Advances in Marine Biology, Volume 39 (Advances in Marine Biology)

Series Contents for Last Ten Years* VOLUME 27, 1990. Dall, W., Hill, B. J., Rothlisberg, E C. and Sharpies, D. J. The bi...

Author: Alan J. Southward | Paul A. Tyler | Craig M. Young | Lee A. Fuiman

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Series Contents for Last Ten Years* VOLUME 27, 1990. Dall, W., Hill, B. J., Rothlisberg, E C. and Sharpies, D. J. The biology of the Penaeidae, pp. 1-461. VOLUME 28, 1992. Heath, M. R. Field investigations of the early life stages of marine fish. pp. 1-174. James, M. A., Ansell, A. Q. D., Collins, M. J., Curry, G. B., Peck, L. S. and Rhodes, M. C. Biology of living brachiopods, pp. 175-387. Trueman, E. R. and Brown, A. C. The burrowing habit of marine gastropods, pp. 389--431. VOLUME 29, 1993. Kicrboe, T. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. pp. 1-72. Kuparinen, K. and Kuosa, H. Autotrophic and heterotrophic picoplankton in the Baltic Sea. pp. 73-128. Subramoniam, T. Spermatophores and sperm transfer in marine crustaceans, pp. 129-214. Horwood, J. The Bristol Channel sole (Solea solea (L.)): a fisheries case study, pp. 215-367. VOLUME 30, 1994. Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambshead, E J. D., Pfannkiiche, O., Soltweddel, T. and Vanreusel, A. Meiobenthos of the deep Northeast Atlantic. pp. 1--88. Brown, A. C. and Odeandaal, E J. The biology of oniscid Isopoda of the genus Tylos. pp. 89-153. Ritz, D. A. Social aggregation in pelagic invertebrates, pp. 155-216. Ferron, A. and Legget, W. C. An appraisal of condition measures for marine fish larvae, pp. 217-303. Rogers, A. D. The biology of seamounts, pp. 305-350. VOLUME 31, 1997. Vinogradov, M. E. Some problems of vertical distribution of meso- and macroplankton in the ocean, pp. 1-92. Gebruk, A. K., Galkin, S. V., Vereshchaka, A. J., Moskalev, L. I. and Southward, A. J. Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic Ridge. pp. 93-144. *The full list of contents for volumes 1-37 can be found in volume 38.

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CONTENTS FOR LAST TEN YEARS

Parin, N. V., Mironov, A. N. and Nesis, K. N. Biology of the Nazca and Sala y Gomez submarine ridges, an outpost of the Indo-West Pacific fauna in the eastern Pacific Ocean: composition and distribution of the fauna, its communities and history, pp. 145-242. Nesis, K. N. Ganotid squids in the subarctic North Pacific: ecology, biogeography, niche diversity and role in the ecosystem, pp. 243-324. Vinogradova, N. G. Zoogeography of the abyssal and hadal zones, pp. 325-387. Zezina, O. N. Biogeography of the bathyal zone. pp. 389-426. Sokolova, M. N. Trophic structure of abyssal macrobenthos, pp. 427-525. Semina, H. J. An outline of the geographical distribution of oceanic phytoplankton, pp. 527-563. VOLUME 33, 1998. Mauchline, J. The biology of calanoid copepods, pp. 1-660. VOLUME 34, 1998. Davies, M. S. and Hawkins, S. J. Mucus from marine molluscs, pp. 1-71. Joyeux, J. C. and Ward, A. B. Constraints on coastal lagoon fisheries, pp. 73-199. Jennings, S. and Kaiser, M. J. The effects of fishing on marine ecosystems. pp. 201-352. Tunnicliffe, V., McArthur, A. G. and McHugh, D. A. biogeographical perspective of the deep-sea hydrothermal vent fauna, pp. 353-442. VOLUME 35, 1999. Creasey, S. S. and Rogers, A. D. Population genetics of bathyal and abyssal organisms, pp. 1-151. Brey, T. Growth performance and mortality in aquatic macrobenthic invertebrates, pp. 153-223. VOLUME 36, 1999. Shulman, G. E. and Love, R. M. The biochemical ecology of marine fishes. pp. 1-325. VOLUME 37, 1999. His, E., Beiras, R. and Seaman, M. N. L. The assessment of marine pollution - bioassays with bivalve embryos and larvae, pp. 1-178. Bailey, K. M., Quinn, T. J., Bentzen, P. and Grant, W. S. Population structure and dynamics of walleye pollok, Theragra chalcogramma, pp. 179-255. VOLUME 38, 2000 Blaxter, J. H. S. The enhancement of marine fish stocks, pp. 1-54. Bergstr6m, B. I. The biology of Pandalus. pp. 55-245.

CONTRIBUTORS TO VOLUME 39

C. D. ELVIDGE,Office of the Director, NOAA National Geophysical Data

Center, 325 Broadway, Boulder, CO 80303, USA W. S. JOHNSON, Department of Biological Sciences, Goucher College,

Towson, MD 21204, USA C. H. PETERSON,University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557, USA P. G. RODHOUSE,British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK M. STEVENS,Department of Biology, Ripon College, 300 Seward Street, Ripon, WI 54971, USA P. N. TRATHAN, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK L. WATLING,School of Marine Science, Darling Marine Center, University of Maine, Walpole, ME 04573, USA

The "Exxon Valdez" Oil Spill in Alaska: Acute, Indirect and Chronic Effects on the Ecosystem C h a r l e s H. P e t e r s o n

University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557, USA FAX." 252-726-2426 e-mail: [email protected]

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. History and Fate o f the Oil Spilled f r o m the " E x x o n Valdez". . . . . . . . . . . . . . . . . . 3. Biological C o n s e q u e n c e s o f the Oil Spill in the Intertidal Z o n e . . . . . . . . . . . . . . . 3.1. E x p o s u r e to oil and c o n t a m i n a t i o n o f o r g a n i s m s . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. C h a n g e s in species a b u n d a n c e s and c o m m u n i t y c o m p o s i t i o n of rocky s h o r e s 4. Biological C o n s e q u e n c e s o f the Oil Spill in the Subtidal Z o n e . . . . . . . . . . . . . . . . 4.1. Effects on eelgrass c o m m u n i t i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Effects on d e e p e r benthic systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Effects on kelp c o m m u n i t i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Impacts on Vertebrates That Use S h o r e l i n e Habitats . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Terrestrial m a m m a l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Terrestrial birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Fishes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. M a r i n e m a m m a l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Shorebirds, seaducks, and seabirds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Discussion 6.1. Interaction w e b s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Ecotoxicology vs field a s s e s s m e n t as a p p r o a c h e s . . . . . . . . . . . . . . . . . . . . . . . . . 6.3. U n d e r s t a n d i n g d e l a y e d recoveries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. S u m m a r y and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements ................................................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

3 6 13 13 16 34 34 39 40 43 43 45 48 60 64 70 70 75 79 81 83 84

Following the oil spill in Prince William Sound, Alaska, in 1989, effects were observed across a wide range of habitats and species. The data allow us to evaluate direct and indirect links between shoreline habitats and the

ADVANCES IN MARINE BIOLOGY VOL. 39 ISBN 0-124)26139-1

Copyright © 2001 Academic Press Limited All rights of reproduction in any form reserved

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CHARLES H. PETERSON

coastal ecosystem in general The intertidal zone suffered from direct oiling and clean-up treatments such as pressurized hot water, resulting in freeing of bare space on rocks and reductions in fucoid algal cover. Grazing limpets, periwinkles, mussels and barnacles were killed or removed. Subsequent indirect effects included colonization of the upper shore by ephemeral algae and an opportunistic barnacle and, in some regions, spread ofFucus gardneri into the lower shore where it inhibited return o f red algae. The loss of habitat provided by the Fucus canopy slowed recovery on high shores, and lowered abundance o f associated invertebrates. Abundance of sediment infauna declined and densities of clams were reduced directly. Their recovery was still incomplete by 1997 on oiled and treated shores where fine sediments had been washed down slope during treatment. Impacts in subtidal habitats were less intense than in the intertidal zone. Kelps were reduced in 1989 but recovered rapidly through re-colonization by 1990. Abundances of a dominant crab and seastar were reduced greatly, with recovery of the more mobile species, the crab, occurring by 1991. For about 4 years, there was reduced eelgrass density and hence less habitat for associated animals. Abundance o f several toxin-sensitive amphipods declined dramatically and had not recovered by 1995. In general, however, many subtidal infaunal invertebrates increased in abundance, especially oligochaetes and surface deposit-feeding polychaetes. This may have resulted from increases in sediment hydrocarbon-degrading bacteria, but may also reflect reduction o f predators. Along northern Knight Island, where sea otter populations had not recovered by 1997, green sea-urchins were larger, compared with those in un-oiled parts of Montague Island. This initial response from reduced predation by sea otters, if sustained, could lead to additional indirect effects of the spill. Scavenging terrestrial birds, such as bald eagles and northwestern crows, suffered direct mortality as adults and reproductive losses, although eagles recovered rapidly. Numbers o f intertidal benthic fishes were 40% lower on oiled than on un-oiled shores in 1990, but recovery was underway by 1991. Small benthic fishes living in eelgrass showed sensitivity to hydrocarbon contamination until at least 1996, as evidenced by hemosiderosis in liver tissues and P450 1A enzyme induction. Oiling of intertidal spawning habitats affected breeding o f herring and pink salmon. Pink salmon, and possibly Dolly Varden char and cut-throat trout, showed slower growth when foraging on oiled shorelines as older juveniles and adults, which for pink salmon implies lower survival The pigeon guillemots that suffered from the oil spill showed reduced feeding on sand eels and capelin, which may also have been affected by the spill, and this may have contributed to failure of guillemot recovery. There was an analogous failure of harbor seals to recover. Sea otters declined by approximately 50%, and juvenile survival was depressed on oiled shores for

EFFECTS OF "EXXON VALDEZ" OIL SPILL

3

at least four winters Both black oystercatchers, shorebirds that feed on intertidal invertebrates, and also harlequin ducks showed reduced abundance on oiled shores that persisted for years after the spill. Oystercatchers consumed oiled mussels from beds where contamination by only partially weathered oil persisted until at least 1994, with a resulting impact on productivity o f chicks A high over-winter mortality of adult harlequin ducks continued in 1995-96, 1996-97 and 1997-98. Delays in the recovery o f avian and mammalian predators of fishes and invertebrates through chronic and indirect effects occurred long after the initial impacts o f the spill. Such delayed effects are not usually incorporated into ecotoxicity risk assessments which thus substantially underestimate impacts o f a spill. Detection o f delayed impacts requires rigorous long-term field sampling, so as to observe the dynamics o f recovery processes.

1.

INTRODUCTION

The high mortality of wildlife, contamination of pristine habitats, and loss of natural ecosystem products such as subsistence and fishing (Wells et al., 1995; Rice et al., 1996) render the oil spill from the tanker "Exxon Valdez" in 1989 an environmental mishap of international concern and significance. Yet the event also represents an opportunity to use the locally intensive perturbation of the oil spill to extract valuable new understanding of ecological interconnections within the ecosystem. The costs of a planned perturbation on this scale and the costs of evaluation of ecosystem response are far higher than could ever be funded by traditional sources of scientific support. Following the oil spill, however, substantial expenditures of funds both by the government trustees for public natural resources and also independently by Exxon Corporation supported extensive field studies of impacts and recovery from the oil spill (Paine et al., 1996). Whereas the initial field studies were largely devoted to assessing injuries to individual species, as required by attorneys for litigation, early studies of coastal habitats possessed a broader community perspective from the start. Subsequent studies of affected species in other habitats conducted after settlement of federal and state claims for compensation also adopted an integrative and functionally based ecological approach to understanding recovery processes (Cooney, 1998; Duffy, 1998; Holland-Bartels et al., 1998; Okey and Pauly, 1998). There is now an immense body of literature on the "Exxon Valdez" spill. Scanning of just one database on CD-ROM shows several hundred publications on Alaskan oil pollution since 1990, and some authors have managed to produce three publications a year in this period. Thus a review

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CHARLES H. PETERSON

is urgently needed to bring this large body of data before a wider readership. The information now available on the response of the coastal ecosystem of Alaska to the oil spill permits a synthesis of direct acute and also chronic and indirect effects of the spill, providing new insights into the functional importance and roles of nearshore habitats. There are two basic scientific approaches available by which to assess biological impacts from an oil spill (Gilbert, 1987). One approach involves modelling the likely impacts based upon laboratory information on toxicological responses of a limited set of individual species to varying concentrations of oil, typically in dissolved phase or as a function of sediment mass. These toxicological data are then used along with information on (1) pre-spill densities of all species, (2) concentration, exposure and uptake of oil, and (3) the transport, transformation and fate of the oil to model the expected mortality (French et al., 1996). Knowledge of the in situ exposure dosage and the time function of exposure dosage are always incomplete and uncertain. Typically, data on toxicological response are available for only a few of the species of interest so that other taxonomically related species are then used as proxies for modelling effects. Toxicity is a function of temperature, so the application of study results at a fixed temperature to field conditions requires some assumptions about how changing temperature would influence the toxicity thresholds. In the absence of field surveys there is great uncertainty over the pre-spill abundances of many of the species in the affected area. The alternative holistic, non-reductionist approach involves use of sampling theory to design field studies of impact. If funds are available, this approach is to be preferred because of several advantages. First, it integrates all mechanisms of impact rather than estimating response by often only a single mechanism, toxicity of dissolved oil. Secondly, chronic effects can be evaluated empirically with an adequate long-term sampling design. Third, this field-based approach can incorporate the web of ecological interactions that induce indirect as well as direct effects of the oil spill (NRC, 1981; Gilbert, 1987; Johnson et al., 1989; Clements and Kiffney, 1994). The field assessment implicitly includes indirect effects driven by changes in habitat, predators, prey and competitors, thereby providing a more realistic, albeit complex, understanding of impacts to the ecological system (Underwood and Peterson, 1984; Peterson, 1993). To some degree, these two approaches can be complementary: toxicology can illuminate mechanistic contributions of one or more pathways of direct impact early in the spill and identify sensitive species, while field-based assessment provides an integration of all pathways including chronic delayed and indirect effects. However, in practice, the toxicological approach is typically adopted simply to minimize the costs of assessment of damages to biological resources despite the penalty of greater uncer-

EFFECTS OF "EXXON VALDEZ" OIL SPILL

5

tainty and exclusion of many potential mechanisms of injury (Kimball and Levin, 1985; Clements and Kiffney, 1994). An oil spill at sea can be dissected into at least three separate phases (NRC, 1985; Wolfe et al., 1994). During the first phase, the oil floats on the sea surface, where injury is inflicted on organisms that use the surface and on those exposed to toxic fumes released by volatilization into the local atmosphere. If wave action is sufficiently intense, the oil may also be mixed to some depth in the water column, where sensitive organisms are exposed and injured. It was during this first phase of the "Exxon Valdez" oil spill that most of the recorded mortality of seabirds and marine mammals occurred (Piatt and Lensink, 1989). The second phase commences with the deposition of the oil on intertidal land masses. Here impacts occur through multiple mechanisms to the plants and animals that occupy the intertidal zone as well as to the abiotic habitat itself. The length of time spent floating at sea affects the physical and chemical nature of the oil once grounded, so it is an important determinant of impact. The third phase of the spill involves deposition of oil in particulate form onto the subtidal sea floor, where it can affect plants, animals, and the nursery and foraging habitats for various species. If the spilled oil never encounters the shore, this third phase can occur in the absence of the second. This review addresses the impacts of these latter two (depositional) phases of the "Exxon Valdez" oil spill and uses data from intensive field assessments to evaluate the network of ecological responses to shoreline oiling and subsequent treatments as a perturbation to the coastal ecosystem. In synthesizing direct as well as chronic and indirect impacts of shoreline oiling, the review is a response to recent appeals for additional scientific study of longer-term impacts of petroleum exposures in the environment (Gray, 1982; NRC, 1985; Boesch et al., 1987; Capuzzo. 1987). The intertidal and shallow subtidal zones of the sea are occasionally dismissed as irrelevant by oceanographers because of the small proportion of the ocean that they occupy. Such a narrow view overlooks the tremendous biological significance of this region of the sea (Mann, 1982; Raffaelli and Hawkins, 1996). The intertidal zone occupies the unique triple interface among land, sea and atmosphere. The land provides a substratum for occupation by intertidal organisms, the seawater is a vehicle for transport and supply of nutrients and larvae, and the air a medium for passage of solar energy and a source of physical stress (ConneU, 1972). Interfaces between separate systems are locations of typically intense biological activity. As a triple interface, the intertidal zone is exceptionally productive (Leigh et al., 1987). Wind and tidal energy combine to subsidize the intertidal zone with planktonic foods produced in the photic zone of the coastal ocean. Runoff from adjacent land injects

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CHARLES H. PETERSON

new supplies of inorganic nutrients to fuel the high coastal plant production (Mann, 1982; Nixon et al., 1986). The consequent abundance and diversity of life and life forms in the intertidal zone serves many valued consumers, including humans, coming to use this habitat from land, sea and air. The aesthetic and cultural values of the intertidal zone and its resources augment its significance. Yet, the same physical transport processes that are responsible for their high level of biological productivity also place the intertidal habitats at great risk to floating pollutants, such as oil. The adjacent shallow subtidal habitats share a high level of biological productivity and typically provide critical biogenic habitat that serves as vital spawning, nursery and foraging grounds. Shallow subtidal areas are also at high risk of injury from oil spills because of their exposure to wave-mixed oil and their role as repositories of sedimented hydrocarbons. Thus, the intertidal and shallow subtidal zones become a natural focal point for understanding injuries and recovery from a coastal oil spill.

