol. Bodokhran. 1, 11-14. Edwards, M. N. (1968). Oil pollution and the law. Proc. 1nt. Conf. Oil Pollut.Sea, Rome, 290-299. Elliott, D. W. (1969). British law in relation to pollution of the seas. M a r . PoEl. Bull., Newcastle, no. 15, 8-14. Elmhirst, R. (1922). Investigation on the effects of oil tanker discharge. Rep. Scott. mar. biol. Ass. 8-9. English, J. N., McDermott, G. N. and Henderson, C. (19634. Pollutional effects of outboard motor exhaust-laboratory studies. J . W a t . Pollut. Control Fed. 35, 923-931.

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English, J. N., Snrber, E. W. and McDermott, J. N. (1963b). Pollutional effects of outboard motor cxhatust-field studies. J . Wat. Pollut. Control Fed. 35, 1121-1132. Erickson, R. C. (1962). Effects of oil pollution 011 migratory birds. Trans. Seminar Biol. Problems Wat. Pollut., vol. 3, 177-181. Fenton, A. F. (1964). Atmospheric pollution of Belfast and its relationship to the lichen flora. I r . Nut. J . 14, 237-245. Foster, N. R., Scheier, A. and Cairns, J. (1966). Effects of ABS on feeding behaviour of flagfish, Jordanella jloridae. Trans. A m . Fish.SOC.95, 109-110. Galtsoff, P. S. (1936). Oil pollution in coastal waters. Proc. N . A m . Wildl. Conf. 1, 550-555. Galtsoff, P. S., Prytherch, H. F., Smith, R. 0. and Koehring, Vera (1935). Effects of crude oil pollution on oysters in Louisiana waters. Bull. Bur. Piah. Wash. 18,143-210. Geddes, Lord (1968). Summing-up of methods of prevention and alleviation of oil pollution. Proc. Int. Conf. Oil Pollut. Sea, Rome, 248-251. George, M. (1961). Oil pollution of marine organisms. Nature, Lond. 192, 1209. Gilet, R. (1959). Water pollution in Marseille and its relation with flora and fauna. Proc. Int. Conf. Waste Dispos. mar. Envir. 1, 39-56. Gillespie, D. L. (1968). A summary of oil pollution in Newfoundland’s coastal waters 1949-1968. Canadian Wildlife Service, Ottawa. Gloyna, E. F. and Malina, J. P. (1963). Petrochemical wastes-effects on water. Wat.Sewage Wks, (1963 Ref. no.), R262-R285. Goad, C. (1968). International action on oil pollution since the loss of the “ Torrey Canyon ”. Proc. Int. Conf. Oil Pollut. Sea, Rome, 268-280. Goethe, F. (1968). The effects of oil pollution on populations of marine and coastal birds. Helgolund. wiss. Meeresunters. 17, 370-374. Goldacre, R. J. (1968). The effects of detergents and oils on the cell membrane. PldStud. 2(suppl.), 131-138. Gowanloch, J. N. (1935). Pollution by oil in relation to oysters. Trana. Am. Fish. SOC.65, 293-296. Greenberg, A. E., Maehler, C . Z. and Cornelius, J. (1965). Evaluation of the carbon adsorption method. J . Am. W a f . W k s Ass. 57,791-799. Greenwood, J. J. D. and Keddie, J. P. F. (1968). Birds killed in the Tay Estuary, March and April, 1968. Scott. Birds, 5, 189-196. Griffith, D. de G. (1969). Investigations into the toxicity of Corexit-a new oil dispersant. Dept. Agric. Fish. (Dublin),Fish. leafl. 6, 1-9. Gross, A. C. (1950). The herring gull-cormorant control project. Proc. Int. orn. Congr. 10,532-536. Gunkel, W. (1967). Experimentell-okologischeUntersuchungen iiber die limitierenden Faktoren des microbiellen Olabbaues im marinene Milieu. HeZgoZii.tzder wiss. Meeresunters.. 15, 210-225. Gunkel, W. ( 1 968). Bacteriological investigations of oil-polluted sediments from the Cornish coast following the “ Torrey Canyon ” disaster. Fld Stud. 2(suppl.), 15 1-1 58. Gutsoll, J. S. (1921). Danger to fisheries from oil and tar pollution of waters. Rep. U.S. Commnr Fish. (Append. 7.) Halasz, I. and Wegner, E. E. (1961). Gas chromatographic separation of lowboiling hydrocarbons using active alumina as support for the liquid phase. Nature, Lond. 189, 570-571.

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Spooner, M. F. (1968b). Scientific aspects of pollution of the sea by oil (p. 67). Institute of Petroleum, London. Spooner, M. F. and Spooner, G. M. (1968). The problem of oil spills a t sea. Marine Biology Association, Plymouth. Stander, G. H. and Venter, J. A. V. (1968). Oil pollution in South Africa. Proc. Int. Conf. Oil Pollut. Sea, Rome, 251-259. Standley, E. W., Acuff, A. D. and Solanas, D. W. (1969). Field report on Union Oil Go. platform A well no. 21. U.S. Geological Survey, Los Angeles. Stehr, E. ( 1959). Berechnungsgrundlagen fur Pressluft-Olsperren. Mitt. hannower. VersAnst. Grundb. WassBau, 16, 275-406. Stehr, E. (1964). 0 1 im Gewasser! Was nun? Wass. Boden, 16, 6-8. Stehr, E. (1967). Uber Olverschmutzung durch Tanlrerunfalle auf hoher See. Gas- u. WassFach. 108,53-54. Stone, R. W., Fenske, M. R. and White, A. G. C. (1942). Bacteria att,acking petroleum and oil fractions. J . Bact. 44, 169-178. Stroop, D. V. (1930). Behavioiir of fuel oil on the surface of the sea. In “ Report on oil pollution experiments ” (pp. 41-49). U.S. House of Representatives Committee on Rivers and Harbors, doct. 10625. Sturmey, S. G. (1967). ‘‘ Shipping; the next hundred years.” J. & J. Denholm, Glasgow. Sturz, 0. and Klein, K. (1964). Erprobung von Bindemitteln zur Beseitigung von Olverunreinigungen auf Wasseroberflachen. Dt. gewiisserk. Mitt. 8, 127-138. Surber, E. W., English, J. N. and McDermott, G. N. (1962). Tainting of fish by outboard motor exhaust wastes as related to gas and oil consumption. Trans. Seminar biol. Problems Water Pollut. vol. 3, 170-176. Tagatz, M. E. (1961). Reduced oxygen tolerance and toxicity of petroleum products to juvenile American shad. ChesapeakeSci.2, 65-71. T h i n g , A. V. (1952). The oil death (in Swedish). Swer. Nat. 43 (5), 114-122 (see Ministry of Transport, 1953, p. 2). Tanis, J. J. C. and Morzer Bruijns, M. F. (1962). Investigation of seabirds killed by oil pollution 1958-62 (in Dutch). Lewende Nut. 65, 133-140. Tanis, J. J. C. and Morzer Bruijns, M. F. (1968). The impact of oil pollution on sea birds in Europe. Proc. Int. Conf. Oil Pollut. Sea, Rome, 67-74. Tarzwell, C. M. (1967). ‘‘ Interim report to U.S. Secretary of the Interior on water quality requirements for fishes, other aquat,iclife and wildlife ” (pp. 108--119). National Technical Advisory Committee, Washington. Tegelberg, H. (1964). Washington’s razor-clam fisheries in 1964. Rep. Wash. St. Dep. Fish. 74,53-56. Tendron, G. (1968). Contamination of marine flora and fauna by oil and biological consequences of the “ Torrey Canyon ” accident. Proc. Int. Conf. Oil Pollut. Sea, Rome, 1 14-1 2 1. Toman, M. and StGta, Z. (1959). Uber die Toxizitiit des Benzols und seiner Chlorsubstitutionsderivate gegenuber Fischen. Bioldgia Bratisl. 14, 674679. Tomczak, G. (1964). Investigations with drift cards to determine the influence of the wind on surface currents. Ozeanographie, 10, 129-139. Treccani, V. (1965). Microbial degradation of aliphatic and aromatic hydrocarbons. 2. allg. Mikrobiol. 5, 332-341.

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Tuck, L. M. (1959). Oil pollution in Newfoundland. Proc. Int. Conf. Oil Pollut. Sea, Copenhagen, 76-77. Tuck, L. M. (1960). The murres: their distribution, populations and biology. Canadian Wildlife Service, Ottawa. Turnbull, H., DeMann, J. G. and Weston, R. F. (1954). Toxicity of various refinery materials to fresh-water fish. Ind. Engng Chem. ind. Edn, 46, 324-333. U.S. Coast Guard (1959). Efforts to reduce oil pollution. Proc. Merchant Marilze Coulz. vol. 16,199-203. U.S. Coast Guard (1968). Sunken tanker project report. Washington. U.S. Congress (1967). Report on international control of oil pollution. Merchant Marine and Fisheries Committee (HR no. 628), Washington. U.S. Department of Interior (1967). Report on wastes from watercraft. Congress doct. no. 48, Washington. U.S. Public Health Service (1939). Industrial waste guide : oil refining. Ohio River Pollution Survey. U.S. State Department (1959). Report of U.S. national committee for the prevention of pollution of the seas by oil. Washington. van de Wiele, C. (1968). Toxicit6 des dhtergents et des p6troles. 4. Toxicit6 de 1’6mulsion. Institut Royal des Sciences Naturelles de Belgique. van Hall, C. E., Safranko, J. and Stenger, V. A. (1963). Rapid combustion method for the determination of organic substances in aqueous solutions. Analyt. Chem. 35, 315-319. van Overbeek, J. and Blondeau, R. (1954). Mode of action of phytotoxic oils. Weeds, 3, 55-65. Veselov, A. E. (1948). Effect of crude oil pollution on fishes (in Russian). Ryb. Khoz. 12,21-22. Voroshilova, A. A. and Dianova, E. V. (1950). Bacterial oxidation of oil and its migration in natural waters (in Russian). Mikrobiologiya, 19,203-210. Wardley Smith, J. (196th). Recommended methods for dealing with oil pollution. Ministry of Technology Warren Spring Laborat,ory, LR 79 (EIS). Wardley Smith, J. (1968b). Scientific aspects of pollution of the sea by oil (pp. 60-65). Instituto of Petroleum, London. Wardley Smith, J. ( 1 9 6 8 ~ ) .Methods of absorbing oil spills a t sea. Fld Stud. 2(suppl. ) , 15-1 9. Webber, L. A. and Burlrs, C. E. (1952). Determination of light hydrocarbons in water. Analyt. Chem. 24, 1086-1087. Weir, P. (1964). Paper read to Amer. Water Works Ass., Joint problems of the oil and water industries (pp. 13-15). Institute of Petroleum, London. Westphal, Althea. (1969). Jackass penguins : their treatment, care and release after contamination by crude oil. Mar. Pall. Bull., Newcastle, no. 14, 2-7. Wilson, D. P. (19688,). Long-term effects of low concentrations of an oil-spill remover (“ detergent ”) : studies with the larvae of Sabellaria apinulosa. J . mar. biol. Ass. U.K. 48, 177-182. Wilson, D. P. (1968b). Temporary absorption on a substrate of an oil-spill remover (“ detergent ”) : tests with larvae of Sabellaria spiiauloaa. J . mar. biol. Ass. U.K. 48, 183-186. Wragg, L. E. (1954). Effect of DDT and oil on muskrats. Canad. Fld Nat. 68, 11-13.

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Wyllie, D. and Taylor, W. E. L. (1967). France and the “Torrey Canyon”. Admiralty Oil Laboratory (Tech. note no. 31), Brentford. Zahner, R. (1962). Uber die Wirkung von Treibstoffen und Olen auf Regenbogenforellen. Vom Warn. 29, 142-177. ZoBell, C. E. (1946). Action of microorganisms on hydrocarbons. Bact. Rev. 10, 1-49. ZoBell, C. E. (1950). Assimilation of hydrocarbons by micro-organisms. Adv. Enzymol. 10,443-486. ZoBell, C. E. (1959). Factors affecting drift seaweeds on some San Diego beaches. Univ. California Institute of Marine Resources, no. 59-3. ZoBell, C. E. (1964). The occurrence, effects and fate of oil polluting the sea. Adv. wat. Pollut. Res. 3, 85-109. ZoBell, C. E. and Prokop, J. F. (1966). Microbial oxidation of mineral oils in Barataria Bay bottom deposits. 2. allg. Milcrobiol. 6, 143-162. Zuckerman, Sir S. (1968). The scientific approach to the problem of oil pollution. Proc. Int. Conf. Oil Pollut.Sea, Rome, 143-159.

Adv. mar. Biol., Vol. 5, 1970, pp. 307-436

SCATOLOGICAL STUDIES OF THE BlVALVlA (M 0LLUSCA) KOHMAN Y. ARAKAWA Hiroshima Fisheries Experimental Xtation Ondo, Aki-gun, Hiroshima, Japan

.. ..

..

I. Introduction ., .. .. .. .. .. . . 307 11. Material and Techniques .. .. .. . . .. . . 309 111. Morphology . .. .. .. .. .. .. .. . . 310 A. Classification of Faecal Pellets . . . . .. .. .. 310 B. Definition of Pellet-types .. .. .. .. *. . . 310 C. Descriptions of Faecal Pellets . . . . .. .. .. . . 317 .. . . 317 I. Protobranchia (Gastroproteia) . . .. .. 11. Septibranchia (Gastrodeuteia) . . .. .. .. . . 320 111. Gastrotriteia .. .. .. .. .. *. . . 320 IV. Gastrotetartika . . .. .. .. .. .. . . 334 V. Gastropempta .. .. .. .. .. .. . . 345 IV. Biological Significance of the Characteristic Form of Faecal Pellets . . 379 A. Relation of Faecal Characteristics to the Feeding Habit and Mode of Life of the Animals . . . . . . . . . . .. . . 379 B. Relation of Faecal Characteristics to the Structure and Function of the Digestive Organs .. .. .. .. . . . . 381 V. Use of Faecal Pellets as a Systematic Index .. .. .. . . 403 VI. Evolutionary Trends of Faecal Pellets .. .. .. .. . . 405 VII. Biodeposition of Suspension Feeding Bivalves . . .. .. 413 A. Factors Influencing Biodeposition .. .. .. *. .. 419 B. Daily and Seasonal Aspects of Biodeposition , .. . . . . 421 C. Effects of Biodeposition upon Various Marine Environmental .. .. .. .. _ . 425 Conditions . . .. VIII. Bibliography .. .. .. .. .. . . .. .. . . 429 .. .. . . . . facing page 436 I X . Plates .. . . . .

.

..

..

.

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..

I. INTRODUCTION Since H. B. Moore’s pioneer work on bivalve faecal pellets (1931, 1931a, 1931b and 1933), valuable additions to our knowledge on the subject have been made from various angles by many workers (Edge, 1934; Schafer, 1953; Manning and Kumpf, 1959; Haven and MoralesAlamo, 1966 ; Ota, 1959; Ota and Fukushima, 1961 ;and Arakawa, 1963, 1965, 1968). Although suggestions have been made about the practical value of the study of faecal pellets in geology, sedimentology, palaeoecology, systematics, marine ecology etc., basic knowledge about bivalve faecal pellets remains scrappy and superficial and no worker has yet given a full and systematic account of them. The present work was designed first to review and enlarge our scanty knowledge on the structure of bivalve faeces and to suggest possible biological interpretations of the 307

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characteristic form of these in relation to feeding habits, modes of life and to the structure and function of the digestive organs. Finally, it was hoped t o clarify the relations of faecal characters and rate of faecal discharge to different environmental factors and to speculate on the evolutionary trends among bivalve groups with regard to the faecal pellets.

Historical: The earliest detailed description of faecal pellets in any species of the Bivalvia was given by Dodgson (1928) for Mytilus edulis L. and the accepted term, “ pseudo-faeces ” originated with him. This was followed three years later by a series of papers on British molluscan faeces by Moore (1931, 1931a and 1931b) who gave elaborate descriptions of the pellets in nineteen bivalve species and emphasized the systematic value of a knowledge of molluscan faeces. Subsequently, he became concerned with its practical aspects in marine geology and indicated the importance of the presence of pellets in marine sediments (Moore, 1933 and 1939). Somewhat briefer descriptions of the pellets appeared in the work of Edge (1934) on thirty-eight Californian invertebrates including eight bivalves, which was planned with a view to possible use in palaeoecology. Schafer ( 1953) noticed the palaeoecological importance of the fossil faecal pellets as facies-index and discussed this possibility in detail for various examples. Moore and Kruse (1956) assembled scattered reports published up to that time into a review of “ present ” knowledge of faecal pellets. Manning and Kumpf (1959) included in their preliminary report on the faecal pellets of the marine invertebrates from South Florida, descriptions of those of thirteen bivalves. The more recent work of Arakawa (1963 and 1965) on faecal pellets from Japanese molluscs has embodied descriptions of those in twenty bivalves. Haven and Morales-Alamo (1965, 1966 and 1966a) attempted a detailed quantitative investigation into seasonal rates of faecal and pseudofaecal production in oysters and other invertebrate filter feeders in relation to ecological conditions, and the terms “ biodeposit ” and b ~ o d e p o ~ ~”t ~originated on with these authors. Previous to this, the pioneer work on this line had been carried out by It0 and Imai (1955) who pursued studies on biodeposition in oyster culture beds. Ota (1959, 1959a, 1959b, 1959c) and Ota and Fukushima (1961) also made an extensive survey on the same subject in pearl oyster culture beds. A somewhat comprehensive review dealing with pellets in all molluscan classes was made by Arakawa (1962). This was followed immediately by interesting work by Kornicker (1962) on evolutionary trends in molluscan faecal pellets. Scattered reports on pellets in various bivalves were given by Winckworth (1931), Popham (1939), Galtsoff

309

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(1964), etc. The results of all these studies will be discussed in relevant sections of the present work.

Acknowledgements: The writer wishes t o extend special acknowledgements t o Professor Akihiko Inaba and Professor Ryozo Yagiu, Hiroshima University, without whose constant guidance and encouragement this project would have been impossible. Thanks are also due to Sir Maurice Yonge, Department of Zoology, University of Glasgow, for editing the original typescript as well as for fruitful discussion during his short stay in Hiroshima. Besides, the writer was much indebted to the following gentlemen who generously offered him useful facilities and aids in various ways in carrying out the present work: Dr. Iwao Taki, Dr. Toshijiro Kawamura, Dr. Takashi Tokioka, Dr. Poshimitsu Ogasawara, Dr. Huzio Utinomi, Dr. Masuoki Horikoshi, Dr. Takashi Okutani, Dr. Taiji Kikuchi, Mr. Akio Taki, Dr. Shigeru Ota, Mrs. Sayoko Sada, Mrs. Setsuko Kawashima and the late Dr. Isao Taki. 11. MATERIALAND TECHNIQUES The faecal pellets of bivalves were easily collected by keeping freshly caught animals in glass vessels containing clean water for a few hours. The first shed pellets were picked out as typical. Each animal was usually kept in a separate vessel t o prevent confusion of samples and to ascertain the effect of possible individual variation. Careful handling makes it possible to extract nearly complete pellets from the rectum of dead and preserved animals with the aid of a needle under a dissecting binocular. For the transport of very delicate pellets, such as those of Mytilus, they should be set in gelatine. Moore (1931a, p. 360) briefly suggested how to collect and examine the pellets as follows

“The pellets have been examined both by collecting those shed by animals while under observation, and also by clearing the rectum in oil, or . . . by embedding the rectum in paraffin wax and sectioning it.” Further, he described in detail the procedure for preparation of sections, his technique being original (Moore, 1931, p. 282 and 1932, p. 236). Manning and Kumpf (1959, p. 292) recommended the use of a solidified non-nutrient agar-agar medium for the preparation of sections of pellets. The material provided in this way was examined either fresh or preserved in 5% formalin. Examinations were carried out under a dissecting binocular or monocular microscope using a low-power objective. Drawings were made with a camera lucida and measurements by means of an eye-piece micrometer. Closer examinations of the structure of the pellets and of the post-intestine of the animals were made, based A.P.H.-~

11

310

IiOHMAN Y , ARAIiAWA

on the histological preparations of sections mounted by the usual techniques ; after fixation in Bouin’s solution, 10 p sections were cut and stained with Delafield’s haematoxylin and eosin. Listed in Table I1 (p. 370) are the scientific name, pellet-type, size and locality of the animals from which the faecal pellets have been collect,ed.

111. MORPHOLOGY A. ClassiJication of faecal pellets The faecal pellets in the Bivalvia can be divided into various types according to structure and form (see Figs. 1 and 2), and attempts at classification have been made by several workers. The first attempt was made by Moore (1931) who roughly divided them into four types, (1) oval pellets, (2) ribbon pellets, (3) triangular and trefoil section rods, and (4) coiled rods. Moore and Kruse (1956) amended this as follows : (1) ovoid or ellipsoid, (2) ellipsoid to rod-like, (3) rod with external longitudinal sculpture, (4) rod with longitudinal and transverse sculpture, and ( 5 ) ribbon-like. A more systematic attempt was made by Arakawa (1962) who divided the faecal pellets into three large categories, oval, rod and ribbon, and then subdivided them under the fourteen types according to shape, subovoid, segmental, rosarioid, orthocylindric, trigonal, spiral, pentafoliate, septemfoliate, multifoliate, trifoliate, bicrescentic, chevron-shaped, plano-concave and bi-cricoid. The number of observed types of pellets has increased remarkably since then, and not all fit within the previous schemes of classification. A thoroughly revised classification and a definition of pellet-types within the Bivalvia are therefore provided, covering over one hundred and sixty-four representatives of forty-five families in five orders concerned. These are summarized in Table I. B. DeJinition of pellet-typps

I. OVAL The following four pellet-types included under this class commonly occur in Gastropempta (classification of Purchon, 1963). Each of these types is distinguishable from the other according to shape, sculpture and ratio of length to breadth of pellets. Pellet-type 1. Ovoid This type of pellet is possibly produced by seven families in the Gastropempta, namely the Tellinidae (Fabulina, Semelangulus, Psam-

r"? ..;....... .

.. : ..::.. .. ,

1

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P

. . ... ~

b

Fig. 1. Illustrating the technical terms denoting various parts of bivalve faecal pellets. 1. Ribbon-like faeces: ac, accessory lateral longitudinal groove, lateral groove, extra longitudinal groove ; b, bi-cricoidal (section) ; bi, bi-crescentic (section) ; lw, lateral wing, lateral region, lateral longitudinal flange; llw, left lateral wing; mdr, mid-dorsal ridge or rib, dorsal ridge, mid-dorsal thickening ; mvg, mid-ventral groove, median longitudinal groove; rlw, right lateral wing; u, upcurled (edge), upturned (edge) ; t , thickened (edge). 2. Rod-like faeces : c, coarse (texture) ; co, constriction, constricted (rod) ; dg, dorso-lateral groove, lateral groove ; dr, dorso-lateral ridge or rib : f, fine (texture) ; h, homogeneity (of material), homogeneous (texture) ; llr, left lateral ridge or rib ; rlg, right lateral groove,: 1, localization (of material), segregation : sg, spiral groove, c*oiletlgroove ; vg, ventro-lateral groove ; vr, ventro-lat,eral rialge or rib. 3. Oval pellets : l), boss; f, flattened (end); p, pointed (ontl) ; r, ronndutl (end); s, sogmenttd (rod), segment, segmentation ; st, spiral striae, spiral striation.

312

KOHMAN P.ARAKAWA

TABLEI. CLASSIFICATION OF TYPESOF BIVALVE FAECAL PELLETS ACCORDING TO SITAPE (see Fig. 2) 1. Ovoid

I. OVAL

1

{

a. Discoid 2 . Ellipsoid

IA

.

i

Mesodesmatidae (C'aecella),Cardiidae (Triguniocardia), Tc.11inidac, Psammobiidac (Gari), Lucinidae,Unguilinidae,Xylophaginidae (Xylophaga) Tellinidae (Macomu),Pholadic'ae (Burma),Semelidae (Abrina) Psammobiidae (Soletellina), Mactridae (Mactra, Raeta), Semclidae (Ahra, Theora), Galeommidae (Scintilla), Erycinida,e (Lasaea)

11. ROD

ITA.

TTI. RIBBON a. Grooved ribbon

1 1 . Pellet of indeterminate shape a. Disjointed particlrs

Pinnidae, Glycymeridae, Carditidae, (?Spondylidae), Unionidae, Anomiidae ( Anomia) Mytilidae, Ostreidae, Isognomonidae, Pectinidae (Delectopccfen) (Cardiomyu, The SEPTIBRANCHIA Plectodon) Galeommidar (Phlyctaenachlamys)

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUTSCA)

313

macoma etc.), Psammobiidae (Gari),Ungulinidae (Joannisiella),Mesodesmatidae (Caecella), Cardiidae (Trigonocardia) and Xylophaginidae (Xylophaga). The shape is oval and rounded in section. Both ends are normally rounded or occasionally flattened. The surface is unsculptured, homogeneous and very resistant. The ratio of length to breadth of pellets usually ranges within the limits of 1.0 to 2.0. Pellet-type la. Discoid This type of pellet is probably produced by Macoma (Tellinidae), Barnen (Pholadidae) and Abrina (Semelidae). The shape is discoidal 1

la

80

3 9

9a

5

10

6

7

II

7a

7b Fig. 2 . Schematic representation of various typw of bivalve faecal pelletn. For numbering see Table T.

314

KOHNAN Y . ARAKAWA

and the pellet consists of compacted detritus. The ends are usually flattened and, a t times, may have a small boss a t the centre. The superficial consistency is fine and homogeneous. The ratio of length to breadth of the pellets is usually smaller than 1.0. Pellet-type 2. Ellipsoid Pellet-type 2 occurs in two families of Gastrotetartika ; Galeommatidae (Scintilla)and Erycinidae (Lasaea),as well as in three families of Gastropempta ; Semelidae (Abra and Theora), Mactridae (Mactra) and Psammobiidae (Soletellina). This type of pellet is elongate elliptic in shape. The surface is normally unsculptured but occasionally feebly marked with a spiral striation (Mactra)or with segmentation (Scintilla). The ratio of length to breadth of pellets is usually greater than 2.0. IA. OVAL-ROD Pellet-type 3. Constricted rod This type of pellet is produced by four families of Gastropempts, namely the Cardiidae (Cardium, Fulvia and Laevicardium), Solenidae (Solen), Veneridae (Protothasa) and Mactridae (Schizothaerus and Tressus). It can be distinguished by the rod-like form with a definite linear segmentation. This type of pellet varies considerably in shape, even in the pellets shed by the same animal in a short time ; they are normally produced in the form of a rod marked with deep transverse constrictions a t regular intervals or occasionally secondarily separated into ovoid pieces with truncate ends. They may have a single spiral striation as in the case of Schixothaerus (Mactridae). Starvation tends to produce the softer and more evenly surfaced continuous rod.

11. ROD This category comprehends five distinct types and three varieties, each of which can be distinguished structurally according t o the number, position and course of the grooves on the surface. It occurs in all of the Protobranchia, some of the Gastrotetartika and Gastropempta. Pellet-type 4. Plain rod This type of pellet shows the simplest structure, being a plain rod rounded in section. It is probably produced by two families of Gastrotriteia (Limopsidae and Spondylidae), five of Gastrotetartika (Chamidae, Laternulidae, Thraciidae, Lyonsiidae and Donaciidae) and six of Gastropempta (Veneridae, Tridacnidae, Petricolidae, Corbiculidae, Novaculidae and Corbulidae).

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315

Pellet-type 5. Rod with a coiled groove Moore (1931a) examined this type of pellet in two families of Gastropempta, Myidae ( M y a truncata) and Pholadidae (Pholadidea loscombiana). The faecal rod is here marked with a dextrally coiled groove unlike those of Tectura and other gastropod species where the coiling is sinistral. Pellet-type 6. Rod with a longitudinal groove This type of pellet is known to occur in some of the Protobranchia (Nuculanidae). It is characterized by bearing one longitudinal groove which may be produced by a major typhlosole in the post-intestine. Pellet-type 7. Rod with jive longitudinal grooves This type can be distinguished by its 5-lobed section, but in addition, the following two forms ( a and b) are peculiar to the Nuculidae (Protobranchia). All consist of a grooved rod of compact detritus. Moore (1933) examined the pellets of NuczLla and noted that there is a significant distinction in position and depth of the grooves between different species within the genus. Pellet-type 7a. Rod with seven longitudinal grooves This type of pellet is characterized by having seven longitudinal grooves and there is a specific difference in both position and depth of the external grooves between different species. Pellet-type 7 b . Rod with nine longitudinal grooves This type of pellet is distinguishable from the preceding two by possessing additional longitudinal grooves. Pellet-type 8. Rodlet wound into a ball This type of pellet consists of a ball which is composed of filiforrn rodlets mixed with a large amount of viscous substance. It is possibly produced by the Amusiidae (Amusium) and some of the Pectinidae (Pecten) (Gastrotetartika). Pellet-type 8a. Rodlet wound into a rod This type of pellet consists of a rod loosely packed by filiform rodlets with a large amount of flocculent material. At times, the constituent rodlets are coiled in regular pattern. It is probably produced by many of the Limidae (Gastrotetartika).

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ICOHMAN Y. ARAICAWA

IIA.

ROD-RIBBON

Pellet-type 9. Rod with a trefoil-shaped section The pellets belonging to this type consist of a rod which is trilobed in section. Of the three longitudinal ridges, the median one is fine in texture with the surface occasionally broken by transverse clefts, while the other two have a smooth but rather coarse surface. The depth and position of the exterior grooves vary according to species. This type of pellet is peculiar to species of Chlamys in the Pectinidae (Gastrotetartika). Pellet-type 9a. Rod with a triangular section Moore (1931a) examined pellet-type 9a in Chlamys triradiata (Muller) (erroneously described as Pecten septemradiatus) and noted that this type of pellet consists of a triangular-sectioned rod with rounded margins, one being sharper than the other two, and with slightly concave sides. 111. RIBBON Ribbon-like pellets are probably defecated by all of the Gastrotriteia and some of the Gastrotetartika, and can be classed under two distinct types according t o whether or not they are grooved. On the whole, ribbon-like pellets are morphologically unstable, because the form of the post-intestinal lumen tends to be affected by the dietetic or physiological conditions of the animal. Pellet-type 10. Ungrooved ribbon This type of faecal ribbon is normally slightly curved and crescentic in section and may be produced by a wide major intestinal typhlosole. Pellet-type 10 probably occurs in nearly all of the Gastrotriteia and some of Gastrotetartika, namely Arcidae, Pteriidae, Glycymeridae, Pinnidae, Plicatulidae, Unionidae, Carditidae, Anomiidae and ZSpondylidae. Pellet-type 10a. Grooved ribbon This type of pellet possibly occurs in four families of the Gastrotriteia, namely Mytilidae, Ostreidae, Isognomonidae and some of the Pectinidae. It can be distinguished from the preceding type by being longitudinally grooved and ridged. The cross-section is usually bicrescentic, two lateral wings rolling up dorsal-wards. This type of pellet comprises several varieties : in Musculus marmoratus, the ribbons have accessory lateral grooves on either side of the mid-ventral one

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

317

(Moore, 1931) ; and in Brachiodontes citrinus they have a median longitudinal groove on both surfaces (Manning and Kumpf, 1959). There is some localization of the contents ; coarse material is concentrated in the centre, with finer material marginally. Pellet-type 11. Pellet of indeterminate shape This type of pellet is probably common to all of the carnivorous septibranchs. It has very soft and loose consistency, thus being of a flocculent and irregular shape which may be associated with the microcarnivorous habit peculiar to this order, Pellet-type 1la. Disjointed particles This type of faeces is reported to occur in Phlyctaenachlamys lysiosquillina, a commensal member of the Erycinacea (Gastrotetartika), by Popham ( 1939).

C. Descriptions of faecal pellets I. PROTOBRANCHIA (GASTROPROTEIA) Moore (1931 and 1933) has studied the faeces in Nucula (Nuculidae) in detail and has figured those of Nuculana (Nuculanidae). With few exceptions, the pellets of the members of this order consist of grooved rods (Pellet-types 6, 7, 7a and 7 b ) . They are shed as a long rod of compact detritus with longitudinal grooves characteristic in number, position and depth for different species. Nuculidae According to Moore (1931), the nuculids pass faecal pellets unlike those of other bivalves. They are characterized by the possession of a series of longitudinal grooves (Fig. 3). This may be due to a peculiar

1

-

A B C D E Fig. 3. Cross-sections of sculptured faecal rods of the genera, Nuculana and Nucula; A. Nuculana minuta; B. Nucula m o o r e i ; C. N . t u r g i d a ; D. N . e u l c a t a ; E. N . n u c l e u s (after Moore, 1931, 1933 and 1939).

internal structure of the gut which has thickened longitudinal ridges with long cilia, varying in position and in number from five to seven or to nine according to the species (Pellet-types 7, 7a and 7 b ) .

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KOHMAN T. ARAKAWA

1. Nucula hanleyi Winckworth “ Seven longitudinal ridges as in N . nitida, but more prominent and with the grooves more deeply cut . . . sometimes more deeply than shown in the figure and even so much so as t o allow the ridges to be split off separately.” (Moore, 1931a, p. 361.) (Pellet-type 11-7a.) Remarks: The pellets of this species have been described by Moore (1931a) under the name of N . radiata Forbes and Hanley. 2. N . moorei Winckworth (Fig. 313)

‘‘ Only five longitudinal ridges, but they are of the nitida type, with the lateral and ventro-lateral ridges fused t o form one broad ridge ; the grooves are shallow and the ventral ridge slightly sunk as in N . nitida.” (Moore, 1931a, p. 361, Fig. 412.) (Pellet-type 11-7.) Remarks: The pellets of this species have been described by Moore (1931a) under the name of N . nitida var. radiata Marshall. 3. N . nucleus (LinnB) (Fig. 3 ~ ) “ Seven longitudinal ridges as in N . nitida, but more prominent and with the grooves more deeply cut . . . sometimes more deeply than shown in the figure and even so much so as to allow the ridges t o be split off separately.” (Moore, 1931a, p. 361, Fig. 3 and Fig. 4 D and F.) (Pellet-type 11-7a.)

4. N . sulcata Bronn (Fig. 3n) “ Nine longitudinal ridges, separated by grooves of medium depth ; the ventral ridge deeply sunk as in Nucula nucleus.” (Moore, 1931a, p. 362, Fig. 4E.) (Pellet-type 11-7b.) 5 . N . tenuis (Montagu)

‘‘ Five very prominent equal longitudinal ridges : all the grooves are deeply cut, and the ventral pair are the most open.’’ (Moore, 1931a, p. 361, Fig. 4A.) (Pellet-type 11-7.) 6. N . turgida Leckenby and Marshall (Fig. 3 ~ ) “ Seven longitudinal ridges, the ventral one being smaller and sunk between the two on either side ; none of the grooves are deeply cut, and in a rubbed or dirty pellet they may appear to be absent.” (Moore, 1931a, p. 361, Fig. 4B.) (Pellet-type 11-7a.) Remarks: The pellets of this species have been described by Moore (1931a) under the name of N . nitida Forbes and Hanley.

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7 . Nucula sp.

“ A second and iiwre complexly sc.ull)t,ured type of rod-shaped pellet was found abundantly a t St. WS 144, and consisted of a rod up to 0.16 mm in diameter with a series of longitudinal grooves on the surface. I n transverse section (Fig. lb) this also appeared to be formed almost entirely from diatom remains and may also therefore be classed as a probable selective feeder. So few pellets have as yet been described that it would be unreasonable to attempt to identify a n unknown pellet with any given animal without a considerable knowledge of the fauna of the locality. But this pellet in all respects resembles those at present known for the genus Nucula, and it is at least reasonable to advance the possibility of its belonging t o this genus.” (Moore, 1933, p. 23, Fig. lb.) (Pellet-type 11-7.) Nuculanidae Faecal pellets produced by the members of this family which have so far been studied are in the form of a rod with a single longitudinal groove (Pellet-type 6). They are extremely fine in surface-texture. 8. Nuculana minuta (Muller) (wig. 3A)

Moore (1939) has figured the pellet of this species by the name of Leda minuta and has noted that the pellet is rod-shaped with a single longitudinal groove (Pellet-type 11-6). 9. Portlandia (Portlandella)japonica (Adams and Reeve) Pellets are rod-shaped with a narrow shallow longitudinal groove, very fine and homogeneous in surface-texture and fulvous brown in colour (Pellet-type 11-6).

Locality : Suruga Bay (80 m in depth) and Sagami Bay (90 m in depth), Japan. Measurements: For an animal with shell 12.0 mm long the faecal rods average 0.26 mm in breadth and for one with shell 19.0 mm long, 0-40 mm. 10. Portlandiella beringii (Dall) (Fig. 5 ~ )

Faecal rods bear a single longitudinal sculpture. They are very fine in texture and greyish-green in colour. They are cut into by numerous fine cracks (Pellet-type 11-6). Locality : Off Kinkazan, Japan.

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Measurements : For an animal with shell 35-0 mm long the rods average 0-70 mm in breadth, and for one 23.0 mm long 0.50 mm. 11. Saccella sematensis Suzuki and Ishizuka (Fig. 5 ~ )

Faecal rods have a single wide longitudinal groove. They are very fine and homogeneous in texture and greyish-green in colour. At times, they are chapped by occasional clefts (Pellet-type 11-6). Locality : Suruga Bay (80 m in depth), Japan. Measurements : Breadth of the faecal rods shed by an animal of shell length 10.5 mm is 0.24 mm on the average. 11. SEPTIBRANCHIA (GASTRODEUTEIA) Faecal pellets in this order were examined for only two representatives belonging to the Cuspidariidae, which are quite indefinable in shape and may be assigned to Pellet-type 11. Purchon (1958 and 1959) has suggested the Septibranchia be placed near to the Protobranchia because of certain similarities between the stomachs of these two groups. But it appears impossible to support his views from a study of the faecal pellets". Cuspidariidae 12. Cardiomya gouldiana septemtrionalis (Kuroda) (Pl. 1-1) 13. Plectodon ligula (Yokoyama) (Pl. 1-2)

Pellets of these two species are similar in nature and appearance. They are flocculent and blurred in outline, coarse and rather frail in consistency and translucent. They are normally made up of a jelly-like substance with admixtures with broken pieces of carcasses, spicules and other undigested skeletal matter which may possibly be of copepod origin (Pellet-type 11). Locality : Chijiwa Bay, off Tomioka, Kumamoto, Japan. Measurements : For a specimen of C. gouldiana septemtrionalis with shell 8.0 mm long, average breadth is 0.62 mm, and for one of P. ligula with shell 5.0 mm long it is 0.07 mm.

111. GASTROTRITEIA Except for the Limopsidae, the representatives of this order may defecate ribbon-type pellets which belong either t o Pellet-type 10 or * The description of Hulicardia nipponensis by Nakazima (1967) indicat,es that septibranchs are specialized eulamellibranchs. (Editorial note-C.M.Y.)

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to 10a according to whether the surface grooves are present or not. More than 60% of the representatives have pellets of the latter type. Arcidae Almost all the representatives of the Arcidae, so far as is known, produce ungrooved ribbons (Pellet-type 10). 14. Arca umbonata Lamarck " 1 animal. This specimen, 42.0 mm in length, produced a wide, slightly curved ribbon 0-43 mm in width and 0.05 mm thick. The ribbon was smooth in consistency and broken into pieces varying in length from 0.2 to 0.6 mm." (Manning and Kumpf, 1959, p. 299, Figs. lb, 4f.) (Pellet-type 111-10.) 15. Anadara (Scapharca) subcrenata (Lischke) (Pl. 4 (no. 37), Fig. 4 (top), Fig. 18, p. 401). " The faecal pellets of this species are ribbon-shaped, without any external sculptures, and usually shed broken to short pieces. Both lateral edges of the pellet are thickened and slightly turn dorsal-wards, while the central area is much thinner and the dorsal side is moderately concave; thus the general appearance of faeces assumes a form of

Fig. 4. Cross-sections of the ribbon-like pellets in some filibranchs. Top : Anadara subcrenata (orig.) ; centre : Mytilus galloprovincialis (orig.); bottom : Musculus marmoratus (after Moore, 1931).

gutter. m they are light yellowish-brown in colour, rather coarse in texture and soft and very frail in consistency. The faeces are made of rather fine materials mixed with diatom frustules and some unidentified larger particles. For an examined animal, the width of ribbons fluctuates in

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the range 0 . 7 3 mm-1-00 mm.” Fig. 41 .) (Pellet-type 111- 10).

(Arakawa, 1965, pp. 14-15, P1. I V ,

16. A . ltroughtoni (Schreack) ( P I . 1-4)

Faecal ribbons of this and the above species are so much alike that it is impossible t o draw a sharp distinction between them. They are ribbon-shaped with no external sculptures. Both edges are thickened and slightly upturned. There is a localization of materials ; the coarse matter concentrates towards the centre and the finer particles lie in the lateral regions (Pellet-type 111-10). Locality : Himeji, Hyogo, Japan. Measurements : For an animal with shell 85-0 mm long, the ribbons are 3.5 mm in average width. 17. Striarca (Didimacar) symmetrica (Reeve) (Pl. 5-53)

The pellets of this species are very similar in type to those of Area and Anadara. They have no grooves and ridges. They are light greyish-yellow in colour and rather coarse in texture (Pellet-type 111-10). Locality : Mukaishima, Hiroshima, Japan. Measurements : The ribbons shed by an animal with a shell 9.0 mm long are 0.26 mm in average width. 18. Barbatia (Xavignyarca) virescens (Rve)

The ribbons are normally ungrooved, but occasionally may possess a shallow mid-ventral groove. On the other side, they are slightly raised along the median line to form a low mid-dorsal ridge. Both edges are turned dorsal-wards and the section is bi-crescentic (Pellet-type 111-10 ( I l O a ) ) . Locality : Tomioka, Kumamoto, Japan. Measurements: For an animal with shell 23.0 mm long, the average width of the ribbons is 0.84 mm. 19. B.

(8.) v. obtusoides (Nyst) (Pl. 1-3 and P1. 4-36)

“ The pellets are ribbon-shaped, about 0.73 mm in width. There are no prominent surface sculptures, but five or six obscure longitudinal striae on each side. They are soft and fragile in consistency and somewhat coarse in texture. The pellets are loosely packed with fairly coarse materials.” (Arakawa, 1965, p. 15, P1. IV, Figs. 40, 46.) (Pellettype 111-10).

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Remarks: Above description may be based on some atypical specimens. Glycy meridae The general plan of the faecal ribbons of this family shows a close resemblance to that of the Arcidae (Pellet-type 111-10).

20. Glycymeris imperialis Kuroda (Fig. 5D) This species passes unsculptured faecal ribbons crescentic in section. They are thin at the centre, while thickened at both edges. They are rather coarse in texture and greyish-chocolate in colour. Sometimes they are cut by fine occasional clefts (Pellet-type 111-10). Locality : Suruga Bay (80 m in depth), Japan. Measurements: For an animal with shell 21.0 mm long, the average width of the faecal ribbons is 0-47 mm, and for one with shell 21.5 mm long it is 0.44 mm. 21. G. rotunda (Dunker)

Pellets are ribbon-shaped without surface sculptures. They are fine in texture and cream yellow in colour (Pellet-type 111-10). Locality : Sagami Bay (87-95 m in depth), Japan. Measurements: Width of faecal ribbons shed by an animal with shell 29.5 mm long is 0.50 mm on average. Limopsidae This family presents a striking contrast in pellet-characters to other families of this order. The pellets of the members of this family so far studied belong to Pellet-type 11-4.

22. Oblimopa forskalii (A. Adams) Faecal pellets of this species consist of an ungrooved cylindrical rod with soft and frail consistency (Pellet-type 11-4). Locality : Chijiwa Bay, off Tomioka, Kumamoto, Japan. Measurements: Faecal rods voided by an animal with 9.5 mm long shells are 0.18 mm in average breadth. 23. ?Limopsis tajirnae Sowerby (Fig. 5c)

Faecal rods of this species are somewhat irregular in shape. They

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are greyish-green in colour and very coarse and soft in consistency. They are cut by numerous transverse clefts (Pellet-type 11-4). Locality : Japan Trench (1 280 m in depth). Measurements : For an animal with shell 23.0 mm long, the breadth of the faecal rods averages 0.20 mm, and for one with shell 30.5 mm long, 0.38 mm. Mytilidae

Almost all the representatives of this family from which faecal pellets have so far been examined produce sculptured ribbons which are referable to Pellet-type 10a. 24. Mytilus californianus Conrad “ I n cross-section, the ribbon-like faeces of the oyster and mussel showed marked longitudinal grooves and ridges.” (Edge, 1934, p. 80, Fig. 2.) (Pellet-type I I I - l 0 a ) .

25. M . coruscus Gould “ The faecal pellets are in the form of a ribbon with two free edges rolled gently upwards t o bear a crescent section and without any external sculptures. They are so delicate that they are usually voided broken into much shorter pieces. They are brownish green in colour and fine and homogeneous in surface texture. For an animal with shell 4.55 cm long, the ribbons average 0.54 mm in width.” (Arakawa, 1963, p. 205, Text-figs. 6 A-B.) (Pellet-type III-IOU).

26. M . galloprovincialis Lam. (Fig. 4 centre)

Ribbons of this species are very similar in nature and form to those of M . edulis (Pellet-type I I I - l 0 a ) . Locality : Ondo, Hiroshima, Japan. Measurements: Ribbons shed by an animal in the shell 75-0 mm long average 1.3 mm in width. 27. M . edulis L. “ The faeces are discharged through the exhalant siphon. They are in the form of a ribbon having characteristic longitudinal folds. . . . The actual width would be from ca 1.5 mm t o ca 0.75 mm. Ribbons of 2 mm or even wider are sometimes seen. The characteristic folds are determined by the shape of the anus through which the soft mass is propelled. This opening is more or less similar in shape to that of a

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cross-section of the lumen of the rectum, which is bi-crescentic, owing to the presence of a double longitudinal ridge, or typhlosole. The ribbons run to a knife-edge, of varying acuteness, a t the margins, which are usually folded over, either inwards or outwards. I n the ribbon of faeces from which the drawings were made, one edge is folded inwards and one outwards. (In turning over the specimen, it has been turned both laterally and longitudinally.) This type of folding is seen very frequently, and may even be more common than a folding inwards of both margins. The central sulcus (seen from above) may be somewhat indefinite a t times. The characteristic shape of the ribbon is easily seen with the naked eye, though a hand lens is useful for observing broken fragments, etc. The consistency of the faeces is finely granular, the surfaces of the ribbon being smooth. The colour, being determined by that of the suspended matter ingested, varies considerably, but is usually a dark chocolate brown, or more rarely slate. Sometimes the faeces are almost white. Such white faeces have been noted almost every spring in the tanks, for a period of a few days to a week. It has been found due to the ingestion of a certain flagellate protophyte, which appears in great numbers for periods such as those indicated, causing a thick yellowish-white scum on the water, disappearing again as quickly as it came.” (Dodgson, 1928, pp. 161-162, P1. 1, Figs. 3-7.) “ The pellet is in the form of a ribbon, thickest a t the centre and the two edges, and with these two edges rolled upwards and inwards towards one another. The exact shape of the pellets seems t o vary somewhat, and in the case of a starved animal they may be thinner and of abnormal shape. The ribbon is formed from fine detritus, with the finest material in the lateral regions where it is closely packed, while the coarser material lies in the central region and is looser. The ribbon is thickened in the centre, and raised to form a mid-dorsal rib, and lying under this on the ventral side is a wide shallow mid-ventral groove, although the latter may sometimes be reduced or altogether absent. The pellet together with certain modifications of it has been described by Dodgson (1928). The faeces are fragile and easily damaged, but the undistorted ribbon from an animal 8 cm long would average 1.5 mm in diameter, and may occur in lengths of 5 cm or more, tholrgh usually breaking into much shorter pieces.” (Moore, 1931, p. 283, PI. 31. Figs. 7, 8.) (Pellet-type 111-IOU). 28. Modiolus modiolus (L.) “ The faeces are in the form of a ribbon of the same general type as those of Mytilus, but with the mid-ventral groove much more pronounced : so much so, in fact, that the whole ribbon usually assumes t’he

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shape of an inverted ‘ V’ in section. There is a slight mid-dorsal thickening corresponding to the mid-dorsal ridge of Mytilus, and the lateral regions are thickened as in that species, but here the edges are very much narrower and are not turned up. The ribbon is formed from similar fine detritus, but there is no such localization of materials, and it appears homogeneous in transverse section. From an animal 10 cm long, the ribbon averages 2.0 mm in diameter, and is often in lengths of two or more centimetres.” (Moore, 1931, p. 283, PI. 31, Pigs. 1 1 , 12,) (Pellet-type III-lOa.) 29. M . phuseolinus (Phi1ipp)i “ The pellet is somewhat intermediate in form between those of the previous two species (Mytilus edulis and Modiolus modiolus). The mid-ventral groove is much smaller than in M . modiolus, and though sometimes deep, it is always narrow, and may even be completely closed ; also in this species the mid-dorsal ridge is a wide thickened area of the ribbon. The lateral regions are relatively longer than those of M . modiolus, though not so long as those of Mytilus, and are thickened at the edges, The pellet is composed of fine detritus, but unlike that of M . modiolus, there is here a sorting of the finer material to the lateral regions of the ribbon, and of the coarser materials to the centre. The ribbons may be several centimetres long, but when the animal is feeding normally they usually break into very short lengths.” (Moore, 1931, p. 283, PI. 31, Figs. 1 1 , 12.) (Pellet-type 111-lOa).

30. M . ugripetus (Iredale) (PI. 5-54)

Ribbons are usually shed broken into short lengths (1.0-1.5 times as long as wide). A low and broad median rib lies on the dorsal side, while orl the other side is a shallow and indistinctive mid-ventral groove. They are very fine in texture, rather stiff in consistency and brownish-grey in colour (Pellet-type III-l0u). Locality : Mukaishima, Hiroshima, Japan. Measurements: For an animal with 11 mm long shell, the ribbons average 0.31 mm in width. 31. M . nipponicus (Oyama) (Pl. 1-5)

Pellets are ribbon-shaped with a bi-crescentic section. The free edges of the ribbons slightly turn dorsalwards. There is a low median rib on the dorsal side and on the opposite side to this, a shallow and narrow longitudinal groove (Pellet-type III-l0a).

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Locality : Tornioka, Kurnamoto, Japan. Measurements : Width of t h e ribbons fluctuates between 0.46 and 0.51 mm, for an animal with shell of length 21 mm. 32. M . Jlavidus (Dkr)

Pellets are ungrooved and ribbon-shaped with coarse texture. They are crescentic in section and greenish-brown in colour. They are usually voided broken into short pieces (Pellet-type III-lOa ( ?10)). Locality : Tomioka, Kumamoto, Japan. Measurements: Pellets shed by an animal with shell 15 mm long average 0.22 mm in width. 33. M . plumescens (Dkr)

This species defecates pellets that are very similar in type to those of the preceding one (Pellet-type III-lOa). Locality : Mukaishima, Hiroshima, Japan. Measurements : Average width of the ribbons is 0.5 mm for an animal of shell length 25.0 mm. 34. Musculus marmoratus (Forbes) (Fig. 4, bottom) “ This pellet also is in the form of a ribbon, bi-crescentic in section, but considerably thicker than that of any of the previous species. There is a wide mid-dorsal ridge, and usually a wide, but not very deep midventral groove, and there may also be lateral grooves on either side of this, but very variable in position and depth. The ribbon is composed of fine detritus, and there is no localization of material in it. From an animal 0.9 em long, the ribbon averages 0.18 mm in diameter.” (Moore, 1931, p. 284, PI. 31, Figs. 13, 14.) (Pellet-type III-l0u).

35. M . (Musculista)japonica (Dkr) (PI. 1-6)

Pellets are ribbon-shaped with a bi-crescentic section, but the external sculpturing is rather indistinct (Pellet-type III- 1 Oa). Locality : Tomioka, Kumamoto, Japan. Measurements : Width of the ribbon discharged by an animal of shell length 13.0 mm averages 0.27 mm. 36. M . ( M . )perfragilis (Dkr) (Pl. 1-7)

I n the faecal ribbons of this species, there is complete absence of external grooves and ribs (Pellet-type III-lOa (?lo)).

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KOHMAN Y. ARAKAWA

Locality : Tomioka, Kumamoto, Japan. Measurements : For an animal with shell 14.5 mm long, average width of the ribbons is 0.13 mm. 37. Brachiodontes citrinus Roding “ 1 animal. An individual 31 mm long produced a ribbon-shaped pellet 0.5 mm wide and 0.15 mm thick. The ribbon was broken into pieces under 1 mm in length. It consists of two lateral longitudinal flanges, a median ridge on one surface. This corresponds quite closely t o the description of the pellets of Mytilus edulis as given by Moore (1931), although these appear t o be intermediate between those of M . edulis and Modiolus phaseolinus. The main difference is the longitudinal groove on both surfaces of the ribbon of Brachiodontes citrinus. However, this extra longitudinal groove was not observed on all of the pieces of the ribbon.” (Manning and Kumpf, 1959, p. 301, Figs. le, 4c.) (Pellettype 111-lOa).

38. Hormomya exustes (L.)

The largest specimen, 11 mm in length, shed a W“ 3 animals. shaped ribbon broken into pieces up to 0.96 mm in length and 0.25 mm in width. The pellet closely resembles that shed by Volsella citrinus. They differ in that the ends taper t o a thin edge and are less recurved, and there is no groove in the centre of the upper side.” (Manning and Kumpf, 1959, p. 301, Figs. lc, 4e.) (Pellet-type 111-lOa). 39. Xeptifer bilocularis (L.) (Pl. 1-8) Faecal ribbons of this species are ungrooved and crescentic in transverse section with both the edges thickened and upcurled (Pellet-type 111-lOa (210)). Locality : Tomioka, Kumamoto, Japan. Measurements: Width of the ribbons voided by an animal with shells 12.0 mm long fluctuates between 0-12 and 0-15 mm. 40. X. bilocularis pilosus (Rve) (Pl. 4-38) “ The present species gives off ribbon-shaped pellets with a bicrescentic section. The dorso-median ridge is small but rather conspicuous. On the contrary, there is a shallow but wide mid-ventral groove on the opposite side. They are greyish-brown in colour, coarse in texture and usually made of somewhat coarse materials. For an animal with shells 2.4 ern long, the width of ribbons is 0-36 mm.” (Arakawa, 1965, p. 15, P1. IV, Figs. 40, 4 6 . ) (Pellet-type 111-lOa).

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41. 8. (Mytilisepta) keenae (Nomura) (PI. I-!)) Pellets of this species are very similar in type to those of the preceding and the following ones. The external sculpture is prominent and the section is bi-crescentic (Pellet-type III-1Oa). Locality : Tomioka, Kumamoto, Japan. Measurements: For animals with 41.0 mm long shells, width of the ribbons fluctuates between 0.71 and 0.75 mm. 42. 8. ( M . ) virgatus (Wiegmann) (Pl. 4-39) " The faeces are ribbon-shaped, and very friable in consistency ; the central portion is thicker than other parts and folded on the side corresponding t o the dorsal side of the alimentary tract t o form a middorsal ridge, and a shallow but wide mid-ventral groove on the opposite side. The free edges slightly turn up dorsalwards so that the ribbon assumes a bi-crescent-shape in cross-section. For an animal 16.5 mm long, the pellets average 0.64 mm in width.'' (Arakawa, 1963, p. 205, Text-Fig. 6, A-B.) (Pellet-type III-loa). 43. Volsella americana Leach " 1 animal. This animal shed pellets which resemble more closely those described by Moore (1931) for M . phaseolinus. The ribbon is thickened laterally and possesses the median longitudinal thickening on one surface and the slight groove opposing it on the other surface. The ribbon was broken into pieces 0-32 t o 0.43 mm." (Manning and Kumpf, 1959, p. 301, Fig. 4g.) (Pellet-type I I I - 1 0 ~ ) .

Isognomonidae (Vulsellidae) Three representatives of this group produce ribbon-like pellets with a median longitudinal groove and with slightly upcurled edges (Pellettype III-1Oa). 44. Isognomon data Gmelin " 1 animal. The faecal matter of this specimen was too flocculent to allow drawings to be made. However, some small portions of a ribbon were observed. Those of the closely related Isognomon radiata are described below." (Manning and Kumpf, 1959, p. 301 .) (Pellet-type III-lOa.)

45. I . radiata Anton " 3 animals. Because of the shape of the animals, only the largest measurement was taken. An animal with a maximum measurement of

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17.5 mm shed small fragments of ribbon-shaped pellets 0.39 mm wide and 0.55 to 0.59 mm long. The edges of the ribbon were highly recurved. On one surface there was a longitudinal ridge ; the other surface was smooth.” (Manning and Kumpf, 1950, I). 301, Figs. If, 4d.) (Pellet-type 111-1Oa).

46. I . legumen (Gmel.) (PI. 1-10)

The faecal ribbons of this and the previous two animals are so much alike in nature and form that it is difficult to draw a clear-cut distinction between them. The ribbons of this species are bi-crescentic in crosssection, coarse and fragile in consistency and greyish-brown in colour (Pellet-type 111-1Oa). Locality : Shirahama, Wakayama, Japan. Measurements : Pellets voided by an examined animal were 0.22 mm in width. Pteriidae (Aviculidae) 47. Pinctada martensii (Dkr) (PI. 4-40) “ The faeces are thin corrugated ribbons with two lateral edges weakly rolled up dorsalwards. As is often the case with ribbon-like faeces, they are fragile and shed broken t o pieces. In cross-section, they are usually crescent ; starved animals seem t o show a tendency t o produce thinner and more delicate ribbons with two lateral edges strongly rolled in to touch each other. The coloration is variable, from greyish-brown t o orange-yellow, according to staple of food taken by the animal. On an average, the width of ribbons is 1-86 mm for an animal with shells 4.92 cm long.” (Arakawa, 1963, p. 206, Text-Fig. 6, D.) (Pellet-type 111-10). Pinnidae Pellets of the members of this family may usually be produced in the form of an ungrooved ribbon with a crescentic section (Pellet-type 111-10). 48. Pinna bicolor Gmel.

Faecal ribbons are thickened at both edges and are raised a t the centre to form a median longitudinal ridge. On the other side of this, there is no surface-sculpture. They are yellowish-grey in colour and coarse in texture. At times, the ribbons may be built up from compacted constituent rodlets (Pellet-type 111-10 ( ? I O U ) ) .

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Locality : Mukaishima, Hiroshima, Japan. Measurements : For an animal with a shell 180 mm high, average width of the faecal ribbons is 2.07 mm. 49. Atrina pectinata japonica (Rve) (Pl. 1-11)

Ribbons of this species are discharged broken into much shorter pieces. They have no grooves and ridges. Both free edges are thickened and strongly turned dorsalwards. The dorsal surface is smooth in contrast to the ventral surface which is rather coarse and uneven (Pellettype 111-10). Locality : Shirahama, Wakayama, Japan. Measurements: Faecal ribbons shed by an animal of shell length 300 mm average 2.5 mm in width. Ostreidae Pellets of members of this family which have so far been examined are, without exception, grooved ribbons bi-crescentic in section (Pellettype 111-l0a). 50. Ostrea edulis L. (PI. 2-12; Fig. 17, bottom, p. 400)

I n the faecal ribbons of this species, the mid-dorsal ridge is large and prominent, and the mid-ventral groove is narrow but very deep. The lateral wings are strongly upcurled. Thus, in transverse section, they are bi-cricoidal rather than bi-crescentic. They are dark chocolate in colour and smooth in surface texture, except over the median longitudinal ridge where the surface is coarse and uneven (Pellet-type 111-10a). Locality : Miyagi Pref, Japan (immigrated from Europe). Measurements : The width of the faecal ribbons fluctuates between 1-46 and 2.28 mm. 51. 0. densebmellosa futamiensis Seki (Pl. 5-55)

Faecal ribbons are very thin, rather coarse in consistency and pale yellowish-brown in colour. They have a thickened mid-dorsal ridge. Both edges of the ribbons are slightly thickened and turned (Pellettype 111-lOa). Locality : Mukaishima, Hiroshima, Japan. Measurements: For an animal with shell 40.0 mm long, width of the ribbons fluctuates between 0.65 and 0.85 mm.

52.

0.lurida Carpenter

l 1 I n cross-section, the ribbon-like faeces of the oyster and mussel showed marked longitudinal gro(o)ves and ridges ; . . . . ” (Edge, 1934, p. 80, Fig. 2 . ) (Pellet-type 111-l0a).

53. Crassostrea gigas (Thunberg) (Pl. 4-41 ; Fig. 17, top, p. 400) “At first sight, this species appears to void typical rod-shaped pellets, but closer examination of cross-sections of pellets shows that they are rather of a modified ribbon type. The ventral side of pellets is smoothly surfaced and unsculptured, while the dorsal side is marked by two deep longitudinal grooves embracing a low narrow longitudiiial ridge in between them. This structure is, however, easily overlooked, as it is wholly covered by well-developed lateral wings of the ribbon. Both edges of the ribbon upcurled over the dorsal side may touch each other and thus the real dorsal side of the pellet is entirely concealed. The pellets are rather stiff in consistency, voided usually in short pieces, and coloured orangy yellow. They are made of undetermined well-digested materials mixed with numerous diatom frustules and other skeletal matter. I n section, there is found a concentration of coarser materials towards the centre. The average diameter of pellets shed by an examined animal is 0.78 mm. “ Remarks : anatomical examination of the alimentary canal of this species demonstrates clearly that the shape of the faecal pellet is determined by the internal structure of the canal. I n P1. VI. Fig. 1, is shown a cross-section of the alimentary canal of a well-fed animal. Here the canal is expanded and roughly rounded in outline, and two prominent typhlosoles applying t o two deep longitudinal grooves on the dorsal side of the pellet are shown distinctly. Then, a cross-section of the canal of a starved animal is shown in Fig. 2 ; now the canal is much more flattened and shows the structure to yield thin ribbonshaped faeces. Finally in Fig. 3, a section of the canal of the animal infected by some parasitic worms is given ; the ventral structure of t’he canal is deformed and the lumen is narrowed tjo produce only flocculent faeces of indefinite shape. Further, a cross-section of the gut of Ostren denselamellosa is presented in Fig. 6 ; this structure is supposed to yield flattened ribbon-shaped pellets with a bi-crescentic section.” (Arakawa, 1965, pp. 16-17, P1. V, Figs. 48-50, P1. VI, Figs. 1-5.) (Pellet-type 111-10a). 54. C . virginiea Gmel. “ The feces of the oyster are voided from the rectum as a compact and slightly flattened ribbon of sufficient consistency to withstand the

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333

velocity of the cloacal current. I n an actively feeding oyster the ribbon is maintained in a horizontal position along the axis of the current, but being heavier than the sea water it sinks down t o the bottom as soon as the cloacal current slows down or ceases. Large masses of fecal ribbons accumulate on the bottom a short distance from the opening of the cloaca. The ribbon remains intact for 2 to 3 days until it is disintegrated through decomposition and mechanical disturbance. The appearance of the fecal masses of the oyster is typical and can be recognized by their shape. It was shown by Moore (1931) that specific identification of fecal pellets can be made for a number of marine invertebrates. Fecal ribbons of oysters contain many live cells-diatoms, dinoflagellates, yeast, and others which are not killed by the gastric and intestinal juices and can be recultured.” (Galtsoff, 1964, p. 228, Figs. 205, 207). “ Freshly deposited oyster feces consist of short green or brown segments from about 1 to 5 mm long. In cross section, they are thickened filaments about 1 mm across with recurved edges and a low median longitudinal ridge. Under certain laboratory conditions, production of fecal ribbons was continuous, but production of short segments was most frequent. Pseudofeces were similar in color but were ejected as clumps loosely aggregated with mucus and occasionally as a continuous string without definite form.” (Haven and Morales-Alamo, 1966, p. 493.) (Pellet-type 111-lOa). 55. Saxostrea echinata (Quoy and Gaimard) (Pl. 4-42)

“Pellets of the present species are ribbon-shaped, and carry a modicum of mucus. Both lateral edges of the ribbon are thickened and slightly turn dorsalwards, and the dorsal side is fairly raised along the median line to form a low dorso-median ridge, while the opposite ventral side is flattened and unsculptured. Pellets are coarse in texture, soft and friable in consistency and dark green in colour. They are formed of rather coarse materials containing numerous larval shells of some lamellibranch. For an animal with shell 5.8 cm long and 2.0 cm wide, ribbons are 1.27 mm in width on an average ” (Arakawa, 1965, p. 17, P1. V, Fig. 47.) (Pellet-type 111-10u.) Spondylidae 56. Spondylus harbatus Rve

This species sheds pellets consisting of a film!: ribbon with no surface sculpturing (Pellet-type ‘1111-10). Locality : Shirahama, Wakayama, Japan.

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KOHMAN Y ARAKAWA

Measurements : Width of ribbon shed by an animal was 0.58 mm Remarks : The material examined may be atypical. 57. 8. candidus Lam. (Fig. 5E)

Pellets are discharged in the form of a rod with an oval section. They are occasionally chapped by transverse clefts. They are soft in consistency, fine in texture and fulvous yellow in colour (Pellet-type 11-4). Locality : Yoron-jima, Amami-ohshima Archipelago, Kagoshima, Japan. Measurements: From an animal with shell 63 mm high, width of the pellets fluctuates between 0-55 and 0.75 mm. Remarks : Cross-sections of rectum show an oval outline.

1v. GASTROTETARTIKA Pellets described here for representatives of fourteen families cover a wide range of types compared with those already described. The pellets range from type 1-1 to 111-10 or Ila exclusive of types IA-3, 11-5, 11-6, 11-7 and its subtypes. I n general, this group displays comprehensive morphological characters of faecal pellets, which include, besides three common rudimentary types (I-2,II-4and 111-lo), several modified forms (11-8, 8a, 11-9, 9a and 1la) which are peculiar to this group. As pointed out by Purchon (1958 and 1959) from the standpoint of his recent survey of the bivalve stomach, this order is also intermediate in general composition of pellet-types between the orders Gastrotriteia and Gastropempta. Plicatulidae 58. Plicatula gihbosa (Lam.) " 1 animal. This individual was 0.7 cm long and produced a ribbon-

shaped pellet that formed a ' W ' in cross-section. Although the ribbon was in fragments, the longitudinal groove was easily seen. The ribbon was 0.3 mm wide." (Manning and Kumpf, 1959, p. 302, Pigs. Id, 4h.) (Pellet-type 111-IOa). Amusiidae The pellets of this family are quite characteristic resembling a small ball of knitting yarn (Pellet-type 11-8).

SCATOLO(:ICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

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B

C

Fig., 5. Faecal pellets of: A. Portlandiella beringii (left, ventral view ; middle, cross-section; right, dorsal view) ; B. Saccella sematensis (left, dorsal view; right, ventral view; below, cross-section): C. ?Limopsis tajimae ; D. Glycymeris imperialis (above, ventral view ; middle, cross-section ; below, dorsal view) ; E. SpondyZu.9 candidus (above, dorsal view ; below, cross-section).

69. Amusium japonica (Gmel.) (Pl. 4-43)

'' Faeces of this species are composed of filamentous cylindric rods loosely entangled and gathered by mucus t o form masses of indefinite

330

K O H M A N Y . ARAKAWA

shape, although it is assumed that the normal faeces are formed much more tightly in the shape of a ball of the size variable with individuals. They are soft and fragile in consistency, usually carrying a large amount

Fig. 6. Fagcal pellets. Loft : Pecten alhicans ; right : Chlamys nohilis. (Photo : Dr. Shigeru Ota, Nansei Regional Fisheries Research Laboratory, Hiroshima, Japan.)

of mucus, and coloured brownish-orange to brownish-green ; the pellet texture is fine and homogeneous in brownish-orange pellets, while it is rather coarse in brownish-green ones. They are made of detrital matter containing numerous unidentified micro-organisms and some small particles. The diameter of rods fluctuates between 0.07 and 0.08 mm, for an animal examined.” (Arakawa, 1965, p. 15, P1. IV, Fig. 43). (Pellet-type 11-8). Pectinidae There is a marked scatological separation among different genera of this family. I n Pecten, the pellets are shed in the form of a continuous rodlet wound into a ball and show a close similarity in general plan to those of Amusium (Pellet-type 11-8); in GhEamys they are discharged in two different types of a grooved rod; and in Palliolum they are defecated in the shape of a grooved ribbon (111-loa). 60. Pecten (Notovola)nlhicans (Schriiter) (Pl. 4-44;Fig. 6, left)

“As in the preceding species, pellets of this species are made of filamentous rods entangled and compacted into a ball by a large amount

SCATOLOCTCAL STUDIES O F THE BIVALVIA (ITOLLTSCA)

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of mucous substance. The balls thus formed by the same animal within a short time vary greatly in size and shape. For an animal with shells 7.7 cm long, the diameter of faecal balls fluctuates in the range 1.8 mm to 2.1 mm and that of constituent rods 0.15 mm t o 0.20 mm.

Fig. 7. Fascal pellets of: A. Chlamys wesiculosus (left, dorsal view ; right, ventral view ; below, cross-section) ; B. PaZZiolum randolphi (above, dorsal view ; below, crosssection).

Remarks : “The general appearance of faecal balls of the present species agrees very closely to that of Pecten maximus (LinnB) described by Moore (1931).” (Arakawa, 1965, p. 16, P1. IV, Fig. 44, Text-Fig. 5 . ) (Pellet-type 11-8). 61. Pecten maximus (L.)

“ A thin, cylindrical rod, wound into a ball, and embedded in a small amount of mucus. The balls may vary greatly in shape. From an animal with a shell 11 cm long, the entire ball may be from 1.5 t o 2.0 mm in diameter, and the constituent rods from 0.15 t o 1.20 mm in diameter.” (Moore, 1931, p. 285, P1. 30, Fig. 5 . ) (Pellet-type 11-8). 62. P. (Evola)ziczac (L.) “ 1 animal. This specimen, 44 mm long, produced only 2 pellets, 0.69 and 1.0 mm long. All of the remainder of the fecal matter was

flocculent. The pellets were yellow in color, slightly granular, homo-

338

KOHMAN Y . ARAKAWA

geneous, and irregular in shape. Moore (1931) observed that all species of this family which he examined shed rod-like pellets having a triangular or trefoil cross-section. The authors feel that those shed by P. ziczac and examined by us were either starvation pellets or were pseudofeces which are given off by all filter-feeding animals.” (Manning and Kumpf, 1959, p. 303.) 63. Chlamys (Cryptopecten) vesiculoides (Dkr) (Fig. 7A)

Pellets are shed in the form of a grooved rod with trilobed section. Of three longitudinal grooves, the ventral one is shallow and wide, while the other two are deep and narrow. I n detailed structure, the pellets consist of two distinctive constituents : the basal part is ribbonshaped with smooth surface and greyish-green in colour, whereas the dorsal part is rod-shaped with uneven surface and dark grey. The coarse materials of food localize in the basal part and finer ones above (Pellet-type IIA-9). Locality : Suruga Bay (80 m deep), Japan. Measurements: Breadth of pellets shed by an animal of shell length 13.5 mm is 0.4 mm.

A

B

C

Fig. 8. Cross-sections of the sculptured faecal rods of the genus Chlamys : A. C. triradiata; B. C . waria; C. C . spuamata. (A. and B. : Redrawn from Moore, 1931 and 1931a.)

64. C. waria (L.) (Fig. 8c)

‘‘ Similar in type to that of C . opercularis, but the ventral groove is usually almost completely flattened, the ventro-lateral ridges wide and comparatively smooth, the dorso-lateral grooves deeply cut, and the dorsal ridge laterally waved.” (Moore, 1931, p. 285, P1. 30, Figs. 3, 6.) (Pellet-type IIA-9). 65. C. Zatiauratus (Conrad) “

The cross-section of the pecta(e)n pellet was trilobed.” (Edge,

1934, p. 80, Fig. 3.) (Pellet-type ITA-9).

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66. C . (Mimachlamys)nobilis (Rve) (Fig. 6, right) This species may defecate pellets that are in the form of a grooved rod with trilobed section. They are usually shed broken into much shorter pieces. The surface of the pellets is normally chapped by numerous occasional clefts (Pellet-type IIA-9). Locality : Kashikojima, Mie, Japan. 67. C. (Aequipecten) opercularis (L.) “ The pellet is in the form of a rod, typically trefoil-shaped in section, and with the dorsal ridge slightly larger than the other two. The depth of the gooves is variable, so that the pellet may approach the shape of C. triradiata in section : most frequently the ventral groove is flattened while the lateral grooves are deeply cut. The colour ranges from dark brown to light grey. Typically the pellet is considerably cut up by transverse clefts, although it may be fairly smooth. From an animal of shell length 2.0 cm the pellets average 0.4 mm in diameter.” (Moore, 1931, p. 284, PI. 30, Fig. 4.) (Pellet-type IIA-9). 68. C. tigerina (Muller) “ Very similar to the previous species, but the pellets are usually smoother, and less cut up by transverse clefts. From an animal with a shell 1.6 cm long, the pellets average 0.4 mm in diameter.” (Moore, 1931, p. 284, P1. 30, Fig. 4.) (Pellet-type IIA-9). 69. C. (Mirapecten)squamata (Gmel.) (Pl. 2-13; Fig. 8c, 16, p. 399) Pellets of this species are very similar in nature and form to those of C . vesiculosus (Dkr) (Pellet-type IIA-9). Locality : Hiroshima Bay, Japan. Measurements: Breadth of pellets voided from an animal of shell length 23 mm was 0.49 mm. 70. C . triradiata (Muller) (Fig. SA) “ This also voids its pellets in the form of a long rod, but the surface is less smooth than in Nucula, and frequently marked by transverse clefts so that the pellet breaks into short lengths. I n section the pellet is triangular with rounded corners, one being usually sharper than the other two, and with slightly concave sides. From a specimen 3.5 cm across the shell the pellets are about 0.6 mm broad and in lengths of one to three millimetres or more.’’ (Moore, 1931a, p. 363, Fig. 5-A.) (Pellettype IIA-9a).

340

ILOHM-43 T.ARAKAWA

Remarks : The pellets of this species have been described by Moore ( I93 1a ) under the name of Pecten septemradiatus. 71. Palliolum randolphi (Dall) (Fig. 7 ~ )

Faecal pellets of this species are discharged in the form of a ribbon with two longitudinal grooves on the dorsal side, unlike those of other species of this family. There is no sculpture on the other side. They are coarse in texture, yellowish-brown in colour but not homogeneous in consistency (Pellet-type 111-1Oa). Locality : Sagami Bay (90 m in depth), Japan. Measurements : Width of the ribbons is 0.3 mm for an animal of shell length 18.5 mm. Limidae Apart from the genus Mantellum in which faecal pellets take the peculiar form of a helical spring, most of the representatives of this family produce considerably blurred rod-like faecal bodies with numerous irregular striae. They consist partially of constituent rodlets interwoven with a considerable amount of flocculent matter entangled with mucus (Pellet-type 11-8a). 72. Lima lima L.

‘‘ 1 animal. This individual, 37 mm long, shed rod-shaped pellets which appeared circular in cross-section. The pellets, 0-9 to 1 . 2 mm long and 0.23 mm wide, were irregular in outline and transversely striated.” (Manning and Kumpf, 1959, p. 303.) (Pellet-type 11-8a). 73. L. sowerbyi Deshayes (Pl. 4-45) “ In this species, thin thread-like constituent rods are compacted into cylindrical rods, usually voided in pieces of a length three to four times as long as the diameter. They are formed almost entirely of detrital matter mingled with some diatom frustules. The pelletdiameter fluctuates from 0.42 mm to 0.44 mm.” (Arakawa, 1965, p. 16, P1. IV, Fig. 45.) (Pellet-type 11-8a).

74. Promantellum orientale (Ad. and Rve)

This species voids short rod-like faecal pellets which consist partially of constituent rodlets with an admixture of flocculent matter entangled by mucus. They are very soft and friable in consistency and very similar to those described above (Pellet-type ZII-8a).

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(MOLLTSCA)

Locality : Hiroshima Bay, Japan. Measurement>s: Faecal pellets discharged by an animal with a shell 2 7 . 0 mm high are 1.09 mm in breadth. 75. Mantellurn amakusaense Habe (Pl. 2-14)

Faecal rods of this species are characterized by their fragility and elaborate transverse markings. They appear to be composed of coiled constituent filaments (Pellet-type '111-8a). Locality : Tomioka, Kumamoto, Japan. Measurements: For a specimen with 4.0 mm high shells, pellets fluctuate in breadth between 0.31 and 0.64 mm. Anomiidae This group produces ribbon-shaped pellets which may belong to Pellet-type 111-1 0a. 76. Anomia Zischkei Dautzenberg and Bavay (PI. 2-15 ; P1. 5-56 ; Fig. 19, p. 402)

Faecal ribbons of this species are usually shed broken into much shorter pieces. They are coarse in texture, frail in consistency and yellowish-brown in colour. There is a tendency for the coarse material to concentrate in the centre with the finer particles towards the periphery. Occasionally, this species releases roughly ovoid or cubiform faecal bodies which are hollowed longitudinally by two wide shallow depressions and have a narrow longitudinal slit along both sides. The faecal bodies are substantially composed of ribbon-shaped constituents which are regularly folded in triplicate or in quadruplicate. The constituent ribbons are slightly thickened along both edges and raised in tthe mid-dorsal line t o form a longitudinal ridge, but there was no evidence of the presence of a mid-ventral groove (Pellet-type 111-10). Locality : Ninoshima, Hiroshima, Japan. Measurements : The width of the ribbons fluctuates between 0 . 7 6 and 0.91 mm. Unionidae 77. Hyriopsis schlegeli (v. Martens) Locality : Sinki Lake (migrated from Kasumi-ga-Ura), Shimane, Japan (Pellet-type ZIII-10). A.l.H.-8

1"

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KOHMAN Y. ARAKAWA

Remarks : According to Nakamura et al. (1963), the transverse section of the rectum in this species is crescentic in outline. 78. Anodonta woodiana (Lea)

Owing to their loose and soft consistency, pellets of this species are usually of indefinable shape. They may be in the form of an ungrooved ribbon (Pellet-type ?III-10). Locality : Lake Shinji, Shimane, Japan. Carditidae It is characteristic of this family that the pellets are voided in the shape of an ungrooved ribbon (Pellet-type 111-10). 79. Cardita leana Dkr (Pl. 2-16)

The faeces are voided in the form of a ribbon with no external grooves. Superficially the ribbon is composed of rather coarse material which is loose and fragile in consistency (Pellet-type 111-10). Locality : Tomioka, Kumamoto, Japan. Measurements: For an animal with a shell 34.0 mm long ribbons average 0.31 mm in width. Galeommidae (Galeommatidae) This and the following families demonstrate a variety of pellettypes. I n some free-living species such as Scintilla japonica (Adams) and Lasaea rubra (Montagu), the pellets are shed in the form of an ellipsoid (Pellet-type 1-2), while in commensal forms such as Phlyctaenachlamys lysiosquillina (Popham), they are suggested to be discharged as disjointed particles (Pellet-type 1 l a ) . 80. Phlyctaenachlamys lysiosquillina (Popham)

“ T h e absence of mucous glands in the rectum is probably also associated with this movement of water through the mantle cavity. Particles of faecal matter will be shot out through the exhalent opening. There is thus no necessity for the formation of firm faecal pellets, because, owing to the violent expulsion of water, there will be less danger of the mantle cavity silting up.” (Popham, 1939, p. 83.) (Pellettype l l a ) . 8 1. Scintilla japonica (Adams) “ This species gives off ovoid pellets with twelve or thirteen constrictions, or sometimes without any surface-sculpturings. The pellets are

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343

dark brownish-green in colour, fine and homogeneous in texture, and mostly composed o f fine detritus containirlg unidentified microorganisms, algal fragments and some diatom frustules (Navicula, Rhizosolenia, Coscinodiscus, etc.). The average proportion of length to diameter of pellets shed by an animal with shell 1.3 ern long and 0.65 em high is 1.68 mm.” Remarks : “ The description of pellets of this scintilloid mollusc with illustrations was made by Arakawa (1962, p. 64) under the name of Scintilla vitrea Quoy and Gaimard, 1832, with which the mollusc has been identified by Japanem malacologists. Recently, however, Dr. Tokubei Kuroda kindly inforrned me that this bivalve should be identified with 8. japonica (Adams, 1862), and hence the pellets are redescribed under the correct name ” (Pellet-type 1-1). Measurements : “ Diam. of pellet (mm) 0.50 0.48 0.46 0.34 0.33 0.50 0.46 0.33 Length of pellet (mm) 0.94 0.86 0.84 0.50 0.55 0.94 0.86 0.51 Lengthldiameter 1.88 1.79 1.82 1.47 1.66 1.88 1.46 1-54’’ (Arakawa, 1965, pp. 17-18.) Erycinidae 82. Lasaea rubra (Montagu)

Morton (1956, p. 583, Fig. 8) has figured the pellets of this species but without morphological description. The pellets may be shed in the form of an elongate ellipsoid (Pellet-type 1-2). Chamidae Pellets of the representatives of this family may be released in the form of a plain rod (Pellet-type 11-4). 83. Chama reJlexa Rve

This species releases rod-like pellets with fine texture. Pellet -colour is greenish-brown (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements: From a specimen of shell length 36.0 mm, rods are 1.8 mm broad. 84. Pseudochama retroversa (Lischke) (Fig. 9 ~ )

Faecal pellets are shed in the form o f a rod with a soft consistency. They are often cut on the surface by numerous occasional cracks. They are fine in texture and brownish-grey in colour (Pellet-type 11-4).

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KOHMAN Y . ARAKAWA

Locality : Shiju-shima, near Onomichi, Hiroshima, Japan. Measurements: Faecal pellets shed by an animal with 4 3 4 mm high shell are 0.52 mm in average breadth. Laternulidae Pellets of members of this family are short rods with irregular outline, which should be referable to Pellet-type 11-4.

85. Laternula (LaternuZina)Jtexuosa (Rve) This and the following species are mu& alike in pellet characters. They are in the form of a rod, usually broken into short lengths. They are somewhat blurred in outline. The surface is not smooth but is occasionally broken by transverse cracks (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements : Breadth of pellets discharged by a specimen 32.0 rnrn in shell length is 0.20 mm. 86. L. Zimicola Rve (PI. 4-46) “ This species sheds roughly oval pellets with truncate ends. They are very firm and densely packed with fine detritus. They are coloured yellowish-brown and occasionally marked with clefts. The pellets average 0.60 mm in length and 0-31 mm in diameter.” (Arakawa, 1963, p. 207, Text-Fig. 6, F-C.) (Pellet-type 11-4). Thraciidae 87. Cyathodonta (Erimiothracia) concinna (Gould) This species produces short rod-like pellets with soft and loose consistency (Pellet-type 11-4).

Locality : Tomioka, Kumamoto, Japan. Measurements: From an animal of shell length 8-5 mm, pellets were 0.24 mm broad on average. Ly onsiidae 88. Lyonsia ventricosa Gould

Faecal pellets of this species closely resemble those of the genus Latemula. They are rod-shaped but somewhat irregular and flocculent. They are usually cut by numerous clefts. They are coarse in texture and greyish-brown in colour (Pellet-type 11-4), Locality : Kaneda Bay (50 m in depth), Japan.

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLLJSCA)

345

Measurements : Breadth of pellets shed by an animal with a 10 mm long shell was 0.54 mm. Donaciidae 89. Donas variubilis Say " 1 animal. This individual, 19 mm long, shed a rod-shaped pellet 1.5 mm in length. The width was not determined as the edges of the

pellet were flocculent. It was brown in colour." (Manning and Kumpf, 1959, p. 304.) (Pellet-type 11-4).

v.

GASTROPEMPTA

This order comprises six pellet-types ranging from 1-1 to 11-5, with the highest frequency in 1-1 and 11-4. I n general, the Gastropempta display the simplest pellets of all the five orders in this class. They include, besides two common basic types (Types 1-1 and 11-4), several transitional forms, most of which are characteristic of this group. Corbiculidae Type of pellets of this family may belong to 11-4 or to 11-6. 90. Pseudocyrena jloridana Conrad " 2 animals. One specimen, 27.5 mm long, shed a rod broken into small pieces up to 1 mm in length. The pellet was slightly compressed in shape, and had along one surface a shallow canal. " The canal was made up of darker and coarser material than was the

remaining surface. The rod was 1 mm wide a t the widest point. There appeared to be a concentration of coarser material towards the center." (Manning and Kumpf, 1959, p. 303, Fig. 4a.) (Pellet-type 11-4 ('26)). 91. Corbicula japonica Prime (Fig. 9 ~ )

Pellets are cylindric and rod-shaped, unsculptured, very fine in texture and somewhat sandy in appearance. The colour is yellowishbrown (Pellet-type 11-4). Locality : Lake Shinji, Shimane, Japan. Measurements : Breadth of pellets fluctuates between 0.20 and 0.34 mm for an animal with a shell 24.5 mm long. 92. C. leana Prime

Faecal pellets of this and the above species are so much alike that no clear-cut distinction can be made between them (Pellet-type 11-4).

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KOHMAN Y. ARAKAWA

Locality : Lake Shinji, Shimane, Japan. Measurements: Pellets shed by an animal with a shell 24.9 mm long fluctuate in breadth between 0.23 and 0.26 mm. Ungulinidae 93. Joannisiella lunaris (Yokoyama) (PI. 2-17) This species produces oval pellets with coarse texture (Pellet-type 1-1).

Locality : Tomioka, Kumamoto, Japan. Measurements : For a specimen examined, the pellets fluctuated in size between 0.20 x 0.24 mm and 0.20 x 0.27 mm. Lucinidae 94. Pillucina pisidium (Dkr)

Faecal pellets of this species are normally voided in the form of a spherule. But a t times, they are shed united in strings. Colour is greyish-yellow (Pellet-type 1-1 (ZIA-3)). Locality : Akitsu, Hiroshima, Japan. Measurements : For an animal with a shell 6.5 mm long, pellets fluctuate in diameter between 0.04 and 0.07 mm. Tridacnidae 95. Tridacna (Vulgodacna)maxima (Roding) (Fig. 9c) Faecal rods are normally cut by transverse cracks. They are fine in texture and rather soft in consistency. The colour is yellowish-brown (Pellet-type 11-4).

Locality : Yoron-jima, Kagoshima, Japan. Measurements: Breadth of pellets averages 0.42 mm for a specimen with a shell 76.0 mm long, and 0.65 mm for one with a shell 71.0 mm long. Cardiidae Most of the representatives of the group which have thus far been examined shed pellets that are either oval or a segmented rod of cornpact detritus (Pellet-type 1-1 and IA-3).

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317

96. Cardium edule L. “ Bei den Lamellibranchiern sind ebenfalls Kot-Pillen von ovalem oder rundlichem Umriss haufig (Cardium edule).” (Schafer, 1953, p. 83,) (Pellet-type I-1? )

A

Fig. 9. Faecal pellets of: A. Pseudochama retroversa; B. Gorbiciila japonira; C. Tridacna maxima (above, anus ; below, faecal pellet).

97. C. quadragenarium (Conrad) “ The faeces of clamlike forms such as Paphia, Schizothaerus and Cardium showed a definite linear segmentation.” (Edge, 1934, p. 80, Fig. 2.) (Pellet-type IA-3).

98. Bulvia hungerfordi (Sowerby)

(PI. 2-19)

This and the following species are much alike in pellet shape. The only distinct difference between the pellets lies in the ratio of length to breadth; it averages 1.85 in the present species and 1.3 in P. mutica (Pellet-type IA-3).

Locality : Tomioka, Kumamoto, Japan.

348

KOHMAPI' Y. ARAKAWA

Measurements when size of producer is 5.5 mm in shell length : Length of pellet (mm) 0.31 0.27 0-24 0.29 0.29 0.35 0.26 0 . 2 2

0.27

Breadth of pellet (mm) 0.15 0.15 0.15 0.15 0.15 0.15 0.15 0.15

0.15

Ratio of lengthlbreadth 2.07 1.80 1.60 1.93 1.93 2.34 1.73 1.47

1.80

99. F . mutica (Rve) (PI. 4-47 ; Fig. 14, p. 397) " Pellets of this species are rod-shaped, deeply constricted at regular intervals of about 1.3 times as long as the diameter and readily broken up into ovoid pieces with truncate end by a slight touch. They are fine, very firm in consistency, coloured uniformly greyish-green and consist entirely of fine detritus containing some diatom frustules. For aii examined animal, the average diameter of pellets is 0.82 mm." (Arakawa, 1965, p. 18, PI. V, Fig. 51.) (Pellet-type IA-3j.