2.

HISTORY AND FATE OF OIL SPILLED FROM THE "EXXON VALDEZ"

Prince William Sound is the water body in which the "Exxon Valdez" oil spill originated. Prince William Sound, on the margin of the northern Gulf of Alaska, is home to a diverse and productive coastal ecosystem, in which charismatic marine mammals and seabirds are especially evident (SAI, 1980; Hood and Zimmerman, 1986). The affected region, from Prince William Sound along the outer Kenai Peninsula and lower Cook Inlet coast to the Kodiak Island Archipelago and out along the Alaska Peninsula, is notable for its wilderness areas and parks, rich fishing grounds, recreational opportunities and cultural heritage for native Americans. The rugged shoreline reflects its recent and, in places, ongoing glaciation. Historically, the northern Gulf of Alaska has seen major changes in its marine ecosystem caused by both natural and anthropogenic perturbations Over-exploitation of sea otters during the fur trade of the 19th and early 20th centuries virtually eliminated sea otters from the system (Simenstad et al., 1978). This produced major alterations in the coastal ecosystem, as sea urchin populations expanded and overgrazed kelps in the nearshore (Estes and Palmisano, 1974; Estes and Duggins, 1995). Conservation measures allowed the return of the sea otter, which has resulted in a restoration of the alternate state of the ecosystem in which sea-urchins are less abundant and kelps and associated organisms dominate the nearshore rocky coasts. The earthquake of 1964 caused massive impacts to the shoreline communities, with uplift of shorelines in

EFFECTS OF "EXXON VALDEZ" OIL SPILL

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Prince William Sound ranging from 1-3 m. In the mid 1970S, the ocean climate of the northern Gulf of Alaska began a major change that dramatically modified the marine ecosystem. The demersal system of the northern Gulf of Alaska around Kodiak Island, previously dominated by crabs and shrimps, changed to one in which groundfish such as walleye pollock and flatfishes now dominate (NRC, 1996; Anderson and Piatt, 1999). Because of the valuable fisheries, wildlife, recreational opportunities, and cultural significance, there was much discussion over the wisdom of permitting the oil pipeline from the North Slope to terminate in Prince William Sound. Indeed, the "Exxon Valdez" tanker ran aground in the process of transporting north-slope crude oil from the pipeline terminus in Valdez. The "Exxon Valdez" grounded on Bligh Reef late on the night of 24 March 1989. An estimated 10.8 million gallons (35 000 tonnes out of a total cargo of 175 000 tonnes) of Alaskan North Slope (ANS) crude oil were released into northern Prince William Sound (Pain, 1989; Dayton, 1990; Spies et al., 1996). ANS, or Prudhoe Bay oil, as it is sometimes referred to, is rich in volatile hydrocarbons (Pain, 1989). The tonnage of oil released in this spill was exceeded by many previous oil spills worldwide. Nevertheless, the magnitude of ecological effects of the "Exxon Valdez" spill makes it by most standards the world's most damaging, because of its proximity to a coastal ecosystem so rich in seabirds, marine mammals and shoreline-dependent species. Approximately 40-45% of the oil was estimated by Wolfe et al. (1994) to have been deposited on intertidal shores of Prince William Sound (Figure 1). About 25% was transported by winds and ocean currents out of the sound, most of which later grounded on shores of the Kenai Peninsulalower Cook Inlet area or the Kodiak Archipelago-Alaska Pensinsula region (Table 1). Two sets of aerial surveys reveal grossly similar extents of shoreline oiling (Table 2). Aerial surveys by the Alaska Department of Natural Resources (ADNR, 1991) showed that by the end of summer 1989: (1) out of 1891 km of Prince William Sound shoreline observed, 446km exhibited light to heavy oil impact; (2) out of 1662km of Kenai-Cook Inlet shoreline observed, 260km exhibited very light to heavy oil impact; and (3) out of 2960 km of Kodiak-Alaska Peninsula shoreline observed, 943 km exhibited very light to heavy oil impact. Heavy stranding of oil was most prevalent nearer the spill site along Prince William Sound shores, where 144km were characterized as heavily contaminated by oil in these aerial surveys, as compared with 28 km in the Kenai-Cook Inlet region and nine in the Kodiak-Alaska Peninsula region. Beachwalk surveys organized by the Alaska Department of Environment and Conservation confirmed the accuracy of the aerial measures of the extent of shoreline oiling. Neff et al. (1995)

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CHARLES H. PETERSON

Figure 1 Map of Prince William Sound and, inset, the northern Gulf of Alaska to Kodiak Island, showing the area transited by floating "Exxon Valdez" oil (coarse stipple), using results integrated from all sources. The oil was released in northern Prince William Sound at Bligh Reef, where the oil track narrows to a point. (Adapted from Babcock et al., 1996.)

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EFFECTS OF "EXXON VALDEZ" OIL SPILL

Table 1 Fate of the approximately 10.8 million gallons of Alaskan North Slope crude oil spilled from the "Exxon Valdez", as percentages on 1 May 1989 (from Wolfe et al., 1994).

% of spilled oil Beached in Prince William Sound Beached on the Kenai Peninsula Transported past Cape Douglas into the Shelikof Strait and probably beached on Alaska Peninsula and Kodiak Archipelago Remained floating in Kenai region (and probably beached later in Shelikof Strait)

41.0

5.2 1.8

Table 2 Estimated extent and intensity of shoreline oiling by "Exxon Valdez" spilled oil by the end of summer (August) 1989.

Kilometers of oiled shore Geographic area

Shoreline aerially surveyed (km)

Light

Moderate

Heavy

1891 1662 2960

190 182 867

112 50 67

144 28 9

1450

549*

94

141

from A D N R (1991)

Prince William Sound Kenai-Cook Inlet Kodiak-Alaska Peninsula from Neff et al. (1995)

Prince William Sound

* Includes very light as well as light oiling.

reported lengths of oiled shoreline by oiling intensity and geographic region that revealed similar patterns (Table 2). The hundreds of kilometers of oiled shorelines within the spill area included segments of all types of intertidal habitats, including exposed rocky shores, exposed wave-cut platforms, sheltered rocky shores, boulder, gravel and cobble beaches, coarse-grained sand beaches, fine-grained sand beaches, exposed and sheltered tidal flats, and salt marshes (see RPI, 1983 for geomorphologic definitions). Of these, the exposed rocky shores, the sheltered rocky shores, and the gravel, cobble and boulder ("coarsetextured") beaches received the large majority of the heavy oiling (Page et al., 1995). The beaches with mostly fine-grained sediments and the salt marshes comprised much less of the potentially, and of the actually, oiled coastline (ADNR, 1991). In the summers of 1989 and 1990, and again at reduced intensity in the summer of 1991, extensive and intensive shoreline

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CHARLES H. PETERSON

Figure 2 An example of the intensive nature of the clean-up operations after the "Exxon Valdez" spill. Spraying a beach with pressurized hot water. Photograph courtesy of "Exxon Valdez" Oil Spill Trustee Council.

treatments were conducted in an attempt to speed removal oil from intertidal shores in the spill area. Several techniques were employed: especially wiping rocks with absorbent cloth, manual bagging and removal of oiled rocks, low-, medium-, and high-pressurized hot-water washing, bioremediation of two main types (fertilization to stimulate bacterial degradation of the hydrocarbons), and hand and mechanical raking and tilling to expose buried pools of oil (Mearns, 1996). Figure 2 gives an idea of the intensity of the clean-up operations. The movement of the oil away from its initial location floating on the sea surface was documented by several studie~ First, direct sampling of the water column by NOAA (Short and Harris, 1996a) and by Exxon researchers (Neff and Stnbblefield, 1995) detected low concentrations of oil (1--8 ppb of total aromatic hydrocarbons) in the first 1-5 weeks after the spill when large masses of floating oil were still moving through Prince William Sound. By the end of the 1989 summer, water-column oil was difficult to detect by direct sampling of the water (Neff and Stubblefield, 1995). Its continued presence in biologically available form was, however, documented by contamination of experimentally transplanted clean mussels (Mytilus trossulus Gould) into cages held at different depths below the

EFFECTS OF "EXXON VALDEZ" OIL SPILL

11

sea surface at several locations within the spill area (Short and Harris, 1996b). Mussels filter particles from large volumes of water so that they concentrate polycyclic aromatic hydrocarbons (PAH) and other lipophilic contaminants, making them better indicators of the presence of biologically active contaminants than water samples. Short and Harris (1996b) used gas chromatography-mass spectrometry (GC-MS) analysis to show that this oil was derived from particulate sources and was not limited to the lighter more water-soluble fractions. Shigenaka and Henry (1995) deployed mussels and a semipermeable membrane sampler at a heavily oiled site at Smith Island and showed that in summer 1992 there was still an operative pathway of exposure and contamination through the water column: the PAH composition spectrum in the experimentally deployed mussels resembled that of oiled sediments and surface oil sheens, suggesting the likely pathways of transport. Studies of the sedimentary habitat also confirmed the transport and deposition of "Exxon Valdez" oil onto shallow subtidal sediments. Sediment traps deployed in the subtidal environment near oiled beaches in 1990 and 1991 collected contaminated sediments, demonstrating one mechanism of movement of the oil to the sea floor (Short et al., 1996). Oil was transported subtidally in association with sediment particles, probably originating from the intertidal beaches, for at least as long as 1-2 years after the spill. PAH composition of these oiled particles matched the "Exxon Valdez" oil (Short et al., 1996). Sampling of the sediments in 1989 and 1990 (Carlson and Kvenvolden, 1996; O'Clair et al., 1996) showed widespread oil contamination in the 0-20 m depth zone within the spill region, and that concentrations were generally highest at shallower depths and from sites near the most heavily contaminated beaches. Hydrocarbon contamination was sometimes detected at 40 and 100 m depths; however, in most cases, the components of the hydrocarbons did not correspond to the "Exxon Valdez" crude oil (Bence and Burns, 1995; O'Clair et al., 1996). Outside Prince William Sound, the concentrations of "Exxon Valdez" hydrocarbons in subtidal sediments were low and patchy, reflecting the discontinuous nature of the oil slick and oiling pattern in the Gulf of Alaska region (O'Clair et al., 1996). Oil concentrations in shallow subtidal sediments decreased greatly from July 1989, when a maximum average concentration was recorded at 0 m on Disk Island of 12 729 ng g-l, to summer 1990, when total PAH concentrations in most intertidal sediments had declined to 100-200ngg -1. By then PAHs recognizably matching "Exxon Valdez" oil were found in shallow subtidal sediments at only a few locations (O'Clair et al., 1996). PAH contamination of shallow subtidal sediments in and around oiled eelgrass beds in Prince William Sound persisted at low (100-200 ng g-~) but statistically significant levels as compared with unoiled control

12

CHARLES H. PETERSON

seagrass beds until at least 1995, when sampling in and around eelgrass ended (Jewett et al., 1999). The persistence and weathering processes of grounded oil varied with physical conditions of the oiled habitat. Visible surface oil was reduced relatively rapidly through shoreline treatment and natural action of winter storms, so that, by 1991, surface oil was found only in small amounts (Owens, 1991; Michel and Hayes, 1993). On sheltered shores, surface oil was more persistent, with "asphalt pavements" and "mousse" remaining in many upper intertidal locations at least until 1993 (Gibeaut and Piper, 1997) and 1994 (Irvine et al., 1999). The continued persistence of oil blemishes in National Parks such as Katmai and Kenai Fjords, on state public trust lands, and on native lands that are the basis for culture and subsistence represents a long-lived injury to human uses and values. The rate of disappearance of surface oil slowed through time, especially in sheltered habitats (Michel and Hayes, 1993; Hayes and Michel, 1999). Surface oil and subsurface oil remained in protected sites on heavily oiled beaches in positions where boulder and cobble armouring protected it from physical disturbance by waves (Owens, 1991; Gibeaut and Piper, 1997; Irvine et al., 1999). As of summer 1993, at least 4.8 km of shoreline in Prince William Sound retained surface oil, while at least 7 km retained subsurface oil-saturated sediments (Gibeaut and Piper, 1997). Additional beach treatments using chemical injections were conducted in summer 1997 on a trial basis to try to remove some of this recalcitrant subsurface oil (Broderson, 1998). The weathering of the oil was rapid except in sheltered rubble shores and armoured subsurface pockets of oil, where physical disturbance and oxygen penetration were limited. For example, by August 1992, the PAHs in sheltered rubble shores still contained some two-ring PAHs (Michel and Hayes, 1993), which are typically considered too volatile to persist for years after an oil spill and represent some of the most toxic constituents of the petroleum hydrocarbon mix. Oil removal and weathering were also inhibited in another type of armoured habitat, underneath mussel beds (Babcock et al., 1996; Boehm et al., 1996; Carls et al., 2000). The persistence of slowly weathering oil underneath mussels has biological significance because the oil is being ingested and concentrated in the mussels (Harris et al., 1996), and because the mussels are such important prey organisms for so many intertidal consumer species. Finally, oil persisted for a long time in another armoured habitat, in the subsurface rocks and cobbles along the intertidal banks of anadromous fish streams (Murphy et al., 2000). This environment was not subjected to pressurized hot-water treatments for fear of harming the salmon eggs. However, the tidal pumping of subtidal oil and slow release into the stream continued for eight or more years after the oil spill and represents a major pathway for chronic biological injury (Heintz et al., 1999).

EFFECTS OF "EXXON VALDEZ" OIL SPILL

3.

3.1.

13

BIOLOGICAL CONSEQUENCES OF THE OIL SPILL IN THE INTERTIDAL ZONE

Exposure to oil and contamination of organisms

The oil spilled by the "Exxon Valdez" rapidly contaminated biological resources along the path of the spill and entered food chains of intertidal and coastal ecosystems. A full list of affected species discussed in this review and their common names will be found in Appendix 1, pp. 101-103. Suspension-feeding invertebrates filter large volumes of seawater, resulting in a high potential for exposure to, and accumulation of, contaminants such as petroleum hydrocarbons. For this reason, suspension feeders such as the relatively long-lived and hardy blue mussel (Mytilus edulis L.), and the other west coast mussel (M. trossulus Gould), have been employed as sentinels of environmental quality (e.g. NOAA Mussel Watch: Goldberg et al., 1983; O'Connor, 1996). Numerous studies that followed the fate of the "Exxon Valdez" oil assessed the levels of hydrocarbon contamination in tissues of mussels and common species of suspension-feeding clams at sites spanning the spill area and extending for several years after the spill. Results of analysing the petroleum hydrocarbon contamination of mussels and four species of infaunal clams demonstrated widespread, locally long-lasting, and ecologically significant injuries in the intertidal system. First, analyses of water samples and tissues of experimentally introduced mussels during the months and early years following the "Exxon Valdez" oil spill confirmed that the activities of the mussels render them a more sensitive sampler of hydrocarbon contamination than direct water sampling (Short and Harris, 1996a, b). When hydrocarbons recovered from seawater fell below detection limits, mussels still contained substantial levels. This sampling of mussels is also ecologically meaningful because mussels are important members of many coastal food chains. Secondly, mussels sampled in 1977-1980 and in 1989 outside the spill area in the Valdez region of Prince William Sound (Karinen et al., 1993) had much lower hydrocarbon levels than those sampled in 1989 after the "Exxon Valdez" spill inside the spill area (Short and Babcock, 1996). Thirdly, the spatial sampling of mussels and clams of four species for analysis of petroleum hydrocarbon contamination revealed geographically widespread contamination within the spill areas both inside and outside Prince William Sound (Short et al., 1993; Short and Harris, 1996b; Trowbridge et al., 1998). Fourthly, while the levels of tissue contamination from petroleum hydrocarbons in mussels and clams declined over time from 1989 to 1990 and beyond, oiling persisted in many mussel beds. Ebert

14

CHARLES H. PETERSON

and Lees (1996) reported sampling data from mid-intertidal mussel beds in Prince William Sound showing that mean PAH concentrations averaged over the years of 1990-1993 increased from unoiled to oiled-but- untreated to oiled-and-hot-water-washed mussel beds. Pools of only partially weathered oil remained at least until 1996 in the sediments below and among the mats of mussel byssus and cobbles and fine sediments. This oil is protected from weathering processes by the shield of overlying rock, sediment, mussels and byssus threads (Babcock et al., 1996, 1997; Boehm et al., 1996; Harris et al., 1996; Cads et al., 2000). During shoreline treatment, dense mussel beds were generally not subjected to application of pressurized hot-water wash for fear of killing large quantities of the mussel resource known to be of high value to nearshore predators (Harris et al., 1996). Nonetheless, one of the surprises of the spill was the realization in 1991 that many mussel beds still contained relatively high concentrations of oiled sediments, oiled mussels and only partially weathered oil that included some of the more toxic constituents (Babcock et al., 1996). Sediments in 31 oiled mussel beds in Prince William Sound targeted for sampling in 1992 and 1993, because of suspected lingering contamination, contained hydrocarbon (TPH) levels greater than 10 000/zg g-1 wet weight. Five of 18 beds sampled along the Kenai Peninsula had TPH concentrations above 5000/~g g-1 wet weight of sediments. Sampling of the mussel tissues also showed contamination, revealed by PAH fingerprinting to be "Exxon Valdez" oil: concentrations in mussels were about two orders of magnitude lower than in the sediments (Babcock et al., 1996; Harris et al., 1996). Spatial contrasts of the covariance of oiled sediments and mussels demonstrated tremendous patchiness of oiling on even fine scales within the beds (Boehm et al., 1996; Harris et al., 1996). Furthermore, while there existed some correlation between sediment oiling and mussel contamination within beds, the relationship was far stronger among beds. The similarity in composition of the oil in the sediments, in the mussels, and in "Exxon Valdez" crude, combined with the spatial correlations between oiled sediments and oiled mussels, indicates that the oil was continuing to be released from the sediments to contaminate the overlying mussels (Harris et al., 1996). Because mussels depurate petroleum hydrocarbons relatively rapidly, the contamination must have been ongoing and the oil itself was barely weathered, with a PAH composition in sediments resembling week-old "Exxon Valdez" oil (Harris et al., 1996). Repeated sampling of selected oiled mussel beds from 1992-1995 showed that contamination in both the underlying substratum and the overlying mussels diminished at a slow rate. Only about half the beds exhibited significant declines in hydrocarbon concentration at rates that would reach background levels within about 10 years (Babcock et al., 1997;

EFFECTS OF "EXXON VALDEZ" OIL SPILL

15

Carls et al., 2000). Unfortunately, the spatial patchiness of oil within the mussel beds produced high variance and low power to estimate precise times to reach background concentrations. Because reduction of oil levels was observed to be so slow in several oiled mussel beds in highly protected areas, various novel clean-up technologies were directed towards these problem mussel beds in 1993 and 1994. Trenching within the bed failed to induce reduction in hydrocarbon levels anywhere except in the trench itself. Temporary removal of the mussel layer followed by replacement of underlying sediments with clean sediments and then return of the mussels was effective in a short-term assessment a few weeks after treatment (Babcock et al., 1997). Over longer time periods, this technique may prove ineffective if it fails to reduce the subtidal pools of oil sufficiently to prevent recontamination by horizontal movement of subsurface oil. The ecological significance of intertidal reservoirs of partially weathered oil that continued for several years to contaminate overlying mussels, and presumably other nearby suspension feeders such as clams, may be substantial. The mussel (Mytilus trossulus), and to a slightly lesser degree the littleneck clam (Protothaca staminea (Conrad)), butter clam (Saxidomus giganteus (Deshayes)), cockle ( Clinocardium nuttallii (Conrad)) and razor clam (Siliqua patula (Dixon)), represent what could be termed the "universal prey" of the intertidal ecosystem. The mussels and these clams are among the most important prey resources for many valued mammals, such as brown bears (Ursus arctus L.), black bears (Ursus americanus Pallas), sea otters (Enhydra lutris L.), and humans, ducks such as harlequin (Histrionicus histrionicus (L.)), surf scoter (Melanitta perspicillata (L.)), other scoters (Melanitta spp.), goldeneyes (Bucephala spp.), oldsquaw (Clangula hyemalis L.), and shorebirds, such as black oystercatcher (Haematopus bachmani Audubon), surf bird (Aphriza virgata (Gmelin)), and black turnstone (Arenaria melanocephala (Vigors)) (Vermeer, 1981; G6tmark, 1984; Hood and Zimmerman, 1986; Irons et al., 1986; Marsh, 1986). In addition, the mussels and clams are important prey for many invertebrate consumers, including several species of seastars, whelks, octopus and crabs (Kitching and Ebling, 1967; Dayton, 1971; Menge, 1972; Fotheringham, 1974). Mussels are a prominent component of the diet of several demersal fishes whose juveniles forage in intertidal habitats. Consequently, the contamination of mussels and clams introduced relatively unweathered oil from the "Exxon Valdez" into important intertidal food chains, and this process continued at least until 1993, and even into 1996 where no clean-up was done (Babcock et al., 1997). Boehm et al. (1996) computed estimates (only 2-3%) of the proportion of contaminated mussels in two of the bays containing oiled mussel beds, but such a calculation ignores the tendency of predators to forage preferentially in protected areas and where mussel densities are

16

CHARLES H. PETERSON

high. I discuss below the potential ecological significance of indirect effects produced by contamination of mussels and other invertebrate prey.

3.2. 3.2.1.

Changes in species abundances and community composition of rocky shores Rocky intertidal community organization

The rocky intertidal ecosystem is probably one of the best known natural communities on earth (ConneU, 1972; Underwood and Denley, 1984; Menge, 1995). Marine ecologists realized over 30 years ago that this system is well suited to experimentation because the habitat is accessible and basically two-dimensional, the organisms are easily observed and they can be manipulated. Consequently, we know a lot about the complex of processes and intense interactions involved in determining patterns of distribution and abundance of rocky intertidal organisms (Branch, 1981; Rafaelli and Hawkins, 1996). Plants and animals of temperate rocky shores exhibit strong patterns of vertical zonation in the intertidal zone. Physical stresses tend to limit the upper distributions of species populations and to be more important higher onshore, whereas competition for space and predation tend to limit distributions lower on the shore (Connell, 1961, 1972). Predation by shorebirds like oystercatchers can also serve to limit the upward extension of some intertidal invertebrates (Raffaelli and Hawkins, 1996). Surface space for attachment is potentially limiting to both plants and animals in the rocky intertidal. In the absence of disturbance, space becomes actually limiting and competition for that limited space results in exclusion of inferior competitors and monopolization of space by a competitive dominant (Paine, 1966; Dayton, 1971; Peterson, 1979). Physical disturbance, biological disturbance and recruitment limitation are all processes that can serve to maintain densities below the level at which competitive exclusion occurs (Menge and Sutherland, 1987). Because of the importance of such strong biological interactions in determining the community structure and dynamics in this system, changes in abundance of certain species can produce intense direct and indirect effects on other species that can influence other components of the ecosystem (Paine, 1966; Menge et al., 1994; Wootton, 1994; Menge, 1995). Intertidal communities are open to utilization by consumers from other systems. The great extent and importance of this habitat as a feeding ground for major marine, terrestrial, and aerial predators render the intertidal system a key to integrating understanding of the damages and responses of the entire coastal ecosystem (see papers in Hood and Zimmerman, 1986). The intertidal habitats of Prince William Sound and

EFFECTS OF "EXXON VALDEZ" OIL SPILL

17

the adjacent geographical areas affected by the "Exxon Valdez" oil spill are critically important feeding grounds for many important mobile consumer species. There are fully marine forms, such as sea otters, juvenile Dungeness (Cancer magister Dana) and other crabs, juvenile shrimps (Pandalus spp.), rockfishes (Sebastes spp.), cod (Gadus macrocephalus Tilesius), cut-throat trout (Oncorhynchus clarki (Richardson)), Dolly Varden char (Salvelinus malma (Walbaum)) and juvenile fishes of other stocks that are exploited commercially, recreationally, and for subsistence, including pink salmon (Oncorhynchus gorbuscha Walbaum). Terrestrial forms include brown bears, black bears, river otters (Lutra canadensis Schreber), Sitka black-tailed deer (Odocoileus hemionus sitkensis (Meriam)), and humans. Avian species include the black oystercatcher and other shorebirds, several gulls (Larus spp.), harlequin duck, surf scoter (Melanitta perspecillata), goldeneyes, other ducks, and the bald eagle (Haliaeetus leucocephalus (L.)). Thus, the intertidal habitat provides vital ecosystem services in the form of prey resources for all coastal habitats, as well as commercial, and subsistence harvesting of shellfishes and aesthetic, cultural, and recreational opportunities. 3.2.2. Impacts of the oil spill on rocky intertidal biota The studies by the Hazardous Materials Response and Assessment Division of NOAA (Hazmat) and initial Exxon-sponsored studies of short-term (3-10 days) impacts of the beach treatments done to displace oil from intertidal shores demonstrated very high rates of mortality of both plants and animals from application of high-pressure hot-water washing (Table 3; see also Figure 2). This treatment was applied over a large fraction of the oiled shoreline in wave-protected habitats (Houghton et al., 1996b; Lees et al., 1996). Injury included high mortality of the brown alga Fucus gardneri Silva and the mussels, two of the functionally most important organisms of the local intertidal community. The Fucus provides habitat and the mussel is both habitat provider and prey. Other shoreline treatments, including chemical applications (Table 3), had smaller impacts (Lees et al., 1996). These observations of the treatment processes can be taken together with the results of experimental testing of the short-term impacts to help interpret the data on long-term consequences of the spill. This is particularly useful for the assessments of rocky shore community composition in Prince William Sound done by NOAA Hazmat over several years following the spill (Houghton et al., 1996a, b, 1997a, b; Coats et al., 1999). By categorizing sites as either unoiled, oiled and treated, or oiled and untreated, the NOAA study provided the only means of separating effects of oiling from those of shoreline treatment, which are confounded on most

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EFFECTS OF " E X X O N VALDEZ" OIL SPILL

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protected shores in all other data sets. The Hazmat study revealed that shoreline treatment caused greater reductions in abundance and cover of intertidal plants and animals than the oil alone and delayed the pace of recovery relative to untreated shores (Houghton et al., 1996b, 1997a). By July 1991, epibiotic communities on oiled but untreated rocky shores were essentially indistinguishable from unoiled, control shores, whereas some oiled and treated shores continued to exhibit differences into summer 1995. Even those oiled and treated shores that had converged in community composition with control shores by 1992 revealed massive mortality of Fucus gardneri in 1994 and 1995 (Paine et al., 1996; Houghton et al., 1997b: Figure 3). This long-term cycle of changes in cover of Fucus on oiled and treated shores has been interpreted as a possible consequence of the induction of an almost single-aged stand of Fucus on oiled shores by the extensive denuding of the shore, such that natural senility and longevity constraints then affected virtually the entire local population simultaneously (Paine et al., 1996; Houghton et al., 1997b). The control shorelines with mixed age distributions of Fucus did not exhibit such cyclic instability because not all individuals were senescing in synchrony. Such cycles could persist for many more years before becoming damped by gradual attainment of broader age distributions. Long-term

20

CHARLES H. PETERSON

studies of the shoreline communities after the "Torrey Canyon" oil spill in Cornwall likewise demonstrated cyclic damping of re-colonization by Fucus, limpets and barnacles. These cycles were driven by intense biological interactions and delayed full recovery for 10-15 years (Southward and Southward, 1978; Hawkins and Hartnoll, 1983; Hawkins and Southward, 1992). The other major studies (by the government-funded scientists: Highsmith et al., 1996; and by Exxon: GilfiUan et al., 1995a, b) of oil spill response and recovery of intertidal epibiota of rocky shores evaluated the joint and confounded effects of the oil plus the shoreline treatment. These studies are characterized broadly by their tremendous geographical scope (covering not only most of Prince William Sound but also the Kenai Peninsula-Cook Inlet region and the Kodiak archipelago-Alaska Peninsula region: see Figure 1) and their coverage of multiple geomorphologic habitats. They also include some major inconsistencies, which can be best understood as the results of differing methodologies that reduced the statistical power and general ability of the Exxon-funded studies to detect many large effects of the oil spill (Peterson et al., 2000). Consequently, this review of impacts to the rocky shore biota will draw most heavily from the government-sponsored studies. All of the studies of shoreline habitats and resources lacked pre-spill information and used contrasts of oiled to unoiled segments of shoreline to assess effects of the spill. Such contrasts run the risk of confounding natural pre-existing differences with spill-induced differences because they lack the before-after control-impact design (BACI) that allows isolation of impacts (Stewart-Oaten et al., 1986). This design limitation injects some additional uncertainty in the conclusions. The most viable practical means of isolating pre-existing spatial differences from spill impacts under these conditions is to follow recovery until natural pre-existing differences can be assumed to have been restored, thereby allowing adjustment of estimates of injury. In some cases (Jewett et al. 1999), such convergence of species abundances on oiled and unoiled shores did take place, allowing the degree of natural site variability to be estimated. For the governmentsupported studies of intertidal and shallow subtidal shores, the most likely bias is the failure of the oil to beach at random in relation to exposure to current flow regime (Laur and Haldorson, 1996; Highsmith et al., 1997). The oiled shores tended to be those exposed to greater current flux (and thus greater risk of oil exposure). This has the effect of making most estimates of injury conservative in that higher flows imply greater larval delivery, greater recruitment and higher growth rates, processes that would tend to make these oiled shorelines naturally more productive. Higher flows at oiled shores would also help enhance rates of recovery after the spill.

EFFECTS OF "EXXON VALDEZ" OIL SPILL

21

The field assessments of impacts on the intertidal biota of rocky shores were grouped by geographic area (Prince William Sound vs. Gulf of Alaska or vs. Kenai Peninsula-lower Cook Inlet and vs. Kodiak archipelagoAlaska Peninsula), by geomorphological habitat, and by elevation on shore. Because oil quantity and quality varied among strata, because removal rate of oil varied, and because biota varied among strata, the impacts of the oiling and subsequent shoreline treatment differed among combinations of these strata in complex ways that make overall generalization difficult. Nevertheless, the major responses of the biota follow certain patterns. Every stratum experienced some detectable impact of the oil spill, meaning that the geography of impact was extremely wide-ranging, that no habitat type enjoyed immunity from spill effects, and that all levels on shore showed some degree of response. Stekoll et al. (1996) made comparisons using a simple measure of the percentage of all individual species tested that showed significant responses to the oil spill. About 12-15% of tests showed significance, pooling results across all three geographic regions, but Prince William Sound and Kodiak-Alaska Peninsula differed from Kenai-lower Cook Inlet by exhibiting more dominantly negative changes (reductions) in density. The percentage of species tests showing significance did not vary much among habitats, with about 11-17% of tests showing significance, of which about two-thirds represent reduced densities at oiled sites. The magnitudes of responses (Highsmith et al., 1996) imply some differences among habitats, with estuarine habitats responding with the largest declines and wave-exposed rocky shores with the generally smallest declines. There was not a large difference among the three vertical elevations examined, with a range of 12-17% of species tests showing significant responses to the oil spill. The highest percentage occurred at the mid-tide level (the second meter of vertical drop) and the lowest at the lowest tidal level (the third meter of drop). Changes at the high and mid elevations tended to represent abundance declines more often than at the lowest elevation. There were many differences in the way the oil spill influenced rocky intertidal biota, depending on geographic areas, habitats, tide levels, and sampling dates (Highsmith et al., 1996; Stekoll et al., 1996). However, some general patterns emerged that allow a characterization of the typical changes in abundance or cover of dominant species and in community composition (Figure 4). Not only have direct acute effects of oiling and treatment been documented but also indirect and chronic delayed effects (Table 4). Cover, abundance and biomass of the F u c u s were generally reduced greatly at oiled sites (Highsmith et al., 1996; Houghton et al., 1996b; Stekoll et al., 1996; van Tamelen et al., 1997). This is consistent with the massive short-term F u c u s mortality following pressurized hot-water

22

CHARLES H. PETERSON Balanus glandula MVD 1

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23

EFFECTS OF "EXXON VALDEZ" OIL SPILL Mussels MVD 1

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treatment (Houghton et al., 1996b; Lees et al., 1996: Table 3). It is also consistent with results of some previous oil spills that showed the sensitivity of Fucus to oil (Thomas, 1973, 1978). Ordinarily, Fucus gardneri represents a dominant occupier of space in the high and often the mid intertidal zones in these rocky habitats. With its removal, bare rock space became much more prevalent (Figure 4). Recovery of Fucus cover has generally occurred from low to high on shore (Stekoll and Deysher, 1996; van Tamelen and Stekoll, 1996a), with recovery in the high intertidal incomplete by 1995 (van Tamelen et al., 1997). The second divergence of oiled and reference shores observed to begin in 1994 in the N O A A Hazmat recovery monitoring (Houghton et al., 1997a, b) implies the potential for continued delay in achieving complete recovery of Fucus in the rocky intertidal of the spill area (Figure 3). Several process-orientated studies were conducted in Herring Bay in Prince William Sound to evaluate the mechanisms by which Fucus recovery occurs and the limitations to recovery rate (DeVogelaere and Foster, 1994; van Tamelen and Stekoll, 1995, 1996a, b; van Tamelen et al., 1997). The immediate effect of the oiling and shoreline treatment was to reduce not only total abundance but also the number of fertile Fucus

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EFFECTS OF "EXXON VALDEZ" OIL SPILL

25

plants on oiled shores. Because Fucus gardneri egg dispersal is limited to a distance of about 1 m from the adult plant, actual rates of recruitment of zygotes were significantly depressed on oiled rocky shores for about 3 years (van Tamelen et al., 1997). Newly recruited Fucus gardneri plants are very sensitive to desiccation, which is reduced under and near the canopy of adult Fucus plants (van Tamelen et al., 1997). The combination of reduction in egg and zygote arrival with distance from mature Fucus and the lower survival of recruits away from the cover of adult plants led to the observed pattern of recovery that was more rapid lower on shore. The "Exxon Valdez" oil spill caused at least modest "greening" of the shore (Houghton et al., 1996b; Stekoll et al., 1996; van Tamelen and Stekoll, 1996a), typical of some other well-documented oil spills (Southward and Southward, 1978; Southward, 1982; Kingston et al., 1997). "Greening" is a reflection of rapid colonization of rock space by annual ephemeral algae, including many green algae, early in the process of succession (Sousa, 1979) during recovery. The typical explosion of green algae after an oil spill is much facilitated by the removal of grazing gastropods, as in the limpet collapse documented after the "Torrey Canyon" spill (Southward and Southward, 1978). The limited evidence of massive growth of ephemeral algae in the early recovery phase after the "Exxon Valdez" spill is somewhat surprising given that there was a large reduction of herbivorous invertebrates in rocky habitats (Highsmith et al., 1996). Caging experiments conducted to explore the implications of reduced grazer abundances did not reveal dramatic increases in algal cover when grazers were excluded (Highsmith et al., 1997; van Tamelen et al., 1997), but these experiments may have been conducted after the spring season of algal recruitment. Perhaps predation by the shorebirds, ducks and invertebrates is sufficient in this system to maintain grazer densities at a level where they cannot normally control algal abundance. However, this speculation has not been tested (however, see Dethier and Duggins, 1988). Alternatively, the small number of quantitative observations in spring 1989 immediately after the spill implies that little evaluation actually took place during the time when this response would have been expected to be strongest. If the enhancement of annual algae demonstrated in 1990 by van Tamelen and Stekoll (1996a) represents only a fraction of the response in 1989, then there may have been a high degree of shoreline greening. The degree of greening that was documented in 1990 after the "Exxon Valdez" oil spill more closely resembled the response to the "Amoco Cadiz" spill in Brittany than to the "Torrey Canyon" spill (Floc'h and Diouris, 1980). The use of toxic oil-spill removers ("detergents") after the "Torrey Canyon" oil-spill (Smith, 1968) led to greater mortality of grazers than occurred after the "Amoco Cadiz" or the "Exxon Valdez" spills.