100. Frigidocardium eos (Kuroda)

Pellets are ovoid in shape with flattened ends. They are fine in surface texture and yellowish-brown in colour. Ratio of lengthlbreadth of the pellets is 1-64 on an average (Pellet-type 1-1). Locality : Sagami Bay (87-95 m in depth), Japan. Measurements when size of producer is unknown : Length of pellet (mm) 0-56 0.53 0.54 0.46 0.56 0.48 0.50 0.57 0.46

0.56

Breadth of pellet (mm) 0.38 0.32 0-34 0.34 0.28 0.30 0.30 0.30 0.30

0.30

Ratio of lengthlbreadth 1.47 1.66 1.59 1.35 2.00 1.87 1.67 1.90 1.53

Measurements when size of producer is 20.5 Length of pellet (mm) 0.42 0.36 0-35 Breadth of pellet (mm) 0-24 0.24 0.26 Ratio of length/breadth 1-75 1.50 1.35

1.87

mm in shell length : 0.36 0.40 0-25 0.24 1.44 1-67

101. Laevicardium undatopictum (Pilsbry) (PI. 2-18)

The pellets are defecated normally in the form of a rod with a definite linear segmentation. Occasionally, they are shed broken into ovoid pieces with truncate ends. The surface of the pellets may be impressed by faint transverse striae. They are fine, homogeneous and

SCATOLOGICAL STlTDIES O F THE BIVALVIA (MOLLUSCA)

349

well consolidated. The ratio of length to breadth of the ovoid pieces averages 1.65 (Pellet-type IA-3). Locality : Tomioka, Kumamoto, Japan. Measurements when size of producer is 10-5 mm in shell length : Length of pellet (mm) 0.51 0.53 0.75 0.89 0.64 0.46 0.46 0.46 0.53 1.00 0.44

Breadth of pellet (mni) 0.34 0.34 0.34 0.34 0.34 0.34 0.34 0.34 0.34 0.34

0.34

Ratio of lengthlbreadth 1.50 1.56 2.21 2.62 1.89 1.35 1.35 1.35 1.56 2.94

1-30

Measurements when size of producer is 7 . 5 mm in shell length : Length of pellet (mm) 0.36 0.44 0.29 0.29 0.31 0-35 0.31 0.35 0-39 0.38

0.35

Breadth of pellet (mm) 0.24 0.26 0.22 0.20 0.20 0.22 0.22 0.22 0.22 0.27 0-20

Ratio of length/breadth 1.50 1-69 1.32 1.45 1.55 1.59 1.41 1.59 1.77 1.41

1.75

102. Trigoniocardia medium L.

This specimen, 20 mm long, released pellets with two " 1 animal. distinct shapes. The first of these pellets was ovoid in shape, and had a maximum length of 0.55 mm and a width of 0-37 mm. The second type of pellet was much more elongate. It was 1.0 mm long and 0.22 to 0.38 mm wide. Both of the pellets were smooth in consistency, and the smaller ones were slightly smoother than the larger." (Manning and Kumpf, 1959, p. 303.) (Pellet-type 1-1.) Ueneridae I n most of the representatives of this family, pellet-type 11-4 is of common occurrence. 103. Circe scripta (L.)

Pellets are oval and uniform in shape with fine surface texture. The ends of pellets are dissimilar; one is normally rounded, the other bluntly pointed. Pellet-colour varies from pale greyish-yellow to greyish-white (Pellet-type 1-1, 1-2). Locality : Mukaishima, near Onomichi, Hiroshima, Japan. Measurements when size of producer is 37.0 mm in shell length :

350

IIOIIMAN Y. ARAKAWA

Length of pellet (mm) 0-38 0-40 0.40 0-41 0.43 0.43 0.45

0.45

0.21 0.21 0.21 0.21 0.21 0.21 0.21

0.21

1.81 1.91 1.91 1-95 2.05 2.05 2.14

2.14

Breadth of pellet (mm) Ratio of lengthlbreadth 104. Cione cancellata L. " 1 animal. This specimen, 28 mm long, produced a curved and twisted rod-shaped pellet with a width of 0.1 mm. It was highly granular and creamy-white in color. It is possible that the constrictions visible in the feces are an indication of a starvation pellet; this was not definitely determined as no others were shed." (Manning and Kumpf, 1959, p. 303, Fig. 3d.) (Pellet-type ?II-4).

105. Callista chinensis (Holten)

Faecal rods of this species are cut by numerous occasionally formed cracks and are usually shed broken into much shorter pieces (Pellettype 11-4). Locality : Mukaishima, near Onomichi, Hiroshima, Japan. Measurements: Pellets voided by an animal with shell 54.0 mm long are 0.69 mm in breadth. 106. Protothaca staminea (Conrad)

Edge (1934, p. 79, Fig. 2) has illustrated the pellet for this species. The faecal rod shows a definite linear segmentation (Pellet-type IA-3). 107. P . jedoensis (Lischke)

The pellets of this species are rod-shaped and circular in section (Pellet-type 4). Locality : Mukaishima, Hiroshima, Japan. Measurements: For an animal with a 38.0 mm long shell the pellet is 0.30 mm in breadth. 108. Ruditapes philippinarum (Ad. and Rve) (Pl. 4-48) " This species sheds pellets that are rod-shaped, somewhat sandy in appearance and roundish in section. They are usually voided together with a large amount of mucus. They are yellowish-brown in colour and formed of somewhat coarse detritus mingled with some sand grains.

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

351

The pellets from an animal with shell 2.73 em long average 0.16 mm in diameter.” (Arakawa, 1963, p. 206.) (Pellet-type 11-4). Remarks: This species has been described by the author under the name of Tapes (AmygdaZa)semidecussata Rve. 109. Pitar (Agriopoma) noguchii Habe

The pellets are rod-shaped, somewhat sandy in appearance and round in section. They are built up from rather coarse detritus containing sand grains (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements: Pellets shed by a specimen with a shell 14.5 mm long are 0.46 mm broad. 1 10. Paphia vernicosa (Gould)

Faecal rods in this species are chapped by many occasional clefts and are usually voided broken into much shorter pieces (1-5to 3.0 times as long as the breadth of the pellets). They are very fine in texture and greenish-grey in colour (Pellet-type 11-4). Locality : Mukaishima, near Onomichi, Hiroshima, Japan. Measurements: Breadth of pellets shed by an animal with a shell 49.0 mm long is on average 0.6 mm. 11 1. VeremoZpa micra (Pils.)

Pellets are discharged in the shape of a plain rod with a circular section. They are formed from coarse detrital matter (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements : Breadth of the pellets fluctuates between 0.09 and 0.16 mm for an animal with. a shell 9.0 mm long. 112.

7. minuta (Yokoyama)

The above description may also be applied to this species (Pellettype 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements : Breadth of the pellet is 0.11 mm for a specimen with a shell 5.8 mm long.

352

KOHMAN Y . ARAKAWA

V . mindanensis (Smith) (Pl. 2-20) Description of the pellet for V . micra may be applied to this species (Pellet-type 11-4). 1 13.

Locality : Tomioka, Kumamoto, Japan. Measurements : For an examined animal, the breadth of the pellets was 9.08 mm. 114. Veremolpa sp.

The pellets of this and the above three species are so much alike in nature and form that it is impossible to draw a marked distinction between them (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements : In specimens examined the breadth of the pellets was 0.26 mm. 115. Venus ( Ventricoloides) foveolata Sowerby

Faecal rods are usually chapped on the surface by occasional cracks. They are coarse in surface texture, containing a considerable amount of undigested matter and sand grains. At times, this species sheds rodlike pellets packed by filamentous constituent rodlets (Pellet-type 11-4). Locality : Sagami Bay (87-95 m in depth), Japan. Measurements : Faecal rods shed by an animal of shell length 37.5 mm were 0.32 mm and the constituent rodlets were 0.10 mm broad. 116. Gomphina (Macridiscus) veneriformis (Lam.)

The faecal rod is somewhat blurred in outline and has irregular surface markings. Though it was conceivably atypical, this was not definitely ascertained as no others were shed (Pellet-type 11-4). Locality : Shikanoshima, Fukuoka, Japan. Measurements : For an examined animal, a pellet was 0.46 mm broad. 117. Anornulodiscus spuamosus (L.)

The pellets in this species are very similar in type to those of Ruditapes, Pitar and Veremolpa (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements : From a specimen with a shell 25.0 mm long, pellets fluctuate in breadth between 0.15 and 0-20 mm.

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLITSCA)

353

118. Meretrix lusoria (Roding) (Pl. 4-49) “ This species gives off the rods that are cylindrical and marked with a slight longitudinal groove presumably printed by the typhlosole. Occasionally, the rod contains a single constituent filament spirally coiled (Fig. 52, middle), or rarely it may be made mostly of a simple very long constituent filament derived from the liver string folded and compacted to form a rod (Fig. 52, below). The diameter of pellets voided by an animal with shell 6.5 cm long fluctuates in the range 1.3 mm-2-0 mm and that of constituent filaments is 0-26 mm.” (Arakawa, 1965, p. 18, P1. V, Fig. 52.) (Pellet-type 11-4 (16)). 119. Dosinia (Phacosoma)japonica (Rve) (Pl. 4-50) “ The faeces are of a typical cylindrical rod and without external sculptures. They are rather coarse in texture, firm in consistency, dark greyish-green in colour, and formed of rather fine detrital matter containing some coarse unidentified organisms. The pellet-diameter fluctuates between 0.51 and 0.53 mm for an animal with shell 4.7 cm long ” (Pellet-type 11-4).

Remarks : “The anatomical examination of the alimentary tract shows that the circular cross-section of the tract coincides exactly with the section of the faecal pellet (Pl. 6, Fig. 7 ) . ” (Arakawa, 1965, pp. 18-1 9, PI. V, Fig. 53, P1. VI, Fig. 7 . ) 120. Saxidomus purpuratus (Sowerby) (PI. 5-57)

Faecal rods of this species are very fine in texture and dark grey in colour (Pellet-type 11-4). Locality : Ondo, Hiroshima, Japan. Measurements: For an animal with a shell 68.0 mm long, pellets fluctuated in breadth between 1.20 and 1.30 mm. Petricolidae 121. Claudiconcha juponica (Dkr) “ The pellets are rod-shaped, circular in section and greyish-brown in colour. The surface is smooth and fine in texture. They are formed of unidentified fine materials and some diatom frustules. The pellets voided from an animal 1-09 em long range from 0.19 to 0.20 mm in diameter.” (Arakawa, 1963, pp. 206-7, Text-Fig. 7 , B.) (Pellet-type 11-4).

354

KOHMAN Y. ARAKAWA

Psammobiidae The representatives of this family produce ovoid faeces of compact detritus which belong either t o Pellet-type 1-1 or to 2. The specific difference may be found in the ratio of length t o breadth of the pellets. 122. Gari hosoyai (Habe) (PI. 2-21)

The pellets of this species usually take the form of an ovoid with flattened ends, but occasionally they vary : some are discoidal ; others are trihedral ; the remainder are dumb-bell-shaped. The surface texture is very fine in normal-shaped pellets while it is coarse in abnormalshaped ones. The ratio of length/breadth averages 1.28 (Pellet-type 1-1).

Locality : Tomioka, Kumamoto, Japan. Measurements when size of producer is 22.0 mm in shell length : Length of pellet (mm) 0.44

0.39 0.44 0-42 0.41 0.41 0.46 0.43 0-39 0.44 0.42

0.44

Breadth of pellet (mm) 0.33

0.33 0-33 0.33 0.33 0.33 0.33 0.33 0.33 0.33 0.33 0.33

Ratio length/breadth 1.33 1.18 1-33 1.27 1.24 1.24 1.39 1.30 1.18 1.33 1.27

1.33

Measurements when size of producer is 15.9 mm in shell length : Length of pellet (mm) 0.37 0.32 0.32 0.55 0.28 0.26 0-28 0.31 0.31 0.28 0.25 0.34 Breadth of pellet (mm) 0.23 0.22 0.28 0.28 0.25 0.25 0.26 0.26 0.25 0.25 0.23 0.25 Ratio length/breadth 1.61

1.45 1.14 1.96 1.12 1.04 1.08 1-19 1.24 1.12 1.09

1.36

123. HiatuZu atratu (Rve) (P1. 2-22)

Here there are wide variations in size and shape even in the pellets voided by an animal within a short period ; some are oval ; others are elongate ellipsoid ; the remainder are short rods. Normally, the pellets of this species are released in the form of an ovoid with rounded ends and with a somewhat uneven surface. They are compacted by fine detrital matter and the surface is usually broken by numerous irregularly formed cracks. Average ratio length/breadth is 1.72 (Pellet-type 1-1).

Locality : Tomioka, Kumamoto, Japan.

SCATOLOGICAL S T U D I E S OF THE B I V A L V I A (MOLLlISCA)

Measurements when size of producer is 54.0 mm in Length of pellet (mm) 1.91 2.18 1-78 1.91 Breadth of pellet (mm) 1.07 1.00 1.27 1.06 1.79 2-18 1.45 1.80 Ratio length/breadth

355

shell length : 1.73 1.22 1.42

Fig. 10. Faecal pellets of: top, Nuttalia olivacea; bottom, Hiatella jlaccida.

124. Nuttalia oliwacea (Jay) (Pl. 2-23; Fig. 10, top)

The pellets are elongated ellipsoidal with round ends. The surface

356

KOHMAN Y . ARAKAWA

is normally smooth but occasionally this is marked by faint spiral striae. The ratio of length to breadth of pellets averages 2-61 (Pellettype 1-2). Locality : Kaita Bay, Hiroshima, Japan. Measurements when size of producer is unknown : Length of pellet (mm) 1.13 1.20 1.37 1-33 1.66 1-55 1-02 1.40 1 . 7 7

Breadth of pellet (mm) 0.55 0.49 0.51 0.51 0.55 0.49 0-56 0.55 0.56

Ratio length/breadth 2.05 2.45 2.74 2.66 3.02 3-16 1.82 2.55

3.16

Remarks : One animal collected at Shikanoshima, Fukuoka, Kyushu, produced rod-shaped pellet with coarse texture, measuring 0.50 mm in breadth. This pellet was formed almost entirely from undigested matter and some sand grains ; it seemed to ‘be atypical. Semelidae Members of this family may produce either discoid (Pellet-type I-la), ovoid (1-1) or ellipsoid pellets (1-2). I n general appearance, the pellets resemble each other, but they may be separated by examination of the lengthlbreadth ratios. 125. Abra alba (Wood) “ The pellets are extremely uniform in shape, parallel-sided with rounded ends and circular in section ;the surface is smooth and regular ; the usual breadth is 0-25 to 0.3 mm, and the ratio of length to breadth about 1.75.” (Moore, 1931a, p. 363, Figs. 1 and 5, B.) (Pellet-type 1-1).

126. A . nitida (Miiller)

“Much less regular in form than S. alba, and frequently either tapered at one end or constricted at one or more points; surface smooth; narrower than S. alba, breadth 0.2 to 0.25 mm.” (Moore, 1931a, p. 363, Figs. 2 and 5, C, D, and E.) (Pellet-type 1-1). 127. Abrina Zunella (Gould) (Fig. l l ~ )

Faecal pellets of this species are disc-shaped and are, at times, voided together in strings. Ratio length/breadth of pellets is 0.61 (Pellet-type I-1a). Locality : Hiroshima Bay (20 m in depth), Hiroshima, Japan.

3.57

SCATOLOGICAI~YTI'DIES OB THE BIVALVIA (MOLLlrSCA)

Measurements when size of producer is 14.0 mm in shell length : Length of pellet (mm) 0.26 0-20 0.22 0-12 0.09 0.20 0.18 0-18 0.12 0.14 0-26 0.28 0.27 0.25 0.28 0.28 0.93 Ratio 1engt h/breadth 0.67 0.48 0.50 0.93

Breadth of pellet (mm)

0.14 0-26 0.26 0.77 0.54

0.15 0.26 0.26 0.85 0.58

0.16 0.26 0.27 0-46 0.59

0.10 0.26 0.24 0.35 0.42

0.06 0.12 0.25 0.26 0.20 0.24 0.80 0.69 0.30 0.50

1%. ThPora Euhrica (Hinds) (Pl. 2-24)

This species defecates typical round-ended oval pellets wittli no grooves. Most of these are fine and homogeneous in surface texture and composed almost entirely of fine grade detritus, but occasionally pellets are coarse and sandy in appearance. Average lengthlbreadth ratio of the pellets is 1.74 (Pellet-type 1-1). Localities : Tomioka ; Kaita Bay ; Kure Bay, Japaii. Measurements when size of producer is 9.5 mm in shell length : Length of pellet (mm) 0.32 0.30 0.29 0.30 0.26 0.28 0.28 0-37 0.37

Breadth of pellet (mm) 0.16 0-16 0.17 0.14 0.14 0.14 0.15 0.22

0.20

Ratio lengthlbreadth 2.00 1.88 1 - 7 1 2.14 1.86 2.00 1-87 1.68

Measurements when size of producer Length of pellet (mm) 0.27 0.18 Breadth of pellet (mm) Ratio lengthlbreadth 1.50 Measurements when size of producer Length of pellet (mm)

1.85

is 8-5 mm in shell length : 0.28 0.33 0.34 0.28 0.34 0.29 0-18 0.14 0.18 0.17 0-18 0.16 1.55 2-36 1.89 1.65 1-89 1.81

is 7.0 mm in shell length :

0.23 0.24 0.23 0.21 0.20 0.24 0.22 0.20 0.22

0.21

Breadth of pellet (mm) 0.12 0.12 0.12 0.13 0.10 0.12 0.14 0-14 0.14 0.13

Ratio lengthlbreadth 1.92 2.00 1-92 1-62 2.00 2.00 1.57 1.43 1.57 1.62

Measurements when size of producer is 6.5 mm in shell length : Length of pellet (mm) 0.22 0.25 0.24 0.24 0.23 0.22 0.22 0.26 0-23 0-23 0.22 0.25 Breadth of pellet (mm) 0.12

0.12 0.11 0.11 0.11 0.11 0.13 0.13 0.12 0-12 0.12

0.12

Ratio length/breadth 1-83 2.08 2-18 2.18 2.09 2.00 1.89 2.00 1.92 1.92 1.83 2.08

358

KOHMAN Y. ARAKAWA

Measurements when size of producer is 5.5 mm in shell length : Length of pellet (mm) 0.14 0.16 0.16 0.17 Breadth of pellet (mm) 0.09 0.09 0.09 0.09 Ratio length/breadth 1.56 1-78 1.78 1-89 Measurements when size of producer is 5.0 mm in shell length : Length of pellet (mm) 0.24 0.22 0.20 0.22 0.18 0.21 Breadth of pellet (mm) 0-13 0.12 0.11 0.12 0.11 0.12 Ratio length/breadth 1.85 1-83 1.82 1.83 1.64 1.75 Tellinidae The representatives in the Tellinidae which have so far been examined defecate either discoid (I-la)or ovoid (1-1) pellets, or rarely, constricted rod (IA-3). The pellets are usually made up almost entirely of compact detritus with uniform consistency and may be separated by the length/breadth ratios among species of the different genera ; e.g. in Tellina this is, as a rule, more than 1 and less than 2 ; in Macoma it is less than 1. 129. Arcopagia crassa Pennant “ The pellet is smooth and sandy in appearance, and light or dark brown in colour, often pellets of both shades being shed by the same animal within a short period. Occasionally the pellet is voided in the form of a rod, but most frequently this is constricted and cut up into the typical rounded ended pellets. I n section these show no localization of the constituent materials, and are formed from detritus containing numerous spicules, and diatom remains. From an animal with a shell 1.3 cm long, the pellets average 0.33 mm in diameter, and have a ratio of length/breadth = 1.35.” (Moore, 1931, p. 282, P1. 30, Fig. 1 . ) (Pellettype 1-1 (?IA-3)).

130. Moerella donacina (L.) “ The above description (Arcopagia crassa) may be applied to this species, except that here the ends are less rounded, and there is a tendency to the formation of rather irregular pellets. From an animal with a shell 1.5 cm long, the pellets average 0.36 mm in diameter, and the ratio lengthlbreadth = 1.30.” (Moore, 1931, p. 282, P1. 30, Fig. 2.) (Pellet-type 1-1 (?IA-3)).

131. M . kurodai (Makiyama) (Pl. 5-60)

Pellets are oval with rounded ends. averages 1.92 (Pellet-type 1-1 (12)).

The length/breadth ratio

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

359

Locality : Hiroshima Bay, Hiroshima, Japan. Measurements when size of producer is 9.0 mm in shell length : Length of pellet (mm) 0.45

0.38 0.39 0.41 0.41 0.40 0.35 0-45 0.38 0.39 0.37

0.43

Breadth of pellet (mm) 0.20

0.21 0-21 0.21 0-21 0.21 0.21 0.21 0.21 0.21 0.21

0.21

Ratio length/breadth 2.25

1.81 1.86 1.95 1.95 1.91 1-67 2.14 1-81 1.86 1.76 2.05

132. Nitidotellina nitidula (Dkr) (Pl. 3-25, P1. 5-61)

The pellets are usually shed in an ovoid form, circular in section. There are several varieties ; some are discoidal and others are short rods transversely constricted at one or two points. There is some localization of the content ; the coarser material tends to concentrate towards the centre and the finer to the periphery. The ratio of length/breadth averages 1.21 (Pellet-type 1-1). Locality : Tomioka, Kurnamoto, Japan. Measurements when size of producer is 13.0 mm in shell length : Length of pellet (mm) 0.27

0.28 0.30 0.32 0-26 0.30 0.26 0.28 0.28 0.27 0.28

0.26

Breadth of pellet (mm) 0.20

0.24 0.23 0.22 0.24 0.24 0.22 0.20 0.26 0.26 0.24

0.24

Ratio lengthlbreadth 1.35 1.17 1.30 1.45 1-08 1-25 1.18 1.40 1.08 1.04 1.17 1-08 133. F. minuta (Lischke) (PI. 3-26) 134. F. iridella (v. Martens) (PI. 5-59)

These two species are very much alike in pellet characteristics. The pellets are normally rounded, but may have a small boss at one or both ends. The lengthlbreadth ratio averages 1.62 for F. minuta and 1.48 for F. iridella (Pellet-type 1-1). Localities : Tomioka (P. minuta) and Hiroshima Bay (P.iridella), Japan. Measurements when size of producer (P. minuta) is 7.0 mm in shell length : Length of pellet (mm) 0.23 0.17 0.30 0-24 0.23 0-24 0.29 0.23

0.30

360

KOIlMAN Y . ARAKAWA

Breadth of pellet (mm) 0.18 0.13 0.15 0.15 0.14 0.14 0.18 0.16

0.15

Ratio length/breadth 1.28 1.31 2.00 1-60 1.64 1.71 1.61 1.44 2.00

Measurements when size of producer length : Length of pellet (mm) 1.30 1.00 Breadth of pellet (mm) 0.80 0.60 Ratio length/breadth 1-70 1.60

( F . iridella) is 17.0 mm in shell 1-10 0.90 0-70 0.70 0.70 0.60 1.60 1.30 1.20

135. Fabulina pallidula (Lischke)

Pellets are normally shed in the form of an ovoid with flattened ends. Ratio length/breadth is 1.11 (Pellet-type 1-1). Locality : Akitsu, Hiroshima, Japan. Measurements when size of producer is 7.0 mm in shell length : Length of pellet (mm) 0-20

0.20 0.20 0.22 0.20 0-25 0.24 0.24 0.22 0.25 0.21

0.21

Breadth of pellet (mm) 0.20

0.18 0.19 0.19 0.19 0.21 0-21 0.22 0.20 0.20 0.20

0.19

Ratio length/breadth 1.00

1.11 1.05 1.16 1.05 1.19 1.14 1.09 1.10 1.26 1.05 1 . 1 1

136. Arcopella isselli (H. Ad.) (PI. 3-27)

The released pellets are ovoid with flattened ends. Occasionally, they may have a small boss a t one or both ends. The superficial consistency is fine, uniform and compacted. The length/breadth ratio is 2.06 (Pellet-type 1-2). Locality : Tomioka, Kumamoto, Japan. Measurements when size of Length of pellet (mm) Breadth of pellet (mm) Ratio length/breadth

producer is unknown : 0-34 0.38 0.38 0.18 0-18 0.18 1.89 2.11 2.11

0.38 0.18 2.11

137. Semelangulus miyatensis (Yokoyama) (PI. 3-28)

The pellet shapes in this and the preceding species are much alike, the difference lying in the length/breadth ratio. I n this species the ratio averages 1.20, i.e. smaller than in the other (Pellet-type 1-1). Locality : Tomioka, Kumamoto, Japan.

SCATOLOQICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

361

Measurements when size of producer is 7 4 mm in shell length : Length of pellet (mm) 0.26

0.26 0.27 0-26 0-27 0.24 0.31 0.27 0-24 0.26 0.27

0-26

Breadth of pellet (mm) 0.22

0.22 0-22 0.22 0-22 0.22 0.22 0.22 0-22 0.22 0.22

0.22

Ratio lengthlbreadth 1.18

1.18 1.23 1.18 1.23 1.09 1.41 1.23 1.09 1.18 1.23

1.18

138. 8. tokubeii Habe (Pl. 3-29)

Faecal ovoids of this species are very similar to those of the above species. The length/breadth ratio is 1.22 (Pellet-type 1-1). Locality : Tomioka, Kumamoto, Japan. Measurements when size of producer is unknown : Length of pellet (mm) 0.25

0.20 0.26 0.32 0.30 0-20 0.20 0.29 0.28 0.28 0.18

0.19

Breadth of pellet (mm) 0.21

0.17 0.25 0.22 0.24 0.17 0.16 0.22 0.22 0.21 0.16

0.16

Ratio lengthlbreadth 1.19

1.11 1.04 1.41 1.25 1.11 1.25 1.32 1.27 1.33 1.13 1.19

139. Macoma tokyoensis Makiyama (Pl. 3-30; Fig. 13, p. 396) 140. M. incongrua (v. Martens) (PI. 3-31) 141. M. praetexta (v. Martens)

The pellets of these three species are very much alike. They are released in a discoid form with a small boss a t one end which is quite characteristic of this group. They are fine and homogeneous in consistency and uniform in shape. The lengthlbreadth ratio varies among species : in M . incongrua it averages 0.77, in M. tokyoensis 0.66, and in M . praetexta 0.53 (Pellet-type 1-la). 142. M. yoldiformis Carpenter

According to Edge’s observations (1934, p. 81, Fig. 4), the pellets are shed in the form of a rod with a linear segmentation, and “ the segmentation a t times was replaced by separate spherical pellets ”. Remarks: From his accompanying figure of the pellets, the length/ breadth ratio is estimated to be 1.0 (Pellet-type I-la ( ?1)). 143. Psammacoma awajiensis Sowerby (Pl. 3-32)

This species sheds ovoid pellets with rounded end, unlike those of members of the genus Macoma. Occasionally they are joined together

362

KOHMAN Y. ARAKAWA

in a short chain. They are rather coarse in texture and dark greenishbrown in colour, sometimes variegated by greyish patches. The length/breadth ratio averages 1.49 (Pellet-type 1-1). Locality : Chijiwa Bay (20 m deep), Kumamoto, Japan. Measurements when size of producer is 21.2 mm in shell length : Length of pellet (mm) 0.52 0.56 0.47 0.53 0.48 0.54 0.35 0.35 0.35 0.35 0.35 0.35 Breadth of pellet (mm) Ratio length/breadth 1.49 1.60 1.42 1.52 1-37 1.54 Mesodesmatidae 144. Caecella chinensis Deshayes (Pl. 4-51) “ The pellets are dark brown in colour, fine in texture and greatly variable in shape. Most frequently faeces are voided in a form of rod, but occasionally in roundish pellets with blunt ends or sometimes with one end blunt and the other sharply pointed. They are composed entirely of fine detritus.” (Arakawa, 1963, p. 207, Text-fig. 6, H-K) (Pellet-type 11-4).

Mactridae I n this family there are two distinct types of faecal pellet. According to Edge (1934), the pellets of Schizothaerus are rod-like with a linear segmentation (Type IA-3), unlike those described here for other representatives of this family. In Muctra, the faeces are ellipsoid or ovoid and belong to Type 1-2. The major difference between species lies in the length/breadth ratio of the pellets. 145. Mactra sulcatariu Rve (PI. 3-33 ; Fig. 15, p. 398)

The pellets are elongate ellipsoid, parallel-sided and truncated at both ends. Occasionally they are impressed indistinctly on the surface by a single right-hand spiral stria. They are made up almost entirely of fine grade detritus. Average length/breadth ratio is 2.09 (Pellettype 1-2). Locality : Tomioka, Kumamoto, Japan. Measurements when size of producer is 23.0 mm in shell length : Length of pellet (mm) 1.18 1.00 0.91 1.09 1.17 0.73 0.91 0.80

Breadth of pellet (mm) Ratio length/breadth

0.46 0.46 0.46 0.46 0.49 0.46 0.46 0.46 2.57 2.13 1.98 2.37 2.39 1.59 1-98 1.74

SCATOLOUICAL STUDIES OF THE BIVALVIA (n1OLLUSCA)

363

146. M . crossei (Dkr) (PI. 3-34)

The pellets of this and the following species are somewhat alike. Here they are elliptical with flattened ends. They are fine and homogeneous in texture and are compacted by fine detrital matter. The surface of the ellipsoids may, at times, be impressed by a single dextrally coiled stria. The lengthlbreadth ratio fluctuates between 3 and 4 and pellets voided by a fully matured animal average 0-28 mm in breadth (Pellet-type 1-2). Locality : Shikanoshima, Fukuoka, Japan. Measurements : For an examined animal the pellets averaged 0.28 mm in breadth. 147. M . pulchella Philippi

Faecal ovoids in this species are well consolidated, fine and uniform in superficial consistency. They are formed almost entirely from fine detritus and may have a small boss at one end. The lengthlbreadth ratio is 1.79 (Pellet-type 1-1). Locality : Tomioka, Kumamoto, Japan. Measurements when size of Length of pellet (mm) Breadth of pellet (mm) Ratio length/breadth

producer is 9.8 mm in shell length : 0-32 0.41 0-44 0.37 0.23 0.19 0.23 0.22 1.39 2.16 1.92 1-68

148. Tressus keenae Kuroda and Habe (Pl. 5-58)

Faecal rods are constricted a t rather regular intervals. The surface is finely striated by a single spiral cord. The texture is extremely fine and homogeneous. The lengthlbreadth ratio of separated ovoids averages 0-82 (Pellet-type IA-3). Locality : Unknown (Japan). Measurements when size of animal is 97.0 mm in shell length : 1-45 1.75 Length of pellet (mm) Breadth of pellet (mm) 1.85 1.85 Ratio length/breadth 0.78 0.95 Measurements when size of animal is 93.0 1.05 1.25 Length of pellet (mm) Breadth of pellet (mm) 1.55 1.55 Ratio lengthlbreadth 0.68 0.81

mm in shell length : 1-25 1.55 0.81

364

I
149. Xchizothaerus nuttalii (Conrad) “ The faeces of clamlike forms such as Paphia, Xchizothaerus and Cardium showed a definite linear segmentation.” (Edge, 1934, p. 80, Fig. 2 . ) (Pellet-type IA-3).

150. Ruetu (Raetellops) rostrnlis (Reeve) (Fig. 1 1 ~ )

Pellets are ellipsoidal with rounded ends. They are impressed by four or five slight transverse constrictions at regular intervals. They are very fine in texture, homogeneous in consistency and greyish-brown in colour. Length/breadth ratio is 2-58 (Pellet-type 1-2). Locality : Kaneda Bay (50 m in depth), Japan.

A

Pig. 11. Faecal pellets of: A. z4brirsa ltrizelln; R. Raeta iostmlis; C. Sinonovacda constricta: D. M y a japonica; E. Barriea japonica.

365

SCATOLOQICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

R;leasurements when size of producer is 9.0 mm in shell length : 0.54 0.58 04i6 0.68 0.66 0.56 0.64 Length of pellet (mm) 0.74

0.66 0.66 0.64 0.72 0.68 0.27 0.26 0.26 0.27 0.26 0.25 0.25 Ratio length/breadth 2.00 2.85 2.54 2.44 2.46 2.88 2.72

Breadth of pellet (mm)

0.67 0.25 0.26 2.32 2.58

0.58 0.25 0.25 2.64 2.08

0 . 7 1 0.70 0.58

0.24 0.23 2.83 3.09

0.25 0.25 2.64 2.80

0.27 0.25 2.07 2.32

0.76 0.25 0.24 2.56 3.17

15 1. Raeta plicatella Lam.

'' The pseudofeces, consisting of particulate material assembled in the incurrent mantle cavity and rejected through the incurrent siphon, are poorly consolidated ropes of sediment, slightly larger than a millimeter in diameter and a few centimeters long. True feces are of two types, which may be called ropes and pellets (Fig. 4). The pellet type was seen in the rectum of the damaged specimens from the beach, and the rope type in the intestine of the intact specimen found in the bay. This specimen voided both types in the laboratory, and from that material Fig. 4 was drawn. The rope type of feces evidently passes through the intestine with little rearranging of the materials involved. It consists of a single strand, 80-100 mm long, with segments of dark tan material alternating with segments of dark olive color. The lengths of the two segment types are not constant. Probably the olive colored material is derived from the liver, and the tan material is of undigested particles which entered the mouth. These were not studied in detail. The packaged configuration of the rope, bent back upon itself several times as shown in Fig. 4, probably occurs as the rope is defecated into the suprabranchial mantle chamber. This package has been passed from the animal, as had numerous pellets. The pellet feces were probably in the specimen when captured. They are constant in diameter, about 0.69 mm, and slightly variable in length, about 0.96 to 1-23 mm long, with longer pellets being more abundant. Each pellet is elaborately constructed. The pellets are smooth, regular cylinders with abruptly truncated ends, one being slightly convex, the other slightly concave, The surface is uniformly light tan colored, evidently of fine particles held compactly together with mucus. There is a single line, slightly incised, which begins in the middle of one end, makes about one complete turn on the lateral surface, and ends a t the middle of the other end of the pellet. Breaking a pellet open gently reveals a central cavity which seems not to extend quite to the ends. I t s diameter is about 113 that of the pellet, and it is reniform in cross section. This cavity is loosely filled with granules of varying sizes, all larger than those of the outer part. The outer part of the pellet has about five layers, probably

366

KOHMAN--Y. ARAKAWA

of only one continuous sheet, wrapped around the central cavity. The innermost layer is wider and less firmly consolidated than the others. The layers bend toward the concave side of the central cavity, and the spiral line on the outside seems to correspond t o this also. At higher magnification, the particles of the outer shell of the pellet all seem to be inorganic, angular granules, rarely as large as 3p. No Brownian movement could be seen in a squash preparation in sea water, possibly because the mucous matrix was too viscous. The granules of the central cavity are irregular spheres, from 10 to 14 p in diameter. These are hyaline, golden brown and bright in reflected light. Also present were a few glassy angular flakes, colorless and polygonal, with sharp edges and angles. These are about 0.30 mm in maximum dimension. I was unable to find any organismal remains in the pellets, such as diatoms, even a t 9 7 0 x magnification.” (Harry, 1969, pp. 5-6, Fig. 4.) (Pellet-type 1-2). Solenidae Pellets of the representatives of this group belong either to Pellettype IA-3 or 11-4 or to 1-2, which may be interchangeable. 152. Xolen roseomaculatus Pilsbry (PI. 3-35)

Faecal rods are segmented a t regular intervals, the length of each segment being approximately 1.4 times the breadth. The segmentation, a t times, is replaced by separate ovoid pellets with truncate ends. The colour and the consistency of pellets appear to vary in relation to the dietetic condition and growth-stage of the animal, viz., pellets are greyish-yellow and coarse in mature specimens, while in immature ones they are fine and yellowish-brown (Pellet-type IA-3). Locality : Chijiwa Bay, Kumamoto, Japan. Measurements when size of producer is unknown : Length of pellet (mm) 0.20 0.21 Breadth of pellet (mm) 0.14 0.14 Ratio lengthlbreadth 1.43 1-50 Measurements when size of producer is 30.0 mm in shell length : Length of pellet (mm) 0-35 Breadth of pellet (mm) 0.24 Ratio lengthlbreadth 1-46 Measurements when size of producer is 10.0 mm in shell length : 0.16 0.15 0.15 0.18 0.15 0.13 0.13 Length of pellet (mm) 0.11 0.11 0.11 0.13 0.11 0.11 0.09 Breadth of pellet (mm) 1.45 1-36 1.36 1-38 1.36 1.18 1-45 Ratio length/breadth

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

367

153. Solen strictus Gould (PI. 4-52) “ The faecal pellets are cylindrical and rod-shaped. The surface is fine and smooth except for occasional transverse cracks. For an examined animal, the pellets range from 0.95 t o 1.08 mm in diameter.” (Arakawa, 1963, p. 207, Text-Fig. 6-L.) (Pellet-type IA-3 (?II-4)). Remarks : The pellets of this species have been described by Arakawa (1963) under the name of S. gouldi Conrad. 154. 8. gordonis Yokoyama Pellets are discharged in the form of a short rod with a faint spiral striation and with truncate ends. They are very fine in surface texture and brownish-grey in colour. The length/breadth ratio is 2.19 (Pellettype 1-2). Locality : Mukaishima, Hiroshima, Japan. Measurements when size of producer Length of pellet (mm) 1.54 1.95 1.12 Breadth of pellet (mm) 0.69 0.69 0.69 Ratio lengthlbreadth 2.23 2.83 1.62

is 85-0 mm in shell length : 1.30 1.30 1.31 1-55 1.55 1-95 0.69 0.69 0-69 0.69 0.69 0.69 1.88 1.88 1.90 2.25 2.25

2.83

Novaculidae 155. SinonowacuEa constricta (Lam.) (Fig. 1lc)

The pellets are plain rods in shape with fine texture. They are fulvous yellow in colour. Frequently they are cut by occasional cracks (Pellet-type 11-4). Locality : Otoshima, Okayama, Japan. Measurements : Breadth of faecal rods fluctuates between 0.28 and 0.30 mm for an animal with a 22 mm-long shell.

Hiatellidae 156. Hiatella Jlaccida (Gould) (Fig. 10 bottom) This species voids segmented rod-like, or truncate-ended ovoid, pellets. The ovoids are very irregular in size and shape, and fine and uniform in surface texture. The lengthlbrendth ratio varies greatly (Pellet-type IA-3 (1-I?)).

368

KOHMAN Y . ARAKAWA

Locality : Hiroshima Bay, Japan. Measurements when size of producer Length of ovoid pieces (mm) Breadth of ovoid pieces (mm) Ratio lengthlbreadth

is 19.0 mm in shell length : 0.55 0.50 0.65 0.55 0.40 0.45 0.40 0.40 1.38 1.11 1.63 1.38

Myidae 157. M y a truncata L.

Moore (1931, p. 286) has briefly stated that the faecal rods are marked with a single dextral spiral groove (Pellet-type 11-5). 158. iVf. (Arenomya)japonicn J a y (Fig. 1 1 ~ )

Faecal rods are sculptured by a single spiral groove. They are usually cut by numerous occasional clefts. They are fine in texture, soft in consistency and greyish-brown in colour (Pellet-type 11-5). Locality : Otoshima, Tamashima, Okayama, Japan. Measurements : Breadth of the faecal rods fluctuates between 0.90 and 1-20 mm, for an animal with a 75.0 mm-long shell. Corbulidae The pellets described here for two representatives of this group belong to Pellet-type 11-4. 159. Varicorbula bifrons (A. Ad.)

Faecal rods are soft, frail and coarse in texture. They are shed carrying a considerable amount of viscous matter (Pellet-type 11-4). Locality : Tomioka, Kumamoto, Japan. Measurements: For a specimen with a shell 3.6 mm long, pellets average 0.18 mm in breadth. 160. Anisocorbula venusta (Gould)

Pellets are shed in the form of a short rod (Pellet-type 1-4). Locality : Tomioka, Kumamoto, Japan. Measurements: For an animal with an 8-5 mm-long shell the pellets are 0.11 nim broad.

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

369

Pholadidae 16 1. Pholadidea Eoscombiam Turton “ The twist in this species is sinistral, but in other molluscs it may be dextral, i.e. Pholadidea loscombiana, Turton . . ..” (Moore, 1931, p. 286.) (Pellet-type 11-5.)

162. Barnea (Umitakea)japonica (Yokoyama) (Fig. 1 1 ~ )

Faecal pellets are discoidal in shape with a single spiral cord. This cord may be absent depending on the nature of the food. The pellets are frequently shed in chains. The finer constituents lie on the periphery while the coarser particles concentrate towards the centre. Ratio of length t o breadth of the pellets is 0.48 (Pellet-type 1-la). Locality : Unknown (Japan). Measurements when size of producer is 40-0mm in shell length : Length of pellet (mm) 0.65 0.70 0.60 0.50 0.60 0.70 0.60 Breadth of pellet (mm) 1.30 1.30 1.30 1.30 1.30 1.30 1.30 Ratio lengthlbreadth 0.50 0.54 0.46 0.38 0.46 0.54 0.46 163. Zirfea gabbi Tryon

Edge (1934, Fig. 4) figured the pellets of this species which form ungrooved short rods (Pellet-type 11-4). Xylop haginidae 164. Xylophaga dorsalis Turton

According t o Purchon (1941), this species defecates ellipsoid pellets and has a habit of accumulating the faeces around the mouth of tubes, giving the appearance of the tubes of Serpula. He states as follows : ‘‘ The faecal pellets are not expelled with sufficient force to carry them out of the burrow and so accumulate at its posterior end as a compact mass, consolidated with mucus, which surrounds the siphonal process through which the exhalant water current passes. The presence of this faecal accumulation prevents any extensive movements of the animal.” (Purchon, 1941, pp. 3, 21, Figs. l b , l l a . ) (Pellet-type 1-1).

2

PELLETS OF FAECAL TABLE11. LISTOF KNOWNPRODUCERS

No,

1. 2. 3. 4. 5. 6. 7. 8. 9.

Pellettypes

Species

Nucula hanleyi A’. moorei

.

.

7a 7 7a 7b

W.nucleus N. sulcata N . tenuis . . N.turgida . “sp. Nuculana minuta Portlandia japonica

10. Portlandiella beringii 11. Saccella sematensis 12. Cardiomya gouldiana septemtrionalis 13. Plectodon ligula . 14. Arca umbonata . 15. Anadara subcrenata 16. A . brougktoni .

7 7a I

. .

. . . . .

6 6

Size of producer (shell length, mm) ca. ca. ca. ca.

10.0 10.0 10.0 10.0

Average size of pellets - Ratio Breadth length/ or width Length breadth (mm) (mm) ?

0.16 0.16 0.16

ca. 10.0 ca. 10.0

0.14 0.14

? ?

? ?

12.0

0.26

-

-

-

-

-

-

-

-

-

-

6

19.0

0.40

-

-

6 6 6

35.0 23.0 10.5

0.70 0.50 0.24

-

-

11 11 10

8.0 5.0 42.0

0.62 0.07 0.43

-

10 10

?

0.73-1.09 3.50

-

-

85.0

-

-

-

-

-

-

0

Locality*

References

Loch Striven Loch Striven Loch Striven East coast of Scotland Loch Striven Loch Striven Loch Striven (England) Suruga Bay (80 m deep) Sagami Bay (90 m dp) Off Kinkazan Off Kinkazan Suruga Bay (80 m dP)

Moore, 1931a Moore, 1931a Moore, 1931a

Chijiwa Bay Chijiwa Bay Florida Shirahama Himeji

z

Moore, 1931a Moore, 1931a Moore, 1931a Moore, 1933 Moore, 1939 This paper This paper This paper This paper This paper

This paper This paper Manning and Kumpf, 1959 Arakawa, 1965 This paper

z

0

F

2

5

E

X

17. 18. 19. 20.

Striarca symmetrica Barbatia virescens B. obtusoides . Glycymeris imperialis

. .

. .

10 10 (?10a) 10 10

9.0 23.0

0.26 0.84

21.0

0.47

10

21.5

0-44

10

29.5

0.50

4? 4?

9.5 23.0

0.18 0.20

4?

30.5

0.38

.

1Oa 1O a 10a 1Oa 1Oa 1Oa 1Oa

35.0 45-5 75.0 32.0 39.0 49.0 80.0

Modiolus rnodiolus M . phaseulinus . M . agripetua . M . nipponicus . M.flavidua . M.plumescem . Musculua marmoratus

,

lOa 1Oa 1Oa 1O a 1Oa 10a (?lo) 10a 10a

.

1Oa

.

21. G . rotunda 22. Oblimopa jorslcalii 23. ZLimspsis tajimae

24. Mytilus californianus 25. M. CUZU8CU8 . 26. M . galloprovincialis

27. M. edulis 28. 29. 30. 31. 32. 33. 34.

35. M.japonica

.

.

. . .

. .

ca. 0.85

0.54 1-30 1.20 1.30 1.60 1.50

-

c.a. 0-75-2-00

100.0 60.0 11.0 21.0 15.0 25.0

2.00 1.80 0.31 0.46-0'51 0.22 0.50

9.0

0-18

13.0

0.27

Hiroshima This paper Tomioka This paper Hakata Bay Arakawa, 1965 Suruga Bay This paper (80 m dp) Suruga Bay This paper (80 m dP) Sagami Bay This paper (87-95 m dp) Chijiwa Bay This paper Japan Trench This paper (1280 m dp) Japan Trench This paper (1280 m dp) Balboa Bay Edge, 1934 Hiroshima Arakawa, 1963 Hiroshima This paper Hiroshima This paper Hiroshima This paper Hiroshima This paper Port Erin, Plymouth Moore, 1931 Conway Dodgson, 1928 Port Erin Moore, 1931 Port Erin Moore, 1931 Hiroshima This paper Tomioka This paper Tomioka This paper Hiroshima This paper Loch Hine, Moore, 1931 Plymout,h Tomioka This paper

TABLE11-contd.

S O ,

Pellettypes

Species

36. J!!. perfragilis . 37. Brachiodontes citrinirs

46. 47. 48. 49. B0.

51. 52. 53.

I . legurnen Pinctada martensii . Pinna bicolor . Atrina pectinata japonica Ostrea edulis . 0 . denselamellosa . f utamiensis 0 . lurida . Crassostrea gigas .