26

CHARLES H. PETERSON

In addition to the evidence in this system for the importance of indirect oil spill effects resulting from the loss of Fucus gardneri, which opened up space for colonization by opportunistic algae, other indirect effects involving Fucus were found (Table 4). At low intertidal sites on the Kenai coast (Highsmith et al., 1996) and at some sites in Prince William Sound (Houghton et al., 1997a), Fucus gardneri increased in abundance and filled available space by 1990 or 1991. This increase effectively prevented return of Alaria spp. and some perennial red algae that are characteristic dominants of the lower intertidal on unoiled control shores (Figure 5). Such inhibition of progress towards the climax successional state is not uncommon on rocky shores (Sousa, 1979). In this case, the consequence was a replacement of one typical set of dominants (Alaria and the red algae) by a perennial canopy-forming alga (Fucus gardneri). Subsequent occupation of space by a long-lived species implies a further time lag in completing the convergence of lower intertidal communities on oiled and control shores of the Kenai coast, but no assessments have been made since summer 1991 to test this prediction. Like the algae, the invertebrates of the rocky shores exhibited a generally large decline in abundance, cover and biomass at oiled sites in all three geographic regions, in all geomorphologic habitats and at all elevations (Highsmith et al., 1996; Hooten and Highsmith, 1996; Houghton et al., 1996b). Although differences in response occurred with area, habitat and tide level, some strong direct and indirect or chronic delayed responses were seen across various sampling strata (Figure 3; Table 4). The limpet Tectura persona (Rathke) was greatly reduced by the oil spill in the high intertidal elevation where it normally dominates the grazer assemblage (Highsmith et al., 1996). Mussels were also generally reduced in abundance by oiling and shoreline treatment, despite the decision not to treat dense mussel beds aggressively during shoreline clean-up programs in 1989-91 (Highsmith et al., 1996). Barnacles exhibited complementary patterns across species in their response to the oil spill. The longer-lived Semibalanus balanoides (L.) was generally reduced in abundance on oiled shores, as was another long-lived balanoid, Balanus glandula Darwin, in Prince William Sound and Kodiak-Alaska Peninsula (Highsmith et al., 1996). Probably in response to a competitive release and thus an indirect effect of available space created by the loss of balanoid barnacles and of Fucus gardneri, the opportunistic barnacle Chthamalus daUi Pilsbry increased dramatically on oiled shores (Highsmith et al., 1996). The explosion of Chthamalus dalli was probably also facilitated by two other indirect effects of the spill. The large reduction in limpet abundance lowered the intensity of radular rasping disturbance on the rock surfaces and probably enhanced survival of newly recruiting barnacles (Dayton, 1971). In addition, the reduction in abundance of predatory gastropods

27

EFFECTS OF "EXXON VALDEZ" OIL SPILL unoiled sites 100. 410,

¢,

80 40 20 0

100

oiled and not cleaned sites

80, 6C

>

o o

40, 20 0

[ ] red algae • Fucus >

0 o

1990

1991

1992

July

Figure 5 Algal cover of rock surfaces in the lower intertidal as a function of oiling and treatment history. Plots illustrate the expansion of Fucus gardneri on shores that were oiled and treated by pressurized hot water and the consequent pre-emption of space that prevented rapid recovery of the red algae typical of that level. Data are taken from the NOAA Hazmat study of Prince William Sound (Houghton et al., 1997a) and represent means of all sheltered rocky sites studied. like Nucella lamellosa (Gmelin) (Ebert and Lees, 1996), which can control barnacle densities, must have enhanced survival of juvenile and adult barnacles. Thus, the sequence of recovery of barnacles before limpets reversed the pattern seen following the "Torrey Canyon" spill (Southward and Southward, 1978). However, on shores affected by the "Torrey C a n y o n " clean-up there was a later decline of limpets when the adult population became too large for the algal resources, and this opened up an opportunity for dense barnacle settlement. The grazing periwinkle Littorina sitkana Philippi generally exhibited higher abundances on unoiled reference shores, although the opposite pattern often prevailed

28

CHARLES H. PETERSON

in the coarse-textured habitat in the Kenai-lower Cook Inlet region (Highsmith et al., 1996). A congener, Littorina scutulata Gould, exhibited many significant responses to the oil spill, but the direction of the effect on its abundance was not consistent (Highsmith et al., 1996). Littorina scutulata produces planktonic larvae, whereas Littorina sitkana is a direct developer producing live crawl-away young. The lack of a consistent pattern of depression in density of Littorina scutulata on oiled shores in 1990 and 1991 may reflect its ability to re-colonize from the planktonic larvae (Highsmith et al., 1996), thus providing good recovery. Analogous early recolonization of littorinids from planktonic larvae occurred on the Cornish coast after the "Torrey Canyon" spill, where species with direct development were much slower to recover (Southward and Southward, 1978). Many of the observed differences in invertebrate abundance narrowed with time from spring 1990 to summer 1991, implying ongoing recovery (Highsmith et al., 1996). The predatory invertebrates of the rocky intertidal zone were not abundant enough in the random samples of this system to allow reliable testing for oil spill effects. Ebert and Lees (1996) did, however, show that the Nucella lamellosa disappeared in markrecapture studies carried out from 1991 to 1992 at higher rates on oiled than on unoiled shores and grew at lower rates on those oiled shores. The higher disappearance rate indicates either higher residual mortality or greater emigration, either cause operating even 2-3 years after the spill. The mechanisms by which the invertebrates of the rocky intertidal shores were affected by the oil spill are not clearly distinguishable. Judging from the short-term demonstrations of mortality of many invertebrates from pressurized hot-water treatments (Houghton et al., 1996b; Lees et al., 1996), much of the immediate loss of animals was probably a consequence of invasive shoreline treatment. Toxicity may have played a role, along with the physical effects of smothering under a layer of oil. However, indirect effects may also have been involved. Experimental removal of the Fucus canopy in Herring Bay on Knight Island was followed by declines in abundance of several rocky shore invertebrates, including the limpet Tectura persona and the periwinkle Littorina sitkana (Highsmith et al., 1997). The fucoid alga evidently provides protection against desiccation and detection by predators. To the degree that such effects of habitat loss determined the abundance of rocky shore invertebrates, recovery of those animals was also delayed by the slow return of the Fucus. This process was demonstrated through experiment by Highsmith et al. (1996) as it affected the limpets and periwinkles that live under and around the Fucus canopy. However, no evaluation was attempted of effects on small mobile crustaceans that also use macroalgae as critical habitat and which are themselves of such value to foraging fishes. Nevertheless, large reductions

EFFECTS OF "EXXON VALDEZ" OIL SPILL

29

in Fucus-associated crustaceans, analogous to the declines in gammarid amphipods and the isopods Idotea spp. and Jaera spp. that followed the "Irini" crude oil spill in Sweden (Notini, 1978), may have occurred after the "Exxon Valdez". Loss of Mytilus also represents a depression in available biogenic habitat that may have affected small invertebrates that live among the byssus threads (Suchanek, 1985), but no study evaluated that possible indirect response. The recovery of Fucus was itself inhibited by an indirect effect involving massive settlement of Chthamalus dalli barnacles (van Tamelen and Stekoll, 1996b). Many Fucus recruits attached to Chthamalus barnacle tests instead of to bare rock or balanoid barnacle tests. Through wave action, those attached to barnacle tests were readily dislodged before the plants could reach maturity (van Tamelen et al., 1997). This loss of Fucus recruits was a consequence of the instability of the substratum to which they were attached, an instability likely to have been enhanced by the substitution of chthamaloid barnacles for Balanus glandula. Chthamalus attaches with a membranous base instead of the more durable calcium carbonate basis secreted by Balanus glandula. Hawkins et al. (1992) describe an analogous instability created for fucoid algae attaching to tests of Semibalanus balanoides, which also has a membranous base.

3.2.3.

Impacts of the oil spill on intertidal biota of sedimentary environments

The oiling of intertidal beaches altered the microbial community in the sediments. Total counts of bacteria per unit weight of sediment were not significantly affected, but counts of hydrocarbon-degrading bacteria were definitely enhanced at two oiled beaches when compared with two control shores (Braddock et al., 1996). The application of fertilizers (bioremediation) in water-soluble form (CUSTOMBLEN) and in oleophilic form (INIPOL) stimulated counts of hydrocarbon-degrading bacteria and increased hexadecane and phenanthrene mineralization potential (Lindstrom et al., 1991). The importance to higher trophic levels of this increase of microbial hydrocarbon degraders was not well established by the field studies. Coffin et al. (1997) used isotope ratios to trace the fate of carbon and nitrogen from the bioremediation fertilizers. They were able to show uptake by bacteria in microcosm experiments but no clear isotopic signal in fieldcollected bacteria at one site in summer 1990 and no isotopic evidence of transfer to higher trophic levels. However, the barnacles, limpets and whelks examined by these workers are not the most likely primary consumers of sediment microbes. They are rocky shore species with diets

CHARLESH.PETERSON

30

6000"

MVD1

~

4000.

2000. 0, 3000.

MVD2 40006A 0008°°~ ~

G

2000 0 sooIo

j

~MVD3 13

control sites

• oiled sites 4000 3000 ~tc-k 2 0 0 0 ~ 1000 0 1989 1990 1990 1991 September

June

August

June

Figure 6 Mean densities (no. m -2) of oligochaetes over 1989-91 (June) at all coarse-textured sites in Prince William Sound at each of three levels (MVD 1-3). Data from the Coastal Habitat Injury Assessment study of the "Exxon Valdez" Oil Spill Trustee Council. Stars (* P<0.10; ** P<0.05; *** P<0.01) indicate statistically significant differences between oiled and unoiled control sites (data from Highsmith et al., 1994).

composed of planktonic microalgae, microalgae attached to rock surfaces and rocky-shore invertebrates, respectively. Ebert and Lees (1996) also failed to show any biomagnification or significantly increased concentration of PAHs in the whelk Nucella lamellosa, although there was a trend of higher concentrations on oiled than on unoiled shores averaged over 1990-1993. Field studies that sampled intertidal sediments after the oil spill did identify a widespread and substantial (often by an order of magnitude) enhancement of oligochaete worms (Gilfillan et al., 1995a; Highsmith et al., 1996), a group that is quite likely to include sedimentary microbes in its diet. Given previous compelling demonstrations that petroleum hydrocarbons can enter into food chains involving sedimentary

EFFECTS OF "EXXON VALDEZ" OIL SPILL

31

deposit feeders (Spies and DesMarais, 1983), it seems reasonable to conclude that the enhancement of production by oil-degrading microbes translated into increased production of some sedimentary deposit feeders, including especially oligochaetes in intertidal sediments. This occurred with a time lag, not appearing until late summer 1990, as would be expected from an indirect effect (Figure 6). Besides acting as an organic carbon source for microbes, the oil and subsequent shoreline treatments also caused a physical and chemical disturbance to the sedimentary animals of oiled intertidal beaches. Direct observations of the short-term effects of high-pressure hydraulic washing of intertidal sedimentary shores showed that the sediments themselves were transported down slope, thereby changing the nature of the habitat (Driskell et al., 1996; Coats et al., 1999). Important species such as the clams Protothaca staminea and S a x i d o m u s giganteus were immediately reduced in abundance by hydraulic washing: the presence of dead and moribund clams on treated beaches implies that they may have suffered toxic effects as well, but that is unconfirmed (Lees et al., 1996). Nevertheless, the multiple-year surveys by the N O A A Hazmat group demonstrated lower densities of these two clams and lowered recruitment through at least 1998 on oiled and treated beaches as compared with unoiled or oiled and untreated beaches (Houghton et al., 1993, 1996b, 1997a; Shigenaka et al., 1999: Figure 7). The total abundance, diversity and composition of sedimentary communities on intertidal beaches changed significantly after the oil spill (Table 5). Oiled and treated beaches showed lower abundance and diversity and incomplete recovery even by 1997, while oiled and untreated beaches converged with unoiled beaches by about 1992 (Driskell et al., 1996; Coats et al., 1999). The toxicity of oiled intertidal sediments of Prince William Sound, as shown by amphipod bioassays in 1989 and 1990 (Gilfillan et al., 1995b), 1990 and 1991 (Boehm et al., 1995; Wolfe et al., 1996), implies that some of the initial impact of the oil spill on this soft-sediment system was chemical. However, the rapid convergence of infaunal communities on oiled-but-untreated beaches and control beaches, in contrast to the persistent differences on oiled-and-treated beaches, seems more likely related to the differences in physical sedimentary habitat, with the deficit in fine sediments being a consequence of hydraulic washing. Densities of infaunal invertebrates on hot-water-treated sedimentary intertidal shores appear to have stabilized, and since about 1992 appear to be changing in parallel with densities on control and oiled-but-untreated shores. In consequence, Coats et al. (1999) argue that complete recovery may have occurred despite the 70% depression in infaunal abundance on shores subjected to pressurized washing. However, they also show a

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33

EFFECTS OF "EXXON VALDEZ" OIL SPILL

Littleneck clams 5O

40

30

20

10

1990

1991 July

1992

Butter clams 6 S 4

~ot oiled )lied

3

)lied and cleaned

2 1 0

1990

1991

1992

July Figure 7 Densities, as numbers 0.25 m -2, of the two largest and more important clam species in the lower intertidal zone at sites sampled in Prince William Sound from 1990-92 by the NOAA Hazmat study. Statistical analysis confirmed a significant effect of pressurized hot water treatment, which reduced the abundance of both clams (after Houghton et al., 1996a).

substantial deficit in fine sediments on these treated shores persisting until the last sampling in 1997. From the field observations on massive sediment erosion and down-slope transport that accompanied pressurized washing (Driskell et al., 1996; Houghton et al., 1996b), and the ongoing deficit in fine sediments on washed beaches (Coats et al., 1999), the most likely explanation for continuing low clam and other infaunal densities on washed beaches is that recovery is inhibited by the deficit in fine sediments. The absence of pre-spill information on beach sediments and on infaunal densities complicates this interpretation, suggesting that monitoring for eventual convergence is the best means of resolving to what degree the remaining differences are related to pressurized washing. Parallelism in year-to-year dynamics is insufficient evidence on which to conclude recovery in the absence of convergence.

34

CHARLES H. PETERSON

25O

Shoot Dens it)' 0C=0.27, Yr=0.12, Int=O.05

.200

,50 100 50 I 19(19 1990

12

l

I

1991

1992

I

1~3

!

I

1994

1996

I

I

Flowering Shoot Density OC=0.02. Yr<0.01. Int=0.13

10 E

8

6 8

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4

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1969

1990

'1

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1¢JG1 1992 1993 Y~r

1994 1995

Figure 8 Densities (_+SE) of shoots (turions) and flowering shoots of eelgrass inside eelgrass meadows averaged across all oiled (black squares) or all unoiled (open circles) control sites from 1990-95. ANOVA results are shown above each graph for oiling and year and their interaction (after Dean et al., 1998).

4.

4.1.

BIOLOGICAL CONSEQUENCES OF THE OIL SPILL IN THE SUBTIDAL ZONE Effects on eelgrass communities

Two studies evaluated the impact of the oil spill on eelgrass (Zostera marina L.) within Prince William Sound. Eelgrass is of substantial ecological importance as a structural habitat for a variety of marine animals. Both studies demonstrated negative but not catastrophic impacts on the eelgrass. Dean et al. (1998) reported evidence of significantly

EFFECTS OF "EXXON VALDEZ" OIL SPILL

35

reduced turion (non-flowering shoot) densities and reduction in densities of flowering shoots by 10-60% at oiled sites in the initial three years of their study: 1990, 1991 and 1993 (Figure 8). By 1995, the oiled sites demonstrated recovery in both of these parameters. Houghton et al. (1993) also reported very similar effects of the oil spill on turion and flowering shoot densities, providing independent confirmation of this response in an important habitat-providing plant. The spatial and temporal patterns in eelgrass turion and flowering shoot density followed very closely the patterns of hydrocarbon concentrations in the sediments. In 1990, total PAH concentrations averaged 5400 ng g-1 at 6-20 m depth and 5000 ng g-1 at <3 m depth in oiled eelgrass sites, as compared with 1300ngg -1 at unoiled 6-20m sites and 600ngg -l at unoiled <3 m sites (Dean et al., 1998; Jewett et al., 1999). By 1993, total polycyclic aromatic hydrocarbon (TPAH) concentrations at oiled sites had declined below 300 ng g-1 and at unoiled sites to below 60 ng g-1. In 1995 there were no significant differences in TPAH concentrations between oiled and control sites. Chrysene concentrations in the sediments in and below eelgrass beds exhibited an identical pattern in space and time, except that the difference between oiled and control values was still statistically significant in 1995 (Dean et al., 1998; Jewett et al., 1999). Fingerprinting analysis of the PAHs revealed that "Exxon Valdez" oil was a contaminant at the control sites as well as at the oiled sites. This helps explain why hydrocarbon contamination in these shallow subtidal sediments declined over time from 1990 and demonstrates that the mechanism of oil transport (largely by attachment to particles; Bragg and Yang, 1995; Short et al., 1996) distributed the oil over large areas that did not correspond completely to the locations of shoreline oiling. This transport did not confuse statistical tests of oil spill effects because shallow subtidal oiling was significantly more intense adjacent to oiled shorelines, but it does imply that the test values are conservative. The percentage of sediment samples identified as containing "Exxon Valdez" oil declined through time at oiled sites, but the significantly elevated chrysene values imply that "Exxon Valdez" oil from the spill was still involved at least through 1995; chrysenes are present in crude oil but not in diesel oil. Patterns of contamination over time in the eelgrass habitat match the general patterns for shallow subtidal sediments in Prince William Sound (Boehm et al., 1995; O'Clair et al., 1996). Wolfe et al. (1994) estimated that 8-16% of the spilled oil was deposited into shallow subtidal sedimentary habitats less than 20 m in depth. Jewett et al. (1999) also reported results of sampling the soft-bottom invertebrates of the shallow subtidal region in (<3 m depth) and below (6-20m depth) eelgrass beds in Prince William Sound. Multivariate ordination analyses of community composition showed no large effect of

36

CHARLES H. PETERSON

1990 INFAUNA Polychaeta Ampharetidae Amphictenida¢ Capitcllida¢ Lumbrineridae Maldanidae Ner¢idae Opheliidae

6-20 m 1991 1993

<3m

1995

1990

1991

O OO

Corophiidae Isaeidae Phoxocephalidae Echinodcrmata Ophiuroidea EHFAUNA Polychacta Spirorbidae Bivalvia Mytilidae Crustaeea Caprellidae

1995

OO0

0 00 ••

• go

O0 OO0

OO

Polynoidac Sabellidae Sigalionidae Spionidae Syllidae Gastropoda Caecidae Lactmidae Olividae Trochidae Bivalvia Tellinidae Crustacca

1993

•

0 oO

000 •

OO

gO

OO0

•

O0

O0

• oo

•

O0

O0

0 000

000

0 O0 000

OO0 ooo

oo

ooo

0

0

O0 000

000

OOO ooo

ooo

ooo

• •

Figure 9 Analyses of variance of observed differences between oiled and unoiled control sites in abundance of the commoner families of invertebrates in soft sediments in (<3 m) and just deeper than (6-20 m) eelgrass beds in Prince William Sound. Open circles: significantly greater density in unoiled sites. Closed circles: significantly higher density in oiled sites. One symbol implies P<0.10; two symbols P<0.05; and three symbols P<0.01. (Data from Jewett et al., 1999.)

the oil spill on either the epi- or the infaunal assemblage. Nevertheless, chrysene concentration joined sediment size variables as significant predictors that distinguished groups of sites and the data point representing the deep (6-20 m) infauna in 1990 at the most highly contaminated Bay of Isles site was strongly divergent from all other sites. Total density of both infauna and epifauna tended to be greater at oiled sites, with many of the differences statistically significant. However, there was no clear

EFFECTS OF "EXXON VALDEZ" OIL SPILL

37

pattern of convergence over time, with some significant differences occurring in all four years of study (1990, 1991, 1993 and 1995). Analyses of individual families of invertebrates from these shallow subtidal habitats revealed a taxonomic complexity of response to oiling that appears to reflect the joint influence of both toxicity and organic enrichment to deposit-feeding food chains (Figure 9). About half of all families showed a significant response to oiling, with fewer declining and more increasing with oiling (Jewett et al., 1999). The five families with significantly lower densities at oiled sites comprised two amphipod and three bivalve taxa (Figure 9). In 1990, there were very few isaeid or phoxocephalid amphipods in either depth stratum at oiled sites. Densities of these two amphipod families had increased only slightly by 1995, when control sites still possessed an order of magnitude of higher numbers (Jewett et al., 1999). Montacutid, thyasarid and tellinid bivalves were also reduced in abundance at oiled sites: of these three only montacutids demonstrated evidence of convergence by 1995. Several families of polychaetes, two gastropods and one bivalve exhibited significantly higher densities at oiled sites, as in the aftermath of the "Amoco Cadiz" (Conan, 1982), with no indication of convergence by 1995. One epifaunal species, the mussel Musculus sp., was dramatically enhanced in abundance at oiled sites (Table 5). The reduced abundance of amphipods in oiled sites agrees with bioassay results showing greater mortality of these animals in oiled intertidal sediments, and occasionally in oiled subtidal sediments (Boehm et al., 1995; Gilfillan et al., 1995b; Wolfe et al., 1996). This is consistent with the results of previous studies that show amphipods are sensitive to oil spills and they may be slow to recover (Bonsdorff and Nelson, 1981; the "Amoco Cadiz" in Dauvin, 1982, 1987; Dauvin and Gentil, 1990; the "Tsesis" in Linden et al., 1979, Elmgren et al., 1983; and the "Braer" in Kingston et al., 1995). The enhancement of sedimentary polychaetes is consistent with the high incidence of opportunism in that phylum, which has a general ability to respond positively to organic enrichment, even by petroleum hydrocarbons (Pearson and Rosenberg, 1978; Gray, 1982: Conan, 1982; Swartz et al., 1986; Warwick and Clarke, 1993; Peterson et al., 1996). This indirect effect of the spill may result from increased production by hydrocarbon degrading bacteria providing more food for the depositfeeding polychaetes in the sediments around eelgrass beds. However~ there may be alternative indirect effects, such as reduction in predators. Some of the larger predatory invertebrates exhibited depressed abundance in oiled eelgrass habitats (Dean et al., 1996b: Table 5). The seastar Dermasterias imbricata (Grube) and the helmet crab Telmessus cheiragonus (Tilesius) were less abundant in oiled eelgrass beds than in unoiled controls, with no significant time × oiling interaction in a twofactor ANOVA to indicate convergence from 1990, 1991, 1993 to 1995

38

CHARLES H. PETERSON

Telmessus cheiragonus Shallow Bays

Eelgrass

87' 65" 43" 21' 0-

1990

1991

1990

1993

1991

1993

Dermastedas imbrfcata Shallow Bays

Eelgrass

1815-

1

12-

1

963-

01990

1991

1993

1990

1991

1993

Figure 10 Average density as number 100 m -2 (+SE) of the crab Telmessus cheiragonus and the seastar Dermasterias imbricata in oiled (black columns) vs~ unoiled (white columns) control sites, 1990-93, in each of two separate habitats, kelp beds of shallow subtidal bays and eelgrass meadows. In both cases, ANOVA showed significant differences in density between oiled and unoiled control sites in all 1990 and 1991 tests, with recovery proceeding more rapidly by 1993 in the kelp habitat. (Data from Dean et al., 1996b.)

(Dean et al., 1996b). This pattern for the two species matches their responses to oiling in the kelp beds except that the rate of recovery in eelgrass was slower (Figure 10). Densities of the sunflower star Pycnopodia helianthoides (Brandt) were slightly lower in oiled eelgrass beds in 1990 and 1991 but recovered and even overshot control abundances by 1993 and 1995 (Dean et al., 1996b). These responses in the numerically

EFFECTS OF "EXXON VALDEZ" OIL SPILL

39

dominant predatory invertebrates imply that predation rates on shallow subtidal invertebrates may have been reduced for some time after the oil spill and could be partially responsible for the generally higher densities observed in the eelgrass habitats. The observed community response includes the confounded effects of both organic enrichment and also reduction in predation by predatory invertebrates (Table 5). The reduction in echinoderms and crustaceans is also consistent with the general sensitivity of these higher taxa to toxic exposures (Warwick and Clarke, 1993; Peterson et al., 1996). No study evaluated whether small mobile crustaceans and other phytal invertebrates declined in abundance with decreasing eelgrass shoot density, as would be expected from the loss of emergent structural habitat.

4.2.

Effects on deeper benthic systems

Although oil from the "Exxon Valdez" spread out onto the seafloor over a wide region of Prince William Sound and the broader Gulf of Alaska, the deeper water ecosystems did not show substantial impact of the oil spill. Species of clams eaten by sea otters (Humilaria kennerleyi Reeve, Mya arenaria L., Protothaca staminea (Conrad), Saxidomus giganteus (Deshayes) and Serripes groenlandicus (Brugui~re)) were sampled in 1991 from the subtidal shelf around a heavily oiled site near Squirrel Island, a lightly oiled site near Coven Island, and an unoiled site near Stockdale Harbor. These populations did not exhibit any significant site differences (Doroff and Bodkin, 1994). Armstrong et al. (1995) showed that in subtidal bays the scallop Chlamys rubida (Hinds) had elevated tissue PAH concentrations of oil with the signature of the "Exxon Valdez" oil in 1989, but that this difference disappeared by 1990. Sampling of clams (Macoma spp., Yoldia spp. and Nuculana spp.) in 1991 from subtidal bays showed slightly elevated TPAH concentrations in oiled bays but only one heavily oiled site, Bay of Isles, revealed detectable alkylated PAH concentrations suggestive of oil (Armstrong et al., 1995). Most analyses of hydrocarbons in sediments from sites deeper than 40 m failed to detect an "Exxon Valdez" fingerprint and deeper bottoms near oiled shorelines generally did not exhibit higher concentrations of TPAHs than near unoiled shores (O'Clair et al., 1996). Armstrong et al. (1995) did detect elevated PAH concentrations in sediments of heavily oiled bays in Prince William Sound with "Exxon Valdez" oil signatures and showed a trend toward but not reaching convergence in PAH concentrations from 1989 to 1991. Feder and Blanchard (1998) reported results of a 1990 sampling study of the soft-bottom infauna in 14 bays inside Prince William Sound at 40, 100 and >100 m depths. No detectable

40

CHARLES H. PETERSON

response was evident in the infaunal community at depth. Similarly, sampling of deep seafloor sites for mobile crustaceans, including several crabs and shrimps of value as targets of fisheries, was unable to detect any evidence of an impact of the oil spill on abundance (Armstrong et al., 1995). However, no evaluation of impacts on the more sensitive larval stages that occupy near-surface waters was conducted during the season when the oil was floating at the surface. Moreover, the wide dispersal of larvae presumably dilutes any local impact, rendering inconclusive any test of spill impacts that is based upon spatial contrasts within the range of larval dispersal. Analysis of bile of several demersal fishes from subtidal depths at 15-60 m demonstrated that fishes in the subtidal zone did receive exposures to oil from the "Exxon Valdez" spill in 1990 and 1991 (Collier et al., 1996).

4.3.

Effects on kelp communities

Kelps provide an important habitat for fishes and invertebrates and the larger kelps extend to the sea surface, where they could be exposed to direct oiling. An evaluation of the effects of the oil spill on kelps and their associated fauna in Prince William Sound (Dean et al., 1996a, b) examined kelp communities in three different types of rocky subtidal habitats: sheltered bays, moderately exposed points of land and very exposed points. The kelp species composition differed somewhat among these three environments, but they were each dominated by combinations of Nereocystis leutkeana Postels and Ruprecht, Agarum clathratum Dumortier (previously A. cribrosum), Laminaria saccharina (L.) Lamouroux, and L. bongardiana Postel and Ruprecht (previously L. groenlandica). Sampling in summer 1990 revealed no dramatic difference between oiled and control kelp beds: total algal density, biomass and cover were statistically indistinguishable (Dean et al., 1996a). However, a general pattern emerged from these contrasts in which one of the dominant species of kelp typically exhibited significantly higher density on the oiled shores because of a greater number of smaller plants in the population (Table 6). This pattern may reflect recovery of the kelp from losses that were related to either the toxic effects of the oil or the intense boating activity associated with the shoreline treatment and assessment programs (Stekoll et al., 1993; Dean et al., 1996a). Analysis of PAH concentrations in the sediments during sampling in 1990 confirmed that the oiled sites possessed higher than average concentrations (Dean et al., 1996a), implying that the characterization of sites was reasonable. The only invertebrate members of the subtidal kelp communities that were initially assayed for possible response to the oil spill were five

EFFECTS OF "EXXON VALDEZ" OIL SPILL

41

dominant species of seastars and one crab species. Among the seastars, Dermasterias imbricata and Evasterias troschelii (Stimpson) both exhibited significantly lower densities in oiled kelp beds of two types in 1990 (Dean et al., 1996b). No significant differences in abundance were demonstrated for three other seastar species that were common enough to test. Furthermore, the helmet crab Telmessus cheiragonus had an 80% lower density in oiled kelp beds than in unoiled controls in summer 1990. Recovery of both Telmessus and Dermasterias populations was well advanced in 1991 and by 1993 appeared complete in these kelp bed systems (Dean et al., 1996b: Figure 10). Of the other seastars, Pycnopodia helianthoides, exhibited a pattern of generally higher abundances in the oiled kelp beds. Overall, this evaluation of abundances of prominent predatory invertebrates of the kelp bed habitats revealed reduced densities and thus reductions in predation pressure on their invertebrate prey (Table 6) for the first 1-3 years following the oil spill and recovery by 1993. In 1996 and again in 1997, sampling was conducted for green sea urchins (Strongylocentrotus droebachiensis (O.E Mtiller)) along a shoreline of northern Knight Island, where their dominant predator, the sea otter, had barely initiated recovery from a loss of at least 53%, and along Montague Island, where no oiling had taken place and where sea otters were not depressed in abundance (Holland-Bartels et al., 1998; Dean et al., 2000). This sampling in the low intertidal and shallow subtidal zones tests the hypothesis that delayed effects of depressed sea otter abundances may be initiating cascades of indirect interactions in the rocky shore ecosystem. The importance of top-down controls of sea otters in the organization of coastal rocky shore communities is the most predictable and well-established set of indirect effects documented for the nearshore marine ecosystem anywhere in the world. In the absence of sea otters for sufficient time, their favorite prey, the green sea urchin, undergoes a population explosion that results in overgrazing of kelps and other macroalgae, creating urchin barrens (Estes and Palmisano, 1974; Estes et al., 1978; Simenstad et al., 1978; Estes and Duggins, t995). The loss of kelp habitat in these urchin barrens then has the consequence of reducing abundances of the many fishes that use this habitat as nursery. Sampling of low intertidal and shallow subtidal rocky shore habitat at replicate sites along northern Knight Island and Montague in summers of 1996 and 1997 revealed that green sea urchins were significantly larger along northern Knight where numbers of sea otters had remained depressed by about 50% for 7 and 8 years since the oil spill (HollandBartels et al., 1998; Dean et al., 2000). On northern Knight 55% of the urchins were larger than 20 mm in diameter in contrast to only 17% on Montague. However, urchin densities were low on both islands and did

42

CHARLES H. PETERSON

Table 6 Effects of shoreline offing and/or treatment on shallow subtidal algal and invertebrate communities.

Effect

Duration

Source(s)

Direct acute responses

Size distributions of dominant kelps in three habitats abnormally skewed towards recruits in 1990, implying adult mass mortality in 1989 Two seastars (Dermasterias, Evasterias) and one crab ( Telmessus) greatly

1989

Dean et al., 1996a

until 1991, recovered by 1993

Dean et al., 1996b

reduced in density Indirect or chronic delayed responses

Enhanced body size of green sea urchins on northern Knight Island where sea otter density remained depressed until at least 1998, potentially beginning a top-down trophic cascade Possible impacts of reduced predation by seastars and helmet crab on their invertebrate prey

observed in 1996

Holland-Bartels et al., 1998; Dean et al., 2000

not studied

Dean et al., 1996b

not differ significantly. In preferred sea urchin habitat (gently sloping boulder-cobble shores), diver searches in 1996 revealed some patches of aggregated sea urchins. The geometric mean urchin density in these patches of 12.11 m -2 at Knight Island was significantly higher than the 0.42 m -2 on Montague (Dean et al., 2000). The size response is what would be predicted from relaxation in sea otter predation, but the density response implies a very modest indirect effect. The observed densities of sea urchins in 1996 and 1997 are far short of those required to initiate the feeding fronts of urchins that create urchin barrens. Indeed D e a n et al. (2000) reported algal reductions only on very scattered patches where urchin densities exceeded 1 0 m -2. Without further monitoring, it is impossible to know whether this slowly developing indirect effect of the

EFFECTS OF "EXXON VALDEZ" OIL SPILL

43

oil spill on green sea urchins will ever result in the subsequent cascade of indirect effects on kelps and kelp-associated fishes.

5. 5.1.