Length (mm)

Locality*

Ref erences

10a

11.0

0.25

Florida

0'12-0.15 0.36 0.7 1-0.75 0.64

. .

10a 10a

12.0 24.0 41.0 16.5

.

10a

?

?

Tomioka Shirahama Tomioka Hiroshima Florida

.

10a

?

?

Florida

.

10a

17.5

0.39

Florida

?

0.22 1.86 2.07 2.50 1.46-2.28 0.65-0.85

Shirahania Oita Hiroshima Shirahama (Miyagi) Hiroshima

This paper Manning a i d Kumpf. 1959 Manning and Kumpf. 1959 This paper Arakawa. 1965 This paper Arakaua, 1963 Manning a i d Kiimpf, 1969 Manning and Kuinpf. 1959 Manning and Kumpf, 1959 This paper Arakawa. 1963 This paprr This paper This paper This paper

ca. 1.00 0.78

Balboa Bay Hiroshima

Edge, 1934 Arakan a, 1963

. 10a ( ? l o ) . 10a

.

(mm)

Tomioka Florida

.

45. I. radiata

mm )

Ratio length/ breadth

0.13 0.50

Septi,fer bilocularis S. b. pilosus . S . keenae S. virgatus . F'olsella americana

44. Isognomon d a t a

Breadth or width

14.5 31.0

.

.

Average size of pellets

10a ( ? l o ) 10a

.

.

-1

. .

38. Horm3mya exustes 39. 40. 41. 42. 43.

Size of producer (shell length,

0

.

10a 10 . 10 (?10a) . 10 . 10a . 10a ,

. .

10a 10a

49.2 180.0 300.0 ?

40.0 35.0 ' I

x

8 z

%

c:

ic

$

>

.

10a

?

?

. .

. .

10a

58.0

?10

.

.

10a

63.0 7.0

1.27 0-58 0.55-0.75 0.30

8 8

77.0

8

110.0

?

?

?

9

13.5

0.40

?

54. C . virginica

Oita Oita

Galtsoff, 1964 and Haven and M.-Alamo, 1966 Arakawa, 1965 This paper This paper Manning and Kumpf, 1959 Arakau-a, 1965 Arakawa. 1965

Port Erin

Moore, 1931

Florida

Manning and Kumpf, 1959 This paper

?

k

I r'

55. 56. 57. 58.

Saxostrea echinata SpondyEus barbatus S. candidus . Plicatula gibbosa

59. Ammiurn japonica 60. Pecten albicans . 61. P.maximus 62. P. ziczac

.

.

63. Chlamys vesiculoides

64. 65. 66. 67. 68. 69. 70. 71.

Ch. varia . Ch. latiauratus . Ch. nobilis Ch. opercularis . Ch. tigerina . Ch. squamata . Ch. triradiata . Palliolum randolphi

72. Lima lima

z

73. 74. 75. 76.

.

. .

.

.

.

L. sowerbyi . Promantellurn orientale Xantellum amakusaense Anomia lischkei

. .

4

?

?

0*07-0.08 0.15-0-20 (1.80-2.10) 0.15-1 '20 (1.50-2.00)

9 9 9 9 9 9 9a 10a

?

? ? ?

20.0 16.0 23.0 35.0 18.5

0.40 0.40 0.49 0.60 0.30

8a

?

0.23

8a ?8a ? 8a 10

?

27.0 4.0

0.42-0.44 1.09 0.3 1-0.64 0.76-0.9 1

28.0

?

Hiroshima Shirahama Yoron Island Florida

Suruga Bay (8m dP) Port Erin Balboa Bay Mie Port Erin Port Erin Hiroshima Loch Striven Sagami Bay (90 m dp) Florida Shirahama Hiroshima Tomioka Hiroshima

Moore, 1931 Edge, 1934 This paper Moore, 1931 Moore, 1931 This paper Moore, 1931a This paper Manning and Kumpf. 1959 Arakawa. 19ti.5 This paper This paper This paper

TABLE11-contd.

0 4 k b

PelletNo.

Species

77. 78. 79. 80.

Hyriopsis schlegeli Anodonta woodiana Cardita leana . Phlyetaenuchlamys lysiosquillina . Scintilla japonica . Lasaea rubra . Chama rejlexa . Pseudochama retroversa Laternula jlexuosa . L. limicola . Cyathodonta concinna . Lyonaia ventricosa .

81. 82. 83. 84. 85. 86. 87. 88.

types

. .

. . . .

?10 ?10 10

Size of producer (shell length, mm)

Average size of pellets Length (mm)

? ?

? ?

-

34.0

0.31

-

-

0.75

1.68

lla

?

?

1

13.0

0.43

2 4 4 4 4 4 4

Ratio length/ breadth

Breadth or width (mm)

-

-

?

?

?

?

36.0 43.0 32.0

-

-

8.5 10.0

1.8 0.52 0.20 0.31 0.24 0.54

4

19.0

90. Pseudocyrena jloridana

4 (?6)

.

4 4 1 1 (?3) 4 4

89. Donux variabilis

91. 92. 93. 94. 95.

Corbicula japonica C . leana . Joannisiella lunaris Pillucina piridium Tridacna maxima

.

. . .

.

Locality"

References

Shinji Lake Shinji Lake Tomioka Great Barrier Reef Hiroshima

This paper This paper This paper

?

-

-

-

-

?

-

-

Tomioka Hiroshima Tomioka Hiroshima Tomioka Kaneda Bay (50 m dP) Florida

27.5

1.00

-

-

Florida

24.5 24.9

0.20-0.34 0'23-0.26 0.20 0.04-0.07 0.42 0.65

0.24-0.27

-

Shinji Lake Shinji Lake Tomioka Hiroshima Yoron Isl. Yoron Isl.

?

?

6.5 76-0 71.0

-

-

-

1.3 -

Popham, 1939 Arakawa, 1965 Morton, 1956 This paper This paper This paper Arakawa, 1963 This paper This paper Manning and Kumpf, 1959 Manning and Kumpf, 1959 This paper This paper This paper This paper This paper This paper

96. Cardiurn edule . 97. C. quadragenarium 98. Fulvia hungerfordi 99. F. mutica 100. Frigidocardium eos

.

. .

101. Laevicardium undatopictum

.

102. Trigoniocardia medium

.

103. Circe scripta 104. Cione cancellata

.

.

105. Callista chinensis . 106. Prototheca staminea . 107. P. jedoensis . 108. Ruditapes philippinarum 109. Pitar noguchii . 110. Paphia vernicoea . 111. Veremolpa micra . 112. V . minuta 113. V. mindanensis . 114. V . sp. 115. Venus foveolata .

.

116. Gomphina venerqormis 117. Anomalodiscua squamosua 118. Meretrix Euaoria .

?

?

60.0 5.5 ? ?

0.87 0.15 0.82 0.35

0.69 0.28 1.07 0.52

1

?

0.30

0.52

1

20.5

0.25

0.38

3 3 1

10.5 7.5 20.0

172 ?4

37.0 28.0

0.34 0.23 0.22-0.38 0.37 0.21 0.10

0.61 0.35 1.00 0.55 0.42 -

?4 3 4 4 4 4 4 4

54.0 50.0 38.0 27.3 14.5 49.0 9.0 5.8

4

? ?

?I 3 3 3 1

.

. .

4 4

37.5

4 4 4 (?6)

25.0 65.0

?

0.69 1.00 0.30 0.16 0.46 0.60 0.09-0-16 0.1 1 0.08 0.26 0.32 (0.10) 0-46 0.15-020 1-30-2.00

1.00 -

-

-

-

-

? Schkfer, 1953 Balboa Bay Edge, 1934 Tomioka This paper Hiroshima Arakawa, 1963 Sagami Bay This paper (87-95 m dp) Sagami Bay This paper (87-95 m dp) Sagami Bay This paper (87-95 m dp) Tomioka This paper This paper Tomioka Manning and Florida Kumpf, 1959 This paper Hiroshima Manning and Florida Kumpf, 1959 Hiroshima This paper Edge, 1934 Balboa Bay Hiroshima This paper Arakawa, 1963 Hiroshima Tomioka This paper Hiroshima This paper Tomioka This paper Tomioka This paper Tomioka This paper Tomioka This paper This paper Sagami Bay (87-95 m dp) Fukuoka This paper Tomioka This paper Oita Arakawa, 1965

so.

Pellettypes

Species

Size of producer (shell length, mm 1

Average size of pellets Breadth or width (rnm)

Len,gth

Ratio length brearltli

Locality*

References

(mm) ~

119. Dosinia japonica . 120. Saxidornus purpuratus 121. Claudiconcha japonica 122. Gari hosoyai .

123. Hiatula atrata . 124. Nuttalia olivacea

125. Abra alba

.

126. A . nitida

.

.

-

-

-

0.32 0.42 0.18 0.18 1.90 1.17 1.44

1

?

0.50

1.28 1.28 1.17 1.06 1.72 2.25 2.73 1.75

1

?

0'20-0'25

-

-

(?4)

47.0 68.0 10.9 15.9 22.0

-

0.5 1-0.53 1.20- 1.30 0.19-0.20 0.25 0.33 0.16 0.17 1.12 0.52 0.53 0.50 0'25-0.30

4 4 4 1 1 1 1 1 2 2

? ?

54.0 ? ? t

-

~

127. Abrina lunella

.

la

14.0

0.26

0.16

0.61

128. Theora lubrica

.

1 1 1 1 1

5.0 5.5

0.12 0.09 0.12 0.13 0.12 0.16 0.33

0.21 0.lG 0.23 0.22 0.21 0.31 (0.45)

1.80 1.75 1.98 1.77 1.81 1.89 1.35

129. Arcopagia crassa

.

1

1 (?3)

6.5

7.0 8.5 9.5 13.0

Hiroshima This paper Hiroshima This paper Hiroshima Arakawa, 1963 Tomioka This paper Tomioka This paper Tomioka This paper Tomioka This paper Tomioka This paper Hiroshima This paper Hiroshima This paper Fukuoka This paper Loch Striven Moore, 1931a (73 m dP) Loch Striven Moore, 1931a (73 m dP) Hiroshima, This paper Kure, Tomioka Hiroshima This paper Hiroshima This paper Hiroshima This paper Hiroshima This paper Hiroshima This paper Hiroshima This paper Moore, 1931 Plymouth

F

2

5

*X *

P

s

130. Moerella donacina . 131. M . kurodai . 132. Pabulina nitidula . 133. P . minuta 134. P. iridella 135. F . pallidula . 136. Arcopella isselli . 137. Semelangulus miyatensis 138. S. tokubeii 139. Macoma tokyoensis

. .

.

140. M. incongrua

.

141. M . praetexta . 142. M . yoldqormis 143. Psarnmacoma awajiensis 144. Caecella chinensis . 145. Mactra sulcataria . 146. M . crossei 147. M . pulchella . 148. Tressus keenae .

.

149. Schizothaerus nuttalii 150. Raeta rostralis . 151. R.plicatella . i52. Solen roseomaculatus 153. S . strictus . 154.S. gordonis

.

.

.

. .

1 (?3) 1 (?2)

1 1 1 1 2 1 1 la la la la la la la (?1) 1 4 2 2 1 3 3 3 2 2 3 3 3 3 (?4) 2

15.0 9.0 13.0 7.0 17.0 7.0 ?

7.4 ? ? ? t

21.0 22.0 ?

4.0 21.2 ?

23.0 ?

9.8 97.0 93.0 21.0 9.0 9.0 ?

10.0 30.0 85.0

0.36 0.21 0.23 0.15 0.68 0.20 0.18 0.22 0.20 0.23 0.19 0.37 0.37 0.48 0.23 0.10 0.35 0.46 0.46 0.28 0.22 1.85 1.55 0.45 0.25 0.69 0.14 0.11 0.24 0.95-1.08 0.69

(0.47) 0.40 0.28 0.25 1.00 0.22 0.37 0.26 0.25 0.16 0.17 0.20 0.30 0.29 0.43 0.10 0.52

1.30 1.92 1.21 1.62 1.48 1.11 2.06 1.20 1.22 0.70 0.76 0.53 0.81 0.73 0.53 1.00 1.49

-

-

0.97 0.84-1.12 0.39 1.60 1.18 0-25 0.65

2.09 3-4 1.79 0.87 0.77 0.56 2.58

0.96-1 '23 0.21 0.15 0.35 -

1.47 1.36 1.46

1.51

2.19

-

Plymouth Hiroshima Tomioka Tomioka Hiroshima Hiroshima Tomioka Tomioka Tomioka Hiroshima Bay Hiroshima Bay Hiroshima Bay Fukuoka Fukuoka Hiroshima Bay

Moore, 1931 This paper This paper This paper This paper This paper This paper This paper

Balboa Bay Tomioka Hiroshima Tomioka Fukuoka Tomioka (Japan) (Japan) Balboa Bay Kaiieda Bay (50 m dp) Galveston Bay Chijiwa Bay Chijiwa Bay Chijiwa Bay Hiroshima Hiroshima

Edge, 1934 This paper Arakawa, 1963 This paper This paper This paper

This paper This paper This paper This paper This paper This paper This paper

This paper This paper Edge, 1934 This paper Harry, 1969 This paper This paper This paper Arakawa. 1963 This paper

n

(li

ti 0

50

i;

z!

2c

i

m

8 e

tc

2 L-

z6 F

h

s $n 3.

u

w

-1

TABLE11.-contd.

N o*

Pellettypes

Species

Size of producer (shell length, mm )

Average size of pellets _ _ I

Breadth, or width

Length

(mm1

(mm)

Ratio length/ breadth

Locality*

References

Okayama Hiroshima

This paper This paper Moore, 1931 This paper This paper This paper Moore, 1931 This paper Edge, 1934 Purchon, 194 1

~~

155. Sinonovacula constricta 156. Hiatella $accida . 157. M y a truncata . 158. M . japonica . 159. Varicorbula bifrons . 160. Anisocorbula venusta . 16 1. Pholadidea loscombiana 162. Barnea japonica . 163. Zirfaea gabbi . 164. Xylophaga dorsalis .

.

4 3 (?1) 5 5 4 4 5 la 4 1

22.0 19.0

0.28-0.30 0.41

0.56

-

?

?

-

?

75.0 3.60 8.50

0.90-1.20 0.18 0.11

-

Okayama Tomioka Tomioka

?

?

40.0 70.0

1.30 1-60

0.62

?

?

-

-

?

~

?(Japa,n) Balboa Bay

-

?

~

* Detailed localities : (Chijiwa Bay (Korean Straight, Kyushu) Fukuoke (Northern Kyushu) Hakata Bay (Northen; Kyushu) Himeji (Hyogo Prefecture, Honshu) Hiroshima Bay (Inland Sea of Seto) Kaneda Bay Kinkazan (North-eastern Honshu) Mie (Honshu) Miyagi (Northern Honshu) Oita (Eastern Kyushu) Okayama (Inla,nd Sea o f Seto) Sagami Bay (Pacific side, Central Honshu) Shinji Lake (Shimane Pref., Honshu) Suraga Bay (Japan Sea side, Central Honshu) I Tomioka (Kumamoto Pref., Western Iiyushu) Yoron Island (near Ryukyu, Kagoshima Pref.)

I

JApANl i

AUSTRALIA

Great Barrier Reef (North-eastern coast of Australia)

I

Conway Loch Hine UNITED Loch Striven KINGDOM] Plymouth I Port Erin 1Scotland Balboa Bay (California) Galvestou Bay

SCATOLOGICAL STVDIES O F THE BIVALVIA (MOLLVSCA)

379

IV. BIOLOGICAL SIGNIFICANCE OF THE CHARACTERISTIC FORM OF FAECAL PELLETS A. Relation of faecal characteristics to the feeding habit und mode of life of the animal As described in the previous section, the nature and form of the faecal pellets varies widely within the ciliary feeding bivalves. This variation seems to be related more t o feeding habit and mode of life than to systematic position. Kornicker (1962) in discussing the effect of feeding and habitat on the nature of pellets suggests “ t h e shape, composition and consistency of faecal pellets might prove useful in interpreting the feeding habit and habitat of the animal from which they were excreted”. With relation to this, Moore (1939) also states, ‘‘ I n general, carnivorous animals tend to produce faeces of loose consistency, vegetable eaters firmer ones, and deposit eaters the most resistant of all.” Although precise biological information on this matter is still far from complete, the data collected from various sources suggest that the nature and form of pellets do have some relationship, both direct and indirect, to the feeding habit and habitat or to the mode of life of the producer. The Bivalvia are almost all ciliary feeders, collecting small food particles from suspensions or from sedimentary deposits by means of ctenidia and labial palps. Considering the feeding mechanisms in the lamellibranchs in more detail, the Filibranchia, Pseudolamellibranchia and Eulamellibranchia possess ctenidia of increasing complexity for the collection of fine food particles. Particulate matter is sieved from the inhalant current and, after sorting by the palps, suitable quantities and grades are passed into the mouth. Unsuitable or over-numerous particles are rejected from the mantle cavity in the form of mucus-laden masses or pseudofaeces. The pellets in the attached, i.e. epifaunal, suspeiision feeders with filibranch ctenidia, belong to Type 111-10 or 10a, whereas those of burrowing forms such as Oblimopa and Lirnopsis (Limopsidae) belong to Type 11-4. Within the Pseudolamellibranchia, the pellets of the freeswimming forms such as Arnusiurn and Pecten belong t o Type 11-8 and the sessile forms such as Ostrea, Pinctada, Isognomon and Atrina to the former Type (111-10 or 10a). Those of the intermediate forms such as Chlamys belong to Type IIA-9 or 9a. It may be of interest t o note in this connection that there is a striking parallelism in pellet shape (Type 111-10) between byssally attached eulamellibranchs such as Cardita (Carditacea) and sessile filibranchs and pseudolamellibranchs. The highest complexity of ctenidial organization is achieved in Eulamelli-

380

XOHMAN Y . ARAKAWA

branchia, where the pellets also exhibit considerable variation according to feeding habit and habitat. The pellets in the deposit feeding d e e p burrowers such as the Tellinacea, where the labial palps are much enlarged in comparison with the ctenidia which play a much smaller role in grading of particles, belong to Type 1-1 and l a or t o 2, while the suspension feeding burrowers with well-developed eulamellibranch ctenidia such as the Veneracea tend to produce more elongate pellets (Type 11-4). The Erycinacea have distinctive habits, most of them being commensal. I n Phlyctaenachlamys lysiosquillina, which is commensal in the burrows of a shrimp, Lysiosquilla maculata, Popham (1939) in discussing the formation of the pellets in relation to digestive system and mode of life states, “ The absence of mucous glands in the rectum is probably also associated with this movement of water through the mantle cavity. Particles of faecal matter will be shot out through the exhalent opening. There is thus no necessity for the formation of firm faecal pellets, because owing to the violent expulsion of water, there will be less danger of the mantle cavity silting up.” While, on the other hand, in non-commensal forms of this super-family, such as Scintilla japonica, the pellets are ellipsoid with many transverse segments and with considerable amount of mucus (Type 1-2). The most strikingly modified feeding habits are those of the Protobranchia and Septibranchia. I n the deposit feeding protobranchs, the palp proboscides instead of the ctenidia play the leading role in feeding. The ctenidia serve primarily as respiratory organs, largely unconcerned with collecting food. Moore (1931a) shows that the pellets in these protobranchs, such as Nucula, are characteristically resistant sculptured rods (Type 11-7, 7a and 7 b ) . The carnivorous septibranchs are another special case. They feed usually on relatively large animals, such as copepods or the carcases of these, drawn into the infra-branchial chamber by means of convulsive muscular pumping action of the ctenidial septum. The pellets in these, the only carnivorous bivalves, belong t o Type 11, which are indeterminate in shape being very soft and loose in consistency. I n this connection it is of interest to note that in the relationship between types of pellet and mode of feeding and habitat, the bivalves are paralleled by other ciliary feeders such as polyzoans, brachiopods, tunicates and Amphioxus. To give some remarkable instances, the faecal pellets of the attached filter-feeding tunicates, Ciona, Ascidia and Styela are ribbon-shaped, quite resembling in type those of the filibranch bivalves with similar habits (Fig. 12). According to Edge’s observations (1934), Styela is less selective in its feeding than Ciona, for its pellets contain much coarser material of an indigestible nature than

SCATOLOGICAL STIJDIES O F THE BIVALVIA (MOLLUSCA)

381

do those of Ciona, while in Dolichoglossus, which lives on the mud flats, the pellets resemble in shape those of a mud-dwelling polychaete, Lumbrinereis, except that the earthy material taken in by Dolichoglossus is in a more finely divided condition. Further notes on this subject are given by Moore and Kruse (1956) who state, " The type of faeces emitted varies according to the type of feeding of the animal. Some deposit feeders such as Holothurians and Polychaeta (Arenicola)

A

B

C

D

Fig. 12. Faecal pellets of tunicatss: A. Ciona intzstinalis; B. Ciona sp.; C. Ascidia ahodori ; D. Styela clava.

pass great masses of sand or mud which may appear temporarily on the surface as coiled rods but rapidly disintegrate. Animals which eat the larger algae, again without taking in skeletal material, usually produce too loose a faecal mass to be either lasting or distinctive. The most characteristic and lasting pellets are found in these grazers and filter feeders which take in a considerable amount of indigestible roughage with their food." I n any case, taken in conjunction with the data on the relations between the various types of pellets and the ctenidia (Table V ; Fig. 22, p. 407), these facts indicate that the mode of feeding in the bivalves is reflected t o a greater or lesser extent in the nature and form of the pellets.

B. Relation of faecal characteristics to the structure and #functionof the digestive organs Although, as mentioned above, the nature and form of the faecal pellets in the bivalves, to a greater or lesser degree, must be related t o feeding habits and mode of life of the producer, they are finally determined by the structure and function of the digestive organs. The stomach, style-sac, digestive diverticula, mid-gut, rectum and anus are all intimately associated with the formation and elimination of faecal pellets.

w

TABLE 111. COMPARISON OF

THE

DISTRIBUTION OF THE PELLET-TYPES WITH VARIOUSSCHEMES OF CLASSIFICATION OF THE BIVALVIA

00 Ei.

Comparison of various schemes Pellettypes

Classijcation (after Purchon, 1963)

Dall Pelseneer (1894) (1911)

Thiele ( 1935)

cox (1960)

References .-

BIVALVIA OLIGOSYRINGIA

P R O T O B R A N C H I A (GASTROPROTEIA)

*z

Nuculacea Nuculidae 1. Nucula hanleyi Winckworth . 2. N . moorei Winck. . 3. N . nucleus (L.) . 4. A7. sulcata Broiiii . 5. N. tenuis (Montagu) . 6. N . turgidu Leckenby and Marshall 7. AT.sp. .

r:

.

. . . . . .

.

11-7a 11-7 11-7a 11-76 11-7 11-7n 11-7

Pr Pr Pr Pr Pr Pr Pr

Tx Tx Tx Tx Tx TX Tx

PI P1 P1 P1 P1 P1 PI

Moore, Moore, Moore, Moore, Moore, Moore, Moore,

Pr Pr Pr Pr

Tx Tx Tx Tx

P2 P2 P2 P2

Moore, 1939 This paper This paper This paper

1931a 1931a 1931a 1931a 1931a 1931a 1933

Nuculanacea Nuculanidae 8. Nuculana niinuta (Muller) . 9 . P o d a n d i a japonica (Adams and Reeve) 10. Portlandiella beringii (Dall) . 11. Saccella sematensis Snzuki and Ishizuka

.

. . .

11-6 11-6 11-G 11-G

P P P P

SEPTIBRANCHIA (GASTRODEUTEIA)

Poromyacea Cuspidariidae 12. Cardiomua qouldiana septemtrionalis (Kuroda) 1 1 " " 11 13. Plectodon ligula (Yokoyama)

A A

S S

Eu(An) Eu(An)

H6 H6

This paper This paper

P

E'

Tx

Pt 1

. . . . .

P P P 111-10 111-10 ( ? I o n ) P P 111-10

F F F F F

Tx Tx Tx Tx Tx

Pt Pt Pt Pt Pt

Manning and Kumpf, 1959 Arakawa, 1965 This paper This paper This paper Arakawa, 1965

.

111-10

111-10

P P

F F

Tx

.

Tx

Pt 1 Pt 1

This paper This paper

. .

11-4 11-4

P P

F F

Tx Tx

Pt 1 Pt 1

This paper This paper

.

111-lcla

P

F

Ariis

Pt 4

Edge, 1934

POLYSYRINGIA

GASTROTRITEIA

Arcacea Arcidae 14. Arca umbonata Lamarck

.

111-10

15. Anadara subcrenata (Lischke) . 16. A . broughtoni (Schrenck) 17. Striarca symmetrica (Reeve) . 18. Barbatia virescens (Rve) 19. 23. obtusoides (Nyst) .

111-10

111-10

1 1 1 1 1

Limopsacea Glycymeridae 20. Clyeymeris imperialis Kuroda 21. G. rotunda (Dunker) .

.

Limopsidae 22. Oblimopa forskali (A. Adams) . 23. ?Limopsis tajimae Somerby .

Mytilacea Mytilidae 24. M y t i l u s ealijornianus Conrad

.

TABLE111-contd.

Comparison of various schemes Classification (after Purchon, 1963) 25. M . curuscus Gould 26. M. galloprovincialis Lam. 27. M. edulis (L.) .

.

28. Modiolus modiolus L. . 29. M. phaseolinus (Philippi) . 30. M . agripetus (Iredale) . 31. M. nipponicus (Oyama) . 32. M. Jlavidus (Dlir) . 33. M. plumescens (Dkr) . 34. Musculus marmoratus (Forbes) 35. M. japonicus (Dkr) . 36. M. perfragilis (Dkr) . 37. Brachiodontes citrinus Roding . 38. Hormomya exustes (L.)

.

39. Septifer bilocularis (L.) . 40. S . b. pilosus (Rve) . . 41. S. keenae Nomura . 42. S. virgatus (Wiegmann) . 43. Volsella americana Leach

.

Pellettypes

Dull Pelseneer (1894) (1911)

Thiele (1935)

cox (1960)

111-1Oa 111-1Oa 111-lOa

P P P

F F F

Anis Anis -lnis

Pt 4 Pt 4 Pt 4

111-l0a 111-lOa 111-l0a 111-lOa 111-l0a (?lo) 111-lOa 111-lOa 111-10a 111-lOa ( ? l o ) 111-lOa

P P P P P P P P P P

F F F F F F F F F F

Anis his Anis Anis Anis his Anis Anis Anis Anis

Pt Pt Pt Pt Pt Pt Pt Pt Pt Pt

111-1Oa

P

F

Anis

Pt 4

111-l0a ( ? l o ) 111-lOa 111-10a 111-l0a 111-lOa

P P P P P

F F F F F

h 1 S

Pt, 4 Pt 4 Pt 4 Pt 4 Pt 4

Anis Anis Anis .his

4 4 4 4 4 4 4 4 4 4

References Arakawa, 1963 This paper Dodgson, 1928 and Moore, 1931 Moore, 1931 Moore. 1931 This paper This paper This paper This paper Moore, 1931 This paper This paper Manning and Kumpf, 1959 Manning and Kumpf, 1959 This paper Arakawa, 1965 This paper Arakawa, 1963 Manning and Kumpf, 1959

E* +

s P

r! ?

Pteriacea Isognomonidae (Vulsellidae) 44. Isognomon alata Gmelin . 45. I . radiata Anton

.

46. I . legumen (Gmel.) Pteriidae (Aviculidae) 47. Pinctada martensii (Dkr)

.

111-lOa

P

Ps

Anis

Pt 2

.

111-IOU

P

Ps

Anis

Pt 2

.

111-lOa

P

Ps

Anis

Pt 2

.

111-10

P

Ps

Anis

Pt 2

Manning and Kumpf, 1959 Manning and Kumpf, 1959 This paper

m d

c

c3 0

F

.

0

Ota, 1959 Ota and Fukushima, 1961 Arakawa, 1963

Pinnacea Pinnidae 48. Pinna bicolor Gmel. 49. Atrina pectinata japonka (Rve) Ostreacea Ostreidae 50. Ostrea edulis L. . 51. 0. demelamellosa futamiensis Seki 52. 0. lurida Carpenter . 53. Crassostrea gigas (Thunberg) . 54. C. virginica (Gmel.) .

.

.

. .

111-lOa (?lo) P 111-10 P

Ps Ps

Anis Anis

Pt 2 Pt 2

This paper This paper

.

111-lOa 111-lOa 111-lOa 111-lOa 111-lOa

P P P P P

Ps Ps Ps Ps Ps

Anis Anis Anis Anis Anis

Pt Pt Pt Pt Pt

Pt 3

This paper This paper Edge, 1934 Arakawa, 1965 Galtsoff, 1964, Haven and MoralesAlamo, 1966 hakawa, 1965

Pt 3 Pt 3

This paper This paper

. . . .

55. Saxostrea echinata (Quoy and Ga.imard)

.

111-lOa

P

Ps

Spondylidae 56. Spondylus barbatus Rve 57. S. candidus Lam. .

. .

?III-lO 11-4

P P

Ps Ps

Ahis Anis

3 3 3 3 3

8 3c U

0 Y

*

B

5

k

f c z 0

h

F r

5

d kv

w CI)

-3

TABLE111.-contd. Comparison of various schemes

Classification (after Purchon, 1963)

Pellettypes

Dull Pelseneer (1894) (1911)

111-10

P

Thiele (1935)

Cox (1960)

References

GASTROTETARTIKA

Pectinacea Plicatulidae 58. Plicatula gibbosa Lam.

.

Ps

Anis

Pt 2

Manning and Kumpf, 1959

Amusiidae 59. Amusium japonieum (Gmel.) . Pectinidae 60. Pecten albicans (Schroter) . 61. P . maximus (L.) . 62. P. ziczac (L.)

11-8

P

Ps

Anis

Pt 2

Arakaw-a, 1965

11-8 11-8 (?II-8)

P P P

Ps Ps Ps

Anis Anis Anis

Pt 2 Pt 2 Pt 2

63. Chlamys vesiculoides (Dkr) 64. Ch. varia (L.) 65. Ch. latiauratus (Conrad) . 66. Ch. nobilis (Rve) . 67. Ch. opercularis (L.) 68. Ch. tigerina (Miiller) . 69. Ch. squamata (Gmel.) . 70. Ch. triradiata (Mul.) . 7 1. Delectopecten randolphi (Dall)

IIA-9 IIA-9 IIA-9 IIA-9 IIA-9 IIA-9 IIA-9 IIA-9a 111-lOa

Ps Ps Ps Ps Ps Ps Ps Ps Ps

Anis Anis Anis Anis Anis Anis Anis Anis Anis

Pt Pt Pt Pt Pt Pt Pt Pt Pt

Arakawa, 1965 Moore, 1931 Manning and Kumpf, 1959 This paper Moore, 1931 Edge, 1934 This paper Moore, 1931 Moore, 1931 This paper Moore 1931a This paper

.

.

2 2 2 2 2 2 2 2 2

x x

0

E Er 5

?

Wacea Limidae 72. Lima lima L. 73. L. sowerbyi Deshayes . 74. Promantellurn orientale (Ad. and Rve) 75. Mantellum amakusaense Habe

II-8a

P

Ps

Anis

Pt 2

11-8a 11-8a? 11-8a?

P P P

Ps Ps Ps

Anis Anis Anis

Pt 2 Pt 2 Pt 2

Manning and Kumpf, 1959 Arakawa, 1965 This paper This paper

z

d

0

r

0

g

b

Anomiacea Anomiidae 76. Anornia lischkei Dautzenberg

111-10

P

Ps

Anis

Pt 3

This paper

i i m

Unionacea Unionidae 77. Hyriopsis schlegeli (v. Martens) 78. Anodonta woodiana (Lea)

.

.

111-lo? 111-lo?

P P

E E

Eu (Sch) H5 Eu (Sch) H 5

This paper This paper

Carditacea

H

E E -4

b

Carditidae 79. Cardita leuna Dkr

111-10

T

E

Eu(H)

H6

This paper

*5

h

z

0

r r

Leptomcea Galeommidae (Galeommatidae) 80. Phlyetaemhhmys lysiosquillina Popham 81. Scintilla japonica (A. Ad.)

.

Erycinidae 82. Lasaea rubra (Montagu)

il)

.

< m

.

I-1

T T

E E

Eu(H) Eu (H)

H6 H6

Popham, 1939 Arakawa, 1965

1-2

T

E

Eu(H)

H6

Morton, 1956

1l a

-e W

a, -J

cx.

cx.

TABLEIII.-contd. Comparison of vario 11s schemes

Classification (after Purchon, 1963)

Chamacea Chainidae 83. Chamn reflexa Rve 84. Psezdochama retroversa (Lischke)

11-4 11-4

T T

E: E

Eli ( H ) Eu ( H )

HB HB

This paper This paper

11-4 11-4

A A

E E

Eu (An) Eu (An)

HI H1

This paper Arakawa, 1963

E

Eu (An)

HI

This paper

Laternulacea Laternulidae 85. Latern irla flexuosa (Rve) 86. L . lirnicola Rve . Thraciidae 87. Cyathodonta concinna (Gould)

.

11-4

il

Pandoracea Lyonsiidae 88. Lyonsia ventricola Gould

IT-4

A

E

En (An)

H1

This paper

11-4

T

E

ELI(H)

H6

Manning and Kumpf, 1959

Tellinacea Donacidae

89. Donax variabilis Say

GASTROPEMPTA

Corbiculacea Corbiculidae 90. Pseudocyrena Jloridana Conrad 91. Corbicula japonica Prime 92. C. Zeana Prime .

. .

.

11-4 ( ? 6 )

T

E

Eu (H)

H6

. .

11-4 11-4

T T

E E

Eu (H)

H6 H6

ELI(H)

Manning and Kumpf, 1959 This paper This paper

**

0

r 0 0

H

Lucinacea

c1

Ungulinidae 93. Joannisiella lunaris (Yokoyama)

P

.

.

1-1

T

E

Eo (H)

m e

H6

Thispaper

9

c

Y

Lucinidae 94. PiZluci.napisidiurn (Dkr)

.

E 1-1 (?IA-3)

T

E

Eu (H)

H6

Thispaper

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"ridacnacea Tridacnidae 95. Tridacna maxima (Roding)

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,

.

11-4

T

E

En (H)

H6

This paper

I-l? IA-3 IA-3 IA-3 1-1 IA-3 I-l?

T T T T T T T

E E E

Eu Eu Eu Eu Eu Eu Eu

(H) (H) (H) (H) (H) (H) (H)

HG H6 H6 H6 H6 H6 H6

Schafer, 1953 Edge, 1934 Thispaper Arakawa, 1963 This paper Thispaper Manningand Kumpf, 1959

E

Cardiacea Cardiidae 96. Cardium edule L. . . . 97. Trachycardium quadragenarium (Conrad) . 98. Pulvia hungerjordi (Sow.) 99. F . rnutiea (Rve) . . 100. Frigidocardium eo8 (Kuroda) 101. Laevicardium undatopicturn (Pilsbry) . . 102. Trigonocardium medium I..

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w

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W

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TABLE111--contd.

CD

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Comparison of various schemes ( 1894)

Pelseneer (1911)

Thiele (1935)

1-2, 1-1 11-4?

T T

E E

Eu (H) ELI( H )

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. . 105. Callista ckinensis (Holten) 106. Prototheca staminea (Conrad) . 107. P . jedoensis (Lischke) . . 108. Ruditapes philippinarum (Ad. and Rve.) 109. Pitar noguchii Habe . . . . 110. Paphia vernicosa (Gould) 111. Veremolpa micra (Pils.) . . . . 112. V . minuta (Yokoyama) . 113. V. mindanensis (Smit8h) . 114. V. sp. . 115. Venus foveolata Sow. . . 116. Gomphina veneriformis (Lam.) . . . . 117. Anomalodiscus squamosus (L.) . 118. Meretriz lusoria (Rod.) 119. Dosinia japonica (Rve) . . 120. Saxidomus purpuratus (Sow.) .

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This paper Manning and Kumpf, 1959 This paper Edge, 1934 This paper Arakawa, 1963 This paper This paper This paper This paper This paper This paper This paper This paper This paper Arakawa, 1965 This paper This paper

Petricolidae 121. Glaudiconcha japonica (Dkr )

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Eu (H)

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Pellettypes

ChssiJcation (after Purchon, 1963)

Dull

Cox (1960)

References

Veneracea Veneridae 103. Circe scripta (L.) 104. Cione cancellata L.

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H6

Tellinaces Psammobiidae (Garidae, Asaphidne, Sariguiiiocolariidae) 122. Gari hosoyai (Habe) . . r-1 123. Hiatula atrata (Rve) . . 1-1 124. Soletellina olivacea (Jay) . . 1-2 Semelidae 125, Abra alba (Wood) . 1-1 126. A . nitida (Mu].) . . r-1 127. Abrina lunella (Gould) . . I-la 128. Theora Zubrica (Hinds) . . 1-1 Tellinidae 129. Arcopagia crassa (Phnnant) . . 1-1 (?3) . 1-1 ( ? 3 ) 130. Moerella donacina (L.) . . 1-1 ( ? 2 ) 131. M . kurodai (Makiyama) 132. Nitidotellina nitidula (Dkr) . . 1-1 133. Fabulina minuta (Lischke) . . r-1 134. F . iridella (v. Martens) . 1-1 135. F . pallidula (Lischke) . . 1-1 . . 1-2 136. drcopella isselli (H. Ad.) 137. Semelangulw miyatensis (Yokoyama) . 1-1 1 3 8 . 8 . tokubeii Habe . . 1-1 139. Macoma tokyoemis (Makiyama) . . I-la 140. M . incongrua (v. Martens) . . 1-la 141. M . praetezta (v. Mart.) . . I-la . . I-la ( 1 ) 142. M . yoldiformis Carpenter 143. Psammacoma awajiensis Sow. . 1-1

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Moore, 1931a Moore, 1931a This paper This paper

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Moore, 1931 Moore, 1931 This paper This paper This paper This paper This paper This paper This paper This paper This paper This paper This paper

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Arakawa , 1963

Edge, 1934 This paper

m

a

z

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8

F

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Mactracea Mesodesmatidae 144. Caecella chinensis Desh.

.

11-4

Eu (H)

0

E

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f3

TABLE111.-contd. Comparison of various schemes

Classification (after Purchon, 1963)

Mactridae 145. Mactra sulcataria Rve . 146. M. crossei (Dkr) . 147. M. pulchella Philippi . 148. Tressus keenae (Kuroda and Habe) 149. Schizothaerus nuttalii (Conrad) . 150. Raeta rostralis (Rve) . 151. R. plicatella Lam.

Dull

Pelseneer (1911)

Pellettypes

(1894)

1-2 1-2 1-2 IA-3 IA-3 1-2 1-2

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IA-3 IA-3 (?4) 1-2

T T T

E E E

11-4

T

I A - 3 (?1)

T

Thiele (1935)

cox (1960)

References

H6 H6 H6 H6 H6 H6 H6

This paper This paper This paper This paper Edge, 1934 This paper Harry, 1969

Eu (Ad) Eu (Ad) Eu (Ad)

H6 H6 H6

This paper Arakawa, 1963 This paper

E

Eu (Ad)

H6

This paper

E

Eu (Ad)

H6

This paper

Solenacea Solenidae 152. Solen roseomaculatus Pils. 153. S. strictus (Gould) 154. S. gordonis Yokoyama

.

Novaculidae 155. Sinonovacula constricts (Lam.)

.

Hiatellacea Hiatellidae 156. Hiatella flaccida (Gould)

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Myacea Myidae 157. M y a truncata L. . 158. M y a japonica J a y

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11-5 11-5

T T

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E u (Ad)

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H2 H2

Moore, 1931 This paper

b-

Corbulidae

159. J'aricorbula bifrons (A. Ad.) 160. Anisocorbula wenusta (Gould)

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. .

11-4 11-4

T T

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Eu (Ad) Eu (Ad)

H2 H2

This papcr This paper

Y 0

P 0

2 Q

k

Pholadacea (Adesmacea) Pholadidae

161. Pholadidea loscombiana Turton 162. Barnea ,japonica Yokoyama . 163. Zirfaea gabbi Tryon .

. . .

11-5 I-la 11-4

T T T

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En (Ad) En (Ad) Eu (Ad)

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Moore, 1931 This paper Edge, 1934

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Purchon. 1941

Xylophaginidae

164. Xylophaga dorsalis Turton

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c Abbreviations : A. Anomalodesmacea ; Anis. Anisomyaria ; E . Eulamellibranchia ; E u (Ad). Eulamellibranchia (Adepedonta): E u (An). Eulamellibranchia (Anomalodesmata) ; Eu (H). Eulamellibranchia (Heterodonta) : E u (Sch). Eulamellibranchia (Schizodonta) : F. Filibranchia ; H1. Eudesmodontida ; H2. Asthenodontida ; H5. Naiatida; H6. Heterodontida : P. Prionodesmacea : P I . Paleotaxodontida ; P2. Lipodontida : Pr. Protobranchia : Ps. Pseudolamellibranchia ; Pt' 1. Eut,axodontida ; Pt 2. Pteroconchida; P t 3. Colloconchida ; P t 4. Isofilibranchida ; S. Septibranchia ; T. Teleodesmacea ; Tx. Taxodonta.

3 5P

5m P

v

0

W

W

394

KOHMAN Y. ARAKAWA

The structure and fuiiction of bivalve digestive organs have been intensively studied by many workers. Owen (1966), in reviewing work on movement of food through them, mentions that primitively within the style-sac the muscular action of the walls forms a faecal rod which is rotated and passed into the mid-gut by the action of the cilia lining the sac, and that the formation of such a faecal rod or protostyle is undoubtedly a primitive function of the style-sac. Yonge (1960) suggests, " The stomach itself probably early contained a ciliated sorting region, an area of cuticle forming a gastric shield, and a ' style-sac ' region initially concerned with the consolidation of faecal material . . . a matter of prime importance when the gut opened into the respiratory (i.e. mantle) cavity. Lengthening of the gut posterior t o the stomach was also associated with the formation of firm faecal pellets. . . " and he (1935) showed that the average p H value of the various parts of the gut in bivalves is concerned largely with controlling the viscosity of the mucus in the food string: in the case of Ostrea edulis, the mucus becomes less viscous in the lower pH of the stomach juice, about 5 . 5 , and this assists the shedding of its load; the intestinal pH is higher, 5.7 in the mid-gut and 6.0 in the rectum, where the more viscous mucus binds the contents into firm pellets. Let us now speculate about the relationships between the nature and form of the faecal pellets and the structure and function of the digestive organs in the bivalves.

Stomach and its associate organs Purchon ( 1963), who surveyed structures of the stomach throughout the Bivalvia, suggests that the class can be divided according to function and structural features of the stomach into five orders: Gastroproteia (Protobranchia), Gastrodeuteia (Septibranchia), GasA comparison of trotriteia, Gastrotetartika and Gastropempta. different types of the faecal pellets with the form of the stomach in various bivalve orders is shown in Table V I and Fig. 25. This would lead us to suppose that the nature and form of the pellets is more closely related t o the structure and function of the stomach than to those of the ctenidia. In the subclass Oligosyringia, the stomach is very primitive and simple in many ways, being characterized by the presence of two or three ducts from the digestive diverticula and of strongly muscular walls which are associated with the need for trituration or squeezing of relatively large and coarse materials. Within this subclass, the deposit feeding Protobranchia with stomach of Type I have very resistant faecal rods with longitudinal surface sculptures (Pellet-type 11-6, 7 , 7a and 7 b ) . It is of interest to note that

SCATOLOGI('AL YTCTDIES OF THE BIVALVIA (MOLLUSCA)

395

the characteristic sculpturing of the pellets in the Nuculidae is produced by appropriate structures in the walls of the mid-gut which possess longitudinal plicate ridges with long cilia which are highly specific in number and arrangement (Moore, 1931a). I n the carnivorous Septibranchia with stomach ofType 11, the pellets are so soft and loose in consistency that they are indefinable in shape (Pellet-type 1 1 ) . Though Purchon (1958, 1959 and 1963) has pointedly emphasized that the Septibranchia and the Protobranchia are related in structure and function of the stomach more closely t o each other than either is t o any other bivalve group, nevertheless there is little resemblance of pellet-characteristics between the two*. This noticeable difference may be due largely t o the kind of food and to the structure of the mid-gut where the removal of water takes place and the resulting solidification determines the final form of the faecal pellets. It is noteworthy that the mid-gut in the septibranchs is much shorter than that in the protobranchs and that the lengthening of tjhe intestine is associated with the formation of firm faecal pellets (Yonge, 1960). In the subclass Polysyringia the stomach is comparatively complex, being characterized by the well-developed sorting area, the intruded major intestinal typhlosole as well as by the large number of ducts from the digestive diverticula. Within this subclass, the Gastrotriteia with stomach of Type 111produce ribbon-like pellets which are assigned to Pellet-type 111-10 or 10a. But there are some notable exceptions, namely the pellets of Ohlimopa and Limopsis in the Limopsidae (Pellet-type 111-4) where the stomach differs considerably from that of other members of this group (Purchon, 1957). I n the Gastrotetartika with stomach of Type IV, the pellet-t,ypes are widely distributed among families and genera, ranging from 1-1 to 111-10, or t o Ila, exclusive of IA-3, 11-5, 6, 7 and their subtypes. Of these, 11-8, IIA-9 and 111-10 are of common occurrence in this group. This uneven distribution of pellet-types seems to have an association with the anomalies in the distribution of Stomach-Type IV. The Gastropempta which achieve the highest complexities of gastric organization (Type V) comprise six pellet-types ranging from 1-1 to 11-5, and the relatively high frequency occurs in Types 1-1 and 11-4. I n view of the above we find it difficult to avoid the conclusion that the stomach in the Bivalvia is concerned with the determination of the primary characteristics of the faecal pellets.