IMPACTS ON VERTEBRATES THAT USE SHORELINE HABITATS Terrestrial mammals

The scientific literature linking terrestrial mammals to intertidal habitats is limited. Natural history observations identify some examples of foraging in intertidal systems at low tide, such as racoons in the southeast United States feeding on oysters in salt marshes, wild horses grazing on Spartina in salt marshes, and mice foraging on gastropods of rocky shores of the Pacific northwest. The "Exxon Valdez" oil spill helped focus tremendous attention on the shoreline, where the oil served not only as a contaminant but also as a marker of any individual animal that contacted the oiled shoreline habitats. The oil spill helped emphasize the seasonal value of intertidal foraging for three species of terrestrial mammals, Sitka blacktailed deer (Odocoileus hemionus sitkensis), brown bears and black bears. In the supralittoral, above the intertidal zone, total summer production of terrestrial grasses and forbs was substantially lower on oiled shores than on unoiled controls in 1990 (Schimel in Highsmith et al., 1990). This effect was especially evident for the dominant species of grass, rye grass (Elymus sp.), which produced only about half as much biomass on oiled shores. Rye grass is important to the terrestrial ecosystem as food for Sitka blacktailed deer and a variety of terrestrial granivores and herbivores. Schimel's study was restricted to the Kodiak-Alaska Peninsula region and was not continued after 1990. Oil was reported by Schimel and others (Highsmith et al., 1990) in the soils of the supralittoral shores in several oiled sites. Given the general absence of clean-up in this environment and the usually long persistence of oil in subsurface soils, this effect of the oil spill on terrestrial plant production may have persisted. The consumer of supralittoral grasses that is of most importance as game and subsistence food is the Sitka black-tailed deer. Especially during winter, when inland food sources are covered in snow, the deer come to the shoreline to feed. Here they consume terrestrial vegetation, including Elymus, as well as drift algae and Fucus on the shore. A study of potential impact on these deer revealed only occasional evidence of oil exposure in deer from oiled areas and no signs of oil ingestion or oil-related lesions or pathologies in a sample of 32 individuals (Lewis, 1993a). No direct oil-related mortality was observed, and the heavy winter mortality that did

44

CHARLES H. PETERSON

occur in the Prince William Sound area could be attributed to starvation (Lewis, 1993a). It is unlikely that the reduced production of forage grasses in the supralittoral zone and the reduction in intertidal algae (especially Fucus gardneri) enhanced the rate of winter starvation in Sitka blacktailed deer. The spatial extent of the reduction in rye grass production is unlikely to be great enough to have meaningful influence on food supply for the deer. Furthermore, despite the loss of Fucus gardneri from many shores, substantial amounts of Fucus persisted within the foraging range of the deer. Brown bears are a prominent element of the coastal terrestrial ecosystem in the spill area, with especially high densities in the Katmai National Park on the Alaska Peninsula. Brown and black bears forage on intertidal bivalves (razor clams and blue mussels, respectively) just after spring emergence from overwintering dens when snow cover inland and seasonal absence of fruits limit availability of terrestrial food resources inland. This link to the marine intertidal habitats exposed bears to the oil just after the spill. Their foraging on returning salmon and salmon carcasses later in the summer likewise placed them at risk to oil exposure and ingestion because the accessible carcasses come to rest on intertidal shores. Bears also scavenge on marine mammal carcasses, which placed them at risk after the spill when so many sea otter carcasses came ashore. Consequently, a study was conducted in the Alaska Peninsula region to assess possible oil spill injury to brown bears. Survival over 2 years for bears outfitted with radio-transmitters was 95% in Katmai, the oiled site, as compared with 93% in the Black Lake control site also on the Alaska Peninsula (Lewis, 1993b). Deaths were largely the result of aggressive fighting among bears. Fecal and blood samples suggested that four of 27 bears in Katmai had been exposed to oil, compared with none of 22 at Black Lake (Lewis, 1993b). One of the bears exposed to oil was a mother whose recently dead cub revealed high levels of oil exposure as assessed by bile hydrocarbons. The death of this cub before sampling its bile renders the integrity of the sample suspect, so the link to oil is not unequivocally established. Overall, the oil spill appeared to have little effect on brown bears, at least in the Katmai area, except possibly on some undetermined number of yearlings. With so little effect on adults, there is little chance of the presence of indirect, secondary effects on the terrestrial ecosystem as a consequence of direct effects on brown bears. Possible effects of the oil spill on black bears were not evaluated, but there is little reason to suspect impacts greater than the minimal effects on brown bears. The islands of Prince William Sound, where the oil spill originated and where heavy oiling of shorelines was greatest, are inhabited by black bears rather than the brown bear. A study of black bears on those islands could have been informative.

EFFECTS OF "EXXON VALDEZ" OIL SPILL

5.2.

45

Terrestrial birds

There is somewhat more scientific literature linking terrestrial birds than terrestrial mammals to the intertidal zone. For example, the use of salt marshes by red-winged blackbirds (Agelaius phoeniceus (L.)) during breeding season is made evident by their singing displays and territorial defences. Seaside sparrows (Ammodramus maritimus (Wilson)) gather seeds from marsh plants and nest within vegetation of this habitat. Marsh wrens (Cistothorus palustris (Wilson)) are characteristic of the habitat that gives them their name. In Prince William Sound and the Gulf of Alaska coast, the birds that use the intertidal zone so prominently are largely scavengers, specifically bald eagles and northwestern crows (Corvus caurinus (Baird)). Both species risked exposure to the oil through their use of the intertidal zone and through feeding on oiled carcasses. One government-sponsored study focused explicitly on how bald eagles responded to the oil spill. This began in summer 1989 (Bowman, 1993; Bowman et al., 1995, 1997). Counts of about 150 dead eagles after the spill were extrapolated to an estimated 900 deaths out of the 8000 bald eagles then inhabiting the coastal area from Prince William Sound to the Alaska Peninsula. This extrapolation assumed that the relative proportion of dead eagles found on the beach compared with those back in the vegetation after the oil spill was similar to that before the spill. This assumption may not hold if oiling induced more direct mortality on the beach. Production of young eagles was also depressed in the Prince William Sound area during summer 1989, when samples of both prey and eggs showed oil contamination and when disturbance of nesting sites by shoreline clean-up crews was intense. Tagging of fledglings in oiled and unoiled areas of Prince William Sound showed no effect of the spill on subsequent survival from summer 1989 on. Thus, the injury done to bald eagles by the spill was an immediate reduction in adult survival throughout the spill area and, in 1989, losses in production of young in Prince William Sound only (Table 7). Surveys of eagles in 1982, 1989, 1990 and 1991 had wide confidence limits and there were no significant differences that could demonstrate the precise date of recovery. However, resumption of the historically observed population growth rate of about 2% per year in this region suggests that recovery was relatively rapid. A similar study of eagles conducted by Exxon scientists collected data that were largely consistent with the results of Bowman (1993) and Bowman et al. (1995, 1997). White et al. (1995) were unable to detect any significant difference in eagle counts between oiled and unoiled areas in Prince William Sound in 1990 or 1991, though they found significantly lower production of young on oiled shores in 1991. These authors did not sample in 1989, when Bowman's study detected negative effects.

46

CHARLES H. PETERSON

Table 7 Effects of shoreline oiling and/or treatment on the guild of birds that scavenge along shorelines or practise omnivory along shorelines.

Effect

Duration

Source(s)

Direct acute responses

Reduction by about 10% of bald eagles in Prince William Sound, based on extrapolation from counts of dead eagles and lower counts in shoreline surveys Reduction in counts of northwestern crows on oiled shores vs. control shores in survey of Prince William Sound Production of young eagles reduced on oiled shores when eggs and prey showed contamination

1989

Bowman, 1993; Bowman et al., 1995, 1997

1989

Klosiewski and Laing, 1994; Day et al., 1995, 1997a

1989

Bowman et al., 1995, 1997

Indirect or chronic delayed responses

Survey counts of bald eagles in Prince William Sound show enhanced abundances on oiled shores compared with controls Survey counts of glaucous-winged gulls in Prince William Sound show enhanced abundances on oiled shores compared with controls Survey counts of northwestern crows on the outer Kenai coast show enhanced abundances on oiled shores compared with controls

1993-1996

Irons (pers. comm.)

1993-1996

Irons et al., 2000

1989

Day et al., 1995, 1997b

EFFECTS OF "EXXON VALDEZ" OIL SPILL

47

Surveys of bird abundances along the shore consistently detected large reductions in northwestern crows on oiled shores in Prince William Sound (Klosiewski and Laing, 1994; Day et al., 1995, 1997a: Table 7). Klosiewski and Laing (1994) compared counts made along the same shoreline segments evaluated in 1972 and 1984-85 to new counts made after the oil spill in 1989, 1990 and 1991. This permitted an analysis similar to a BACI design, which has data from before and after an event at both control and treated sites (Stewart-Oaten et al., 1986). Using this approach, northwestern crows were shown to have declined in average abundance on oiled shores relative to the temporal change exhibited on unoiled reference shores. Analysis by Day et al. (1995, 1997a) of their own independent surveys conducted in the same three post-spill years showed a decline in northwestern crows and no clear evidence of recovery in Prince William Sound by 1991. Surprisingly, analogous surveys along the Kenai coast, Day et al. (1995, 1997b) reported increased counts of northwestern crows on oiled shores relative to unoiled controls. Eagle counts along the same transects were consistent with those of Bowman. Day et al. (1995) demonstrated a lower use of oiled shores by eagles in 1989 in Prince William Sound followed by recovery by 1990, while Klosiewski and Laing (1994) showed no difference in how counts of eagles in Prince William Sound averaged over 1989-91 were distributed between oiled and unoiled shoreline segments. An even more powerful analysis of bird abundances in these surveys, including more recent surveys in 1993 and 1996 revealed a long-term increase in bald eagle abundances along oiled shorelines of Prince William Sound as compared with unoiled segments (Irons et al.. 2000, pers. comm.). Bird counts made in oiled and unoiled stretches of shoreline confound changes in overall population size with changes in behaviour. The large numbers of dead eagles resulting directly from the oil spill clearly demonstrate that some population decline took place over the short term. However, the absence of lasting effects on reproduction and the inability to detect population differences in later years imply that large populationlevel effects on eagles are unlikely to have lasted beyond a year or two. Over the long term, eagle abundances even appear to be enhanced in the spill area as compared with unoiled shores. Another scavenger along shorelines, the glaucous-winged gull (Larus glaucescens (Naumann)), also exhibited long-term enhancement of abundance on oiled shores relative to unoiled shores in the spill region (Irons et al., 2000, pers. comm.). Mew gulls (Larus canus (L.)), which scavenge along the shore, showed no significant change in abundance in the short or long term following the "Exxon Valdez" oil spill (Irons et al., 2000, pers. comm.). For northwestern crows, the distinction between behavioural and population responses is more difficult. Klosiewski and Laing (1994) report a long-term decline in

48

CHARLES H. PETERSON

total abundance of northwestern crows in Prince William Sound between 1972-73 and the post-spill period, but how much of that occurred at the time of the spill is unclear. In any event, the rapid recovery of eagles and the possibility that the pattern exhibited by northwestern crows was largely behavioral imply that indirect effects of these long-term changes in scavenging bird abundances on the terrestrial ecosystem are unlikely.

5.3.

Fishes

The "Exxon Valdez" oil spill had impacts on nearshore fishes of three different types: (1) those that permanently reside in nearshore habitats; (2) those that spawn and reproduce in nearshore habitats; and (3) those that forage during some major portion of their life cycle in nearshore habitats. Impacts include evidence of exposure of fish to PAHs in the oil, resulting in cases of physiological responses of at least sublethal significance, reproductive impairments and population declines in spill areas. Most impacts were detected soon after the oil spill when study effort was most intense, but many impacts of oiling of nearshore habitats on fishes have been shown to persist for years after the spill. 5.3.1.

Impacts on resident fishes of shoreline habitats

Immediately following the oil spill, kelp greenling (Hexagrammos decagrammus (Pallas)) exhibited hemosiderosis, a liver abnormality induced by exposure to toxic compounds, including petroleum hydrocarbons (Khan, 1991; Khan and Nag, 1993: Table 8). Hemosiderosis is evidenced by centers of accumulation of hemosiderin in the liver and spleen, resulting from excessive destruction of erythrocytes in fishes. Histological sections of livers from prickleback (Stichaeus spp.) and spleens from crescent gunnel (Pholis laeta (Cope)) collected in oiled eelgrass beds in Herring Bay in 1993 revealed hemosiderosis in all individuals (10 of each species), while no individuals collected from unoiled eelgrass beds in Lower Herring Bay exhibited this response (Jewett et al., 1995). Although average concentrations of TPAHs in shallow sediments of eelgrass bed habitats in Herring Bay had declined to 40 ng g-1 by July 1993, these characteristic demersal fishes of the eelgrass and other nearshore habitats were still being exposed to a toxic pollutant at this oiled site three and a half years after the spill (evidence of hemosiderosis lasts only about 6 weeks after removal of the pollutant). Similarly, the masked greenling (Hexagrammos octogrammus (Pallas)) still exhibited induction in their livers of the cytochrome P450 1A enzyme in

49

EFFECTS OF "EXXON VALDEZ" OIL SPILL

Table 8 Effects of shoreline oiling and/or treatment on fishes that are resident in the intertidal or shallow subtidal habitats.

Effect

Duration

Source(s)

Direct acute responses

Reduced abundance and biomass of intertidal fishes in several rocky shore habitats Hemosiderosis induced in kelp greenling, pricklebacks and crescent gunnel

1990, with only partial recovery by 1991

Barber et al., 1995

1990

Khan and Nag, 1993; Jewett and Dean, 1996

Indirect or chronic delayed responses

Juvenile cod and Arctic shanny increased by >100% at oiled sites perhaps in response to enhanced Musculus prey, themselves released from Telmessus predation Parasite burdens enhanced in some demersal fishes of shallow water Hemosiderosis continued to be induced in pricklebacks and crescent gunnel P450 detoxification enzyme induced in masked greenling

1990

Laur and Haldorson, 1996; Dean et al., 1998

1989

Khan, 1990

1993

Jewett and Dean, 1996

1996

Holland-Bartels et al., 1998

1996 in collections from Herring Bay, while enzyme levels in fish collected from unoiled Jackpot Bay were low (Holland-Bartels et al., 1998). This too implies continuing exposure and physiological response to an organic contaminant, most likely residual oil from the spill. One other study of responses of intertidal fish (Woodin et al., 1997) confirmed the induction of cytochrome P450 1A in benthic fishes by exposure to " E x x o n Valdez" oil months and years after the spill had occurred. Khan (1990) also showed an indirect effect of the " E x x o n Valdez" oil through its induction of greater loads of parasites in some of the demersal fishes of shallow-water habitats in Prince William Sound. The community of intertidal fishes was sampled quantitatively in a paired design, comparing oiled and unoiled control pairs of sites using transects spanning four elevations (the first, second, third and fourth

50

CHARLES H. PETERSON

meter of drop in the intertidal zone). Sampling was conducted in three rocky shore habitats, sheltered rocky habitat, coarse-textured rocky habitat, and exposed rocky shores on two dates (spring and summer) in both 1990 and 1991 (Barber et al., 1995). A total of 20 species of demersal fishes was collected, with five species comprising 90% of the total and one species, the high cockscomb (Anoplarchus purpurescens Gill) representing 74% of all fish sampled. The abundance and biomass of intertidal fishes analysed over all three habitats exhibited significantly lower values on oiled shores in 1990 visits (Figure 11). By 1991 both abundance and biomass had increased on oiled and unoiled shores, with larger increases on oiled shores indicative of the process of recovery (Barber et al., 1995). The pattern of impact on these small demersal fishes differed somewhat among habitats. On sheltered rocky shores, abundance on control sites was initially 3.4 and 1.4 times as high as on oiled shores on successive sampling visits in 1990, but differences disappeared by 1991. On coarse-textured shores, abundances were consistently greater on control shores across all samplings with the ratio of abundances declining progressively from 4.8 to 3 to 2 to 1.6. Biomass remained about twice as high on unoiled control shores through 1991. In exposed rocky habitat, abundance and biomass of demersal fishes was about twice as high on unoiled shores as on oiled shores in 1990, with differences disappearing by 1991. The results of this study of resident demersal fishes thus show an intense depression of abundance and biomass caused by the oil spill and shoreline treatments. The increases in 1991 on both oiled and unoiled shores imply that the differences observed in 1990 underestimated the magnitude of the impact because no sampling was conducted in the first summer (1989) after the March spill date and because mobility of these fishes helped spread the spill effect to unoiled shores. Removal experiments by Barber et al. (1995) confirm that the high cockscomb is highly mobile. The partial convergence of abundances and biomass on oiled and control shores demonstrates that recovery of intertidal demersal fishes was occurring but incomplete by summer 1991, two and a half years after the oil spill. The benthic fishes of the shallow subtidal zones of vegetated habitats in Prince William Sound did not show similar patterns of declines in oiled locations, although again no assessment was conducted in 1989 (Laur and Haldorson, 1996). Sampling was conducted by diver counts in summer 1990 at two depths (2-11 m and 12-20 m) within eelgrass beds and beds of small kelps. Densities of adult fishes revealed no significant relationship to oiling, whereas juvenile Pacific cod (Gadus macrocephalus Tilesius) and arctic shanny (Stichaeus punctatus (Fabricius)) showed densities at oiled sites more than double the levels at paired control sites. The mobility of these fishes and the open nature of fish recruitment through larval

51

EFFECTSOF "EXXON VALDEZ" OIL SPILL

~k'~.ltered rocky

1.5"

1.o. 0.5,

o.o

Coarse textured 1.5

I~

1.0

E

0.5

!.._ Ill t~

:3 Z o.o

1.5-1

Expo=ed rocky

[ ] control sites [ ] oiled sites

1.0

0.5 QO spring

summer 1990

spring

summer 1991

Figure 11 Densities of intertidal fishes pooled over three levels (MVD 2--4) in each of three habitats averaged over replicate oiled and unoiled control sites in Prince William Sound. Stars indicate significance of Wilcoxon signed rank tests (P<0.05) comparing densities across oiled and unoiled control sites. (Data from Barber et al., 1995.)

transport make evaluation of the spill impact difficult. It is possible that higher current fluxes at oiled sites resulted in naturally higher recruitment rates. Alternatively, the enhanced abundances of epifaunal invertebrate prey, especially the mytilid bivalve M u s c u l u s sp., demonstrated by Jewett et al. (1999) for eelgrass beds, may have attracted the young-of-the-year (0+) cod to oiled seagrass beds (Jewett et al., 1995; Laur and Haldorson,

52

CHARLES H. PETERSON

1996). This explanation gains some support by the demonstration that gut fullness indices for juvenile fish (Figure 12) were higher in oiled sites (Jewett et al., 1995). This response of juvenile fishes living in shallow subtidal vegetation a year after the oil spill may reflect atrophic cascade created by removal of the predatory helmet crab Telmessus and seastars, enhancing abundances of small invertebrate prey and the impacts of organic enrichment likewise enhancing invertebrate prey abundances (Table 8). This hypothesis has not been directly tested. 5.3.2.