Mid-gut The mid-gut appears to be still more closely associated with the formation of the faecal pellets. After digestion has occurred in the * See footnote on p. 320.

396

KOHMAN . ' 1 ARAKA\VA

stomach the faecal strings are conveyed into the mid-gut where the ciliary action of the epithelium instead of pcristaltic motion is primarily concerned with transport, since a muscular layer is either absent or poorly developed in the gut-wall. When passing through the gut, the mucus-bound faeces may be gradually solidified into firm pellets by the withdrawal of water as well as by the high intestinal p H value, and a t t.he same time they may be moulded externally by structures on the gut-wall, such as cilia, longitudinal folds, plicate ridges and typhlosoles. The moulding of the ovoid pellets such as those of the Tellinacea (Pellet-type I) may take place at the rear of the stomach where the faecal material is subdivided or pinched off by a periodical contraction of t,he " pyloric sphincter," since a series of small pelletts are observed lining up throughout the tract, one directly behind the other (Fig. 13). A similar process of formation may occur in the Cardiidae with seg-

Fig. 13. Faecal pellets aiirl initl-gut ( ~ f 'nlcwotrttr toLyortisis: A . Faecal pellets ( x 2 0 ) : B. Cross-section of mitl-gut ( x 100) ; C . Imigitidinal section of mid-gut ( x 30) ; D. Same as C .

SCATOLOGICAL STPDIES OF THE BIVALVIA (MOLLUSCA)

3%

rnented rod-type pellets (Pellet-type I A ) (Fig. 14). In relatJionto this, Jegla and (ireenloerg ( 1 988) suggest, “ If the feces arc of appropriate consistency, and if the peristaltic contractions are sufficiently powerful, the gut contents will be molded into a string of oval pellets.” Kornicker (1962) also makes some suggestions : “ I n general, oval pellets are not completely isolated from each other, but appear like strung

Fig. 14. Longitudinal section of the mid-gut of Fulvia nmlicn to show the faecal rod with segmentation (greatly magnified).

beads, one connected to the other. After elimination, the slender connecting links are broken and the oval pellets become discrete bodies.” I n most of the Veneridae with unsculptured faecal rods (Pellet-type 11-l),the lumen of the mid-gut is very simple and is circular in crosssection. The pellets with a slight spiral groove, such as those of Mya (Pellet-type 11-5), Mactra and of Tressus (Pellet-type I-2), may be rotated rather rapidly as they emerge (Moore and Kruse, 1956), because there are no appropriate structures on the gut walls which could be responsible for this grooving (Fig. 15). The three prominent longitudinal grooves impressed on the outside of the faecal rod in Chlamys (Pellettypes I I A - 9 and 9a) are apparently formed by corresponding longitudinal thickenings of the gut-wall (Fig. 16), as previously mentioned for Nuculu (Moore, 1931a). The faecal pellets in Pecten (Pellet-type 11-8) may be formed where the gut (mid-gut) is narrow and may afterwards be wound into a ball where the gut (rectum) is wide (Fig. 20). I n the sessile bivalves with ribbon-shaped pellets (Pellet-types 11- 10 and lOa), such as Ostrea, Anadara and Anomia, the lumen of the mid-gut is nar-

398

Fig. 15. Mid-gut of Maclra snlratarirr : A . Cross-scction ; R. Longitudinal section: C. Same RS B (greatly magnifird).

SCATOLOGICAL STUDIES O F THE HIVALVIA (MOLLUSCA)

399

rowed by one or two parallel-running intestinal typhlosoles which are applied to the surface of the ribbons (Figs. 17, 18 and 19). On the formation of faecal ribbons in Mytilus edulis, Dodgson (1928) suggests ‘< the characteristic folds are determined by the shape of the anus through

Fig. 16. Faecal pdlets and mid-gut of Chlarnys spuamata. Top : Vaocal pcllets ( x 50) ; bottom : Mid-gut (cross-section).

which the soft mass is propelled. This opening is more or less similar in shape t o that of a cross-section of the lumen of the rectum, which is bicrescentic, owing t o the’ presence of a double longitudinal ridge or typhlosole.” Rectum

Jegla and Greenberg (1968) who carried out a n intensive study of the structure of the bivalve rectum emphasize that the shape and composition of the faeces are useful indicators of the functional mor-

403

KOHMAN Y . ARAKAW’A

phology of the rectum. In discussing the role of the rectum in faecal formation, they suggest that : “ Sculpturing and particle distribution are largely dependent upon the mechanism by which feces are propelled through the rectum. If propulsion is by means of ciliary tracts,

Fig. 17. Mid-gut in the genera Crassostrea and Ostrea. Top : Crassostrecc gigas (orig. ;) bottom: Ostrea edulis (after Yonge, 1926).

with little muscle involvements, then there can be no gross mechanical activity accompanying the passage of the fecal rod. Consequently, the distribution of sediments determined by the ciliary sorting systems of the stomach and gut will be undisturbed; similarly, the surface sculpturings of the rod will be preserved. On the other hand, a muscular rectum would probably obliterate surface sculpturing, and also thoroughly mix the sediment.” They continue : “ the distribution of muscle among bivalve rectums is well correlated with the distribution of sculptured and unsculptured feces : muscular rectums are found mainly among the Heterodonta. Protobranch and anisomyarian rectums have, characteristically, thin walls with little muscle.” Making r2

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

401

rough comparison between the nature of the rectum and that of the stomach type, they suggest, further, that the distribution of the anisomyarian rectum (except for the Pectinacea which have a Type 4 stomach) is identical with that of the stomach Type 3 and not of the ctenidium-palp association (Stasek, 1963).

Fig. 18. Mid-gut and anus in Anadara subcrenata. Top : Mid-gut (cross-section) ( x 30) ; bottom : Anus ( x 12).

These findings demonstrate that the bivalve rectum is concerned in determining the final characteristics of the faecal pellets. Though these investigations need t o be carried out on a much larger scale, the general conclusion to be drawn is that the structure

402

KOHMAN Y . ARAKAWA

and function of the stomach, mid-gut and rectum assume the principal role in deciding the characteristic form and nature of the bivalve pellets.

LA..-.: Fig. 19. Mid-gut of Anonzia Zischkei (cross-section).

n

Fig. 20. Mid-gut, of Pecten albicaras (cross-section).

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

403

V. USE OF PAECAL PELLETS AS A SYSTEMATIC INDEX It has been stated that the nature and form of many bivalve faeces although so varied are yet so constant within the smaller taxonomic divisions that they are a useful index for identification. Moore (1931) adduced typical examples of this sort, using a number of British marine molluscs, and since then much attention has been drawn to their use in classification. Winckworth (1931) used the faecal characters along with other criteria as a basis for the separation of several species of the genus Nucula. Subsequently to this, Moore (1931a) showed many illustrative examples from a variety of molluscan species. Abbott (1954) employed successfully the faecal characters together with other indices as a basis for removing the gastropod genus Echininus from the family Modulidae and placing it in the Littorinidae. The more recent work of Taylor (1966) demonstrates a difference in faecal characters between the fresh-water gastropod families Bithyniidae and Hydrobiidae. On the other hand, Dinamani (1969) demonstrates that there is a conspicuous variation in faecal characters in an animal as a result of his recent feeding experiments on bivalves ( M y t i l w , Gardium), using different algal cultures. According to his observations, the form and type of faecal ribbon greatly vary depending upon : (1) the time ingested material is retained within the g u t ; (2) the type of food ” material used; (3) the rate of its passage through the gut. I n the course of the study on the seasonal change of the rate of faecal discharge in Pinctada martensii, it was shown by Ota (1959)that during a certain period prior to the spawning season, these pearl oysters tend to produce atypical continuous ribbons of soft consistency and considerably flattened in transverse section. He suggests that this characteristic change in nature and form of the ribbons may possibly be related t o certain physiological conditions (e.g. unusual high p H value) in the animal which take place prior to the spawning season. Moore (1931a) also noted that in Mytilus edulis the typical pellets of well-fed animals are ribbon-shaped and bi-crescentic in section, while the starved animals tend to produce a thin and fragile ribbon which is often atypical in shape. It is apparent from Tables 111 (p. 382) and IV that the systematic value of the faecal pellets is not always positive. While the nature and the form of bivalve faecal pellets are variable, generally there is uniformity within a family. This familial similarity seems generally t o agree with the form of the rectum as suggested by Jegla and Greenberg (1968). Within 45 families in which faecal pellets have been studied, those within 20 or more are strikingly similar whereas in only some 6 I‘

404

KOHMAN Y . ARAKAWA

are there marked scatological differences between genera and species (Tables I11 and IV). Apart from the Limopsidae and the Spondylidae, there is remarkable uniformity of pellets within the order Gastrotriteia. TABLEIV. SIMILARITIESOF PELLET-TYPES AMONG VARIOUS TAXONOMIC DIVISIONS Order level (Pellet-type)

Familial level (Pellet-type)

Generic a n d specific level (Pellet-type) -~

Nuculidae GASTROTRITEIA (PROTOBRANCHIA) Nucula hanleyi] (111-10, 10a) Nuculanidae (11-6) N. nucleus (SEPTIBRANCHIA) (except for N . turgida Spondylidae a n d Cuspidaridae ( 1 1) N. rnoorei 7 Limopsidae) (GASTROTRITEIA) N . tenuis ](II-7) Arcidae (111-10) N. sp. Glycymeridae (111-10) N . sulcata (11-7b) Limopsidae (11-4) Pectinidae -Oa) Mytilidas (1111 Pecten (11-8) Isognomonidae (111-10a) Chtamys (IIA-9) Pinnidae (111-10, l O a ) Delectopecten (111-lOa) Ostreidae (111-lOa) Spondylidae (11-4, ?III-10) Galeommidae Phlyctaenachlamys (GASTROTETARTIKA) lysiosquillina ( 1 la) Limidae ( ? I I - S a ) Scintilla japonica (I-1) Unionidae (111-1O ? ) Tellinidae Chamidae (11-4) Laternulidae (11-4) Tellina-form (1-1) Macoma-form (I-la) (GASTROPEMPTA) Mactridae Corbulidae (11-4) Mactra, Raeta (1-2) Veneridae (11-4, etc.) Tresaus, SchizoPsammobiidae (1-1, 2) Myidae (11-5) thaerus (IA-3) Semelidae (1-1,la) Pholadidae Pholadidea (11-5) Solenidae (IA-3, 1-2) Barnea (I-la) Corbiculidae (11-4) Zirjaea (11-4) Cardiidae (IA-3, 1-1)

While it was recognized that no one characteristic feature of the pellets would be a satisfactory index, yet taken in combination the following features should be of major significance : ( 1 ) external sculpture (cross-section) ; (2) size (length/breadth ratio) ; (3) colour ; (4)texture.

External sculpture The external sculpture or markings are a reliable criterion for the pellets of a number of species, e.g. in the Nuculacea and Pectinacea.

405

SCATOLOGICAL STUDIES OF THE BlVALVIA ( iMOLLTTSCA)

Thus in Nuculn and ChZam,ys the number and position of the surface sculpturing are so constant within a species that it, is easy to distinguish between species. The best way to observe these sculpturings is to make cross-sections (Figs. 3, 4 and 8). However, the texture of'the waste or undigested matter in some cases, e.g. in the Mactridae and the Mytilidae, is often so coarse that it fails t o take some of the minor striations usually impressed on the pellet surface.

Size The size is variable depending, as it does, on the stage of growth even in the same species (Table 11, p. 370), but in the ovoid pellets with little specific character, such as those of the Tellinidae, the ratio of length t o breadth of the pellets may be of some value in identification of different genera and species (Table 11).

Colour As a rule, the colour varies depending on the food taken in by the animal. On the effect of food on the nature of pellets of Mytilus edulis, Dodgson states: '' The colour, being determined by that of the suspended matter ingested, varies considerably, but is usually dark chocolate brown, or more rarely slate. Such white faeces have been noted almost every spring in the tanks, for a period of a few days to a week. It has been found due to the ingestion of a certain flagellate protophyte, . . ." But colour may a t times serve as a criterion for identification when taken in combination with other criteria.

Texture This is fairly constant for many species because the size of food particles sorted by the ctenidia and the labial palps is approximately constant in any species. Internal texture is also an important criterion. Kornicker (1962) points out that the constituents of the sediment in sculptured faeces are segregated in different regions whereas the composition of unsculptured, shapeless and oval pellets is uniform. The conclusion is that, though faecal characteristics in the Bivalvia are not so significant for the identification of genera and species as suggested by some former workers, yet there is a remarkable uniformity of pellet types within a family and this can be of great value in clarifying the relationships and the systematic status among larger taxonomic divisions as will be discussed in the next section.

VI. EVOLUTIONARY TRENDS OF FAECAL PELLETS There are indications that the structure and form of faecal pellets may be of phylogenetic significance and therefore provide evidence for A.M.R.-S

14

406

KOHMAN Y. ARAKAWA

relationships between bivalves. Moore (1931) and Moore and Kruse (1956) considered the various forms of pellets to be modifications of the unsculptured rod, oval or ellipsoidal pellets being produced by way of the constricted rod. Kornicker (1962) disproved Moore's idea and provided a fairly reasonable hypothesis that the various types of pellets may be simplifications of the sculptured rod, because of the predomiDoll (1894)

I

-8

I

60

t

Order ANOMALOD€SMAC€A

Order TELEODESMACEA

Pellet-types

Fig. 21. Frequency distribution of types of pellets produced by the bivalve orders Prionodesmacea, Anomalodesmacea and Teleodesmacea (Dall, 1894).

nance of such rods among both primitive gastropods and bivalves. He comments, " The unsculptured rod may be a type transitional between the sculptured rod and oval pellets and shapeless pellets, but the scarcity of unsculptured rods among pelecypods suggests that oval and shape-

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

407

less pellets may have evolved directly from sculptured pellets. If, as suggested here, the primitive fecal pellet is the sculptured rod type, there has been considerable similarity in the development of fecal pellet types among diverse groups." He continues, " In general, the separaPelseneer (191I) loor Order PROTOBRANCH~A

'""l

n

Order FILIBRANCHIA

Order PSEUDOLAMELLIBRANCHIA

_ I

FT

EULAMELLIERANCHIA

0 r der SEPTIBRANCHIA

1

2

3

4

5

6

7

8

9

1011

Pellet- types

Fig. 22. Frequency distribution of types of pellets produced by the bivalve orders Protobranchia, Filibranchia, Pseudolamellibranchia, Eulamellibranchia and Septibranchia (Pelseneer, 191 1).

tion of pellet constituents seems to be a primitive trait with composition being more nearly uniform in advanced forms." Arakawa (1962) described the probable course of descent of the bivalve pellets in his preliminary communication and suggested that the common anc2stral

408

KOHMAN Y . ARAKAWA

type of the pellets was the sculptured rod from which may be evolved more complex forms, e.g. unsculptured rods, ribbons and ovoids. Sculptured rod-types faeces prevail in the phylogenetically lower bivalves, such as the Protobranchia, whereas in the higher ones, such as the Eulamellibranchia, the rod and ovoid pellets predominate. Thiele (1935)

50

II

Order TAXODONTA

n

n

Pel let-types

Fig. 23. Frequency distribution of types of pellets produced by the bivalve orders Taxodonta, Anisomyaria and Eulamellibranchia (Thiele, 1935).

To facilitate comparison the distribution of the various types of bivalve faeces in relation to different schemes of classification proposed by various authorities has been set out in tabular and histogrammatic forms (Table V ; Figs. 21 to 25). Of these schemes, that of Purchon (1963) appears as the best when considered in relation to the distributions of pellet-types, because the grouping of these agrees more closely with his classification than with those proposed by Dall (1894), Pelseneer (1911), Thiele (1935) and Cox (1960).

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

409

ISOFILIBRANCHIDA

t

I1

40t

II

8o

i

1

100 ;01

Ord. EUDESMODONTIDA

60

40 20 EUTAXOOONTIDA

0 c

Ord. ASTHENODONTIDA

60 40 20

401 Ord PTEROCONCHIDA 20

0

loot

Ord CALLOCONCHIDA

80

60 40

20 0

20

1 2 3 4 5 6 7 8 9 1 0 1 1

0

Pellet-types

Fig. 24. Frequency distribution of types of pellets produced hy the bivalve orders in t,he classification of Cox (1960).

410

KOHMAN Y. ARAKAWA

Throughout the Bivalvia, the phylogenetically most primitive form may be grooved rods, because the above data show that in the Protobranchia more than 60% of species have multi-grooved rods (Types 7, 7a and 7 b ) and 30% or more singly grooved ones (Type 6). It is worthy of note that Cox (1959) provided geologic evidence of this in certain fossil species of the Protobranchia. " Of great interest is the preser-

8ol Purchon (1963)

Order PROTOBRANCHIA

461- Order GASTROTETARTIKA 20

"1

n Order GASTROPEMPTA

40

20

0 1

2

3

4

5 6 7 Pel let- types

8

9

1011

Fig. 25. Frequency distribution of types of pellets produced by the bivalve orders in the classification of Purchon (1963).

vation of moulds of the actual intestine in fossil specimens of a species of Nuculana from the Lias of Gloucestershire. . . . The intestine has several coils, more as in Nucula than in Nucubna a t the present day, and its internal mould has longitudinal grooves very similar to those on the faecal psllets of modern species of Nucula. . ." These data suggest t o us that within the Protobranchia the evo-

.

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLWCA)

41 I

lutionary progress of faecal pellets is monophyletic and that the multigrooved rod (such as that of Nucula sulcata (Type 7 b ) ) may have evolved continually into a simply grooved one (such as that of Nuculana (Type 6 ) ) through a series of transitional forms (such as those of Nucula tenuis (Type 7 ) and N . nucleus (Type 7 a ) ) . It has been traditional to treat the Septibranchia as the climax of evolution of the Eulamellibranchia on account of the peculiarities in structure and function of the ctenidia. The available scatological data, however, are not yet sufficient to warrant final conclusions on this subject*. As described in Section 111,the Septibranchia show no similarity to the Protobranchia in faecal characteristics, the faeces in the Septibranchia being extruded as shapeless pellets with soft and fragile consistency (Type 11) quite unlike those of the Protobranchia. Kornicker (1962) in commenting on the evolution of the molluscan faeces suggested that the shapeless pellets may have arisen directly from sculptured rods due to the “ scarcity ” of unsculptured rods which might be transitional between the sculptured rod and shapeless pellets. But there is no evidence (Table V) in favour of his hypothesis. From the data given in Table V, it should be noticed that in the Polysyringia with some exceptions the production of ribbon-like faecal pellets (Types 10 and 10a) may well be associated with byssal attachment or cementation. All the Gastrotriteia apart from the Limopsidae in which the habit of byssal attachment seems to be lost early in life have ribbon-shaped pellets. The present writer cannot satisfactorily explain the significance of this phenomenon, but it may throw some light on this problem that byssal attachment or cementation have some direct or indirect influence on feeding habits, in view of the fact that the retention of the filibranch ctenidium in the Anisomyaria is closely associated with byssal attachment (Yonge, 1962). I n giving a brief explanation of this fact, Yonge states as follows : “Although the filibranch ctenidium is clearly less efficient than the much more compact eulamellibranch ctenidium, this will be of no more than minor disadvantage if the animals are epifaunal and so live in relatively clear water.” There are, of course, exceptions to this rule. To mention a single example, unattached unionids such as Anodonta and Hyriopsis may produce ribbon-like pellets (Type 10a). The rectal lumen in these species is flattened to a crescentic shape by an unusually developed typhlosole which may assist in osmoregulation in view of their freshwater habitat. Speaking phylogenetically, while the unionid rectum

* But justified by the structure of Halicardia nipponensis (Nakazima, 1967). (C.M .Y.)

412

KOHMAN P.ARAKAWA

might have evolved as an environmental adaptation, this has happened only once (Jegla and Grrenberg, 1968). I n any case, it may be suggested that within the Gastrotriteia the ungrooved ribbon (Type 10a) may be more advanced than the grooved one (Type l o ) , because the latter is generally present in primitive heteromyarians, such as Mytilus, and the former in higher heteromyarians and monomyarians such as Pin,na and Pinctada. As previously discussed, the faeces in the Gastrotetartika take on a great variety of form, probably in correlation with wide diversity in habit and the structure and function of the digestive organs. To take the concrete instance of the Pectinacea, the habits of adult members of this group can be distinguished into three categories : cementation, byssal attachment, and freedom. According t o Yonge (1951), the phylogenetically primitive habit must have been byssal attachment which is universal in early life. From this the habit of cementation and of freedom may have separately diverged. I n the cemented species of this group, e.g. Plicatula, the pellets are ungrooved ribbons which resemble those of other cemented members of the Gastrotriteia, such as Crassostrea, Ostrea and Xaxostrea. I n most, of the byssally attached members, such as Chlamys, the pellets are grooved rods trefoiled or triangular in section (Types 9 and 9a) which, though quite different in appearance, have a basic connection with the grooved ribbon with bicrescentic section (Type 10a) in other byssally attached members of the Gastrotriteia. Finally, in the unattached members such as Amusium in the Amusiidae and Pecten in the Pectinidae, the pellets are in the form of rodlets wound into a ball (Type 8) which is characteristic of this group. These interesting facts might be interpreted as evidence that the ancestral pellet form in this group may be a trefoiled section rod, and then, in correlation with the change of habit, it may have altered in two directions ; e.g. ungrooved ribbons (cementation) and rodlets wound into a ball (freedom). It should be mentioned in this connection that a close parallel to this could be found among the members of the Anomiacea, e.g. permanently attached Anomia, temporarily attached Enigmonia and unattached Placenta, though the investigation of this possibility must be the subject of future research. The evolution of faecal pellets in the Erycinacea may also be worth special attention, since the members of this group have distinctive habits most of them being commensal. I n commensal species such as Phlyctaenachlamys lysiosquillina, the faecal material is discharged as disjointed particles unlike those of non-commensal ones such as Scintilla and Lasaea in which they are discarded as firm ovoid pellets. T t i s also noteworthy that in the byssally attached Cardita (Carditacea)

SCATOLOCJICAL STUDIES OF THE HIVALVIA (MOLLUSCA)

413

the pellets are emitted in the form of ungrooved ribbon (Type 10) as in the case of other byssiferous members of the Gastrotriteia and that in the majority of the Lucinacea the faecal pellets are in the form of a plain rod (Type 4), a feature they have in common with the primitive groups (such as the Veneracea) of the Gastropempta. Last but not least, the facts mentioned above strongly support Purchon’s view that the Gastrotetartika are an ancestral group which persists to the present day, and from which the Gastrotriteia and Gastropempta arose by specialization. The data drawn from Table VI suggest that the faecal pellets in the Gastropempta exhibit little variation in type, the majority of them (60% or more) being ovoids (Type 1) and plain rods (Type 4). However, there is a gradual transition from plain rods such as those of the Veneracea (Type 41, through rods constricted a t regular intervals to give short cylinders with rounded ends such as those of the Cardiacea, Solenacea and some spp. of the Mactracea (Type 3) into ellipsoid (Type 2), ovoid (Type 1) and discoid pellets (Type I b ) such as those of the Tellinacea. I n view of the above facts, it may be concluded that, as suggested by Purchon (1959) on the basis of evidence drawn from anatomical investigation of the bivalve stomach, the Protobranchia, Septibranchia, Gastrotriteia and the Gastropempta are monophyletic stocks whereas the Gastrotetartika must be polyphyletic. I n some families which should belong to the Gastropempta, there is reversion to the ancestral condition and in others, which should belong to the Gastrotriteia, paedomorphosis has occurred. However, while there is a considerable degree of correspondence between the views of this writer and those of Purchon on the phylogenetic trends within the Bivalvia, there remains a serious difference of opinion about the status of the Septibranchia. OF SUSPENSION FEEDING BIVALVES VII. BIODEPOSITION It is a well-known fact that the defecation activities of earthworms play a major role in the modification of the physical and chemical characteristics of mould (Darwin, 1881). Recently, Ito and Imai ( 1955), Lund ( 1 957) and Haven and Morales-Alamo (1966) drew attention t o the fact that faecal production of some filter-feeding marine invertebrates profoundly influences deposition, transport and the physical and chemical composition of the sediments in estuaries and bays. As a designation for convenience, faeces and pseudofaeces of these animals that settle to the bottom are termed “ biodeposits” ; the process involved in production of these biodeposits-filtration of seston, compaction within the animal, and subsequent deposition-are

414

TABLEV. COMPARISON OF FRECCTENCY DISTRIBUTIONOF TYPESOF PELLET WITH VARIOUSSCHEMES OF CLASSIFICATION OF THE BIVALVIA Pellet-types I1

I Schemes of classification 1 ____

_

_

~

-

~~

2

3

4

5

6

8

7

IIA

I11

9

10

8 10.5

4 6 60.5 2 33.3 1 1 1.2 1.2

Total 11

~

3 3.9 4 66.7 1 0 2 9 3 12.2 3.5,4 3.7 -

-

ANOMA4LODESMACEA

~

TELEODESMACEA

4 5.3 -

-_

-

7 9.2

-

8

10.5 -

-

-

-

76 spp. 100% 6 SPP.

looyo

82spp. l000/,

Pelseneer ( 1911)

Ord. PROTOBRSNCHIA FILIBR ANCHIA PSEUDOLAMELLIBRANCHIA EULAMELLIBRANCHIA (No.) (YO)

SEPTIBRANCHIA

(No.) ((30)

-

-

-

-

2 6.7 1 3.0 33 36.7 -

28 93.3 16 48.5 3 3.3 -

-

-

11 spp.

looyo

30 spp.

looyo

33 spp.

looyo

88 spp. 100% 2 SPP.

loo?/,

KOHMAN Y . ARAIIAWA

Dall (1894) Ord. PRIONODESMACEA

Thiele (1935) Ord. TAXODONTA

ANISOMYARIA

(NO.)

(9,)

(No.)

(70)

EULAMELLIBRANCHIA (No.) (9b) Subord. HETERODONTA (No.) (90)

ADEPEDONTA

(No.) (90)

ANOMALODESMATA (No.) (O6)

SCHIZODONTA Cox (1960) Subclass PROTOBRANCHIA

(No.)

-

28 31.1

_

-

10 11.1

10 11.1

9

7

37.7 2 15.4

13.0

10.1 3 23.1

_ _

_ -

26

_

1

7.7

_

_ _

-

-

2

5

-

30.8 4

_

-

-

_

_

-

(No.)

_

-

_

_

-

-

-

(No.)

(96)

-

-

-

-

-

-

4

-

36.4

7 33.3 8 8 15.1 15.1 - - -

8

-

-

-

-

1

-

-

-

_ -

7 63.6

-

-

-

-

1.4

-

-

_ _

-

-

38.1 3 6 67.9 3 3 3.3 3.3 1 1.4

2 33.3

2 100.0 -

-

69spp. 10O0, 13spp. 1000, tiSPP. 100~, 2SPP. 1000, 11 spp.

-

-

21 spp. 1OOo0 53spp. 10Oo0 90spp. l00O0

-

1000,

m 0

2;

0

fl

0

8 $

rn

rj

4

Ei ?! Y

g M

$P 5

P h

-

-

_

_

-

-

_

-

-

_

-

_

-

-

-

4

(No.)

(06)

-

-

3 23.1

4

(36.7

-

-

36.2

-

-

4 19.0 -

2 9.5 I 1.9 33 3 36.7 3.3

-

_

(Oh)

Subclass

_ _

-

_

Ord. PALAEOTAXODONTIDA (NO.)

PTERIOMORPHIA

_

(96)

(Ob)