Impacts on fishes that spawn and reproduce in nearshore habitats

The most important forage fishes of the coastal ecosystem of the northern Gulf of Alaska are closely tied to the intertidal and shallow subtidal habitat through the use of this environment for spawning and egg deposition and development. Pacific herring (Clupea pallasi Valenciennes) spawn on intertidal Fucus thalli and on shallow subtidal kelps like Nereocystis. Pink salmon spawn in gravel stream beds, with the majority of the spawners in Prince William Sound using intertidal sites for egg deposition. Sand lance (Ammodytes hexapterus Pallas) spend much of the day buried in shallow sediments, which is also where their eggs are deposited. Capelin (Mallotus villosus (Mtiller)) lay eggs on gravels of open beaches. These species of schooling fishes constitute a large fraction of the forage fish base for higher-level predatory vertebrates in the coastal ecosystem of Prince William Sound and the northern Gulf of Alaska spill area (Hood and Zimmerman, 1986; Duffy, 1998). The timing of the "Exxon Valdez" oil spill matched the season of adult return, spawning, and larval and postlarval development of Pacific herring (Clupea pallasi). The spill began on 24 March while adult herring were returning to spawn. Spawning occurred in early-to-mid April 1989: eggs hatched in early May and larval herring occupied nearshore areas until late spring (Brown et al., 1996). This period coincided directly with the presence of large masses of floating oil, under and through which the adults swam and which contacted eggs and larvae over a large fraction of the spawning habitat in Prince William Sound (Brown et al., 1996). No significant effect of oiling was detected on egg survival (Brown et al., 1996), except at one site with detectable oil on kelp (Pearson et al., 1995), but newly hatched larvae exhibited many abnormalities in oiled areas (Hose et al., 1996). Field sampling demonstrated much higher rates of larval mortality in oiled areas (McGurk and Brown, 1996). From the observed egg deposition counts on oiled and unoiled shores and the observed differential in larval mortality rates, Brown et al. (1996) estimated that 40-50% of the eggs deposited in 1989 were exposed to oil and 99% of expected herring survivors were killed on the oiled shores,

53

EFFECTS OF "EXXON VALDEZ" OIL SPILL

% of Gut Capacity Filled With Food Eelgrass

A

100 90 80 70 60 50 40 30 20 10 0 15

16

18 17 Site N u m b e r

26

25

Mollusks in Guts Eelgrass P=0.12

S

0.500.40 0.30 0.20 0.100.0015

16

18 17 Site N u m b e r

26

25

Crustaceans in Guts Eelgrass P=0.02

C

1.o. 0.9" 0.8" 0.7" 0.6" 0.5" 0.4" 0.3" 0.2" 0,1" 0.0" 15

16

18 17 Site N u m b e r

26

25

Figure 12 Differences in feeding by young-of-year (0+) cod sampled in three replicate pairs of eelgrass sites in Prince William Sound in 1990, comparing oiled (black columns) and unoiled (white columns) control sites. A) percent volume of food in guts; B) percent volume of molluskan food; C) percent volume of crustacean food. Gut fullness was greater at oiled sites, where there was more ingestion of mollusks, especially the bivalve Musculus that was abundant. Feeding on crustaceans, including the amphipods that were depressed in abundance, was reduced relative to control sites. B and C show significance limits. (After Jewett et al., 1995.)

54

CHARLES H. PETERSON

resulting in reduction of over 40% of the expected total production of the 1989 year class of herring from Prince William Sound. Indeed when spawning adults from this 1989 year class returned in 1993, this year class from the spill year represented one of the smallest on record despite the high spawn deposition reported by the annual survey carried out by Alaska Fish and Game (Brown et al., 1996). A study of herring response to the oil (Pearson et al., 1995) concluded that only about 4% and no more than 9-10% of the shoreline that contained herring spawn was oiled in 1989, as opposed to the 40-50% calculated by Brown et al. (1996). The conflicting estimates arise from different methods for determining shoreline oiling. Pearson et al. (1995) used a criterion of visible oiling during aerial overflights at the time when eggs were present, whereas Brown et al. (1996) used accumulated oil in mussel tissues as the oiling criterion and measure. The integrated estimate of miles of oiled shoreline measured by bioaccumulation in mussels is understandably much greater than the instantaneous aerial observations of visible oil. Brown et al. (1996) defend their measure by noting that the rise and fall of the tides exposed the intertidal and shallow subtidal herring eggs on shore to direct oiling in the surface microlayer that is best assessed by a biological sampler like the mussel. The study by Pearson et al. (1995) also produced lower estimates of effects of that oil on larval mortality, in large part because the exposure was estimated by concentration of oil remaining attached to kelps. Kelp blades are slippery and mucus-covered, unable to retain and accumulate a history of oil exposure. The mussel oil concentrations used by Brown et al. (1996) would appear to represent a biologically more relevant sampler of integrated oiling. The oil spill thereby appears to have reduced reproductive success of this intertidal and shallow subtidal spawner, with some acute consequences at a population level (Table 9). The loss of herring from the oil spill may also have occurred through enhancement of susceptibility to viral hemorhagic septicemia (VHSV) (Carls et al., 1998), so the impacts on reproductive success in 1989 do not represent all of the spill effects. However, the disease outbreak occurred in 1993 four years after the spill, requiring a compelling explanation for the time lag to link disease induction to the oil spill. Nevertheless, no matching disease outbreak and no herring crash occurred in Sitka Sound to the south, a Pacific herring population far enough distant to be outside the influence of the oil spill yet similar enough in its environment, historical population dynamics, and fisheries landings to serve as a reasonable control. Pink salmon, a species of great importance to higher-level vertebrate consumers in the spill area ecosystem suffered depressed reproductive success because of oiling of the intertidal habitat in which eggs are deposited and develop (Table 9). Adult pink salmon return in summer to

EFFECTS OF "EXXON VALDEZ" OIL SPILL

55

natal streams to spawn, where eggs remain developing until hatching in winter. Fry grow and develop in the streams until spring migration to the nearshore marine system, where they feed and grow before late summer departure into the Gulf of Alaska system. The oil spill in March 1989 exposed some fraction of the 1988 year class to oiling. A total of 31% of the salmon streams in the southwest district of Prince William Sound was estimated to have been exposed to oiling (Geiger et al., 1996). Coded wire tags were used to follow the growth and fate of pink salmon in this 1988 year class. Willette (1996) found slower growth during the first 2 months of their marine phase, when the fish are feeding on invertebrates in the nearshore zone and about a 2% reduction in numbers of those fish that returned to spawn as adults the next summer. Wertheimer and Celewycz (1996) confirmed this reduction in growth of pink salmon during the early marine phase in summer 1989. The growth reductions were smaller in 1990 and 1991 (Willette, 1996). In addition to this effect of oiling on growth of juvenile salmon, the residual oil in the gravel increased embryo mortality in developing pink salmon eggs deposited in summers from 1989 and for several successive years thereafter (Bue et al., 1996, 1998). Because the enhanced egg mortality in oiled streams reappeared in 1997 after 2 years of apparent convergence, the hypothesis of pre-existing geographic differences in egg mortality was advanced. As a test of this hypothesis, experimental exposures of pink salmon eggs to oiled gravel, including even oiled gravel after years of weathering, reproduced these lethal effects on developing embryos (Heintz et al., 1999). The laboratory results provide strong support for the interpretation that oiling was the cause of the chronic mortality of pink salmon eggs in the field. Year-to-year differences in the effects of gravel oiling may possibly be explained by varying degrees of lateral movement of subsurface oil into stream gravel (Murphy et al., 2000). Another study of the response of pink salmon eggs to stream bed oiling (Brannon et al., 1995; Brannon and Maki, 1996) failed to detect greater embryo mortality in oiled streams except in one elevation stratum. However, this less powerful study examined far fewer eggs per sample, a smaller area within the stream bed, a single year as opposed to 1989-98 in the Bue et al. (1996, 1998) studies, and a much smaller number of eggs. There is evidence that exposure to oil may induce a genetic change in pink salmon that also contributes to chronic reduction in egg survival in oiled streams. Study of eggs stripped from groups of returning pink salmon, then reared under common conditions, showed that even without exposure to residual oil in the streams, eggs from females returning to oiled streams have lower survival than those from females returning to unoiled streams (Bue et al., 1998). Consequently, the use of oiled intertidal

56

CHARLES H. PETERSON

Table 9 Effects of shoreline oiling and/or treatment on fishes that use shallow subtidal habitats for spawning, egg deposition.

Effect

Duration

Source(s)

Direct acute responses

Premature hatch, larval abnormalities and mortality in Pacific herring Enhanced egg mortality of pink salmon in oiled gravel Probable egg mortality in sand lance, which use low intertidal sands and fine gravel for spawning and egg deposition and burial as adults Likely egg mortality in capelin, which use gravel beaches for spawning and egg deposition and showed low population sizes after the spill as compared with 1978-80

1989

1989 not studied directly

Pearson et al., 1995; Brown et al., 1996; Hose et al., 1996; McGurk and Brown, 1996 Bue et al., 1996, 1998 Kuletz et al., 1997

not studied directly

Indirect or chronic delayed responses

Enhanced egg mortality of pink salmon in oiled gravel Possible contribution of oiling stress to disease induction that caused the 1993 crash in Pacific herring in Prince William Sound Possible genetic damage to pink salmon affecting their productivity

1990-93, 1997 crash in 1993

Bue et al., 1996, 1998; Heintz et al., 1999; Murphy et al., 2000 Carls et al., 2000

indefinite

Bue et al., 1998

areas by this important fish, for both reproduction and foraging, produced an effect of the oil spill that spread out beyond the boundaries of the intertidal habitat as the decline of pink salmon affected both their pelagic prey and their predators. Capelin and sand lance are forage fishes of great importance in the spill region. This is because of: (1) their typically high abundance; (2) their shallow schooling behavior in the nearshore environment that may

EFFECTS OF "EXXON VALDEZ" OIL SPILL

57

enhance their visibility and suitability as prey for seabirds (Piatt and Anderson, 1996); and (3) their high lipid content that can affect energetics of consumers and their reproductive success (Van Pelt et al., 1997). No field study was conducted to test the hypothesis that these forage fishes were affected by the oil spill. However, their use of shallow nearshore sediments for burial and egg laying (sand lance) and nearshore gravel beaches of egg deposition (capelin) implies a high likelihood of extensive exposure to oil (Pinto et al., 1984; Robards et al., 1999). The sensitivity of the egg and early life history stages to oil toxicity (Capuzzo, 1987; Heintz et al., 1999) makes the probability high that both of these forage fishes suffered some decreases in abundance following the oil spill, but it is impossible to judge how large such decreases may have been (Table 9). The diet of the pigeon guillemot, a nearshore piscivore, showed a decline in sand lance after 1978-80 and an increase in small demersal fishes after the oil spill in the Naked Island colonies in the spill area within Prince William Sound (Kuletz et al., 1997). The long time interval between sampling in 1978-80 and 1989 does not allow these data on changing diet to be used to infer a spill effect on abundance of the sand lance. However, this use of the seabird as a sampler of relative fish abundance implies a reduction in forage fish after the spill. 5.3.3.

Impacts on fishes that forage in shoreline habitats

Exposure of sensitive early life stages of fish to the oil in the intertidal and nearshore habitats represents a functionally important linkage between these shoreline habitats and the pelagic ecosystem. In addition, juvenile and adult fishes that obtain a substantial fraction of their food from intertidal and shoreline systems also showed effects of the oil spill (Table 10). The pink salmon is an intensely studied species that demonstrated both effects on embryo mortality (Bue et al., 1996, 1998) as well as reduced juvenile growth when feeding later in the marine shoreline habitats (Wertheimer and Celewycz, 1996; Willette, 1996). The lower growth was detected in 1989 in each of two field studies, but the difference in growth had declined by 1990 and 1991 to a degree that suggested convergence in one study (Wertheimer and Celewycz, 1996) and small residual differences in the other (Willette, 1996). The latter author examined sizes of hatchery-released fish, whereas Wertheimer and Celewycz (1996) sampled wild pink salmon. Examination of hatchery-released fish to assess growth rates probably is a more powerful approach because the fish are released together at the same place, same times, and same sizes for any given hatchery and release date. This could control for a substantial amount of error variance otherwise present in wild fish that emerge from streams at different times, places and sizes. Another study of wild-stock pink salmon

58

CHARLES H. PETERSON

Table 10 Effects of shoreline oiling and/or treatment on fishes that use the intertidal and nearshore habitats for summer foraging. All species listed showed chronic effects after 1989.

Effect

Duration

Source(s)

Direct acute responses

Reduced growth of pink (and likely also chum) salmon juveniles, which lowers survival probability Reduced growth and possibly also survival of Dolly Varden char and cut-throat trout, which feed in intertidal rocky shore in summers Enhancement of P450 detoxification enzyme and other biochemical evidence of exposure and physiological response in pink salmon, Dolly Varden (very high), yellowfin, rock, and flathead soles, and walleye pollock

1989-90, with Werthheimer and diminished effect Celewycz, 1996; in 1991 Willette, 1996 1989-90, 1990-91 Hepler et al., 1996 (cut-throat trout); 1989-90 (Dolly Varden) 1989-91

Armstrong et al., 1995; Carls et al., 1996; Collier et al., 1996

(Brannon et al., 1995) produced results similar to those of Wertheimer and Celewycz (1996) in that no growth difference was detected in 1990. Growth rate of pink salmon during their juvenile residence period in the nearshore habitats translates directly to population effects because smaller size and slower growth lead to higher mortality rates (Willette et al., 1999). The zooplankton and epibenthic crustacean prey of juvenile pink salmon during this early marine phase did not exhibit detectable differences in density between oiled and control shores (Celewycz and Wertheimer, 1996). Furthermore, gut fullness measures suggested that feeding rates of juvenile pink and chum salmon did not differ with oiling in 1989 or 1990 (Sturdevant et al., 1996). Consequently, the reduced growth rate is most likely a sublethal effect of ingesting toxic hydrocarbons that cost energy to depurate. Indeed, the cytochrome enzyme system was significantly activated in juvenile pink and chum salmon collected in 1989, indicative of such detoxification induction (Carls et al., 1996). The reduced abundance of amphipods in oiled eelgrass beds (Jewett et al., 1999) is the only evidence that a food source of value to these foraging salmonids was reduced by the oil spill. Independent of the mechanism by which the oil spill affected growth, this perturbation once again

EFFECTS OF "EXXON VALDEZ" OIL SPILL

59

demonstrated the functional linkage between the shoreline habitats and the pelagic system. Two other anadromous salmonids of ecological importance and of value to sport fisheries, the Dolly Varden char (Salvelinus malma (Walbaum)) and cut-throat trout (Oncorhynchus clarki (Richardson)), were studied after the oil spill. Both species migrate from streams to the shallow sea in spring and a large fraction of their annual growth results from summer feeding on shoreline invertebrates. Both species had lower growth on oiled shores in 1989-90 as compared with unoiled controls, with differences of 22-45% (Hepler et al., 1996). Cut-throat trout continued to show lower growth on oiled shores in 1990-91, whereas this negative effect of the oil spill lasted only a year for Dolly Varden. The growth reduction may have led to reduced survival in both species, but observed reductions in survival of 22-32% were not statistically significant (Hepler et al., 1996). Doubt exists over whether pre-existing geographic differences in temperature-dependent growth rates were partly responsible for these growth differences observed between oiled and unoiled streams. This alternative explanation cannot be fully dismissed, but pre-existing geographic differences cannot explain the convergence in growth rates exhibited by Dolly Varden char in 1990-91. Furthermore, an oiling effect on cut-throat trout and Dolly Varden char is consistent with the results of studies of pink and chum salmon, fishes that share similar habitats and feeding ecology during summer. The mechanisms by which the oil influenced growth and possibly survival of these anadromous fishes are probably the same as for pink and chum salmon because most of their feeding and growth also take place during summer in the shoreline habitat. Because cut-throat trout and Dolly Varden char spend much of the year in rivers and streams, this response to the oil spill represents a connection that moves from the shoreline system inland to affect freshwater aquatic systems. Demersal fishes that range into deep water, and undergo extensive movements within the Gulf of Alaska, showed activated cytochrome enzyme systems and other biochemical indicators of induction of the detoxification processes after exposure to the oil (Armstrong et al., 1995; Collier et al., 1996). Dolly Varden also demonstrated high levels of exposure in 1989 via analysis of aromatic compounds in the bile, but these declined in 1990. This evidence of high exposure of Dolly Varden char in 1989 with a reduction in 1990 also provides support for the interpretation of observed growth differences as an effect of oiling rather than geography. For the other species tested, yellowfin sole (Pleuronectes asper Pallas), rock sole (P. bilineatus (Ayres)), and flathead sole (Hippoglossoides elassodon Jordan and Gilbert) and walleye pollock (Theragra chalcogramma (Pallas)), oil exposure continued into 1991, the final year of

60

CHARLES H. PETERSON

the study (Collier et al., 1996). Flathead sole also had elevated concentrations of fluorescent aromatic compounds (an indicator of exposure to petroleum hydrocarbons) in bile from the liver in 1990 and 1991 (Armstrong et al., 1995). Consequently, the mobility of these fishes, including entry into and use of shallow shoreline habitats for feeding, provided a vector whereby oil effects were transferred to a depth and to a great distance from the source, up to 640 km for some pollock.

5.4.