LEPIDONTIDA

_

-

_

_

-

-

-

7 100.0 -

-

-

100.0

3

-

-

-

-

-

4.8

-

-

-

-

-

-

8 12.7

12.7

8

-

-

-

-

-

-

4 4 69.8 -

7spp. 1000, 4spp. 1000,

s

0

r F

< ra

-* d

ti3 spp. 100O0

5 Ln

e

Q,

TABLEV-contcl. Pellet-tupes I1 1-

I

IA

IIA

I11

8

9

10

-

-

8 33.3 _

8 33.3 -

Tohl

Schemes of classification 1 __

-

2

3

4

5

6

7

11

-

~~~

Ord. EUTAXODONTIDA

2 20.0 -

PTEROCONCHIDA

1 11.1

CALLOCONCHIDA

-

.

Ord EUDESMODONTIDA

ASTHENODONTIDA N AIATIDA

HETERODONTIDA

33.3

-

8 88.9 20 100.0 -

10 spp. 100~, 24spp. 100~" 9 SPP. 1000/, 2ospp. 1oO?o

g m

E

5

g

c

x

c

Subclass HETEROCONCHIA

8

~

-

ISOFILIBRANCHIDA

8 80.0 -

28 31.1 2 25.0 -

-

26 34.2

10 11.1

10 11.1

33 36.7

3 3.3

5

1 12.5 2 50.0

62.5 2 50.0 -

-

-

-

26 34.2

-

-

-

3 3.3

3 3.3

9ospp. 1009,

Purchon (1963) Subclass OLIGOSYRINGIA

Ord. PROTOBRANCHIA

cn

(%)

_ _

_

-

- - -

(No.)

_

-

-

-

(No.)

(%I SEPTIBRANCHIA

(No.)

(%)

_ _ -

_ _ _

_ _

_ _

-

Q

4 30.8

7 53.8

-

4 36.4

7 63.6

-

-

-

-

-

2 15.4

13spp.

looo/,

(No.) (YO)

Ord. GASTROTRITEIA

GASTROTETARTIKA

(No.) (Yo)

(No.)

(%) GASTROPEMPTA

(No.)

(%)

28 18.5 -

_ 1 3.1 27 36.0

10 6.6

-

10 6.6

_ -

36 23.8

0 0

-

_

-

-

-

-

-

-

2 100.0

llspp. 1000, 2SPP. 100%

1 0.7

l5lspp. l00qb

41 93.2 1 6 18.8 3.1

44SPP.

-

-

Subclass POLYSYRINGIA

$

3 2.0

-

-

-

-

3 6.8 - 1 7 3.1 21.9 9 1 0 2 6 3 12.0 13.3 34.7 4.0 -

8 5.3

8 5.3

8 8 25.0 25.0 -

47 31.1

loogo 32spp.

looo.,

75spp. -

-

looq,

8

L g c,

E

ifl

0

1

F2

M

p+ 4 c r

2

h

z

0 F F

cn

0 k-

v

418

TABLEVI. FREQUENCY DISTRIBUTION OF VARIOUS TYPESOF FAECAL PELLETS PRODUCED BY THE BIVALVEORDERSAS CLASSIFIEDBY PURCHON (1963) Pellet -types

I

IA

I1

Classi$cation 1

(%)

I11

la

2

1l a

8a

3

4

5

6

7

7a

7b

8

-

21.9

-

-

-

-

-

12.5 12.5 21.9 3.1

9

9a

10

10a

11

3.1

-

KOHMAN Y . ARAUAWA

Purchon (1963) Order PROTOBRANCHIA (NO.)

IIA

.....................

-

-

SEPTIBRANCHIA (NO.) (%I GASTROTRITEIA (NO.) (%I GASTROTETARTIKA (No.) 1

(Yo)

GASTROPEMPTA (No.)

(yo)

3.1 21 28.0 8.0

3.1

15.6

3.1

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

419

included under the term " biodeposition " (Haven and MoralesAlamo, 1966). I n this Section, reviews and discussions about the principal features of this pioneering work done within comparatively recent years will be presented. A. Factors injluencing hiodeposition A number of environmental factors are known that influence the rate of defecation of the suspension feeding bivalves. From the data of Korringa (1952), Jorgensen (1965) and others, Haven and MoralesAlamo (1966) pointed out that the amounts of faeces or pseudofaeces produced by filter-feeders are determined by the physiological responses of the animals to environmental stimuli, and that particle filtration is the most important of these responses which may depend on particle size and concentration, algal species, temperature, salinity and other characteristics of the surrounding water.

Temperature Discharge of faecal matter takes place only within certain temperature limits. In Pinctada martensii (Gmelin), Ota (1959) ascertained experimentally that the optimum temperature for the rates of faecal and pseudofaecal discharge range from 27.0 to 29.5OC and the discharge of faeces is impaired or stopped when the temperature falls below lO"C, while in Crassostrea virginica (Gmel.),Haven and MoralesAlamo (1966) stated that at temperatures lower than 2.8"C measurable quantities of faeces and pseudofaeces were not produced and that when temperature decreased to 6.7"C there was an 850/, decrease in weight of faeces and pseudofaeces. Loosanoff (1958) found that at temperatures between 2.0 and 3-0"C, 1.1% of 90 oysters producedfaeces and only 15% produced pseudofaeces. Ito and Imai (1955) stated that, when kept in water at 9°C and with poor suspension of food, a single oyster (C. gigas) weighing 90 g produced a minimum of 0.03 g faeces (dry weight) daily. Galtsoff (1964) showed that the average rate of discharge of faecal ribbons in actively feeding oysters, C. virginica, in laboratory sea-water at temperatures of 154-15-7"C was 8-1 cm in length/h and he estimated that the time of passage of food through the entire alimentary tract was 95 min. According to Ota (1959) the time of passage of food in P. martensii observed ranged from 4+ to 10 h or more according to the water temperature (29-5-15.5"C) during the summer season. Sabinit y The effect of the low salinity on the rate of faecal and pseudofaecal production was shown by Ota and Fukushima (1961), who found

salinities of 24.6-27-2%, in P . martensii, while Yuiki (1951) and Kobayashi and Matsui (1953) demonstrated that the effects on the ciliary activities of the gills were conspicuous below salinities of 20.0 and 22.6%, respectively. n conspicuous effect below

Suspended solids The quantities of suspended matter contained in the surrounding water may be one of the leading factors influencing faecal and pseudofaecal production in suspeiision feeders. I n P . martensii, Ota (1959) demonstrated that, during summer and autumn, the variation of the total amounts of faeces and pseudofaeces is essentially similar to that o f the amounts of suspended matter per unit volume of the surrounding water. Lund (1957) obtained similar results to Ota and found that faecal and pseudofaecal production positively correlated with materials (ground Ulva) added to water flowing over oysters. While on the other hand, Haven and Morales-Alamo (1966) demonstrated in C. virginica that there was no correlation between quantities of faeces collected daily with those of seston, whereas pseudofaeces were positively correlated with seston when temperatures were a t mid-range but not during the warmest period in midsummer Similar results to those were also obtained by Loosanoff and Engle (1947) who pointed out that pseudofaeces were approximately proportional to the concentration of added materials (Chlorella suspensions), whereas the rate of faecal discharge decreased as the concentrations increased. The reasons for this wide difference are unexplained, but, as suggested by Haven and Morales-Alamo (1966), it is likely that the bivalves were not able to filter all the available organic matter and that a portion occurred as particles too small t o be filtered from suspension. Size of producer In the course of the study on the seasonal variations of faecal and pseudofaecal production of P. martensii, it was shown by Ota (1959) that the smaller the size of the animal, the larger the faecal and pseudofaecal production per unit weight of the producer became, though quantities of faeces and pseudofaeces were approximately proportional t o the size of the animal. Haven and Morales-Alamo (1966) obtained similar results in C. virginica and found that there are positive correlations between faecal and pseudofaecal production and the weight of the producer. Other factors Ota (1959a) showed that the post-operative shock resulting from operations of nuclear insertion for cultured pearl oyters had a great

SCATOLOGICAL STUDIES OF THE BIVALVIA (hfOLLUSCA)

121

cffect on the rate of faecal discharge during a certain period subsequent to the operation. Consequently, he suggested that the rate of faecal discharge of the operated oysters may serve as a useful index in evaluating the period of post-operative care. B. Daily and seasonal aspects of biodeposition Daily aspects: Loosanoff and Nomejko (1946) demonstrated that t'he feeding activities in Ostrea edulis L. had no relationship to the period of light and darkness, whereas in P.,martensii, Okawa ( I 959) obtained 1969. Aug. 23-24 Crassostrea

c

..Exp. No. I

$

40

a

5 20

c

d

o 1968 Oct, 29-30

c

5

Night

0Daytime

Crassosfrea

i

EXP.NO 2

40

U

.E c

20

FIG.26. Comparison of relative quantities of faeces produced by Crassostrea and Mytilus during the period of light and darkness (Arakawa et al., in press).

results opposite to the above and found that the pearl oysters feed actively from evening till midnight and not actively in the daytime. Data from daily studies relating the defecation cycle of C. gigas and Mytilus galloprovincialis Lam. by Arakawa, Kusuki and Kamigaki (in press) indicate a positive correlation. Both produce larger quantities of faecal matter at night than in the daytime (Tables V I I and VIIa ; Fig. 26). Further studies on the daily cycle of the rate of water transport in these bivalve species in relation to the period of light and darkness seem t o support the above findings (Table V I I I ; Fig. 27). But in either case, such a rhythm tends gradually to show more irregular patterns due to repeated use of the same materials for the experiments.

422

KOHMAN Y. ARAKAWA

8

80

L

i

60

1

Crassostrea Exp. NO.

Mytilus

c

2 L:

801

Exp. No. 1

c

In

FIG.27. Comparison of relative volumes of water transport supplied by Crmsostyea and Myt&ts during the period of light and darkness (Arakawa et d).

TABLEV I I I . DAILYRATESOF WATERTRANSPORT IN Crassostrea T'ol. of

water transported (night) CC

__~________

1'01. of water trans-

ported (daytime) ee

Total volumes

Ratio (n:d)

cc

-

_____.__

AND

Mytilus

Fater temperalure

("C) ~

___

I

E x p . No. Crassostrea gigas M . galloprovincialis

3 600 1 500

3 150 600

6 750 2 100

Exp. No. Crassostrea gigas M. galloprovincialis

79 875 9 000

21 150 3 000

101 000 12 000

E x p . No. Crassostrea gigas M. galloprovincialis

13 200

-

2400

8:7 5 :2

24.0-26.2 24.0-26.2

355: 94 3:1

26.0 24.4-25.9

-~

-

15F00

11 : 2

24.8-25.4

I1

I11

Seasonal aspects Haven and Morales-Alamo (1966) showed that quantities of faeces and pseudofaeces produced by oysters (C. virginica) varied seasonally, reaching maxima in September, and that during winter with the

TABLEVII. DAILYRATESOF BIOLJEPOSITION IN Crassostrea AND N y t i l w i (23-24 August 1969) Total amounts of biodeposits Interval of time produced 15.00- 18.00- 21.00- 00.00- 03.00- 06.00- 09.00- 12.00at night 18.00 21.00 00.00 03.00 06.00 09.00 12.00 15.00 (18.00-06.00), dry wt/12 h per animal

Grassostrea

Total aniounfs of biodeposits produced iv the daytime (06.00-18.00). dry wt/l2 h per animal

Faeces (mg)" 2-1 Pseudofaeces(mg) 11.3 13.4 Total (mg)

6-8 10.6 17.4

6.0 13.1 19.1

5-2 21.0 26.2

5.3 27.1 32.4

3.7 23.0 26.7

5.9 17.4 23.3

3.6 17.6 21.2

23.3 71.8 95.1

15.3 69.3 84.6

Mylilus Faeces (mg)" 3.3 galloprovincialis Pseudofaeces (mg) 12.7 Total (mg) 16.0

12.3 21.4 33.7

10.4 24.8 35.2

8.8

25.4 34.2

11.1 19.3 30.4

6.9 16.7 23.6

5.8 15.4 21.2

6.9 13.0 19.9

42.6 90.9 133.5

22.9 57.8 80.7

giga

a

3s M

m

Faeces and pseudofaeces in dry weight (mg)/3h per animal.

P

1.3

to

TABLEVIIa. DAILYRATESOF BIODEPOSITION IN Crassostrea

AND

Mytilus

(29-30 October 1968)

Total amounts Total amounts of biodeposits of biodeposits produced produced in Interval of time 09.00- 12.00- 15.00- 18.00- 21.00- 00.00- 03.00- 06.00at night the daytime 12.00 15.00 18.00 21.00 00.00 03.00 06.00 09.00 (18.00-06.00), (06.00-l8.00), dry wt/12 h dry wt/12 h per animal per animal

Z

5 Crassostrea gigas

Faeces (mg)" Pseudofaeces(mg) Total (mg)

7.2 0.9 8.1

9.5 1.0 10.5

8.6 0.4 9.0

7.1 2.7 9.8

10.0 2.3 12.3

15.4 2.0 17.4

18.4 5.2 23.6

10.1 2.4 12.5

50.9 12.2 63.1

35.4 4.7 40.1

Mytilus Faeces (mg)" galloprovincialis Pseudofaeces(mg) Total (mg)

5.4

7.8 1.2 9.0

7.7 1.2 8.9

8.7 1.7 10.4

8.5 3.3 11.8

10.4

16.0 5.1 21.1

4.7 3.0 7.7

43.6 17.6 61.2

25.6 7.0 32.6

a

1.6 7.0

Faeces and pseudofaeces in dry weight (mg)/3h per animal.

7.5

17.9

bk-

R k-

?

425

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

temperature below 2-8"C measurable quantities were not produced. Data from seasonal studies on faecal and pseudofaecal production of TABLEIX. SEASONAL RATESOF BIODEPOSITION I N Crassostreu

Date Water temperature ( " C ) Chlorinity Crassostrea gigus

(X)

Shell height (mm) No. animals Faeces (mg)" Pseiidofaeces (mg)" Total (mg)"

Mytilus Shell height gallo(mm) provincialis No. animals Faeces (mg)" Pseudofaeces tmg)" Total (mg)" a

1968 August

AND

Mytilw

1968 1968 1969 October December February

April

1969

25-2-26.8 20.6-21.2 13.0-13-7 10-1-10-6 12-5-14.5 16.75

-

17.75

17.36

16.75

53-66 7

70-85 6 219.8

85-91 5 117.4

76-86 5 78.4

75-91 5 37.6

68.7 288.5

18.8 136.2

9.3 87.7

4.1 41.7

40-53 8 72.9

37-45 7 46.3

56-68 7 56.5

59-68 6 42.0

76.4 149.3

7.2 53.5

18.7 75.2

5.9 47.9

? ?

99.9

26-30 7 ? ?

14.3

Faeces and pseudofaeces in dry weight (mg)/day per animal.

Japanese oysters (G. gigas) and other invertebrate filter-feeders in oyster beds of Hiroshima Bay by Arakawa et al. (in press) are similar to those of Haven and Morales-Alamo (1966) and show that within an oyster culture cycle (from August t o April ; 9 months) the rate of defecation largely increases during autumn, passes through a maximum in October, and gradually falls in winter (Table IX ; Fig. 28).

C. Effects of biodeposition upon various marine environmental conditions It has previously been pointed out (It0 and Imai, 1955 ; Haven and Morales-Alamo, 1966, etc.) that the biodeposition of marine organisms may influence the physical, chemical and ecological conditions of the surrounding seas. Consequently, it is important t o settle the magnitude of biodeposition as it may occur in the sea. The results of a survey on

426

KOHMAN Y. ARAKAWA

tnhebiodeposition in oyster beds of Matsushirna Bay, Japan, by I t o and Imai (1955) show that the annual deposition of faecal matter produced by a raft of cultured oysters (C. gigns) is estimated a t 8-10 tons on a wet basis. Arakawa et nl. (in press) demonstrated that a raft of oysters

Faeces Pseudofaeces

Mytilus

Oct. Oec. Feb. Apr.

Oct. Dec. Feb. A!& Month

Fig. 28. Seasonal rates of biodeposition in Crassostrea ant1 Mytilns (Arakawa et al., in press).

SCATOLOGICAL STUDIES OF THE BIVALVIA (MOLLUSCA)

if7

9 nI l.oH

in Hiroshima Bay may deposit within a single oyster culture cycle (9 months) 20 tons or more of biodeposits on a dry basis at a conservative estimate. It is possible that the discrepancy between our findings and those of Ito and Imai lies in the size of the raft", the number of oysters held by a single raft"" and in the basis for estimation of faecal production of a single oystert. I n C. virginica, Haven and Morales-Alamoreported Faeces

1-1

Pseudofaeces

+

n

Crassostrea

p 2.0

U

._ "-

.-

-ij

0.5

8,

.

a"

-

0 Oct. Dec. Feb Apr. Month

Fig. 29. Seasonal rates of quantities of organic nitrogen contained in the biodeposits of Crasssstrea and Mytilus (Ara!mwa et al.,in press).

that in the estuary of York River weekly deposition of faecal matter is calculated to be 981 kg in dry weight1250 000 small oysters/acre. Lund (1957) estimated that oysters would deposit 7.58 metric tons of

* The standard size of the rafts used in Matsushirna Bay is 10 x 6 m2, while those in Hiroshima Bay rneasurc 20 x 10 m2. ** A single raft holds 60 000 t,o 100 000 oyxt,crs in Matsunhima Ray, while in Hiroshima, Bay it holds 420 000 on average. t According to Ito and Imai (1965), a single oyster weighing 90 g produced a minimum of 0.3 g faeces on R dry basis. This estimation of faecal production seems to be rather conservative compared with our findings (Table IX).

‘428

KOHMAN Y. ARAKAWA

faecal matter on a dry basis in 11 days, when they covered an acre of the .bottom. Besides, Verwey (1952) calculated that Cardium in Waddenzee deposits 100 000 metric tons (dry weight)/year and that Mytilus deposits between 25 000 and 175 000 metric tons annually. The effects of bulky biodeposits by marine organisms upon marine environmental con.ditions have been noticed by some Japanese workers

PERMANENT SEDIMENTS

DETRITUS FEEDERS

BACTERIAL DECOMPOSITION

Fig. 30. Biodeposition cycle in the York River estuary (after Haven and MoralesAlamo, 1966).

in the case of oyster culture beds in Japan, where the oysters are commonly cultured by the hanging method. I n this method there is an unusually high estimated density of 420 000 oysters/200 m2or 420 000 oysters/200 m 2 x LO m2, because the middle stratum of water is used for culturing. An instance only remotely comparable to this in Japan is that of the pearl oyster beds. Consequently, recent studies on oyster and pearl oyster culture beds have been focused on the organic

SCATOLOGICAL STUDIES OF THE BIVALVIA

(MOLLUSCA)

429

pollution of the bottom under the beds chiefly caused by the bulky biodeposits of these filter feeding bivalves and other fouling organisms such as Mytilus and tunicates which compete with oysters for space as well as for food. Detailed analytical studies on the chemical composition of the oyster biodeposits by Haven and Morales-Alamo (1966) showed that these contained approximately 14% of organic matter and 5% of total organic carbon and that there is no evident seasonal trend. Ito and Imai (1955) also demonstrated that in the Japanese oyster the biodeposit is composed of 9.1% of humus and O.Syoof total nitrogen. Our results are similar to those of the above authors and show that the total nitrogen contained in the biodeposits is approximately l.Oyo(Fig. 29). Considering the quantities of biodeposits on thc bottom under the beds, it may be supposed that the bottom sediments will be greatly polluted by organic matter. As a matter of fact, it has been known among Japanese commercial oyster growers that in many of the oyster beds the oyster crops decrease with the years, owing to their repeated use. Biodeposits thus accumulated gradually modify the physical and chemical nature of the bottom sediments and not only interfere with the lives of the oysters but also often cause a high mortality during the summer season when temperatures ara high. To facilitate explanation of the complex process of biodeposition involving many groups of animals and physical and chemical factors as mentioned above, a clear illustration of the biodeposition cycle in the estuary of the York River was furnished by Haven and MoralesAlamo (1966) (Fig. 30). VIII. BIBLIOGRAPHY Abbott, R. T. (1984). “American Seashells.” D. Van Nostrand Co. Inc., New York. Abbott, R. T. (1954a). Review of the Atlantic periwinkles, Nodilittorina, Echininus and Tecturius. Proc. U.S. natn. Mus. 103 (3328), 449-4G4. Allen, J. A. (1962). Preliminary experiments on the feeding and excretion of J . nmr. biol. Ass. U . K . 42, 609-623. bivalves using P32. Amstutz, G. C. (1958). Coprolites: A review of the literature and a study of specimens from Southern Washington. J . sedim. Petrol. 28(4),498-508. Arakawa, K. Y. (1960). Some ecological accounts on Scintilla witrea Quoy and Gaimard. Venus, Tokyo, 21(1), 61-66. Arakawa, K. Y. (1962). A coprological study on the molluscan faeces (A preliminary note). (In Japanese with summary in English.) Vcnus, Tokyo, 22(2), 151-172. Arakawa, K. Y. (1963). Notes on the faeces of Macroch.eira kaenipferi de Haan. Res. Crustacea, 1, 7 - 8 . Arakawa, K. Y. (1963). Studies on the molluscan faeces (I). Prrbls Set0 mar. biol. Lab. 11(2), 185-208.

430

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(MOLLUSCA)

435

Purchon, R. D. (1963). Phylogenetic classification of the Bivalvia, with special reference to the Septibranchia. Proc. malac. SOC.Lond. 35(2/3), 71-81. Reineck, H.-E. (1963). Sedimentgefugsl im Bereich der siidlichen Nordsec. Abhandl. Sencken. Natur. Cesel. 505, 1-137. Richter, R . and Richter, E . (1939). Marken und Spuren aus allen Zeiten LV. Die Kotschniir Tomaculum Groom (Syncoprulus Rud. and Richter), iihnlich Scheitel-Platten und beider stratigraphische Bedeutung. Sencken bergiana, 23, 127-132. Righi, G. (1966). On the Brazilian species in the Acmaea subrugosa complex (Gastropoda : Prosobranchia : Patellacea). Malacologia, 4, 282. Robertson, R. (1961). The feeding of Strornbus and related herbivorous marine gastropods : with a review and field observations. Notulae Naturae, 346, 1-9. Robertson, R. (1963). Wentletraps (Epitoniidae) feeding on sea-anemones and corals. Proc. Malac. SOC.Lond. 35, 53. Rothpletz, A. (1892). On the formation of oolite. Am. Ceol. 10, 279-282. Sato, T. Matsumoto, S. and Tsujii, T. (1964). Filtering and feeding rate of the pearl oyster, Pteria (Pinctada)martensii Dkr determined with crude silicate as an indicator. Bull. J a p . SOC.scient. Fish. 30, 717-722. Sawada, Y. and Taniguchi, M. (1968). The oceanographical studies of the pearl culture ground. 11. On the seasonal changes of organic matter and phaeophyt,in contents in bottom mud of the super annuated pearl culture ground. Bull. Nat. Pearl Res. Lab. 13, 1689-1702. Sawada, Y. and Ueno. F. (1966). Studies on the acetone extracts from marine mud and faeces of pearl oyster (Pinctada maTtensii). I. On the absorption spectra of acetone extracts. Bull. Nat. Pearl Res. Lab. 11, 1290-1307. Schafer, W. (1953). Zur Unterscheidung gleichformiger Kot-Pillen meerischer Evertebraten. Senckenbergiana, 34( 1/3), 81-93. Stasek, C. R. (1963). Synopsis and discussion of the association of ctenidia and labial palps in the bivalved mollusca. The Veliger, 6(2), 91-97. Takahashi, J. and Pagi, T. (1929). Peculiar mud-grains and their relation to the origin of glauconite. Econ Ceol. 24, 838-852. Taki, Iw. (1941). On keeping octopus in an aquarium for physiological experiments with remarks on some operative techniques. Venus, Tokyo, 10, 146- 147. Taylor, D. W. (1966). Comparison of fecal pellets. I n “A remarkable snail fauna from Coahuilax, Mexico”. The Veliger, 9(2), 170-171. Thiele, J. (1931). ‘‘ Handbuch der systematischen Weichtierkunde.” Bd. I. Jena. Thiele, J. ( 1935). ‘‘ Handbuch der systematischen Weichtierkundo,” Teil IV, 1023-1 154. Thorpe, E. M. (1931). Descriptions of deep-sea bottom samples from the western N. Atlantic and Caribbean Sea. Bull. Scripps Inst. Ocean. Tech. Ser. 3(1), 1-31. Thorpe E. M. (1936). Calcareous shallow-water marine deposits of Florida and the Bahamas. Pap. Tortugas Lab. 29(452), 120. Utinomi, H. (1958). “ Coloured illustration of sea shore animals of Japan.” pp. 43-44. Hoikusha, Osaka. Van Weal, P. €3. (1961). The comparative physiology of digestion in molluscs. Am. Zoologist, 1, 245-252. Vaughan, T. W. (1924). Oceanography in its relation to other earth sciences. J . Wash. Acad. Sci. 14(14).

436

HOHMAN T. ARAKBWA

Vwdcoiirt,, B. (1946). 'I'hc microscopical investiga,t,ion of' t,he fond of snn,ils. Microscope, 6, 1. Verwey. J. (1952). 0 1 1 t.hr ccology (if distribut,ioii of' cockle and mussel in t h o Dutch Waddensea, their role in sedimentation and t,ho soiirce of their food supply, with a short review of the feeding bchsviour of bivalve molluscs. Arch. Need. Zool. 10, 172-239. Weiss, H. B. and Boyd, W. M. (1950). Insect, feculae. J l N . Y . ent. Soc. 58(3), 154-168. Weiss, H. B. and Boyd, W. M. (1952). Insect feculae. 11. ?Jl N . Y . ent. Soc. 60(1), 25-30. Wells, G. P. (1949). Behaviour of Arenicola marina L. in sand and the role of spontttriwus activity cycle. J . mar. biol. A s s . U .K . 28(2), 465-478. Wells, G. P . and Dales, R . P. (1951). Spontaneous activity pat,terns in animal behaviour : the irrigation of the burrow in the polychaetes Chaetopterus variopedatus Renier and Neries diversicolor 0. F. Miiller. J . mar. biol. Ass. U . K . 20, 341-346. Wilbur, K. M. and Yonge, C. M. (1964). " Physiology of Mollusca." I. Academic Press, New York and London. Winckworth, R. (1931). On Nucula nitida. Proc. malac. SOC.Lond. 19(6), 280281. Wint-r, J. (1969). CTber den Einfluss der Nahrungslronzentration und anderer Faktoren auf Filtrierleistung und Nahrungsausnutzung der Muscheln Arctica islandica und Modiolus modiolus Mar. Biol. 4, 87-135. Yonge, C. M. (1926). Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J . mar. biol. Ass. U .K . 14(2), 295-386. Yonge, C. M. (1927). Formation of calcareous tubes round the siphons of Teredo. Nature, Lond. 11-12. Yonge, C. M. (1935). On some aspects of digestion in ciliary feeding animals. J . mar. biol. Ass. U . K . 20(2), 341-346. Yonge, C. M. (1951). Studies on Pacific Coast mollusks. 111. Observations on Hinnites multirugosus (Gale). Univ. Calq. Publs Zool. 55(6/8), 409-419. Yonge, C. M. (1960). General characters of Mollusca. I n " Treatise on Invertebrate Paleontology " ( 1 ) Mollusca, 1, 5. Yonge, C. M. (1962). On the primitive significance of the byssus in the Bivalvia and its effects in evolution. J . mar. biol. Ass. U .K . 42, 113-125. Toshiba, S. (1965). Ecological studies on the life history of Lymna,ea (Radix) onychia (Preston). Venus, T o k y o , 24(3), 247-248. Yuiki, R. (1951). On ciliary movements of ctenidia in pearl oyster. (In Japanese). S h i n j u n o K e n , k y u , 2(1/2), 44-55.

PI. I . Faecal pellets of: 1. Cardiomya gouldianu septemtrionalis (Dkr); 2 . Plectodon Zip& (Yokoyama); 3. Barbatia obtusoidea (Nyst) a. dorsal view, b. cross section : 4. Anadaru broughtoni (Schrenck) c. dorsal view, d. cross section ; 5 . Modiolus nipponicua (Oyama) e . dorsal view, f. cross section; 6. M. japonicus (Dkr) g . dorsal view, h. cross section; 7. M . perjragilia (Dkr) i. dorsal view, j. cross section; 8. Septifer bilocularia ( L . )k. dorsal view, 1. cross section; 9. S. keenae Nomura-A. Atypical pellet shed by a starved animal (m. dorsal view, n. ventral view, 0. cross section), B. Typical pellet shed by a well-fed animal (p. dorsal view, q. cross section) : 10. lsognomon legurnen (Gmel.) r. ventral view, a. cross section; 11. Afrina pectinntu jnponica (Rve) t,. dorsal view, u. cross section.

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PI. 2. Faecal pellets of: 12. Oetrea edulia L. v and w. dorsal view, x. ventral view; 13. Chtamya aquamata (Gmel.) y. dorsal view, z. cross section; 14. Mantellum nmakusaense Habe ; 15. Anomia lkchkei Dautzenberg a. dorsal view, b. side view, c. cross section; 16. Cardita Zeana Dkr; d. dorsal view, e. cross section; 17. Joantiisiella lunaris (Yokoyama) ; 18. Laevicardium undatopictum (Pilsbry) ; 19. Fulvia hungerfordi (Sow.); 20. Veremolpa mindanenaia (Smith) ; 21. Gari hoaoyai Habe ; 22. Hintuln ntratn (Rve); 23. Nuttnlia olivncen (Jay): 24. Theorn lubricn (Hinds).

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PI. 4. Faecal pellets of: 25. Fabulina nitdula (Dkr); 26. F . minutu (Lischke) ; 27. Arcopella isselli (H. Ad.) ;28. Semelangulus mdyaterrsis (Yokoyamo) ;29. S.tokubeii Hebe : 30. Macoma tokyoenais (Makiyama) f. frontal view, g. side view; 31. M . incoitgrua (v. Martens) h. frontal view, i. side view; 32. Psammacoma awajiensia Sow.: 33. Mactrn sulcatarin Rve : 34. M . crossei (Dkr) ; 36 SoZen roaeomaculatus Piln.

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PI. 4. Faecal pellets of: 36. Barbatia obtusoides (Nyst) j. dorsal view, k. cross section: 37. Anadara subcrenata (Lischke) ; 38. Septqer bilocularis pilosus (Rve) ; 39. S. virgafus (Wiegmenn) 1. dorsal view, m. ventral view, n. cross section; 40. Pinctada m a r t e d i (Dkr); 41. Crassostrea g i g a s (Thunberg) 0. ventral view, p. dorsal view, q. cross section; 42. Saxostrea echinata (Quoy et Geimard) ; 43. Amuaium japonicum (Gmel.) r. constituent pellet of faeces; 44. Pecten albicana (Schroter) s. constituent pellet of fmces; 45. Lima sowerbyi Deshayes; 46. Laternula limicola Rve t. side view, u. cross section ; 47. Fulvia mutica (Rve) ; 48. Ruditapes philippin,arum (Ad. e t Rve); 49. Meretrix lusoria (Roding); 60. Dosinin japonica (Rve): 51. Caecella chinensis Desh. ; 52. Solen strictw, Could.

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PI. 5. Faecal pellets of: 53. Striarca symmetrica (Rve) v. dorsal view, w. cross section : 54. Modiolus agripetua (Iredale) x. dorsal view, y. ventral view ; 65. Ostrea denselamelloaa futamienaia Seki ; 66. Anomia Ziachkei Dautzenberg z. cross section ; 57, Saxidomua purpuratua (Sow.); 58. Treaaw, keenae Kuroda et Habe; 59. Fabulina iridella (v. Martens) (Faecal ovoids line up within the gut,); 60. MoereZZa kurodai (Mekiyame); 61. NdidoteZZina ndiduZa (Dkr).

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Author index Numbers in, italics refer to pages on which f u l l reference is given

A Abagoii, M. A., 174, 177, 208 Abbott, B. C., 254, 290 Abbott, M. B., 226, 290 Abbott, R. T., 403, 429 d’Acosta, P. A., 178, 193, 194, 208 Acaff, A. D., 234, 304 Adam, N. K., 266, 290 Adana. A M., 174, 212 Aldrich, E. C., 258, 290 Alfert, M., 12, 35, 116 Alikhuri, K. H., 150, 210 Aljakrinskaya, I. O., 269, ‘?YO Allen, D. L., 231, 300 Allen, J. A., 429 American Fisheries Society, 140, 208 American Merchant Marine Institute. 224, 290 Amrricaii Petroleum Institute, 225, 230, 236, 240, 241, 290, 2 9 1 American Public Health Association, 241. 2 9 1 Amio. M., 434 Amstutz, C. C., 429 d’Ancona, U., 122, 135, 141, 182, 199, 208 Aiidrrson, E. K., 234, 297 Arigelw, H., 164, 176, 212 Angelis, R. de, 126, 129, 140, 182, 184, 199, 208 Anon, 225, 228, 230, 272, 273, 291 Anraku. M., 154, 158, 208 Antia, N. J., 93, 112 Antipa, G.. 121, 208 Arakawa, K. Y., 248, 300, 307. 308, 310, 322. 324, 328, 329, 332, 333. 336, 337, 340, 343, 344, 348, 351, 353, 362, 367, 370, 371, 372, 373, 374, 375, 376, 377, 383, 384, 385, 386, 387, 388, 389, 390, 391, 392, 407. 421, 422, 425. 426, 427, 429, 430

Ardiwiriata, R., 199, 210 Arey, L. B., 430 Am&,P., 123, 134, 182, 205 Arnold, E., 152, 208 Arons, A. B., 86, 117 Arthur, B. R., 290, 2 9 1 Asia Kyokai, 178, 193, 208 Azeta, M., 154, 158, 208

B Babnian, K. E., 180, 208 Baker. C. M. A ,, 283, 299 Baker. J. M., 231, 256. 258, 284, 291, 293

Hallantine, D., A30 Bandaruk, W., 241, ,103 Barise, K., 3, 6, 37, 116 Barber, R. T., 46, 47. 103, 112 Barclay-Smith, P., 218, 258, 2 9 1 Rardach. J . E., 281, 2 9 1 Batelle-Northwest Institute, 219, 227, 233, 234, 254. 262, 291

Batoosingh, E., 6, 47, 48, 56, 57, 79, 112

Baylor, E. R., 3, 9, 25, 26, 38. 40, 41, 75, 79,112,118

Bayoomi, A. R., 154, 208 Beadle, L. C., 123, 182, 199, 208 Beaumont. I?. N.. 274, 2 9 1 Beduhri, G. E., 227, 271, 302 Bow, J. V., 263, 2 9 1 Beklemishev, C. W., 430 Bellamy, D. J., 261, 283, 201 Relloc, G., 121, 199, 208 Ben-Shachar, A., 151, 164, 168, 223 Bergman, G., 259, 2 9 1 Bernard, I?.. 91, 1 1 2 Berridge, S. A., 234, 236, 237, 238, 267, 291

Beynon, L. It., 275, 291 Bhattacharya, S. N., 243, 2 9 1 Bidder, A. M., 4.30

437 A &IB-S

15

438

AUTHOR INDEX

Biggs, R. B., 27, 113 Birkholz, D. O . , 266, 292 Blade, 0. C., 223, 235, 292 Blanchard, D. C., 40, 113 Blanco, G. J., 178, 193, 194, 200' Blokker, P. C., 236, 291 Blondeau, R., 257, 305 Boleyn, B. T., 67, 117 Bone, G., 272, 292 Boney, A. D., 283, 292 Booth, C. R . , 19, 63, 65, 91, 111 Bose, B. B., 172, 208 Boswell, J. L., 239, 292 Botke, F., 199, 210 Bourcart, J., 262, 292 Bourne, W. R. P.. 233, 244, 258, 264, 292 Boyd, W. M., 430' Brewer, P. A. 12, 35, 115 Brisou, J., 263, 299 British Petroleum Company, 216, 292 Brockis, G. J., 219, 220, 292 Bromhall, J. D., 152, 209 Brown, S. O . , 239, 268, 292 Brummage, K. G . , 223, 292 Brunelli, G., 142, 169. 209 Brunnock, J. 8.. 234, 235. 236. 292 Buck, W. I?. A., 246, 257, 296 Bumpus, D. F., 81, 105, 116 Runag, D. M..155. 157. 174, 177.

259,

217,

242.

208.

209 Burke, B., 39, 117 Burks, C. E., 240. 305 Bnrnett, F. L., 258, 292 Bursa, A. S.. 9, 113

C Caces-Borja, P., 159. 163, 170, 188, 200, 204, 209 Cairns, J., 249, 251, 281, 292, 295, 302 California Department of Fish and Game, 247, 255, 29.3 Capart, A.. 287, 293 Carey, .'?I ('c., 104, 116 Carlin, B., 139, 209 Carrick, R., 259, 303 Carter. R . C., 241, 298

Casoy, R., 130 Castellanos, E., 274, 293 Chacko, P. I., 150, 209 Chadwick, H. K., 281, 293 Chakraborty, D., 150, 184, 202, 203, 212 Chakraborty, S., Jr., 150, 184, 202, 203, 212 Chave, K. E., 9, 37, 76, 113 Cheri, S., 147, 166, 174, 213 Chen, T., 157, 209 Chen, T. P., 173, 223 Chiba, K., 430 Chipman, W. A., 237, 248, 250, 252, 254, 272, 293 Chow, T., 134, 150, 209 Chumak, M. D., 109, 115 Clark, R. B., 258, 259, 263, 264, 293 Clarke, P., 261, 283, 291 Clendenning, K. A., 247, 249, 252, 254, 255, 259, 260, 275, 293, 301 Cobb, J., 120, 123, 134, 170, 181, 199, 201, 209 Coe, Wesley R., 431 Cole, A. E., 248, 293 Cole, H. A., 139, 206, 2W Collett, W. F., 232, 29G Connor, P. M.,281, 287. 301 Conover. R. J., 107, 113 Cooper, L. H. N., 145, 209 Corcoran, E. F., 29, 113 Cornelius, J., 241, 295 Corner, E. D. S.. 282, 284, 293 Corwin, N., 21, 115 Cowari, E., 265, 289, 293 Cowell, E. B., 240, 256, 258, 284, 293 Cox, L. R., 382, 384, 386, 388, 390, 392. 408, 409, 410, 415, 430 Crapp, G. B., 231, 251, 254, 261, 277, 281, 284, 286, 287, 293 Croft, E. D., 265, 293 Cronin, J. F., 289, 298 Crosby, E. S., 255, 268, 293 Crozier, W. T., 430 Cruz, A. de la. 142, 212 Cunningham, M. B.. 232, 294 Cure, V., 248, 249, 253, 298 Currie, R. I., 430 Currier, H. B., 256. 257, 294 Ciivilhw, J . . 4.30

439

AUTHOR INDEX

D

E

Dales, R . P., 436 Eales, N. 13.. 431 Dall, W. H., 382, 384, 386, 388, 390. Eardley, A. J.. 431 392, 406, 408, 414, 430 Earland, A., 431 Dal Pont, G . , 16, 20, 30, 86, 113 Edge, E. R., 307, 308. 324, 332, 338, Damas, D., 430 347, 350, 361, 362. 364, 369, 371, Dangl, F., 240, 294 372, 373, 375, 377, 378, 380, 383, Darlre, T., 261, 283, 291 385, 386, 389, 390, 391, 392, 393, Darnell, R. M., 141, 142, 144, 146, 209 431 Darwin, C.. 413, 430 Edwards, M. N., 218, 220, 230, 294 Das, P. R., 123, 127. 133, 169, 171. Efumov, B. B., 28, 84, 116 179, 184, 185, 188, 189, 199, 202. Elbert, W. C . , 243, 302 203, 212 Elliott, D. W., 228, 294 Davies, J. A., 268, 272, 29-1 Elmhirst, R., 252, 254, 294 Davis, F. M., 120, 209 Engle, J. B., 420, 433 Davis, G. M., 430 English, J. N., 224, 248, 294, 29S, -3U4 Davis, J. A., 223, 228, 294 Erickson, R. C., 244, 295 Davis, J. B., 284, 291 Esguorra, R. S.. 171. 173, 174, 176, Day, C. G., 22, 1 1 3 192, 209, 212. 21.3 Day, J., 122, 209 Ettmger. M. R.. 266, 267, 298 De, B., 150. 184, 202, 203, 21% Evclyn. T. P. T.. 9. 50. 56, 78, 117 Dean, R. A., 234, 236. 237. 238, 267. 291 Degens, E . T., 29. 34, 103, 113 F De Mann, J. G., 248, 249, 305 Faller. A. J.. 80, 113 Demian, E. S., 430 Fallows, R. G .. 234. 236, 237. 238. 267, Dennis, J. V., 233, 237. 244, 29d Department of Scientific and I I ~ U S 291 Federov, K. N., 27, 117 trial Research, 274, 281, 294 Felix. S. S., 174. 212 Devanesan, D. W., 150, 209 Fenske, M. R.. 266, 267, 304 Devliri, T. R. E., 258, 292 Fenton, A. F., 257, 295, 431 Dianova, E. V., 266, 268, 3U.i Fenton, C. L., 431 Diaz-Pfiferrer, M., 256, 294 Piah. A., 234, 236, 237, 238, 267, 291 Dietrich, K. R., 224, 294 Dilling, T., 220, 294 Fleming, R. H., 23. 99. 101, 118 Fohl, J., 243, 297 Dillon, W. P., 431 Fontaine, M., 182, 202, 209 Dinamani, P., 403, 431 Forster, G. R., 277, 283, 294. 301 Djahjadiredja, R., 176. 209 Dlaingsastro, A. S., 150, 159, 173, 209 Foster, N. R.. 281, 29; Dodgson, R. W., 308, 325, 371. 384, Fournier. R. 0.. 91. 113 Pox, D. L., 29, 113, 4.31 399, 431 Fox, F. E., 40, I 1 3 Doroshev, S. I., 149, 151, 209 Frankenberg, D., 431 Douglas, E., 223, 303 Fretter, V., 431 Drew, E . A,, 277, 283, 294 Duckworth, D. F., 234, 235, 236, 242. Frey. D., 192, 199, 202. 209 Frost, A . , 139, 153. 209 292 Frost. S. W.. 4.31 Dudley, G., 223. 225, 228, 275, 291 Fujiya, M., 281, 291 Dundee Corporation. 227, 294 Fukuda, M.. 3, 116 Dnursma, I?. K., 16, 30, 45, 102, 1 1 3 Fnknshima. Y., 307, 308, 385. 419. U-1 Dxyaban. I.. 266, 294

440

AUTHOR INDEX

G Gage, J., 277, 283, 294, 301 Galliher, E. W., 451 Galtsoff, P. S., 237, 248, 249, 250, 252, 254, 272, 293. 295, 308, 333, 373, 385, 419, 431 Ganpati, S. V., 150, 210 Garrett, W. D., 76, 113, 114 Geddes, Lord, 290, 29s George, M., 268, 275, 281, 29.j Ghazzawi, F.. 150, 152, 168, 210 Gianotto, F.. 210 W e t , R., 250, 252, 259, 29.5 Gillespie, D. L., 258. 295 Giraud, A., 280, 301 Gloyna, E. F., 231, 29.; Goad, C., 218, 296 Goering. J. J., 4. 16, 66, 83, 1l.i Goethc, F., 244, 258. 296 Goldacrc, R. J., 41, 113, 255. 262. 29; Goldman, C. R., 94, 113 Goodsell, W., 204, 210 Gordon. D. C., 4, 5 , 7. 9, 12. 14. 18, 20, 21. 25, 30, 35, 37, 39. 66, 78, 88. 107, 11.7, 114. 118 Gowailloch, J . N.. 250, 29.5 Graham, A., 431 Greenberg, A. E., 241, 1-92 Qrcenberg, M. J., 397, 399, 403, 412, 4.32 Greenwood, J. J. D., 227, 295 Gribanov, L. V . . 207. 210 Griffith, D. de G., 288, 29,; Gross, A. C., 246, 29.7 Gunkel, W., 267, 284, 29; Gmither. A. C. I,., 167, 210 ClllltS41. J . 8.. 247, 249, 295

H Habc, T.. 4;'l Hagrneicr. E.. 3. 6 , 37, 11.; Halaaz. I.. 243, ,295 Hall. D. N. F.. 133, 158. 170. 186, 310 Hamilton. R.D., 91. 93, 94, 102. I14 Hitrida. N.. 30. 33, 111Hardenberg, J. D. F.,122. 210 Harder. W., 27, 114 Harrison, J. G . , 246. 257, 2.96

H a r r y , H. W., 366, 377, 392, 131 H a r t u n g , R., 237, 241, 244, 246, 296 H a r v a , O., 242, 296 Harwood, G., 277, 283, 294 Hasegawa, I.,241, 303 H a t a i , K., 431 Haven, D. S., 307, 308, 333, 373, 385, 413, 419, 420, 422, 425, 428, 429, 131, 432 Hawkes, A. L., 215, 244, 250, 251, 296 Headington, C. E., 240, 241, 243. 299, 303 Hedgpeth, J. W., 140, 141. 210 Hcllebust, J. A., 43. 94, 95, 114 Helson, V. A., 257, 300 Henderson, C., 224, 294 Henderson, E. M.,231, 296 Herd. M., 242, 2.96 Herzfeld, K. F., 40, 113 Heukelekian, H., 255, 268, 29.3 H m t t , R. A,. 146, 165, 167, 170. 194, 201, 203, 210 Hickling, C. F.,128, 136, 146, 154, 158, 168, 169, 176, 178, 210, 211 Hidu, H., 281, 296 Higashi, S., 432 Hirasalra, R., 432 Hirschfold, D. S., 3, 25, 40. 75, 112 Hobble, J. E., 93. 118 Hobson, L. A., 17, 21, 33, 37, 66. 114 Hodgman, C. D.. 235, 296 Hofmann. R . E., 271, 296 Hofstede. A,. 199. 210 Hogg, C., 232. 296 Holdsworth, M. P., 221, 272. 274, 296 Holl, A , 281, 291 Holmc, N. A., 224, 268, 272. 275, 276, 292, 298 Holm-Hansen, 0.. 17, 19, 20. 25, 29, 30, 31, 32, 63. 65, 91. 92. 93, 94, 102, I 1 1 Hopkins, S. H., 233, 2.98 Hornell, J.. 120, 210 Howe, M. R.. 27. 28, 29, 118 Howe, R. E.. 228, 296 Hubaiilt, E., 249, 2.96 Hiidinagn, M., 136, 150. 210 Hughes, D. E., 268, 272. 296 Hughes, P., 238, 296

44 1

AUTHOR INDEX

Hunt, 0. S., 244, 296 Hunt,ress, C. O., 231, 296 Hydraulics Research Station. 225, 296

I Iliii, B., 121, 123, 126. 140, 150. 154, 163, 199, 201, 210 Illing, L. V., 432 Imai, T., 308, 413, 419, 425, 426, 427, 429, 432 Ineson, J., 240, 241, 296 Ingram, W. M., 266, 298 Inoue, H., 3, 116 Inouye, H., 136, 167, 210 Institute of Petroleum, 230, 231, 233, 297 Intergovernmental Maritime Consnltative Organization, 217. 218, 223,

297 Iiiternatioiial Committre for Bird Prpservatioii, 244, 297 Isaacs, J. D., 29, 113 Iselm, C. O’D., 23, 24, 114 Itagaki, H., 432 Ito, S., 308, 413, 419. 425, 426, 427, 429, 4.32 Izyurova. A. I., 268. 297

J Janak, J., 243, 297 Jannasch, H. W., 62, 92, 96, 111. 118 Jarvis, N. L., 76, 114 Jee, E. C . , 247, 252, 302 Jegla, T. C., 397, 399, 403, 412, 432 Jensen, A., 51, I I 7 Jespersen, P., 102, 114 Jesus, A. de, 212 Johannes,R. E., 7, 51, 96, 98, 102, 111, 114, 116, 118, 332 Johannesson, J. K., 242, 297 John, D. M., 261, 283, 291 Johnson, M. W., 23, 99, 101, 118 Jones, D., 261, 283, 291 Jones, G. E., 62, 114 Jones, J. R. E., 280, 297 Jones, L. G., 234, 297 Jsrgensen, C. B., 419, 432 Jouanin, C., 246, 297

K Kalle, K., 140, 210 Kamps, L. F., 432 Kaplan, A. M., 266, 292 Keddie, J. P. F., 227, 292 Kennedy, R. J . , 263, 293 Kennedy, W. A., 206, 211 Kenny, G. S., 243, 299 Keshwar, Barbara, 6, 47, 48, 56, 57, 79,112 Ketchum, B. H., 21, 1 l . i . 144, 145, 211 Kim, 153 Kimura, T., 432 King, C . L., 232, 297 Kirby, J . H., 230, 297 Kirschman, H. D., 241, 297 Klein, K., 273, 304 Khiigler, Gwendolyn W., 237. 296 K~USS. W. M., 220, 221, 222, 225, 297 Kobayashi, H.. 420, 432 Koe, B. K., 262, 303 Koehring. Vera, 250, 254, 29.i Kolpack, It.. 239, 297 Korneev, A. N.. 207. 210 Korneeva, L. A., 207, 210 Kornicker, L. S., 308, 379, 397. 408, 406, 411, 432 Korringa, P., 140, 146, 211, 264. 297, 419, 432 Kosnge, S., 432 Kotaka, T., 431 Kotin. P., 262, 302 Krey, J., 3, 6, 10, 37, 11.7 Kriss, A. E., 64, 109, l I 6 Kromov, A. V., 180, 208 Kruse, P., 308, 310, 381. 397, 406. 433 Kubecova, V.. 243, 297 Kucharczyk, N., 243, 297 Kumpf, H. E., 307, 308. 309, 317, 321, 328, 329, 330, 334, 338, 340, 345. 349, 350, 370, 372, 373, 374, 375, 383, 384, 385, 386, 387, 388, 389, 390, 433 Kusuki, U.. 421, 422, 425, 426, 427, 430 Kutukuhn, J. H., 154, 211 Kuwatani, Y., 432

442

AUTHOR INDEX

L Lackey. J . B., 140, 146. 147, 176. 211 Lane, E. J.. 227. 297 rmlgston, P., 237, 297 Lanskaja, L. A., 254, 300 Larkuni, A. W. D., 277. 283. 298 Lavrovsky, V., 207, 211 Leavitt, B. B., 90. 105. 11; Lebour, M. V.. 432 le Dantec, J., 182, 211 Leenhardt, H., 250, 297 le Mare, D. W., 179. 186, 199, 211 Lemmctyinen, R.. 244, 258, 29; L w i n e . W. S . , 241, 298 Lewis, J. R., 261. 298 Lichtenberg, J. J., 233. 242. 302 Lillie. H., 247, 298 Limbaugh, C.. 27, 115 Lin. S. Y., 123, 126, 128, 130. 151. 154, 155, 157. 161, 162, 164. 166, 172, 175. 176, 195. 199, 200, 202, 211 Lister, M.. 432 Lodge. 8. M., 262, 298 Loosanoff, V. L.. 419. 420. 421, 4.33 Lopez. J. V., 174, 212 Loriston-Clarke, A. G.. 237, 238. 267. 291 Lovett, J. I%., 27, 28, 1l.i Ludwig. H. F., 233, 241, 208 Ludzack. I?., 266, 267, 298 L u n d , E. J., 413, 420. 427. 4 6 3 Lunz. R. G.. 250, 298 Lythgoe. J . N., 277, 283, 294

M McCauley. R. N., 252. 254, 299 McDermott, G. N.. 224, 248. 294. 304 McDermott, J. N.. 224, 29,5 McGill. D. A., 20, 21, 31, 86, 11.; McKay, H. A. C., 272, 299 McKee, J. E., 232, 234, 235, 249. 266. 299 Mackin, J . G., 233, 250, 251. 256, 298 McKinney, R. E., 266, 299 McLeish, W.. 26, 115 MacNae, W., 148, 211 Madigan, C. T., 433 Maehler, C . Z., 241, 295 MAlbcea, I., 248, 249. 253, 298

Maldura, C.. 281. 298 Malma, J. P., 231, 295 Mallet, L., 262, 263, 292, 298, 299 Malone, T. C., 141. 142, 170, 203, 211 Mane, A., 159, 161, 177. 192, 193, 211 Mann, H., 248. 273, 281, 299, 302 M m n i n g , R . B., 307, 308, 309, 317, 321, 328, 329, 330, 334, 338, 340, 345, 349, 350, 370. 372. 373, 374, 375, 383, 384. 385. 386. 387, 388. 389, 390, 433 Manwell, C., 283, 299 Mapes, G. S., 241. 298 Marchetti, R., 280, 281, 299 Marsault, B. M. (Mrs.), 264, 299 Marshall, J. M., 218. 299 Marsland, D., 254, 299 Matsui, I., 434 Matsui, J., 420, 432 Matsumoto, S., 435 Matsunaga. N., 433 Matthiessen, G., 205. 212 Matulova, Dragica, 280. 281, 299 Maybourn, R., 223, 292 Mayo, F., 225, 273. 275, 280, 299 Mazia, D., 12, 35, 115 Meinschein, W. G . . 243, 299 Melpolder, F.W.. 240. 243. 299 Menon, M. K., 189, 211 Menzel, D. W., 3, 4, 6. 13, 16, 17. 18, 20. 22, 25, 26, 30, 31, 38. 40. 41. 46. 47, 66, 75, 79. 83, 86, 87, 89. 90, 94, 96, 100, 102, 105, I l 5 , 118 Merizel, R. W., 251, 300 Merz, R. C.. 233, 241, 300 Meyer, R. R., 231. 300 Middleton, F.M., 241. 242, 302 Ministry of Housing arid Local Goveriiment, 274, 300 Ministry of Transport, 217, 218, 224, 234, 238, 251, 300 Minshall. W. H., 257, 300 Minter, K. W., 254, 300 Mironov, 0. G., 251, 254, 300 Mishustina, I. E., 109, 115 Mitchell, C. T., 234, 297 Mitzkevich, I. N., 109, 115 Miyamura, M., 136. 156, 210 Miyauti, T., 433 Moffitt. J.. 258, 300

443

AUTHOR INDEX

Montes, G . E . , 231, 300 Montgomery, R. B., 82, 117 Moore, H. B., 307, 308, 309, 310, 315, 316, 317, 318, 319, 321, 325, 326, 327, 328, 329, 333, 337, 338, 339, 340. 356, 358, 368, 369, 370, 371, 373, 376, 377. 378, 379, 380, 381, 382, 384. 386, 391. 393, 395, 397, 403, 406, 433 Moore, T. W., 237, 271, 277, 300 Moorehouse, I?. W., 433 Morales-Alamo, R., 307, 308, 333, 373, 385, 413, 419, 420, 422, 425, 428, 429. 431. 432 Monta, R. Y., 109. 118 Morovic, D., 151, 211 Mortimor, C . H., 176, 211 Morton, J. E., 343. 374, 387, 430, 13.1 Morzer Hrmjns, M. F., 258. 504 Moyso, J., 250, 262, ,300 Munk, W. H., 74, 113 Murip, 0.. 434 Murray, J.. 434 Musgrave, L. R . , 233, 242, 30% Muskip. Senator E.. 274, 300

Nomejko, C. A., 421, 433 North, W. J., 234, 247, 249, 2 5 2 , 254. 255, 259, 260, 275, 293, 297, 301

N

Packham. R . F.,240. 241, 290‘ Pakrasi, R . B., 123, 127, 133, 169, 171, 179, 184, 185, 188, 189, 199. 202, 203, 212 Baramonov, A. N., 28, 84, 116 Parejas, E., 434 Parslow, J. L. F.,216, 259, 301 Parsons, T. R., 6, 9. 16, 29, 31, 32, 33, 36, 50, 51, 56, 78, 90. 92, 93, 96, 112, 116, 117 Patnaik, S., 153, 211 Pearcg, W. G., 104, 116 Pearse, A. 0. E., 116 Peller, E., 246, 301 Pelseneer, P., 382. 384, 386, 388. 390. 392, 407, 408, 414, 434 Peoples, S. A., 256, 257, 294 Perdriau, J., 262, 301 Perlrins, E. J., 282, 287, 301 Permutit Company, 223, 301 Petter, A. E. J., 232, 296 Pfaff, J. D., 243, 602

0 Odum, E. P . , 142. 21% Odum, W. E., 144. 146, 167, 168, 211 Ohio River Valley Water Sanitation Commission, 231. 301 Ohshiba, Y., 430 Okawa, T., 421, 434 Okubo, K., 248, 300 Okuho, T., 248, 300 Onodera, K., 169, 198, 207, 212 Organmation for Economic Co-operation and Devcloprnent , 23 1. 301 Orr, A. P . , 145, 212 Orr, R. T., 258, 300 Orton, J. H., 237, 252. 268, 301 O’Sullivan, A. J., 283, 286. 301 Ota, S., 307, 308. 385, 403, 419, 420, 434 Otsuki. A.. 51. l l / i Owen, G . , 394, 434

P Nakamiua, M., 342, 4.34 Nakazima, M., 320, 434 Napora. T. A., 104, 116 Nash, C., 206, 211 Natarajan, A. V.. 153, 211 Natural Environment Research Council, 275, 300 Naylor, E.. 224, 252, 300 Nelson-Smith, A., 225, 227, 250, 251, 253, 261, 262, 280. 283, 284, 285, 286, 300 Neumen, G. G., 28, 84, 116 Neushul, M.. 247, 249, 252. 254, 255, 259, 260. 275, 301 Newell, B., 16, 20, 30, 86. 113 Newell, R. S., 31, 116 Newell, R., 143, 144, 211, f34 Nietsch, B., 240, 294 Nishizawa, S., 3, 116 Nitta, T., 248, 300 Noda. H., 432

444

AUTHOR INDEX

Philippi, E., 434 Pillay, T. V. R., 122, 127, 132, 141, 146, 150, 158, 159, 167, 168, 171, 184, 185, 199, 202, 203, 207, 21% Pilpel, N., 236, 266, 268, 301 Poirier, 0. A., 237, 301 Pomeroy, L. R., 7, 96, 98, 111. 116 Pomeroy, R., 241, 297 Popham, M. L.. 308, 317, 342, 374, 380, 387, 434 Portier, P., 244, 301 Portmann. J. E.. 2.51. 252, 253, 281, 284, 287, 301 Potter, W. G., 259, 303 Potts, G. W., 277, 283, 294, 3 0 f Prat, J . , 280, 301 Priou, Marie-Louise, 262, 298 Prokop, J. F., 266, 268, 301, 306 Provasoli, L., 29, 30, l l G Prytherch, H. F., 250, 254, 295 Parchon, R. D., 310, 320, 334, 369, 378, 382, 384, 386, 388. 390, 392, 393, 394, 395, 408. 410, 413, 417, 418, 434, 4 3 5 Purdy, E. G., 4.32

R Rabanal, H.. 159, 161, 177, 192, 193. 211 Rabanal, H. R., 123. 128, 171, 174, 176, 199, 202, 204, 212, 216 Raffy, A., 244, 301 Rakestraw, N. W., 103, 116 Ramos, V., 174, 212 Ramsdale, S. J., 237, 243, 267, 301 Ranwell, D. S.. 236, 257, 284, 286, 301 Rasalan, S. B., 159, 163, 170, 188, 200, 204, 209 Rechnitzer, A. B., 27, 115 Redfield, A. C . , 99, 116 Reichenbach-Klinke, H., 248, 302 Reid, B. L., 239, 268, 292 Reineck, H. E., 435 Reish, D. J., 252, 259. 30% Remard, A. F., 434 Ricci, G . , 265, 302 Rich, L. G., 233, 298 Richardson, A. J., 283, 286, 301 Richter, E., 435

Richter, It., 435 Riggs, C., 153, 21% Righi, G., 435 Riley, G. A., 3, 4, 6, 7. 10, 11, 12, 14, 16, 21, 37, 42, 43, 44, 47, 48, 49, 56, 57, 66, 74, 79, 81, 82, 83, 84, 86, 89, 90, 94, 99, 100, 101, 102, 105, 106, 109, 112, 115, 116, 117 Rittinghaus, H., 246, 302 Roberts, C. H., 239, 301 Roberts, L. E. J., 272. 302 Robertson, R.. 435 Rocquement, Y., 274, 302 Roddy, M. J., 241, 298 Rogers, M. It., 266, 29% Ronquillo, I. A., 164, 176, 212 Rosen, A. A., 233, 241, 242, 302 Rossby, C. G., 82, 117 Rothpletz, A., 435 Round, F., 125, 212 Rudolfs, W., 2.55, 268, 293 Rushton, W., 247, 252, 302 Russell, F. E., 262, 302 Ryther, J., 205, 212 Ryther, J. H., 13, 16, 18. 22, 30, 31, 86. 87, 89, 90, 94, 96, 100, 102, 105, 115

S Saanin, H., 174, 21% Sabioncello, I., 151, 211 Safranko, J., 240, 305 Saha, K., 150, 184, 202, 203, 21% Saito, M., 136, 210 Samson, V. H. F., 232, 302 Sardu, J., 263, 299 Sato, T., 435 Satomi, M., 432 Sawada, Y., 435 Sawicki, E.. 243, 302 Sawyer, M. P.,223, 292 SchBfer, W., 307, 308, 347, 375, 389, 435 Schaut, G. C., 248, 249, 302 Scheier, A., 249, 251, 281, 292, 295, 302 Scheiman, M. A., 76, 114 Scherer, F. L., 232, 302 Scherfig, J., 241, 298

445

AUTHOR INDEX

Schmid, 0. J., 281, 299, 302 Schmidt, R., 205, 212 Schneider, R. J., 227, 271, 30% Schuldiner, J. A., 242, 302 Schuster, W., 123, 125, 126, 131, 143, 146, 147, 148, 151, 158, 159, 160, 162, 164, 165, 166, 169, 174, 176, 178, 189, 192, 194, 199, 202, 204, 212 Schuurman, J. J., 127, 128, 132, 166, 174, 213 Sebba, F., 38, 1 1 7 Sedgwick. S. D., 139, 21.3 Seki, H., 51, 116 Selby, S. M., 235, 296 Select Committee on Science and Tpchnology, 215, 216, 219, 502 Shabad, L. M., 263, 302 Shackleton, L. R. B., 223, 303 Sharp, J., 19, 114 Shaw, J. M., 252, 256, 303 Shelbourne, J. D., 206, 213 Sheldon, R. W., 5, 9, 50, 56, 78, 1 1 7 Shelford, V. E., 248, 249, 303 Sherratt, J. G., 242, 303 Shimkin, M. B., 262, 303 Showell, E. B., 231, 300 Siebnrth, J. M., 51, 1 1 7 Siegel, A., 39, 117 Silsby, G. C., 280, 303 Simard, R. G., 241, 303 Simpson, A. C., 247, 250, 264, 284, 303 Singapore Fisheries Division, 200, 213 Skopintsev, B. A., 2, 1 1 7 Small, L. F., 104, 116 Smayda, T. J., 67, 117 Smith. J. E., 234, 238, 239, 247, 254, 261, 262, 267, 268, 271, 272, 275, 276, 277, 282, 283, 284, 286, 290, 303 Smith, K. L., 431 Smith, R. F., 122, 213 Smith, R. O., 250, 254, 295 Smithsonian Institution, 234, 239, 247, 254, 303 Snyder, D. E., 258, 292 Snyder, L. R., 243, 303 Solanas, D. W., 234, 304 Solozano, L., 33, 1 1 7 Somersalo, O., 242, 296

Sorokin, J. I., 91, 1 1 7 Sorrentino, R., 226, 303 Southern, H. N., 259, 303 Southward, A. J., 261, 262, 282, 284, 293, 303 Southward, Eve C., 282, 284, 293 Spagnoli, G., 290, 303 Sparks. A. K., 233, 250, 251, 298 Spencer, J. F., 240, 30.3 Spooner, G. M., 221, 224, 268, 275,287, ,096, 504 Spooner, M. F., 221, 247, 250,254,262, 268, 269, 271, 275, 282, 283. 287, 288, 303, 304 Stander, G. H., 237, 304 Stanley, E. W., 234, 304 Stanley, T. W., 243, 302 Staruschenko, I. L., 180, 208 Stasek, C. R., 401, 435 Steele, J. H., 81, 1 1 7 Stehr, E., 226. 237, 304 Stenger, V. A ,, 240, 305 Stephens, G. G., 234,235,236,242,292 Stephens, K., 93, 112 Steven, G. A., 145, 209 Stommel, H., 24, 27, 80, 81, 86, 105, 116, 117 Stone, R. W., 266, 267, 304 StBta, Z., 249, 304 Straughan, D. M., 254, 290 Strickland, J. D. H., 6, 16, 17, 20, 25, 29, 30, 31, 32, 33. 3G, 90, 91, 92, 93, 94, 96, 102, 112, 114, 116. 1 1 7 Stroop. D. V., 236, 240, 304 Sturmey, S. G., 288, 304 Sturz, O., 273. 304 Suess, E., 37, 76, 118 Sulit, J. I., 171, 170, 223 Surber, E. W., 224, 248, 29S, 304 Sutcliffe, W. H., 3, 5, 9, 19, 25, 26, 38, 40, 41. 75, 79, 112, 114, 117, 118 Sverdrup, H. V., 23, 99, 101, 118 Szekielda, K.-H., 14, 17, 118

T Tabata, K., 248, 300 Tagatz, M. E., 248, 304 Tait, R. I., 27, 28, 29, 118 Takahashi, J., 435

446

AUTHOR INDEX

Takeuchi, T., 421,428,425,426,427,430 Taki, Iw., 435 Tang, Y. A., 147, 152, 155, 156, 166, 173, 174, 176. 194, 196. 199, 202. 204, 207, 213 Tanigiichi, M., 434 Taning. A. V., 244, 304 Tanis. J. J. C., 258, 304 Tarzwell, C. M., 233, 304 Tati, Ramelan, 174, 212 Taylor, D. W., 403, 436 Taylor, W. E. L., 272, 280. 306 Teal, J. M.. 104, 1lX Tegelberg, H.. 250, ,304 Tendron. G., 247, 304 Thalrurta. S. C., 123, 127. 133. 169, 171, 179. 184. 185. 188. 189. 199, 202, 203. 212 Tham, A. K., 186, 213 Thew, M. T., 237, 238, 267. 291 Thlel, G. A., 237, 301 Thiele, J.. 382, 384, 386. 388. 390. 392, 408, 415, 435 Thompson. J., 152, 208 Thomson, J.. 150, 151. 213 Thorpe, E. M., 435 Timmoris, C. 0 . .76, 114 Timmons, F. L., 252, 256. -303 Toman, M.. 249. 304 Tomczak. G., 238. 304 Treccani. V.. 268, 304 Tripp, R. R.,93, 112 Tsujii, T., 435 Tuck, L. M., 244. 258, 259, 90.j Tnrnbnll. H.. 248. 249. ,?0.5

U Ueno. P..435 U.S. Coast Guard, 222, 30.; U.S. Congress, 220, 305 U.S. Department of Interior. 223, 305 U.S. Public Health Service, 249, 305 U.S. State Department, 218. 30.5 Utinomi. H., 435

V Vaccaro. R. F.. 6, 18. 92, 96. 115, 118 Van De Wiele, C., 287. 30.5

Van Hall, C. E., 240, 305 Van Hemert, D.. 4, 10, 11, 12, 14, 16, 21, 37, 42, 43. 44. 49, 66, 83. 84. 89, 90, 94, 102, 105, 109, 117 Van Horn, Virginia, 268, 292 Van Overbeeli, J., 257, 305 Van Weel, P. B., 435 Vatova, A., 148, 149. 182, 213 Vaughan, T. W., 435 Venter, J. A. V., 237, 304 Vera, A. M. de, 174, 177, 208 Verdcourt, B., 435 Verwey, J., 428, 436 Veselov, A. E., 248, 305 Vik, K. O., 138, 213 Villadolid, D., 213 Villaluz, D.. 159, 161. 177. 192. 193. 211, 213 Villamater, E., 164, 176, 21% Vinogmdov. M. E.. 106, 118 Vinogradova, N. G., 109, 11s Voroshilova, A. A., 266, 268. 30,; Vymetal, J., 243, 297

w Walsh, T., 223, 303 Wangersky, P. J., 4. 10. 11. 12. 14. 16. 21, 36, 37, 38, 39, 42, 43. 44. 45. 49, 66, 76, 77, 83, 84, 89. 90, 94. 102, 105, 109, 117, 118 Wardley Smith, J., 235, 239. 271, 272, 275, 277, 286, 306 Warfield, C. W., 240, 243. 299 Weast, R. C., 235, 296 Webb, K. L., 102, 114, 118 Webber, L. A., 240, 305 Webster, F., 22, 113 Wegner, E. E., 243, 293 Weiner, L.. 248, 249. 253. 298 Weir, P., 240, 305 Weiss, H. B., 436 Wells, G. P., 436 Weston, R. F., 248, 249. 30.i Westphal, Althea, 264, 305 Wetzel, C. D., 27, 113 Wheeler, E. H., 106, 118 White, A. G . C., 266, 267, 304 Whittick, A., 261, 283, 291 Wilbur, K. M., 436

417

AUTHOR INDEX

Wilkirisori, R. E.. 237, 243, 267, 301 Williams, P. M., 13, 17, 20. 25. 29, 30. 31. 32, 114, 118 Wilson, A. T., 40, 118 Wilsoii, D. P., 282, 284. 30.i Wilson, R. F., 6, 118 Winckworth, R., 308, 403. 43fi Winter, J.. 436 Wood, E. J. V., 91, I 1 8 Woodcock, A. H., 25, 40. 80. 113, 118 Wragg, L. E., 246, 305 Wright, R. T., 93, 118 Wust, G., 86, 118 Wyllie. D.. 272, 280, .PIC

Y Yagi, T.. 4.3.; Yang, 153

Ynshouv, A., 151, 159, 163. 164. 168. 213 Yoiige, C. M . , 394, 395, 400. 411. 412. 4 3 ti Yoshiaki, T., 136, 211) Yoshiha, 8.. 436 Puiki. R . , 420, 4;36

Z Zahiier, K., 248, 30(i Zambrihortsch, E’. S., 154. 163. 164. 181,213 Zanghi, Lima, 263, 299 Zechmeister, L., 262. 303 Zenkevitch, L. V., 140, 21 1 ZoBell, C. E., 64, 109. 118, 236. 239, 266, 267, 268, 306 Zuckerinan, Sir S.. 274, 275, ,306

This Page Intentionally Left Blank

Taxonomic Index A d b r a , 312, 314 alba, 356, 376, 391 nitida, 356, 376, 391 Abrina, 312, 313 lunella, 356, 364, 376, 391 Acanthopleura granulata, 270 Acetes, 179 Acrochaetium infestans, 283 Actinia equina, 285 Adepedonta, 415 Adosmacea, 393 Alaria esculenta, 261 A k a torda, 243 Algae, 1, 2, 43, 46, 51, 91, 93, 94, 95, 120, 147, 171, 255, 256, 268, 281, 283, 284, 343, 381 Slosa sapidissima, 248 Ambassis, 153 Amoeba, 254 dubia, 254 Amphioxus, 380 Amusiidae, 312, 315, 334, 335, 336, 386, 412 Amiwium, 315, 336, 379, 412 japonica, 335, 373, 386 Anacharis (Elodeu) canadensis, 256 Anadurn, 322, 397 broughtoni, 322, 370, 383 Anadurn (Scnphnrca)suberenufa, 321. 370, 383, 401 Anus plutyrhynchos, 246 platyrhynchos rubripes, 244 rlnguilla, 151 anguillu, 135, 169 japonica. 135, 169, 194, 198 Anisocorbuln venusta, 368, 378, 393 Anisomynria, 383, 384. 385, 386, 387, 408, 41 1, 415 Anodontu, 41 1 wootliana, 342, 374, 387 Ariomalodesmacea, 383, 388, 406, 414 Anomalodosmsta, 415

Anomalodiscus squamosus, 352, 375, 390 Anomia, 312, 397, 412 lischkei, 341, 373, 387, 402 Anomiacea, 387, 412 Anomiidae. 312, 316, 341, 387 Anthopleura xanthograrnmia, 252 Aracea, 383 Arca, 322 umbonata, 321, 370, 382 Arcidae, 312, 316, 321, 322, 323, 383, 404 Arcopagia c r a s a , 358, 377, 391 Arcopella isselli, 360, 377, 391 Arenicola, 381 Armeria rnaritimu, 256 L4rternia. 3, 26, 157 salinu, 287 Ascidia, 380 ahodori, 381 Ascophyllum nodosum, 261, 283, 2886 Asteriu rubens, 252, 282 Asthenodontida, 393. 409, 416 ,4therina, 170 Atrina. 379 pectinata japonica, 331, 372. 385 Aurelia aurita, 252 Avicennia, 174 Aviculidae, 330 Aythya, 244

B Ralanus balanwides, 254, 262, 286 qLandula, 254 Harbatiu (Savignyurcn) obtusoides, 322, 371, 383 vireucens, 322, 371. 383 Harn,ea. 3 12. 3 13, 404 japonica, 364, 378, 393 Rurn,eu ( ~Jmitnkea) japonica, 369 Bithyniidae, 403

449

450

TAXONOMIC INDEX

Hittiurn refzcrclotitm. 25 1 Boda, 254 Brachiodontes citrinus. 317, 32.8, 372, 384 Uryopsis hypnoides, 283 Ettccinum undatum, 282

C Cuecella. 312, 313 chinensis, 362, 371. 391 Calanus jinmar chicus, 253 hyperboreus, 107 Calliblepharis jubata, 283 lanceolnta. 283 Cullistn chinensis. 350. 375, 390 Callocoiichida, 409, 416 Cambarus, 252 Capitella capitata. 252 Carassius r~uratus.28 1 carassius , 24 8 Crircinus. 283 maenas, 252 Cardiacen, 389, 413 Cardiidae. 312, 313. 314, 346-349, 389. 396, 404 Carrliomya, 3 12 gouldiana septewrtrzonalis, 320, 370, 383 Cardita, 379, 412 leana, 342, 374, 381 Carditacea, 379, 387, 412 Carditidae, 312, 316, 342, 387 Cardium, 142. 314, 347, 364, 403, 428 edule, 251, 281, 287. 347, 375. 389 y uadrugenariztm. 341. 315 Castor jiber. 246 Catenella repens, 285 Chaetoceros curvisetus. 254 Chaetowhorpha, 164, 166 Chawka reflem, 343, 374, 388 Chamacea, 388 C’hamidatr. 312. 314. 343, 344. 388. 404

Chanos, 120, 130, 135, 143, 144, 146, 150. 151, 152, 153. 154, 155, 157. 159, 160, 161, 162, 163, 164, 165, 166, 167, 169, 171, 172, 173, 174, 175. 176, 177, 178, 179, 181, 188, 189, 190, 191. 192. 194, 195, 196. 197, 200 chanos, 151, 152 Chiton polii, 250 Chlamydomonas, 281 Chlamys, 312, 316, 336, 338, 379, 397, 404. 405, 412 latiauratus, 338, 373, 386 nobilis, 336, 373, 386 opercularis, 283, 373, 386 squamata, 338, 373, 386, 399 tigerina, 339, 373, 386 triradiata, 316, 338, 339. 373, 386 varia. 338. 373, 386 vesiculosus, 337, 339, 386 Chlamys (Aeyuipecten) opercularis, 339 Chlamys (Cryptopecten) vesiculoides, 338, 373 Ghlamys (Mimachlamys) nobilis, 339 Chlamys (Mirapecten) squamata, 339 Chlorella, 203, 281, 420 Chrysophrys, 182 Chthamalus, 262 Jissus. 254 stellatus, 254, 262, 28.5 Ciona, 380, 381 intestinalis, 381 Cione cancellata, 350, 375, 390 Circe scripta, 349, 375, 390 Cladophora, 166, 283 rupestris, 283, 285 Clangula hyemalis, 244, 259 Claudiconcha japonica, 353, 376, 390 Goccolithus huxleyi, 95 Codium fragile, 285 Colloconchida, 385, 387 Colpomenia peregrina, 261, 285 Corallina oflcinalis, 277. 283. 285

45 1

TAXONOMIC INDEX

Co&c ula japonica, 345, 347, 374. 389 leana, 345, 374, 389 Corbiculacea, 389 Corbiculidae, 312, 314, 345, 346, 389, 404 Corbulidae, 312, 314, 368, 393. 404 Coscinodiscus, 343 Coscinodiscus granii, 254 Crangon erangon, 253, 282, 287 Crassostrea. 250, 400, 412, 421, 422, 426, 427 angulata, 250 signs, 332, 372, 385, 400, 419. 421, 422. 423, 424, 425, 426 virgin&, 250, 251, 281, 332, 373, 385, 419, 420, 422, 427 Crenimugil, 151 labrosus, 146, 150, 151, 156, 168 Ctenopharyngodon idella, 149 Cuspidariidae, 320, 383, 404 Cyathodonta (Eximiothracia) concinna, 344, 374, 388 Cyclops, 163, 252 Cyprinodon , 170

D Daphniu. 163. 164, 178 magna, 253 pulex, 287 Delectopecten, 3 12, 404 randolphi, 386 Delemeria sanguinea, 283 Desulfomnculum, 268 Desulfovibrio, 268 Diophrys, 254 Distychlis spicata, 256 Ditylum brightwelli, 254 Dolichoglossus, 381 Donacidae, 312, 314, 345, 388 Donax variabilis, 345, 374, 388 Dosinia ( Phacosoma) japonica, 353, 376, 390

E Echininus, 403 Echinus esculentus, 252 Elminius modestus, 254, 282

Enigmonia, 4 12 Enteromorpha. 164, 166, 283, 285 compressa, 261 intestinalis, 261 Epinephelus sp., 121 Erycinacea, 317, 380, 412 Erycinidae, 312, 314, 343, 387 EschricUiw glaucw, 247 Etroplus, 154 Eudesmodontida, 388, 393, 409. 416 Eulamellibranchia, 379, 380, 388, 389, 390, 391, 392, 393, 407, 408 Eulamellibranchia (Adepedonta), 392, 393, 411 Eulamel libranchia (Anomalodesmata) , 383, 388 Eulamellibranchia (Heterodonta). 387, 388, 389, 390, 391, 392 Eulamellibranchia (Schizodonta),387, 414 Eupagurw bernhardus, 282 Eutaxodontida, 383. 409, 416

F Fabulina, 310 iridella, 359, 360. 377, 391 minuta, 359, 377, 391 nitidula, 377 pallidula, 360, 377, 391 Festuca rubra, 256 Filibranchia, 379, 383, 384, 407. 414 Fratercula arctica, 243, 259 Frigidocardiurn eos, 348, 375, 389 Fzccus, 51, 261, 262 evesiculosus, 262 linearis, 262 serratus, 285 spiralis, 285 vecriculosus, 2 62, 2 85 vesiculosus vesiculoszrs, 262 Fugu, 122 Fulmarus glacialis, 2 58 Fulvia, 314 hungerfordi, 347, 375, 389 mufica, 348, 375, 389, 397

G Galeommatidae, 342, 343, 387 Galeommidae, 312. 342, 343, 387, 404

152

TAXONOMIC INDEX

Gambusia afinis, 248

Gammarus, 252 pulex, 252 Gari, 312, 313 hosoyai, 354, 376, 391 Gastrodeuteia, 320, 383, 394 Gastropempta, 310, 314, 315, 334, 345-369, 389, 394, 395, 404, 410, 413, 417, 418 Gastroproteia, 317, 382, 394 Gastrotetartika, 314, 315, 316, 317, 334, 386, 394, 395, 404, 410, 412, 413, 417, 418 Gastrotriteia, 316, 320. 334. 383, 394, 395, 404, 410, 411, 412, 413, 417, 418 Gavia, 243, 258 CXbbula, 261 cineraria, 282, 285 divaricata, 251 umbilicalis, 282, 285, 286 Gigartina stellata, 285 Glycymeridae, 312, 316, 323, 383, 404 Cl'lycymeris imperialis, 323. 335, 371, 383 rotunda, 323, 371, 383 Gomphinu (Macridiscus) veneriformis. 352, 375, 390 Gracilaria, 193 confervoides, 174. 177 Grccmmatophora marzna. 254

H Hall currlia YI ipponens is, 32( Halzdrys siliquosa, 261, 385 Halim iorie portulacoirles, 256 Haliotis, 249, 259, 261 Hesperoph ycus harveyunus, 255 Heterocoiichiit, 416 Heterodonta, 400, 415 Hrtrrodontida. 383, 387. 388, 389. 390. 391, 392, 409, 416 Hiatella fluccitla, 355, 367, 378, 392 Hiatrllacca. 392 Hintellidae, 3G7, 368, 392 Hzatula atmta, 354, 376, 391 Himanthulia elonyutu, 261, 283, 285

Holothurians, 381 Hormomya exustes, 328, 372, 384 Hydrobates pelagicus, 258 Hydrobia ulvae, 143 Hydrobiidae, 403 Hydrocharitaceae, 193 Hypophthalmichthys molitrix, 149 Hyriopsis, 41 1 schlegeli. 341, 374, 387

I Isofilibranchida, 383, 384, 409, 416 Isognomon, 379 aluta, 329, 372, 385 legumen, 330, 372, 385 radiata, 329, 372, 385 Isognomonidae, 312. 316. 329,330,385. 404

J Jounnisiella. 31 3 lunaris, 346, 374, 389

L Laevicardium, 314 undatopictum, 348. 375, 389 Lamellibranchia, 379 Laminaria, 261, 285 Larus, 244, 246, 258 argentatus, 263 mtrrinus, 263 Ihsaea, 312. 314, 412 rubru. 342, 343, 374, 387 Latern ula, 344 limicolu. 344, 374. 388 Laternula (Laternulina) jlexuosa, 344, 374, 388 Laternulacea, 388 Latornulidae, 312, 314, 344, 388. 404 Lates, 185 calcarifer. 185 Luurencia pirinntific-a, 285 Leancler serrutus, 253 Lebistes reticulatus, 287 Leda minuta. 319 Lepas fascicularis, 253 Lrpidontida, 409, 415 Lepomis w~acrochirus,248

TAXONOMIC INDEX

Leptonacea, 387 Lichina pygmaen, 285 Lima lima, 340. 373, 387 sowerbyi. 340. 373, 387 Limacea. 387 Limidao, 315, 340, 341, 387, 404 Limopsacea, 383 Limopsidao, 312, 314, 323, 324, 379, 383, 395, 404, 411 Limopsis, 379, 395 tajimae, 323, 335, 371, 383 Lipodontida, 382 Lithothamnion, 277, 283 Littorina, 261 Zittorea, 251, 281, 282, 283, 286, 288 neritoides, 285, 286 obtusata, 251, 282, 285, 286, 288 saxatilis, 251, 282, 286 Littorinidae, 403 Liza, 135, 151, 152 uurata, 121, 150, 163, 167, 180, 181 macrolepsis, 121, 153 provensalis, 150 ramada, 150 saliens, 150 speigleri, 150 Lucinacea,, 389, 413 Lucinidae, 312, 346, 389 Lumbrinereis, 38 1 Lyngbya, 175 Lyonsia ventricosa, 344, 374, 388 Lyonsiidae, 312, 314, 344, 345, 388 Lysiosquilla maculata, 380

M Macoma, 312, 313, 358, 361, 404 incongrua, 361, 377, 391 praetexta, 361, 377, 391 tokyoensis, 361, 377, 391, 396 yoldqormis, 361, 377, 391 Macrocystis, 255, 261 pyrqera, 255, 259, 260 Mactra, 312, 314, 362, 397, 404 crossei, 363, 377, 392 pulchella, 363, 377, 392 sulcataria, 362, 377. 392, 398 A . M 33-8

453

Mactracea, 391, 413 Mactridac, 312. 314. 362 366, 392, 404, 405 illmtelli~m.340 umakusaense, 341. 373, 387 Melosira moniliformis, 254 Mercenaria mercenaria, 250, 281 Meretrix, 312 lusoria, 353, 375 390 Mesodesmatidae, 312, 313, 362, 391 Metapenaeus brevicornis, 170 ensis, 170 masters& 170 Microcystis, 168 Micromesistius poutassou, 247 Mirounga angustirostris, 247 Modiolus agripetus, 326, 371, 384 jlavidus, 327, 371, 384 modiolus, 325, 326, 371, 384 nipponicus, 326, 371, 384 phaseolinus, 326, 328, 329, 371, 384 plumescens, 327, 371, 384 Modulidae, 403 Moerella donacina, 358, 377, 391 kurodia, 358, 377, 391 Monodonta, 268 lineata, 261, 262, 282, 285, 286, 289 Mugil, 135, 151 capito, 150 cephalus, 121, 135, 146, 150, 151, 152, 155, 163, 167, 168, 181, 193, 195 chelo, 150 parsia, 185, 203 saliens, 163, 181 tade, 146, 168, 185 Musculus japonicus. 384 marmoratus, 316, 321, 327, 371, 384 Musculus (Musculista) japonica, 327, 371 perfragilis, 327, 372, 384 Mya, 312, 397 japonica, 364, 378, 393 truircata, 315, 368, 378, 393 M y a (Arenomya) japonica, 368 1 fi

454

TAXOXOMIC INDEX

Myacea, 393 Myidae, 312, 315, 368, 393, 404 Mystus gulio,185 Mytilacea, 383 Mytilidac, 312, 316, 324-329, 383, 404, 405 Mytilus, 269, 282, 309, 325, 326, 403, 412, 421, 422, 426, 427, 428, 429 calijornianus, 324, 371, 383 coruscus, 324, 371, 384 edulis, 251, 282, 283, 285, 288, 308. 324, 326, 328, 371, 384, 399, 403, 405 galloprowincialis, 250, 321, 324, 371, 384, 421, 422, 423, 424, 425

N Naias, 177 Naiatida, 387, 409, 416 Navicula, 343 Nitidotellina nitidula, 359, 391 Nitzschia closterium, 254 Nostoc, 125 Novaculidae, 312, 314, 367, 392 Nucella. 282 lapillus, 282, 285 Xucula, 312, 315. 317, 319, 339, 370, 380, 382, 397, 403, 404. 405. 410 harleyi, 318, 370, 382, 404 moorei, 317. 318, 370, 382, 404 nitida, 318 nucleus, 317, 318, 370, 382, 404, 411 radiata, 318 sulcata, 317, 318, 370, 382, 404, 411 tenuis, 318, 370, 382, 404, 411 turgida, 317, 318, 370, 382, 404 Nuculacea, 382, 404 Nuculana, 317, 410, 411 minuta, 317, 319, 370, 382 Nuculanacea, 382 Nuculanidae, 312, 315, 319, 320, 382, 404 Nuculidae, 312, 315, 317-319, 382, 395, 404 h’uttalia oliwacea. 355, 376

0 Oblimopa, 379, 395 forskalii, 323, 371, 383 Ocenebra erinacea, 285 Oligosyringia, 382, 394, 41 7 Ondatra, 246 Ophryotrochu, 268 puerilis, 252 Opsanus tau, 248 Oscillatoria, 172 Ostrea, 250. 379, 397. 400, 412 denselarnellosa, 332 denselumellosa futarniensis, 331, 372, 385 erlulis, 250, 282, 331, 372, 385, 394, 400, 421 ltirida, 332, 372, 385 Ostraacea, 385 Ostreidae, 312. 316, 331, 332, 333, 385, 404 Oxyrrhis marina, 254

P Pachygrapsus crassipes, 252 Paleotaxodontida. 382, 409. 415 Palliolum, 336 randolphi, 337. 340. 373 Pandalus montagui, 282 Pandoracea, 388 Panu1iru.s interruptus, 252 f’aphia, 347, 364 vernkosa, 351, 375. 390 Patella, 268 nspera, 261, 285 depressa, 261 wulgata, 251, 261, 269, 283, 285, 288 Pecten, 312, 315, 336, 379, 397, 404 albicans, 336, 373, 386, 402 maximus, 337, 373 septemradiatus, 316, 340 Pecten (Ewola) ziczac, 337, 338, 373, 386 Pecten (Notowola) albicans, 336 Pectinacea, 386, 401, 404, 412 Pectinidae, 312, 315, 316, 336-340, 386, 404, 412 I’ehetia canaliculutn, 255, 261, 285

455

TAXONOMIC INDEX

Penaeus brevicornis, 152 indi ct s , 170 japonicus, 136, 156 monodon, 159, 170, 188 Perca, 249 Peridinium trochoideum, 44 Petricolidae, 312, 314, 353, 390 i’halacrocorax, 258 carbo, 246 Phlyctaenachlamys, 3 12 lysiosquillina, 317, 342, 374, 380, 387, 404, 412 Phocaena, 247 Pholadacea, 393 Pholadidae, 312, 313,315, 369, 393, 404 Pholadidea, 312, 404 loscombiana, 315, 369, 378, 393 Phoxinus phoxinus, 248 Physa heterostropha, 251 Pilaster, 252 Pillucina pisidium, 346, 374, 389 Pinctada, 379, 412 marten&, 330, 372, 385, 403, 419, 420, 421 Pi nna, 412 bicolor, 330, 372, 385 Piiinacea, 385 Pinnidae, 312, 316, 330, 331, 385, 404 Pitar, 352 I’itar (Agriopoma) n,oguchii. 351, 375, 390 Placenta, 412 Planorbis, 287 Plectodon, 3 12 ligula, 320, 370, 383 Plicatula, 412 gibbosa, 334, 373, 386 Plicatulidae, 312, 316, 334, 386 Polychaeta, 381 Polysiphonia lanosa, 283 Polysyringia, 383, 395, 411, 417 I’omatoceros triqueter, 285 Poromyacoa, 383 Porphyra umbilicalis, 256, 283, 285 Portlandia (Portlandella) japonica, 319, 370, 382 Portlandiella beringii, 319, 335, 370, 382

Prasinocladus marinus, 2 83 Prionodesmacea, 382, 383, 384, 385, 386, 387, 406, 414 Pristiopoma hccsta, 185 I’romantellum orientale, 340, 373, 387 Protobranchia, 315, 317, 380, 382, 394, 395, 404, 407, 408, 410, 411, 413, 414, 415, 417, 418 Prototheca, 312, 314 jedoensis, 350, 375, 390 staminea, 350, 375, 390 Psammacoma, 3 13 awajiensis, 361, 377, 391 Psammobiidac, 312, 313, 314, 354356, 391, 404 Pseudochama retroversa, 343, 347, 374, 388 Pseudocyrena Jloriclana. 345, 374, 389 Pseudolamellibrarichia, 379, 385, 386, 387, 407, 414 Pseudomonas, 52, 53, 57, 58, 61, 62, 63, 64, 266 Pteriacea, 385 Pteriidae, 312, 316. 330, 385 Ptenomorphia, 415 Pteroconchida, 385, 386, 387, 409, 416 Puccinellia, 256 maritima, 256, 284 P u f l n u s p u f l n u s , 258 Puntius javanicus, 150

R Raeta, 312, 404 plicatella, 365, 377, 392 Raeta (Raetellops) rostralis, 364, 377, 392 Rhizophora, 256 Rhizosolenia, 343 IZhodeus sericeus, 249 Rissoa euxinica, 251 Roccus saxatilis, 28 1 Ruditapes, 352 philippinarum, 350, 375, 390 Ruppia, 125, 165, 177, 180 Rtctilus, 249

456

TAXONOMIC INDEX

S Sabellaria spinulosa, 282 Sacella sematensis, 320, 335, 370. 382 Saccorhiza polyschides, 261 Salicornia, 256 Salmo gairdneri, 249, 281 trutta, 247, 281 Sardina pilchardus, 247 Sargassuno. 26 Saxidomus pawpuratus, 353, 376, 390 Saxostrea, 4 12 echinata, 333. 373, 385 Scatophagus. 121 Scenedesmus, 51, 281 Schizodonta, 415 Schizothaerus, 312, 314, 347, 362, 364, 404 nuttalii, 364, 377. 392 Scintilla, 312, 314, 412 japonica, 342, 343. 374, 380, 387, 404 vitrea. 343 Scylla serrata. 195 Semelangul us, 310 miyatensis, 360. 377, 391 tokubeii, 361, 377, 391 Semelidae, 312, 313. 314, 356-358. 391, 404 Septibranchia. 312, 317, 320, 380. 383, 394, 395, 404, 407, 410, 411, 413. 414, 417. 418 Septifer bilocularis, 328, 372. 384 bilocularis pilosus, 328, 372, 384 Septifer (Mytilisepta) keenae, 329, 372, 384 virgatus, 329, 372, 384 Seriola, 122 quinpueradiata, 136, 154, 158 Serpula, 369 Siliqua patula, 249 Sinonovacula constricta, 364, 367, 378, 392 Skeletonema costatum, 44 Solea solea, 283, 284 Solen, 314 gordonis, 367, 377, 392

gouldi, 367 roseomaculatus, 366, 377, 392 strictus, 367, 377, 392 Solenacea, 392, 413 Solenidae, 312, 314, 366, 367, 392, 404 Soletellina, 312, 314 oliwacea, 391 Somateria mollissima, 259 Spartina, 125, 142, 145, 256 townsendii, 256, 286 Sparus, 182 Sphemiscus demers u.9, 264 Spirorbis borealis, 285 corallinae, 285 rupestris, 285 Spondylidae, 312, 314, 316, 333, 334, 385, 404 Spondylus barbatus, 333, 373, 385 candidus, 334, 335, 373, 385 Sterna sandvicensis, 246 Striarca (Didimacar)symmetrica, 322, 371, 383 Strongylocentrotus. 252, 259 Styela, 380 clava, 381 Suaeda. 125 maritima, 256 Sula, 244 hassana, 246, 258 Systellospis debilis, I04

T Tatlorna ladorna, 259 Tapes (Amygdala) semidecussata, 351 Taxodonta, 382, 383, 408, 415 Tectura, 315 Teleodesmacea, 387, 388, 389, 390, 391, 392, 393, 406. 414 Tellina, 358, 404 Tellinacea, 380, 388, 391, 396, 413 Tellinidae, 310, 312, 313. 358-362, 391, 404, 405 Teuthia, 121 Theora, 312, 314 lubrica. 357. 376 Thraciidae, 312, 314, 344, 388 ,

,

457

TAXONOMIC INDEX

Tl~ysanopodamonocantha, 104 Tilapia, 151, 153, 154, 155, 164, 173; 178, 179, 180, 188, 199 mossambica, 151, 152, 154, 168, 169, 173, 179 Zillii, 154 Tivela stultorum, 249 Trachycardium quadragenarium , 389 Tressus, 312, 314, 397, 404 keenae, 363, 377, 392 Tridacna (Vulgodacna)maxima, 346. 347, 374, 389 Tridacnacea, 389 Tridacnidao, 312. 314, 346, 389 Triglochim maritima, 256 Triyoniocardia, 3 12, 3 13 medium, 349, 375, 389 T u b v e x , 252 Tubularia crocea, 252 Tursiops truncatus, 247

U Ulva, 283, 420 lactuca, 261, 285 Unguilinidae, 312, 313, 346, 389 Unionacea, 387 Unionidae, 312, 316, 341, 342, 387, 404 Uria, 243 aalge, 245, 259, 263

v Valamugil sheli, 150 Varicorbula bvrons, 368, 378, 393 Veneracea, 380, 390, 413 Veneridae, 312, 314, 349-353, 390, 404 Venus ( Ventricoloides) ,foveolata, 352, 375 Veremolpa, 352, 375, 390 micra, 351, 352, 375 m i d a n e n s i s , 352, 375, 390 minuta, 351, 375, 390 lrolse11a americana, 329, 372, 384 citrinus, 328 Vulsellidae, 329, 330, 385

X Xylophaga, 312, 313 dorsalis, 369, 378, 393 Xylophaginidae, 312, 313, 369, 393

Z Zalophus californianus, 247 Zirfea, 404 gabbi, 369, 378, 393 Zostera, 168, 180

This Page Intentionally Left Blank

Subject Index A Abalone, 249, 259, 260, 261 Acorn-barnacle, 254, 261, 269 Adenosine triphosphate anaIy5is. 63, 65, 91, 92, 102 Advection, 99, 100, 101 Aggregation, 26, 41, 47, 48, 50. 51, 53, 75, 76. 78 Algae bathypelagic, 3, 29. 97, 98. 103, 104, 106. 107, 109, 110 benthic, 2, 98, 108, 109. 172. 173. 175 hliir-grcen, 143, 164, 165, 167, 168. 171. 172, 174, 175, 179, 192 bott om-living, 146 brown, 255, 261. 278. 283 compositioii. I64 conversion rate iiito fish. 147, 148 effects of oil pollution 011. 255. 256 epibenthic, 98 filamentous. 144. 166, 167 fucoid, 261, 283 green. 164, 165, 167, 168, 172. 173, 174. 175, 177. 179, 192, 261, 283. 285 gTO\\rbh 0 1 1 ITllldbE€JlkS, 125 heterotrophic uptake. 93, 94 in faecal pellets, 343 organic excretion, 43 pelagic. 1, 2, 101 production, 2 red, 256. 261, 278, 283 sublittoral, 283 Algal pasture, culture, 170-178, 197, 198, 203 Amorphous aggregates composition, 7, 8 pale primordia, 8 particle size, 7, 68, 71, 72 sinking rates, 68, 69, 70, 71. 74, 75 size range, 68, 71, 72 specific gravity, 74 Ainpliipodr, 252.

Anadromous species, 122, 149 Anaerobic degradation of spilt oil, 267, 268 Anguzlla angcdla food, 169 natural history, 153 salinity tolerance, 135 Anguzlln. japonica culture in Talnaitli, 193 food, 169 iiatural history, 153 rate of production in Japan, 198 salinity tolerance, 135 Animals, effwts of oil polhition on, 251-255 Antarctic. 17. 18, 20 Circiimpolnr i t ate,,, 17 Iiitermediate water, 17 Aiabiaii Sea, 17, 20 Atheriiies, 182 Atlantic Oceaii deep water age, 102 dissolved organic carhon coiltent, 102 osygcri d i S t l . l b ~ i t i ~ li ln , 86, 87, 100. 101, 102 particulate organic matter 111, 12, 14. 15, 16, 20, 30, 37, 55, 86, 97 Auks, 243. 244, 259. 263, 264

B Bacteria ATP content, 91 carbon content, 63, 64 consumptioil, 99, 102, 103 determination, 63, 64 effect on particulate carbon production, 50, 51, 52, 53, 54, 56, 57, 58, 59, 61, 62 filtration, 64, 65 hetcrotrophic uptalrc, 93, 94 i n deep ocean, 91, 99, 103, 108, 109, I10 i t i rniitl-flats. 147

460

SCBJECT INDEX

Bacteria-continued L phases, 65 nutritive value, 143 oil-degrading, 266-270, 272, 284 plate counts, 61, 62. 63, 64, 65, 91 pleomorphic, 65 poisoning, 55 production, i n situ, 61, 62, 63, 64, 65 saprophyt,ic, 144 senescent stages, 65 size range, 64 sterilization, 48 utilization, i n s i t u , 49 Bacterial degradation of spilt oil, 266270 Bacterial oil decomposers, 266, 267, 268 Pseudoinonas, 266 Bantry Bay, 228 Barnacle, 253, 254. 263. 282, 284, 285 Barracouta. 120 Bass, 182 striped, 281 Batelle-Northwcst Report,, 219, 227. 233. 234, 254. 262 Bathypelagic zone carbon consumption in, 99, 103, 111 Beavers, 246 Benthos, 134, 136, 140, 180 Benz(a)pyrene, 262, 263 Bermuda Biological Station, 11 Bheris of West Bengal, 127, 132, 133, 141, 158, 169, 171, 189, 202 management, 184, 185 stocking, 184, 185, 203 Biodeposit,ion daily aspect,s, 421-422, 423, 424 effect of salinity, 419-420 effect of size of producer, 420 effect of suspended solids, 420 effect of temperature, 419 effect on environmental conditions, 425 in York River, 427, 428 of suspension feeding bivalves, 413429 seasonal aspects, 422-425, 426 Biodeposits, 413, 419 annual production, 426, 427, 428 chemical composition. 427, 429 effect on marine environment, 428

Birds, effects of oil pollution on, 243246, 258 Bird cggs, effect,s of oil polliitiori 0 1 1 , 246 Bittjerling, 249 Bivalviti anus, 381, 399, 401 burrowing forms. 379, 380 commensal forms, 380 Cox classification, 382-393, 408, 409, 410, 415 Dall classification, 382-393, 406, 408, 414 digestive diverticula, 381 epifaunal, 379 feedirig experiments, 403 feeding habit, 379-381 free-swimming forms, 379 fimction of digcstivc? organs, 381. 394-402 gut,, 394, 400 intjermediatjeforms, 379 mid-gut, 381, 394, 395-399, 400. 401, 402 modc of life, 379-381 paedomorphosis, 413 Pelsenem classification, 382--393, 407, 408, 414 Purchon classification, 394, 395, 410. 413, 417, 418 rectum, 381, 399-402, 403, 411 scatological studies of, 307-429 sessile forms, 379, 397 stomach, 381, 394-395, 400, 401, 402, 413 structure of digestive organs, 381, 394-402 style-sac, 381, 394 Thiele classificat,ion, 382-393, 408, 415 Bivalvia, classification schemes and distribution of faecal pellettypes, 382-393, 414-418 Bivalvia, faecal pellets biological significance of characteristic form, 379-402 classification, 310, 312, 382-393, 414-41 8 definition of types 310-317 description, 317-378

46 1

SlJBJECT INDEX

Bivalvia, faecal pellets-continued evolutionary trends, 405-413 examination, 309-310 frequency distribution, 406,407,408, 409, 410, 414-418 Gastropempta, 345-369 Gastrotetartika, 334-345 Gastrotriteia, 320 history, 307-309 list of known producers, 370-378 morphology, 310-378 Protobranchia, 317-320 relation of faecal characteristics t’o feeding habit, 379-381 rela,tion of faecal characteristics to function of digestive organs, 381-403 relation of faecal characteristics to mode of life, 379-381 relation of faecal characteristics to structure of digestive organs, 381-403 Septibranchia, 320 similarities among various taxonomic divisions, 404 use as a systematic Index, 403-405 Bivalvia, suspension feeding biodeposition, 41 3-429 feeding activities, 421 rate of defecation, 419, 421-425 rate of water transport, 421, 422 Black Sea, 121, 123, 124, 126, 140, 180 Bloodworms, 163, 164, 178 Brackish-water fishponds, 123, 126, 127, 128, 129, 130, 131, 134, 135, 141, 148, 150, 151, 152, 155, 170 a t Arcachon, 182, 202 management, 178-198 profitability, 199-205 Branchiopods, 380 Brantas River, 125 British molluscan faeces, 308 Bubbling experiments, 3, 38, 40,41, 42, 43, 44, 45, 46, 47, 48, 49, 52, 53, 54, 55, 56, 58, 59, 71, 76 bacterial effects, 55, 56, 58. 59 on Nova Scot,ia coastal wat,er, 45. 46, 47 on Sargasso Sea water, 46 total carbon yields, 45, 46

C Calcium carbonate geochemistry, 39 in deep water sediments, 39 Caribbean particulate organic matter in, 16 Carp, 153, 169, 178, 179, 190, 193, 194, 248 Chinese, 150, 155 common, 194, 207 Grass (White Amur), 149 Indian major, 150, 155 silver (White Tolstolobik), 149, 194 Caspian Sea, 215 Cerithiid snails, 172, 1 7 3 Chanos availability of fry in Taiwan, 155 breeding pattern, 151, 152 capture of fry, 157, 192 culture in Java, 189-192 culture in Philippines, 192-1 93 culture in Taiwan, 194-198 features, 165 fishpond stocking rate, 160 food, 164, 165, 166, 171, 172, 173, 174, 177 fry, 151, 155, 159-163, 196 growth, 166, 167, 196 natural history, 151 overwintering, 162, 196 principal food, 144, 146, 166 rearing, 120, 130, 143, 159-163, 192 rearing of fry, 159-163, 192 requirements, 155 salinity tolerance, 135, 150, 160 sources, 155 spawning, 151 temperature tolerance, 154 Chesapeake Bay, 140 Chironomid larvae, 172, 173, 197 Chiton, 250, 268, 270 Chlorophyceae, 144 Cladoceran, 253 Clam, 281 Cleansing shores of‘ oil, 274-280 burning, 275, 276 by “German Machine”, 280 by solvent emulsifiers, 276, 277, 278, 280

Cleansing shores of oil- corrtirr ued mechanical collection, 275, 276, 280 “Plan Offset”, 274 Senneri Cove, Cornwall, 276, 278 Coastal oil refineries, 230 efflrients, 230, 231 Fawley, 231 Milford Haven, 231 C‘occolithophores. 91 Cockles, 146, 251, 281. 282 Commoii scoter, 258 Copepods, 27, 102, 106, 107, 168, 2 5 2 . 320 Cordgrass, 256, 284 Cormorants, 246, 258 Coulter Counter measuremciits, 6, 37, 50, 51, 66 Crahs, 195, 252 hermit. 282 sublittoral. 282 Crassostrea daily rate of hiodeposition, 421. 423-424 daily rates of \cater transport, 422 seasonal rate of biodepositioil, 425. 426 Crawfish, 138 Crayfish. 252 Crenimuyil lnbrostrs breeding pattern, 153 food, 168 natural history. 153 principal food, 146 salinity tolerance, 150, 151 Crepol. 255 Crude oil bacterial degradation, 266, 268 behaviour when spilt on coast, 238. 239, 240 behaviour when spilt on sea, 236, 237, 238 composition, 234. 235 decomposition by Pseuclomonas, 266, 267 density, 234 effect on beaches, 238, 239 emulsification, 237, 238 evaporation. 234, 236 identification. 243 pour point, 234

Crude oil-cowtmtied viscosity. 234, 235 water solubility, 235, 236 Cultivated fish, food, 164-178 algae, 166. 170. 171 algae, blue-green, 164, 165, 166, 167, 168. 171, 172. 174, 175 algae, filamentous, 166, 167, 168, 169 algac. green. 164. 165, 169, 172, 173, 174, 175, 177 blood\vorm. 164. 178 cliiroiiomid larvae, 168 cladoceraiis, 168 copepods, 168 Chaetornorphw, 166 Daphniu, 164, 178 dctritu5. 168, 169 diatoms, 164, 166, 188, 175 ‘digman’. 177 Crwcrlnria, 177 ‘gulaman dagat,’ 177 ‘lab-lab’, 167. 171. 173, 174 ‘lumut’, 165, 173, 174, 177 mysids, 168 phytoflagcllates. 166 planktoil, 164. 168 Rtcppim, 165 supplementary, 164. 176. 177. 178 ‘tai-ayer’. 167, 171 zooherithos, 168 zooplankton, 164, 168 Zontern. 168 Cultivated prauns, food, 164-178 algae, 170 crustaceans. 170 detritus, 170 polychaetes, 170 supplementary, 178 Current movements, 22, 23, 24 in Atlantic Ocean, 23 in Gulf Stream, 22, 23, 24 in Sargasso Sea, 23

D Deep occaii, 42, 86. 88, 89, 99, 108, 110 age. 99, 102 ATP content. 92 bacteria content, 91. 109 biological changes in, 100, 103

463

SUBJECT INDEX

Deep oceari---co.ntin;ued B.O.D., 103 carbon consumption in. 99 carbon content, 29 dissolved organic matter in, 103 nitrogen consumption, 103 nitrogen content, 29, 103 oxygen consumption in, 87, 90, 99, 100, 103 oxygeii distribution in, 87, 100 particulate matter in, 42, 86. 88, 89, 90, 99, 108, 110 Deer, 246 Detergents, 280 anionic, 280, 281 non-ionic, 280, 281, 284 t80xicitjy,280, 281 Detritus, 3, 6, 7, 11, 26, 36, 106, 108, 167, 180, 247, 314, 315 allochthonous sources, 144, 145 autochthonous sources, 144 breakdown, 142, 144, 145 feeders, 110 fertilization of fishfarms, 126, 141. 142 from death of phytoplankton, 144 from filamentous algae, 144 from marine scston, 145 from mud-flat diatoms, 144 from submerged vegetat,ion, 144, 145 in estuaries, 141. 142, 143, 144, 145. 146 in faecal pellets, 314, 315, 325, 326. 327, 336, 340, 343, 344. 348, 351. 354, 357, 358, 362, 363 oxygen consumption, 142 particulate organic, 146 production. 141, 142, 144, 145 Spartirm. 142 Diat>oms, 11. 19, 38, 43, 44, 95, 164. 165, 166. 167. 168, 175. 179 benthic, in estuaries, 140 effects of oil pollution on, 254 growth on mudbanks, 125 in deep ocean, 91 in faecal pellets, 319, 332, 333. 343. 348, 358 planktonic, in estaaries, 140 sinking rates, 67 Digmafc. 177. 193

Dinoflagellates, 11. 43, 44, 95. 166, 168 in faecal pellets, 333 Divers, 244, 258 Dog-whellr. 282 Dolphin, 247 Dorade, 142 Ducks, 243, 244, 246. 258 eider, 258, 259 long-tailed, 244. 258. 259

E Earthworms, 413 Echinoderms. 251 Eels, 134, 135, 142, 149, 151, 153, 157, 162, 164, 169, 170, 178. 182, 184, 193, 194, 198. 204, 2132 Equatorial Currents North, 87 oxygen distrib1it)ioriin, 87 South, 87 Estuaries accretion of soil, 125 algal pastiires, 144, 147 Brantas River, Java. 125 Chesapeake Bay, 140 definition. 122, 123 detrit,us enrichment, 142 ecosystem, 141, 142, 144 enclosed nature, 124 fatility, allochthonous sources of detritus. 145 fertility, aut*ochthonous sources of detritus, 144 fertility, benthic production, 140, 141 fert>ility,colloidal organic material. 146 fcrtility, detritus breakdown, 144 fertility, detrit,ns enrichment, 142, 143 fertility, detritus production, 141 fertility, dissolved organic material. 146 fertility, microflora, 147 fertilit,y, natural, 140 fertility, nutrient trap. 145 fertility, particulate organic detritus, 146 fert.ility, plankton production, 140, 141

464

SUBJECT INDEX

Estuaries-continued fertility, source of nutrients, 148 future development, 205-208 physical environment, 135 Sea of Azov, 140 sediments, 413 South American, 125 St. Lucia, South Africa. 122 suitability for fish farms. 124 tidal, 126 topography, 124 et seq. upkeep, 124 West African, 125 Estuarine soils organic matter content, 147 Euglenoids, 147 Enphausiids, 104 Europoort, 228, 230 Expedition data ‘Atlantis’, 87 ‘Dana’, 87 ‘Discovery’, 87 ‘Hudson’, 56 ‘Meteor’, 86, 87 ‘Tridentr’, 12

F Faecal pellets, 9, 107, 108. 143, 146 Adepedonta, 415 Adesmacea, 393 Amusiidae, 334-336, 386, 412 Anisomyaria, 383, 384, 385, 386, 387. 408, 411, 415 Anomalodesmacea, 383, 388, 406, 414 Anomalodesmata, 415 Anomiacea, 387, 412 Anomiidae, 341, 387 Arcacea, 383 Arcidae, 321, 383, 404 Asthenodontida, 393, 409, 416 Aviculidae, 330 biological significance of characteristic form, 379-402 Californian invertebrates, 308 Calloconchida, 409, 416 Cardiacea, 389, 413 Cardiidae, 346-349, 389, 396, 404 Carditacea, 379, 387, 412

Faecal pellets-continued Carditidae, 342, 387 Chamacea, 388 Chamidae, 343, 344, 388, 404 classification, 310, 312, 382-393, 414-418 collection, 309 Colloconchida, 385, 387 colour, 405 Corbiculacea, 389 Corbiculidae, 345, 346, 389. 404 Corbulidae, 368, 393, 404 Cuspidariidae, 320, 383, 404 definition of types, 310-317 description of, 317-378 disjointed particles, 312, 317, 342 Donaciidae, 345, 388 Eryciriacea, 380, 412 Erycinidae, 343, 387 Eudesmodontida. 388, 393, 409, 416 Eulamellibranchia, 380, 387, 388, 389, 390, 391, 392, 393, 407, 408, 415 Eulamellibranchia (Adepedonta), 392, 393 Eulamellibranchia (Anomalodesmata), 383, 388 Eulamellibranchia (Heterodonta), 387, 388, 389, 390, 391, 392, 411, 414 Eulamellibranchia (Schizodonta), 387 Eutaxodontida, 383, 409, 416 evolutionary trends, 405-41 3 examination, 309, 310 external sculpture, 404-405 factors influencing productJion, 41942 1 Filibranchia, 383, 384, 407, 414 form, 311, 313, 403, 405 frequency distribution, 406, 407, 408. 409, 410, 414-418 Galeommatidae, 342, 387 Galeommidae, 342, 343, 387, 404 Gastrodeut,eia, 320, 383 Gastropempta, 345-369, 395, 404, 410, 413, 417, 418 Gastroproteia, 317-320, 383 Gastrotetartika, 334-345, 386, 395, 410, 412, 413, 417, 418

SUBJECT INDEX

Faecal pellets-continued Gastrotriteia, 320-334, 383, 395, 404, 410, 411, 413, 417, 418 Glycymeridae, 323, 383, 404 Heteroconchia, 416 Heterodonta, 415 Heterodontida, 383, 387, 388, 389, 390, 391, 392, 409, 416 Hiatellacea, 392 Hiatellidae, 367, 368, 392 history, 307, 308, 309 Holothurians, 381 identification, 333 Isofilihranchida, 383, 384, 409, 416 Isognomonidae, 329, 330, 385, 404 Laternulacea, 388 Laterniilidae, 344, 388, 404 Lepidontida, 409, 415 Leptonacea, 387 Limacea, 387 Limidae, 340, 341, 387, 404 Limopsacea, 383 Limopsidae, 323, 324, 379, 383, 395, 404, 411 Lipodontida, 382 list of average sizes from known producers, 370-3 7 8 list of known producers, 370-378 list of localities of known producers, 370-378 Lucinacea, 389, 413 Lucinidae, 346, 389 Lyonsiidae, 344, 345, 388. Mactracea, 391, 413 Mactridae, 362-366, 392, 404, 405 Mesodesmatidae, 362, 391 morphology, 310-379 mussel, 324 Myacea, 393 Myidae, 368, 393, 404 Mytilacea, 383 Mytilidae, 324-329, 383, 404, 405 Naiatida, 387, 409, 416 Novaculidae, 367, 392 Nuculacae, 382, 404 Nuculanacea, 382 Nuculanidae, 319, 320, 382, 404 Nuculidae, 317, 318, 319, 382, 395, 404

465

Faecal pellets-continued of indeterminate shape, 312, 317, 380, 395, 404, 411 Oligosyringia, 382, 417 Ostreacea, 385 Ostreidae, 331, 332, 333, 385, 404 oyster, 324, 332, 333, 419, 420, 421, 422 Paleotaxodontida, 382, 409, 415 Pandoracea, 388 pearl oysters, 403, 420, 421 Pectinacea, 386, 404, 412 Pectinidae, 336-340, 386, 404, 412 Petricolidae, 353, 390 Pholadacea, 393 Pholadidae, 369, 393, 404 phylogenetic significance, 405 Pinnacea, 385 Pinnidae, 330, 331, 385, 404 Plicatulidae, 334, 386 Polychaeta, 381 Polysyringia, 383, 411, 417 Poromyacea, 383 Priondesmacea, 382, 383, 384, 385, 386, 387, 406, 414 Protobranchia, 317-320, 380, 383, 394, 395, 404,407, 408, 410, 414, 415, 417, 418 Psammobiidae, 354-356, 391, 404 Pseudolamellibranchia, 385,386,387, 407, 414 Pteriacea, 385 Pteriidae, 330, 385 Pteriomorphia, 415 Pteroconchida, 385, 386, 387, 409, 416 rate of discharge, 413-429 relation af characteristics to feeding habit of animal, 379-381 relation of characteristics to function of digestive organs, 381-403 relation of characteristics to mode of life of animal, 379-381 relation of characteristics to structure of digestive organs, 381-403 Schizodonta, 415 Semelidae, 356-358, 391, 404 Septibranchia, 320, 380, 383, 395, 404, 407, 410, 411, 414, 417, 418 size, 405

466

SUBJECT INDEX

Faecal pellets-continued sizes of known producers, 370-378 Solenacea, 392, 413 Solenidae, 366-367, 392, 404 Spondylidae, 333, 334, 385, 404 structure, 311, 313, 405 Taxodonta, 382, 383, 408, 415 technical terminology, 31 1 Teleodesmacea, 387, 388, 389, 390, 391, 392, 393, 406, 414 Tellinacea, 380, 388, 391, 396, 413 Tellinidae, 358-362. 391, 404, 405 texturc, 405 Thraciidae, 344, 388 Trrdacnacea, 389 Tridacnidae, 346, 389 tunicates, 380 Ungulinidae, 346, 389 Unionacea, 387 Unionidae, 341, 342, 387, 404 use as a Bivalvia systematic index, 403-405 Veneracea. 380, 390, 413 Veneridae, 349-353, 390, 404 Vulselhdae, 329, 330 Xylophagidae, 369 Xylophagiiiidae, 393 Faecal pellets, oval, 310, 311, 396, 406 constricted rod, 312, 314, 346, 347, 348, 349, 350, 358,362, 363, 364, 366, 367, 397, 404, 406, 413 discoid, 312, 313. 343, 356, 358, 360, 361, 369, 380, 404, 413 ellipsoid, 312,314,349,354. 356, 358, 362, 363, 364, 366, 367, 380, 397, 404, 406, 413 ovoid, 310, 342, 343, 345, 346, 347, 348, 349, 354, 356, 357, 358, 359, 360, 361, 362, 363, 367, 369, 380, 404, 408, 412, 413 Faecal pellets, ribbon, 311, 312, 316, 408, 411 grooved, 312,316, 321, 322, 324, 325, 326, 327, 328, 329, 330, 331, 332, 333, 334, 336, 340, 341, 379, 395, 397, 404, 411, 412 ungrooved, 312, 316, 320, 321, 322, 323, 327, 328, 330, 331, 333, 341, 342, 379, 395. 397. 404, 411. 412, 413

Faecal pellets, rod, 311, 312, 314 plain rod, 312, 314, 323. 324, 334, 343, 344, 345, 346, 349, 350, 351, 352, 353, 362, 366. 367, 368. 369, 379, 380, 404, 406, 408, 413 rodlet wound into a ball, 312, 315. 334, 336, 337, 379, 397. 412 rodlet wound into a rod, 312, 315, 340, 341 with a coiled groove, 312, 315, 345. 368, 369, 397, 404 with a longitudinal groove, 312, 315, 319, 320, 345, 353, 394,404, 410, 41 1 with a trefoil-shaped section, 312. 316, 338, 339, 379, 397, 412 with a triangular section, 312, 338, 339, 379, 397, 412 with five longitudinal grooves, 312, 315, 317, 318, 380, 394, 410,411 with nine longitudinal grooves, 312, 315, 317, 380, 394, 410, 411 with seven longitudinal grooves, 312, 315, 317, 318, 380, 394, 410, 411 Faulkner Report, 223, 238, 251 Fertilizers, use in fishponds, 175, 176, 203, 204 Filter-feeding organisms, 3, 25, 26, 29, 36, 82, 83, 103, 106, 107, 110, 146, 308, 338, 413-429 hiodeposition, 4 13-429 distribution, 25 effects of oil pollution on, 250 structure, 31 1 Filters glass fibre, 5, 29, 42, 43, 59 Millipore, 5, 42, 44, 47, 54 silver, 5, 18, 19, 35, 46, 47, 54, 56 Fish-corrals, 119 barrachois, 120 in Britain, 120 in Mauritius, 120 Fish culture brackish-water, 119, 121, 130, 151 flitwe prospects, 206 in Java, 189-192 in paddy fields, 188 in Philippines, 192, 193 in power station cooling ponds, 136, 206, 207

SUBJECT INDEX

Fish culture continued in Taiwan, 194-198 intensive,in cages, 135, 136,137, 138, 139, 140 intensive, in open nets, 135, 136, 137 species cultivated, 151- 155 Fish, effects of oil pollution on, 247-249 Fish farms brackish-water. 123, 126, 151, 155, 170, 183, 184 estuarine, 119 et seq. fertilization, 126 fresh-water, 153, 193 future prospects. 205---208 Hitsuishi, Japan, 135 in Adriatic, 126 in Black Sea, 121, 123, 124, 140, 180 in Japan, 122, 135, 169 in Mediterranean, 121 in Niger delta, 208 in north Adriatic, 121, 122, 129 hmans, 121, 123, 124, 134, 140, 163. 167, 168, 170. 178. 180, 181 mariagementj, 178-198 profitability, 199-205 salmon. 138 salt-water, 138 sea water supply, 126, 127, 128, 129 selection of organisms by salinity. 149 species culturcd, 149--155 total area, 123 trout, 138, 139 valli, 121, 122, 129, 135, 140, 142, 155, 162, 169, 183, 184, 201 Fish farms, species cultured Chanos, 151 eels (Anguilla), I51 grey mullet (Mugil, Liza, Crenimu&). 151, 152 milkfish (Chanos chanos), 151, 152 penaeid prawn (Penaezis breaicornis), 151, 152 salmon, 151 sea trout, 151 Tilapia. 151 Tilapiw mossclmhiw, 15 1 Fish fry availability, 155, 156, 184, 203 captlire, 155, 157, 158

467

Fish fry --contzn uerl C h ~ n o s 159-162 , eels, 162, 163 grey mullet, 162, 163, 180 industry, 157-159 rearing, 159-164 Fish fry industry, 157-159 E’ish lice, 198 Fishponds barrachois, 181 bheris, 127, 132, 133, 141. 158, 169, 171, 184. 185, 189, 193, 202 bottom fauna content, 148 brackish-water. 127, 128, 129, 130, 131, 134, 135, 141, 148, 150, 152, 155, 178-198, 199-205 construction, 130, 131, 132, 133, 134 embankments. 130, 131. 132, 133, 134 fertilization, 126, 129, 175, 176 filling, 126, 127 financial assistance for, 204, 205 floor level, 127, 128 ‘Heemrad’ near Djakarta, 179, 180 ideal layout, 131, 132, 133 in Borneo, 132 111 France, 134 in Ganges Delta, 132 i n Hawaii, 120, 130, 134, 141, 142, 165, 170, 181, 182, 199, 201, 203 i n Hong Kong, 134, I50 inItaly, 121, 135, 148, 149, 170, 182. 183, 184 111 Java, 121, 124, 128, 129, 131, 132, 135. 148, 169.178, 189-192, 200. 202, 204, 205 1 x 1 Pearl River, China, 134 in Philippines, 120, 128, 131, 192193, 196, 197, 200, 202, 204 in Taiwan, 121, 128, 129, 130, 132, 149,164,169, 193,194-198,200, 202 in West Rengal, 127, 141, 179, 184186 irrigatioii, 126, 127. 128 irrigation by pumping, 128, 129 management, 17 8- 198 nursery, 133 Porong type, 132 productivity, 170

468

StrBJECT INDEX

%ishponds-colztzlzued~ profitability, 199-205 pupukan, 120 rate of fish production, 198, 199 rearing, 133 salinity, 135 selection of organisms by salinit,y, 149 species cultured, 149-155 s b r m dykes, 130, 131, 133, 134 supplement)a.ryfood. 176, 177, 178 supply canals, 127, 128, 129, 131 tidal, 120 water renewal, 127 wintering, 132, 133 yield, 128, 132 Fishponds, Hawaiian, 120, 130, 134, 141, 142, 165, 170 Chano8 rearing, 181 decline, 201 management, 181, 182 mullet rearing, 181 rate of fish production, 199 Flagellates, 198, 325, 405 Flatfish plaice, 206 soles, 206 Flemish Cap waters particulate organic matter in, 56 Flounders, 149 Fuel-oil, 221, 224, 232, 234, 235, 242, 243, 247, 253, 262, 267 Fulmar, 258

G Gannets, 244, 246, 258 General-cargo shipping, 21 9-224 Glasswort, 256 Goldfish, 281 Goose-barnacle, 253 Grand Banks waters particulate organic matter in, 56, 57 Grey mullet, 134, 159, 179, 184 breeding, 155 capture of fry. 157, 158, 163 ‘chulari’, 180, 201 cultivation, 149, 150, 151, 152, 153. 154 culture in Japan, 193 culture in naddy fields, 188

Grey mullet- continued culture in Taiwan, 194 farming in Luzon, 193 features, 165 food, 142, 143, 144, 145, 146, 164, 165, 167, 171, 177, 178 rearing of fry, 162, 163 requirements, 155 salinity tolerance, 135 spawning in captivity, 156 temperature tolerance, 154 Guillemots, 243, 245, 258, 259, 263, 264 Guinea Current oxygen distribution in, 87 particulate organic matter in, 16 Gulaman dagat, 177, 193 Gulf of Aden particulate organic matter in, 17 Gulf Stream, 23, 24 particulate organic matter in. 22, 95 Gulls. 244, 246, 258 greater black-baclied, 263 herring, 263

H Heterotrophic processes, 91, 93, 94, 96, 97. 102, 103, 108, 111 Heterotrophs, 2, 90, 92, 93, 96, 98, 101, 103 Hexahydrobenzoic acid, 249 Hibernacula, 121 Hydrocarbons bacterial degradation, 266, 267 Biochemical oxygen demand (BOD), 266 carcinogenesis, 262, 263 Hydrocarbons, toxicity t o algae, 256 t o Amoeba, 254, 255 to fish, 249, 252 to marine plants, 256 to molluscs, 251 to terrestrial plants, 257

I Indian Ocean particulate organic matter in, 17

SVBJECT I N D E X

Intergovernmental Maritime Consultative Organization (IMCO), 218, 223 Ion flotation, 38 Irminger Sea particulate organic matter in, 12, 14, 20 Isles of Scilly, 216 Isotope fract,ionation, 103

J Jelly-fish, 252

K Kelp, 255, 259, 261 giant, 259, 260 Kiel Bight particulate organic matter in, 10 ‘Kuruma’ prawn cultivattion, 156 rearing, 156

L ‘Lab-lab’, 167, 188, 192 production, 171, 173, 174 Labrador Current particulate organic matter in, 57 Land reclamation, 125 Lagoons Adriatic, 123, 126, 149 benthos content, 140 Black Sea, 124 Mediterranean, 123 Langmuir circulation, 26, 79, 80 Laverweed, 256, 283 Lias of Gloucestershire, 410 Limpet, 251, 261, 268, 269, 277, 288 Liza aurata capture, 121, 163 cultivation, 180, 181 food, 167, 168 salinity tolerance, 150 Lobsters, 138, 252 Long Island Sound particulate organic matter in, 3, 10, 11, 37, 38, 44 ‘Lumut’, 165, 173, 174, 177, 192

M Mackerel, 169 Macrozooplankton, 112 Mallard, 246 Mammals, effects of oil pollution on, 246-247 Management of brackish-water fishponds, 178-198 Manganese geochemistry, 39 in deep water sediments, 39 Manx shearwater, 258 Marine communities, effects of oil pollution on, 258 Marine oil terminals Rantry Bay, 228 Europoort, 228, 230 Milford Haven, 225, 227, 228 off-shore, 228 Thames Haven, 230 Tranmere, 230 Marine plants, effects of oil pollution on, 255-258 Marine sediments, 103, 108, 109, 110 Marine snow, 3, 107 Mediterranean, 121, 123 Microflagellates, 73 Milford Haven, 225, 227, 228 Milkfish, 151, 152, 154 Minnow, 248, 249 Molluscs British marine, 403 effects of oil pollution on, 249-251, 290 scatological studies of, 307-429 Mosquito fish, 248, 249 Mud banks colonization with mangroves, 125 formation, 125 vegetation growth on, 125 Mugil cephalue breeding pattern, 152, 153, 155 culture in Japan, 193 culture in Taiwan, 195 fry, 153 food, 168 in fresh-water fish farms, 153 in fresh-water lakes, 153 natural history, 152

470

SUBJECT INDEX

Mugil cephalus-continued salinity tolerance, 135, 150. 151 spawning, 152 Mugil tarde food, 146, 168 Mullet, 120, 121, 181, 182 Muskrats, 246, 247 Mussel, 250. 251. 259, 261, 269, 282, 288, 324 Mytiluv annual rate of biodeposition, 428 daily rate of biodeposition, 421, 423424 daily rate of water transport, 422 seasonal rate of biodeposition, 425, 426

N Nanoplankton, 13, 77 Naphthenic acids, 249, 251. 253, 255, 256 Natural history An,guilla anguilla. 153 Anguilla japonica, 153 Chunos. 151 Creninaugil labrosua, 153 M u g i l cephalus, 152 penaeid prawn, 154 Tilupia, 154 Tilupia Etroplw, 154 Tilupia mossambica, 154 Tilapia Zillii, 154 Niger delta, 208 ‘Nori’, 203 North Atlant,ic oxygen distribution in, 87 North At,lantic Deep Water, 17 North Italian lagoons management, 182, 183, 184 ‘sergei’, 182 Nova Scotia coastal water, 45, 46, 47 Nncleic acids, 31, 32

0 Oceanic aggregates, 7, 8 , 9, 26, 31. 35. 36, 38, 39 Oil emulsifiers, 276, 277, 278 BP 1002, 271, 282, 284, 288 Corexit, 271, 288

Oil emulsifiers-continued Dispersol OS, 271, 288 Essolvene, 271 Fina-Unisol, 271 Gamlen, 271 mode of action, 280-288 Polyclens, 283 Polycomplex-A, 271 toxicity 280-288 Tricon, 281 Oil in Navigable Waters Act of 1922, 216 of 1955, 218 Oil pollution. 215 et seq. at Santa Barbara, California, 233, 239, 247, 254. 255, 274 at sea, 219-224 carcinogenesis, 262-263 control, 215-234 from bunkering, 224 from coastal refineries, 230-234 from general-cargoshipping, 219-224 from off-shore oilfields, 233, 234 from pipelines. 231, 232 from tanker operation, 219-224 in Caspian Sea, 215 i n harbours, 224-230 in marine terminals, 224-230 in Volga, 216 off Cornwall coast, 218 off European coasts, 216 off Isles of Scilly, 216 rehabilitation of oiled birds, 263-264 soiirces, 219-234, 242 Oil Polliition Act of 1924, 216 Oil pollution. effects, 243-265 on animals, 251-255 on birds, 243-246 on fish, 247-249 on larger plants, 255-258 on mammals, 246-247 on marine communities, 258-262 on molluscs, 249-251 on plankton, 251-255 on public amenity, 264-265 on shore, 238, 239, 240 on tourist industry. 264-265 Oil shipments t,o western Europe, 217 Oil slicks prediction of‘ movement, 289

47 1

SUBJECT I N D E X

Oil sinking by Carbosand, 27 1 by “craie de Champagne”, 273 by sand, 271 by stearabd whiting, 272 by “Stucco”, 272 Oil spillage behavionr on sea, 236-240 behaviour on shore, 236-240 Oil spillage, collection by expanded mica, 273 by india-rubber dust, 273 by paraffin wax, 274 by polyvinyl plastic, 274 by shredded polyurethane foam, 273 by siliconized sawdust, 273 by straw, 272, 273 by vermiculite, 273 by volcanic glass, 273 Oil spillage, control by “Norfolk Skimmer”, 227 by pneumatic booms, 226 by “Port Service”, 227 by “Sea Sweeper”, 227 by “Seaspray”, 227 by sinking, 237 by spillbooms, 225 by “Waterwisser”, 227 Oil spillage, removal by bacterial degradation, 266-270, 272 by biological processas, 266-270 by dispersal, 271-274 by recovery a t sea, 271-274 by sinking, 271-274 from shores, 274-280 Oiled birds rehabilitation, 263-264 Oligochaete, 252 Organic carbon aggregation, 26, 41, 47, 48, 51, 56. 58, 107 analysis, 37, 38 bacterial utilization, 51, 54, 103 cellular, 91 consumption, 94, 95, 96, 97, 102, 108, 109 determination, 6 dissolved, 2, 6. 34, 46, 51, 53. 54, 66, 86, 102, 104

Organic carbon--continued eddy flux. 85 filter-passing, 2, 50 filt,erable, 2 formation, 47 harvesting, 59, 60 in transition zone, 84, 8 5 , 86 particulate, 2, 12 et seq., 47, 50, 51, 52, 53, 104 production, i n situ, 49. 51. 52. 53. 54, 56, 57, 58, 59, 60 regional variations, 19 et seq. sinking rate, 85, 107 utilization, i n s i t 2 4 49. 52 vertical flux, 85 vertical gradient, 85 yields on bubbling. 45, 46. 47, 48. 52 Organic phosphorus distribution, 86 Oxygen minimum layer, 97, 99, 100, 102, 111 Oyster. 250, 251, 256, 281, 282, 308, 324, 332, 333, 419, 420, 422, 425. 426, 427, 428, 429 annual faecal matter deposition, 426. 427, 428 defecation cycle, 421, 422. 423, 424, 425, 426, 427, 428 feeding activit,y, 421 pearl, 403, 420, 421, 428

P Pacific Ocean particulate organic matter in. 1 ti, 17. 20, 37, 86 Paddy fields fish and prawn culture in, 188, 189 Particulate matter, living determination, 63, 91 Particulate matter, non-living adsorption on bubbles, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 59 aggregation process, 41, 50, 51, 53, 78 amorphous aggregates, 7, 8, 9, 31, 35, 36, 38, 53, 67 biological effects on distribution, 88 biological effects on concentration, 88

472

SUBJECT INDEX

Particulate matter, non-livingcontinued convective circulation, 79, 80, 82, 83 deposition on sea bottom, 108 depth distribution, 43, 83, 98 determination, 63, 91 dynamics of consumption, 79, 111 dynamics of production, 79 filter preparations, 8 formation, 9, 40 et seq., 77, 79, 83 general appearance, 7 in deep waters, 42, 86, 88, 89, 99, 108, 110 in Irminger Sea, 12 in North Atlantic, 12, 30, 97 in Kiel Bight, 10 in Long Island Sound, 10, 11, 44 in Sargasso Sea, 10, 11, 12, 42, 46, 84, 89, 94, 95, 97, 111, 112 in surface waters, 42, 79, 80, 81, 84, 88, 95, 105, 111 in transition zone, 83, 84 micro-distribution, 25, 27, 84 microscopic examination, 12 organic aggrcgates, 7 organic carbon, 12 et seq., 42 organic components, 9, 41, 42 organic staining reactions, 7, 8, 9, 12 origin, 9, 10 particle counts in offshore waters, 10, 11,12 production by bubbling, 41, 43, 44, 45, 46, 79 production/consumption balance, 88, 89, 111 production, in situ, 49, 51, 52, 53, 54, 55, 56 phosphate distribution, 40, 41 regional variation, 11, 12 residence time, 66, 86, 108 seasonal cycles in inshore waters, 10,

12 semi-transparent flakes, 7, 8, 9, 12, 31, 35, 36, 37, 38, 67, 69, 71, 72, 77, 78, 79 sinking rates, 66, 67, 68, 69, 70, 72, 73, 74, 75, 80, 81, 82, 83, 107, 108, 110 size range, 66, 67, 70, 72, 75 specific gravity, 73, 74

10, 70, 71, 84,

Particulate matter, non-livingcontinued utilization by bacteria, 43 utilization, in situ, 49, 52, 53 utilization on sea bottom, 108, 109, 110 variation in consumption with depth, 94, 95, 96, 97, 98, 99, 100, 101 variation in production with depth, 94, 96 vertical distribution, 12, 49, 81, 83, 84, 86, 98, 108 visual examination, 7 Particulate organic carbon aggregation, 26, 47, 48, 51, 53, 56, 57, 58, 61, 62, 67 analysis, 18, 19 bacterial utilization, 54 circulation pattern, 26 cropping, 60 deepwat)er values, 15, 16, 17, 20, 21, 24, 37, 42, 91, 99, 106, 107 distribution, 18, 24, 42 filtration, 18, 29, 42, 47, 48, 54, 56, 57, 58, 60 heterotrophic consumption, 102 horizontal layering, 27 in Antarctic, 18, 20 in Arabian Sea, 17, 20 in Atlantic Ocean, 16, 86 in Caribbean, I 6 in Flemish Cap waters, 56 in Grand Banks waters, 56, 57 in Guinea Current, 16 in Gulf of Aden, 17 in Gulf Stream, 22, 95 in Indian Ocean, 17 in Irminger Sea, 14, 20 in Labrador Current, 57 in North Atlantic, 14, 15, 16, 20, 55 in North Pacific, 16, 17, 20 in Red Sea outflow, 17 in Sargasso Sea, 14, 16, 21, 25, 28, 42, 57, 80, 84, 105 in Scotian Shelf waters, 56, 71, 95 in Slope Water, 21, 60, 70, 85 in Somali coast region, 17 in Somali Current, 14 in South Pacific, 16, 20 in subtropical waters, 12

SUBJECT INDEX

Particulate organic carbon-continued in temperate waters, 13 in tropical waters, 12 living fraction, 63 microstratification, 25, 27 near-surface gradient, 25 particle count, 12, 13 production, 25, 45, 46, 51, 52 production, i n situ, 52, 53, 54, 55, 56, 57, 58, 59, 60, 62 regional variation, 12, 13, 14, 15, 16. 19, 20 sampling, 18, 25 seasonal variation. 15, 16, 17, 19. 21, 22, 24 small-scale variations, 25 ‘steady state’, 55, 57, 84 surface values, 13, 14, 19, 25, 26, 42 utilization, in situ, 52, 53, 55 vertical gradient, 12, 13, 14, 15, 16, 17, 20, 21, 24, 25, 26, 27, 28, 29, 57, 84, 85 Particulate organic matter aggregation, 26, 41, 47, 48, 50, 51, 53, 56, 57, 58, 67 amino acids content, 32, 34 assimilable fraction, 66 biochemical composition, 32 biological attack, 35 buoyancy, 66 calcium carbonate content, 37,38,39 carbohydrate content, 32, 33, 34 carbon content, 32, 35, 37 Cl3 : CI2 ratio, 35, 103 C : N ratio, 30, 31, 32, 33, 34, 51, 143 C : P ratio, 31 chemical composition, 29 clay content, 38 collection, 4, 5, 29 content in sea water, 2, 3, 4 deep water values, 37, 39, 110 degradation, 2, 3 determination of living content, 63, 91 determination of non-living content,, 63, 91 dissolved fraction, 29 distribution in sea water, 4 et seq. elementary composition, 29, 30, 31 enrichment in estuaries, 143

473

Particulate organic matter-continued enzymatic hydrolysis, 66 experimental formation, 3, 49 fat content, 32 fibre content, 32, 36 filtration, 5, 6, 29, 46, 54, 57, 58 formation, 3, 4, 38 hydrolysis, 32, 33, 36 in Long Island Sound, 3, 37, 38 in mud-water, 110 in North Atlantic, 37 in North Pacific, 37 in Sargasso Sea, 37 in South Atlantic, 86 in South Pacific, 86 in various oceanic regions, 3 in organic fraction, 36, 37, 38 living material content, 6 living/non-livingmaterial balance, 64 manganese content, 39 molecular structure, 34, 35 molecular weight, 34 nitrogen content, 32, 33 non-living, 1, 2, 3, 4, 7 et seq. organic carbon content, 6, 12 et seq., 37 phosphorus content, 32, 33 production, i n situ, 52, 53, 54, 55, 56, 57, 58 properties, 4 protein content, 6, 32, 35 saccharides content, 32, 33, 34 separation, 29 sinking rates, 66, 69, 70, 71 size-€requency distribution, 66, 67, 70, 72 sodium chloride content, 38 trace element content, 39 utilization, in s i t u , 52, 53 Pearl River, 134 Pelecypods, 406 Penaeid prawn, 151, 152 cultivation, 155 natural history, 154 principal food, 146 Penguins, 243 jackass, 264 Perch, 249 Periphyton, 144 Petrel, 258

474

SUBJECT INDEX

Petroleum oils Prawn-continued analysis in water, 241, 242 culture in paddy fields, 188, 189 behaviour when spilt, on sea, 236food, 170, 188 240 ‘kuruma’, 136, 156, 178, 204 hehaviour when spilt, on shore, 236penaeid, 135, 146, 151, 152, 154, 170, 240 179, 191 detection, 240-243 priiieipal food, 146 identification, 240-243 ‘sugpo’, 159. 163, 170, 188. 191, physico-chemical charact.eristics. 200 234-236 Prawn fry toxicity, 243-262 capture, 158, 159, 188, 189 Phenol, 248, 249, 251, 252, 253, 254, industry, 157 255, 256 rearing, 156, 163 Phosphate Prawn fry industry, 157-159 in snrfaee water, 40, 41 Prawn ponds of Singapore, 133. 191 Phytoplankton, 3, 4. 11. 25, 31. 36. 44, investment requirements, 201 95. 98, 144 management, 186-188 consumption, 90, 99 profitability, 200, 201 depth range, 99 Protein analysis, 3, 6 effects of oil pollution on. 254 Protista, 111 flowering, 10, 19, 20 Pseudofaeces, 308, 413, 419, 420, 423, in estuaries, 146 424, 425, 426 micro-distribution, 27 Puffer fish, 136 production, 1. 2, 22, 43. 89, 90, 94. Puffins, 243, 259 112 regionaI variation, 82 Q respiratory requirements, 89 seasonal variation, 12, 19 Quahog, 250, 251 sinking rate, 81, 82, 99 vertical distribution, 81, 84 R Pilchard, 247 Pismo clam, 249 Rainbow tjrout, Plankton, 26,27,31.112.134, 142.146. breeding in capt)ivit>y,138, 139 164, 168, 272 Razor clam, 249 benz(a)pyrene content, 263 Razorhills, 243 C13 : ClZratio, 103 Red Sea outflow effects o f oil pollution on, 251-255 particulate organic matJterin, 17 in estuaries, 140, 141, 145 Roach, 249 micro -distribution, 2 8 Rome Conference (l968), 290 Polychaete worms, 197, 252. 284, 381 Russian limans, 121, 123, 124, 134. 140, Polyzoans, 380 163, 167, 168, 170, 178 Pondweed, 256 definition, 123 Porphyra, 203 in Black Sea, 121, 123, 126, 140 Porpoises, 247 management,, 180-181 Prawn, 133, 155, 164, 185, 195. 201. mullet rearing, 180, 181 253 profitahility, 201 capture, 159, 187, 188, 191 rate of fish production. 199 capture of larvae, 158 salinity, 123 cultivation, 135, 159, 179, 180, 186. Shabolat, 181 187, 188, 191 Siwash, 140

SUBJECT INDEX

S Salinity-Temperatiire-Depth recorder, 28 Salinity tolerance Chanos, 150 Crenimugil labrosus, 150, 151 Ctenopharyngodon idella (Grass Carp), 149 grey mnllet, 150, 151 Hypoph~th,almicl~thys mo1itri.r: (Silver Carp). 149 Indian major carp, 150 Liza aurnta, 150 Liza provensalis. 150 Liz% ranwdu, 150 Liza suliens, 150 Liza speigleri, 150 Mugil capito, 150 Mugd cephalus, 150, 151 M u g i l chelo, 150 Puntius javanicus, 150 I.,rulamugilseheli. 150 salmon, 151. 153, 155, 206 breeding in captivity. 138, 140 Santa lhrbara. California, 233, 239, 247, 254, 255, 274 Saltgrass, 256 Saprozoites, 147 Sardine, 169 Sargasso Sea animals in, 104 organic product,ioii in, 89 oxygen consumption in, 90 particulate organic matt,er in, 10, 1 1 , 12, 14, 16. 21, 25, 28. 37, 42, 46,-80, 84. 89, 94, 95, 97, 105, 111,112 Scallop, 259 Scaup, 244 Scotian Shelf waters particulate organic matter in, 56, 71, 95 Sea-anemone, 252 Sea-elephants, 247 Sea foam production, 41 stabilization. 40, 41 Sea-lions. 247 Sea of Azov, 140

475

Sea salts adsorption of organic matter, 76 crystal st#abilization,38, 76 nuclei, 40 Sea-star, 251, 252 Sea trout, 138, 151, 153, 206, 207 Sea-urchin, 252, 259, 260 Seals, 247 Seaweed, 261 Sediment feeders, 110 Semi-transparent flakes, 7, 8. 9, 10, 12, 30, 35, 36, 37, 38, 110, 111 bacterial attack, 78 enzymatic hydrolysis, 78 formation, 77, 78, 79 sinking rates, 67, 69, 70, 71, 72, 110 vertical distribution, 84 Sennen Cove, 276, 278 Seriola quinqueradiata, cultivation, 136, 154 Seston feeders, 110 Seston, marine, 145 Seston weights, 3 Shad, 248 Shelduck, 259 Ships “Anne Mildred Brnvig”, 220, 222, 237 “Argea Prima”, 256 “Atlantis”, 87 “Bakuin”, 21 6 “Benjamin Coates”, 225 “Blucher”. 222 “Chryssi P. Goiilandris”, 225, 256, 286 “Dana”, 87 “Daylight”, 216 “Discovery”, 87 “Drupa”, 229 “Esso Margarita”, 220, 221 “Fina NorvBge”, 224 “Ford Mercer”, 258 “Frank H. Buck”, 258 “General Colocotronis”, 220, 221, 268, 270 “Gerd Maersk”, 238, 258 “Gluckauf”, 2 16 “Hudson”, 56 “Megara”, 229 “Meteor”, 86, 87

476

S U B J E C T INDEX

Ships-contznuerl “Ocean Eagle”, 274 “Pendleton”. 258 “Petrobourg”. 274 “Seaspray”, 227 T 2 tanker, 219 “Tampico Maru”, 247, 249, 251, 252, 254, 255, 259, 260 “Tank Duchess”. 227 “Thomas W. Lawson”. 216 “Torrey Canyon”. 218, 219. 220, 222, 234, 236,237, 238. 245, 247, 250, 254, 256, 261.262. 263, 264. 265, 267, 268, 272, 273, 274, 275, 280, 283, 284, 286, 289. 290 Tribal-class destroyers, 216 ‘Trident”, 12 “Universe Ireland”, 223 “Universe Kuwait”. 223 “Vulcanus”, 216 Shrimp. 179, 253. 380 brown, 282 pink, 282 Silkworm pupa?. 207 Singil. 167 Sinking rates of particulate matter, 67 et seq.. 79-84. 107. 108, 110 Skipjack. 169 Slope Water particulate organic matter in, 21, 60, 70, 85 Snails, 197, 251 Sole, 283, 284 Somali Current particulate organic matter in, 14. 17 Starch grains, 9 Sources of young fish and prawns, 155157 Sparids, 149 Storm dykes construction, 130, 131, 134 sluices, 131, 134 Storm-petrel, 258 Sunfish, 248, 249 Surface films chemical analysis, 76 compression, 76 physical properties, 76 Suspension feeding bivalves biodeposition, 413-429

Surface layer, 79, 80, 81, 80 Surface waters, 13, 14, 19, 25, 26 biological oxygen demand (B.O.D.), 103 carbon distribution, 29 nitrogen distribution, 29 particulate matter in, 42, 79, 80, 81, 84, 88, 95, 105, 111 phosphate distribution, 40, 4 1 Suspension feeding bivalves, factors influencing biodepositiori temperature, 419 salinity, 419-420 size of producer, 420

T ‘Tai-ayer’, 167 production, 171 Tankers construction, 219, 220, 222 loading, 228 “load-on-top” system, 222 oil discharge a t sea, 223 operation, 219-224 salvage, 220, 221 unloading, 228. 229, 230 Tarpon, 121 Tcrns, 246 Thames Haven. 230 Thermoclines, 27, 28, 81, 82, 83, 85, 88, 97, 98, 100, 104 Tilupia hreeding, 155 cultivation, 154, 178-180 food, 168, 169, 173, 178 growth, 179 natural history, 154 runting, 178 Toadfish, 248 Topography of estuaries, 124 et seq. Topshell, 261, 286, 289 Tourist industry, effects of oil pollution on, 264-265 TOVALOP plan, 218 Trans Arabia oil pipeline, 231, 232 Transition zone, 83, 84, 85, 86 Tranmere, 230 Trout, 138, 169, 247, 249, 281 rainbow, 138, 281

477

SUBJECT I S D E S

Y

Tubeworm, 282 Tunicates, 380

U Ultraplankton, 7, 97, 98, 111

V Vertical flux, 85, 98 Volga, 215

w Whales, 247 Whelk, 282 White Amur, 149 White Tolstolobik, 149 Winkle, 251, 261, 281, 282, 286, 28s World petroleum production, 216, 218, 288

X X-ray diffraction analysis, 38

Yellowtail, 155, 204 capture of fry, 158 cidt,ivntion, 136, 154, 206 food, 178 principal food, 158 rate of production in Japan, 198 York River biodeposition cycle, 427, 428, 429

Z Zoobenthos, 168 Zooplankton, 9, 26, 27, 28, 44, 96, 106, 112, 158, 164, 168. 175 consumption, 95, 105, 107, 111 diurnal migration, 98 effeck of oil pollution on, 254 cxcretorv rates, 103 food requirements, 104, 107, 109 feedillg rates. 104, 105. 107 herbivorous, 105, 106. 112 in deep waters, 106 in estuaries, 146 in surface waters, 106 respiratory requirements, 89, 90, 98, 104, 105, 107

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Cumulative Index of Authors Arakawa, K. Y., 8, 307 Rlaxter, J. H. S., 1, 262 Boney, A. D., 3, 105 Bruun, A. F., 1, 137 Carroz, J. E., 6, 1 Cheng, T. C., 5, 1 Clarkr, M. R., 4, 93 Cushmg, J. E., 2, 85 Davis, H. C., 1, 1 Fisher, L. R., 7, 1 Ghirardelli, E., 6, 271 Gulland, J. A.. 6 , 1 Hiclrling, C. I?., 8. 119 Holliday, F. G. T., 1, 262 Loosanoff. V. L., 1, 1 Macnar, W., 6, 74 Mauchlinc, J., 7, 1 Naylor, E., 3, 63 Nelson-Smith, A . , 8, 215 Nicol. J. A. C., 1, 171 Riley, G. A., 8, 1 Russell, F. E., 3, 256 Scholos, R. H . , 2, 133 Shelbourrie, J. E., 2, 1 Shewan, J. M., 2, 133 Sindermann, C. J., 4, 1 Wells, M. J., 3, 1 Yonge, C. M., 1, 209

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Cumulative index of Titles Artificial propagation of marine fish, 2, 1 Aspects of the biology of seaweeds of economic importance, 3, 105 Behaviour and physiology of herring and other clupeids, 1, 262 Biology of coral reefs, 1, 209 Biology of euphausiids, 7, 1 Blood groups of marine animals, 2, 85 Breeding of the North Atlantic freshwater eels, 1, 137 Diseases of marine fishes, 4, 1 Effects of heated effluents upon marine and estuarine organisms, 3, 63 Estuarine fish farming, 8, 119 General account of the fauna and flora of mangrove swamps and forests in the Indo-West Pacific region, 6, 74 Learning by marine invertebrates, 3, 1 Management of fishery resources, 6, 1 Marine molluscs as hosts for symbioses, 5, 1 Marine toxins and venomous and poisonous marine animals, 3, 256 Met,hods of sampling the benthos, 2, 171 Particulate and organic mattJer in sea water, 8. 1 Present, status o f some aspccts of marine microbiology, 2, 133 Problems of oil pollut,ion of t,he sea, 8, 215 Rearing of bivalve mollusks, 1, 1 Review of the systematics and ecology of oceanic squids, 4, 93 Scatological studies of the bivalvia (molhisca), 8, 307 Some aspects of the biology of the chaetognaths, 6, 27 1 Some aspects of photoreception and vision in fishes, 1, 171

481

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