Marine mammals

Marine mammals, such as sea otters and harbor seals (Phoca vitulina (L.)), were exposed directly to floating oil during the spill because of their need to come to the sea surface to breathe and their use of oiled shoreline rocks for haul-outs. Widespread acute mortality was observed (Table 11), estimated from carcasses to be at least 1000 and up to 2800 sea otters (Garrott et al., 1993) and at least 302 harbor seals within Prince William Sound (Frost et al., 1994). In the case of sea otters, the mechanism of mortality involved oiling of the fur, followed by loss of its insulating capacity and ingestion of the oil by preening. In the case of the harbor seals, exposure to toxic fumes in the air just above the oiled sea surface was implicated. However, even after the direct effects of exposure to the spilled oil had ended, both sea otters and harbor seals showed several years of delay in recovery in the spill area, indicative of some chronic lingering effect of the spill (Ballachey et al., 1994). Some lines of evidence suggest that, like the direct effects of the spill, much of this chronic effect may be mediated through the oiling of the intertidal and shoreline habitats and resources. The chronic effects of the spill (Table 11) on sea otters have been indicated by three major lines of evidence (Rotterman and Monnett, 1991; Ballachey et al., 1994; Holland-Bartels et al., 1998). First, sea otter abundance in the spill area has not yet returned to pre-spill levels despite the high reproductive potential of this species (Dean et al., 2000). Second, overwinter mortality of juvenile sea otters was higher at oiled sites than at unoiled controls in 1990-91 and 1992-93 (Rotterman and Monnett, 1991; Monson et al., 2000). Third, beached carcasses included abnormally high proportions of prime-aged animals for years following the spill (Ballachey et al., 1994; Holland-Bartels et al., 1998; Monson et al., 2000). The mechanisms responsible for delayed recovery have not been unambiguously established, but ingestion of persistent oil and reduced numbers of prey are possibilities. The persistent contamination seems more likely, especially when recognizing that juvenile sea otters feed heavily on mussels, which in certain dense beds retained high levels of only partially

EFFECTS OF "EXXON VALDEZ" OIL SPILL

61

Table 11 Effects of shoreline oiling and/or treatment on the marine mammals that occupy shoreline habitats.

Effect

Duration

Source(s)

Direct acute responses

Over 1000 sea otter corpses recovered after the spill with projections of about 2800 total mortalities from oiling of fur and subsequent ingestion Harbor seal mortality estimated as 300 in Prince William Sound from inhalation of toxic fumes Likely mortalities of Steller sea lions from same mechanism that affected seals

1989

Garrott et al., 1993

1989

Frost et al., 1994

not studied

Indirect or chronic delayed responses

Overwinter mortality of juvenile sea otters higher in oiled areas Counts of carcasses of winter-kill sea otters show abnormally high proportion of prime breeding-age otters Sea otter recovery grossly delayed on northern Knight Island Reduction in seal and sea lion prey may soon force killer whales to switch to include sea otters in their diets, as in Aleutians where trophic cascades are then initiated P450 detoxification enzyme elevated in sea otters on oiled shores Harbor seal counts failed to initiate convergence between oiled and unoiled trajectories River otters showed larger home ranges (indicating a need for larger foraging areas to meet energetic demands), greater abandonment of latrine sites (suggesting emigration) River otters showed elevated haptoglobin counts

1990-91, 1992-93 until about 1994

through 1997 not occurring yet as of 1998

Rotterman and Monnett, 1991; Ballachey et al., 1994 Ballachey et al., 1994; Monson et al., 2000 Holland-Bartels et al., 1998 Estes et al., 1998; Estes, 1999; Garshelis and Johnson, 1999

1996-98 through 1997

Holland-Bartels et al., 1998 Frost et al., 1994

1990 Bowyer et al., 1995

until 1991 Duffy et al., 1994a, b

62

CHARLES H. PETERSON

weathered oil for years after the spill (Babcock et al., 1996). However, the degree to which the juvenile sea otters use mussels from oiled mussel beds is unknown. Because sea otters in the spill area prey on intertidal and shallow subtidal invertebrates, whether the mechanism involves prey quality or quantity, it still represents a reasonable route of chronic injury operating through impacts to the shoreline habitat and resources. The chronic effects of the spill on harbor seals are implied by the continuing decline in harbour seal abundance in the spill area and failure to initiate convergence with simultaneous moulting survey counts made in unoiled control areas (Frost et al., 1994, 1999). Harbor seals in Prince William Sound exhibited 7-13 times higher levels of hydrocarbon metabolites in their bile in 1989, displayed lethargic behaviour after the spill, had brain lesions consistent with inhalation of organic solvents, had elevated PAH concentrations in blubber and milk, and produced fewer pups in oiled areas in 1989, 1990 and 1991 (Frost et al., 1994). The harbor seal feeds on nearshore fishes. The most likely explanation for the long-term decline of harbor seals and Steller sea lion (Eumetopias jubatus Schreber) in the northern Gulf of Alaska from the late 1970s is a decline in availability of forage fish. This was made especially acute by fishery extractions in nearshore waters at times when feeding young require high energy intake (NRC, 1996). The delayed recovery of harbor seals in the oiled portions of Prince William Sound may be a response to low availability of forage fishes, including those such as herring that were depressed in abundance by the spill. Alternatively, but less likely, there were sublethal effects of continued exposure to contamination through the diet affecting reproduction. If these are the causes, then the chronic effect of the "Exxon Valdez" oil spill on harbor seals represents an indirect effect operating through impacts in the intertidal and shallow subtidal habitats (Table 11). However, the contribution of the oil spill to the long-term depression of abundance of herring and other forage fishes remains uncertain. The river otter (Lutra canadensis Schreber) occupies a riparian habitat that provides access to nearshore marine fishes, which form its prey base. Consequently, river otters can be considered yet another vertebrate consumer with strong connections to those shoreline habitats that suffered the most intense impact of the oil spill and post-spill treatments. Some river otters were killed by acute contact with oil during the spill, but losses were not massive and river otters continued to occupy oiled shorelines (Testa et al., 1994). However, in 1990 home ranges on oiled shores were twice as high as on unoiled shores, implying a reduction in habitat value that forced broader foraging to meet energetic needs (Bowyer et al., 1995). The abandonment of latrine sites, possibly suggestive of local population change through migration or mortality,

EFFECTS OF "EXXON VALDEZ" OIL SPILL

63

was three times greater on oiled shores (Bowyer et al., 1995). This set of chronic impacts of the oil spill lasting for at least a year after the spill is most likely an indirect effect of oiling of the intertidal and shallow subtidal habitat (Table 11). Otters in oiled locations showed elevated haptoglobin, an indicator of physiological stress, through at least 1991 (Duffy et al., 1994a, b). In addition, numerous prey found in diets from unoiled control shores were missing in diets of otters feeding on oiled shorelines (Bowyer et al., 1994). Unanticipated changes in killer whale ( O r c i n u s orca L.) feeding behavior in the Aleutian Islands suggest possible future indirect and chronic effects of the "Exxon Valdez" oil spill in Prince William Sound. Estes et al. (1998) reported that killer whales in the Aleutians have been forced to switch to consuming sea otters because of the long-term declines in their traditional marine mammal prey, especially harbour seals and Steller sea lions. The consequent removals of sea otters from several Aleutian Islands led to the trophic cascades that alter the coastal rocky shore ecosystem. If declines in harbor seals and Steller sea lions continue in Prince William Sound, this switch in killer whale diet may occur there, with potentially dramatic implications for indirect ecosystem changes. Such a switch in diet would be partly in response to the oil spill because of the failure of harbor seals to recover from losses after the spill. Because of the lack of suitable groups of Steller sea lions that remain faithfully associated with fixed sites inside and outside the oil spill trajectory, no study of the impact of the "Exxon Valdez" oil spill was conducted on sea lions. Nevertheless, it is reasonable to expect that some sea lion losses were the result of the same factors that reduced the numbers of harbor seals. It would appear that the oil spill has reduced the availability of traditional marine mammal prey for killer whales passing through Prince William Sound, thereby increasing chances of diet switching to include sea otters. This does not appear to have happened yet, judging from the slowly increasing or stable populations of sea otters in unoiled portions of Prince William Sound compared with the rapidity with which the sea otters would be decimated by feeding killer whales (Estes, 1999; Garshelis and Johnson, 1999). The continuing decline in harbor seals and their lack of recovery may also have the chronic effect of inhibiting recovery of transient killer whales such as the AT1 pod which consume them and which apparently suffered large losses after the oil spill (Matkin et al., 1994, 1997). Because environmental contaminants become concentrated in the tissues of these mammal-eating killer whales, there is also a potential for petroleum hydrocarbon contamination to affect reproductive success and provide a lingering effect of the oil spill (Matkin et al., 1997).

64

5.5.

CHARLES H. PETERSON

Shorebirds, seaducks and seabirds

The immediate impact of the oil spill on seabirds of all types was large, with more known deaths than have occurred in any other oil spill (Piatt and Lensink, 1989). Losses were evidenced by collections of oiled dead birds made during the extensive shoreline walks in the months following the spill (Piatt et al., 1990). In addition, declines in bird abundances and changes in bird distribution were evident for many species in analysis of results of shoreline bird surveys made in several of the years following the oil spill for comparison to analogous pre-spill surveys from 1984-85 (Murphy et al., 1997; Irons et al., 2000). From these two types of information, it is clear that there was substantial acute mortality of shorebirds and seaducks that forage on shore invertebrates and seabirds that feed on coastal forage fish (Tables 12, 13). Wiens et al. (1996) performed community analyses on survey data from 1l cruises between summer 1989 and summer 1991. These authors demonstrated that the numbers of species in each of three guilds of birds that feed near shore exhibited immediate reductions with oiling whereas the offshore feeding guilds did not show the same level of response to the spill. Impacts on bird numbers persisted at a statistically detectable level only through summer 1990 (Wiens et al., 1996), although densities of several individual bird species continued to suffer chronic effects for some years (Irons et al., 2000). Several species of shorebirds and seaducks forage on invertebrate prey from the intertidal zone or shallow subtidal zone of the coast, where exposure to residual oil during feeding might be anticipated to cause chronic injuries after the acute effects of the spill had passed. Those abundant birds that consume shoreline invertebrates in the spill area include black oystercatcher, glaucous- winged gull, mew gull, surfbird (Aphriza virgata), surf scoter ( Melanitta perspicillata), Barrow's goldeneye ( Bucephala islandica (Gmelin)), black turnstone (Arenaria melanocephala (Vigors)), and harlequin duck. Of these species, direct studies of the black oystercatcher and harlequin duck were conducted in response to the oil spill, with some additional biochemical data taken on Barrow's goldeneye (Table 12). Black oystercatchers are the only shorebird examined in targeted evaluations of impacts following the "Exxon Valdez" oil spill. Survey data comparing pre-spill counts in 1972 or 1984-85 to post-spill counts of all birds demonstrated significant declines in oiled areas relative to control areas for black oystercatchers in multiple years after the oil spill, despite using differing methodologies and spatial scales (Klosiewski and Laing, 1994; Day et al., 1995, 1997a; Irons et al., 2000). The Klosiewski and Laing (1994) analyses suggested that the negative effect of the oil spill on black

EFFECTS OF "EXXON VALDEZ" OIL SPILL

65

Table 12 Effects of shoreline oiling and/or treatment on the guilds of birds that feed prominently on intertidal and shallow subtidal invertebrates (shorebirds, seaducks).

Effect

Duration

Source(s)

Direct acute responses

Substantial numbers of dead oiled birds recovered on shore (seaducks second only to alcids in numbers) Shoreline surveys show statistically detectable declines in abundance of some groups on oiled shores vs. control shores in contrast to pre-spill expectations

1989

Piatt et al., 1990

1989

Klosiewski and Laing, 1994; Day et al., 1995, 1997a, b; Irons et al.. 2000

1990, with recovery by 1993 1990

Klosiewski and Laing, 1994

Indirect or chronic delayed responses

Black oystercatcher counts showed further declines on oiled shores after 1989 drop Black oystercatchers that used oiled mussels fed chicks more to achieve less growth, fledged them later, and laid fewer eggs on renesting Nesting of black oystercatchers on oiled Green Island disrupted while stable on Montague Harlequin duck counts show recovery not initiated until 1991 at earliest Harlequin duck counts show depressed overwinter survival of adult females Harlequin duck shows P450 induction Winter counts of harlequin ducks are declining in western (oiled) Prince William Sound as compared with the east Barrow's goldeneye counts show growing divergence between oiled and unoiled areas Barrow's goldeneye shows elevated P450 enzyme

Andres, 1996, 1997

recovery by 1993

Sharp et al, 1996

until at least 1991

Klosiewski and Laing, 1994; Day et al., 1995, 1997a; Irons et al., 2000 Esler et al., 2000

1995-96, 1996-97, 1997-98 1998

Trust et al., 2000

through 1997-98

Rosenberg and Petrula, 1998; Rosenberg, 1999

through 1998

Holland-Bartels et al., 1999; Irons et

1996-97

Trust et al., 2000

al., 2000

66

CHARLES H. PETERSON

oystercatchers increased between 1989 and 1990. Irons et al. (2000) show that the significant depression in black oystercatcher abundance in oiled areas disappeared by 1993 and 1996. Day et al. (1995, 1997a) and Murphy et al. (1997) show evidence of black oystercatcher recovery in oiled habitats by 1991. The synthesis of these analyses of survey counts would suggest that black oystercatchers suffered an immediate effect of the oil spill on abundance in oiled shores, that the effect may have grown between 1989 and 1990, but it had largely disappeared by 1991-93. The Klosiewski and Laing (1994) analysis implied that about 25% of the March population for Prince William Sound was removed by the oil spill, so a large part of this response occurred at a population rather than simply at a behavioral level. Nevertheless, only nine black oystercatchers were recovered as dead oiled birds, so the magnitude of the immediate, direct spill impact to the population abundance is still in doubt. A study of potential chronic effects on black oystercatchers feeding on oiled mussels showed that the proportion of non-breeding pairs was higher on oiled shores, that oystercatcher eggs were smaller and, in 1989, that chick mortality was enhanced on oiled shores in direct proportion to the degree of oiling in foraging territories (Sharp et al., 1996). Chick production in 1990 continued to be depressed on oiled shores. Because of the territorial nature of black oystercatchers during the breeding season these birds are not only a good candidate for rigorous study but also at risk of greater injury from shoreline alterations. The observations of Sharp et al. (1996) demonstrate a chronic effect of the oil spill on the population of black oystercatchers, operating through impacts of hydrocarbon contamination of the intertidal feeding areas. Andres (1996, 1997) showed that in 1991 and 1992 black oystercatchers foraged within oiled mussel beds, consumed and did not avoid oiled mussels, and fed chicks more to achieve less growth when foraging on oiled sites (Figure 13). Renesting produced fewer and smaller eggs on oiled than on unoiled sites. These results indicate chronic reproductive impairment of black oystercatchers operating through continuing exposure to hydrocarbon contamination of prey, including mussels from oiled mussel beds. None of the other shorebirds that consume mussels and other intertidal invertebrates was the target of an explicit study to evaluate impacts of the oil spill. Furthermore, the other shorebirds, black turnstone (Arenaria melanocephala (Vigors)), surfbird and ruddy turnstone (Arenaria interpres (L.)), were not sufficiently abundant in the shoreline surveys (Day et al., 1995, 1997; Murphy et al., 1997; Irons et al., 2000) to allow analysis of their abundance patterns. The gulls (mew gull, and glaucous-winged gull that often consume benthic invertebrates from intertidal shores, also scavenge fish, so their abundance changes after the oil spill cannot be readily related to impacts on shoreline invertebrate prey quality and quantity.

67

EFFECTS OF "EXXON VALDEZ" OIL SPILL 0.6'20 -

~:

B

A

3.8

3.6

o e >

0.010

3.4 .9 ° 3.2

'5 E:: ._m

3.0

0.000 oiled

-

-

unoiled

oiled

2.0 ¸

unoiled

i

C 1.0

0.0

I! oiled

unoiled

Figure 13 Black oystercatchers in Prince William Sound in 1992. Mean differences (+SE) in: A) daily growth rate of chicks (log. of daily weight gain/1. daily tarsus change); B) ratio of food eaten by chicks relative to chick weight; and C) numbers of eggs laid in second nesting after loss of the first nest. White columns unoiled sites; black columns oiled sites. (Data from Andres, 1997.)

The harlequin duck is the only seaduck for which directed studies assessed the response to the oil spill (Table 12). Seaducks were second only to alcids in numbers of dead oiled birds recovered after the spill (Piatt et al., 1990). The harlequin duck consumes benthic invertebrates, especially gastropods and a small proportion of mussels. Harlequins suffered losses of about 1000 individuals from direct oiling during the spill (Piatt et al., 1990; Holland-Bartels et al., 1998). This loss affected the total population in the spill area sufficiently to be detectable as a significant decline in 1989 abundance in oiled areas relative to unoiled controls in almost all of the analyses of shoreline survey data (Klosiewski and Laing, 1994; Day et al., 1995; Irons et al., 2000; but not in Murphy et al., 1997). Recovery of harlequin ducks has not occurred rapidly following this acute-phase mortality and there is evidence of persistent chronic effects of the oil spill. All analyses of the survey data show delayed recovery through at least 1991. In the three summers following the oil spill,

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CHARLES H. PETERSON

breeding was apparently unsuccessful over much of the spill area in western Prince William Sound in contrast to the modest amount of reproductive output of harlequins in the eastern sound (Patten, 1993). Given the shy nature of harlequin ducks, this response may have been induced by continued disturbance during shoreline treatment (Wiens, 1995) rather than through changes to the shoreline habitat and resources. Furthermore, habitat differences in the western portion of Prince William Sound may naturally depress breeding success compared with the eastern sound (Rosenberg and Petrula, 1998). However, overwintering survival of female harlequins has been shown through individual tracking by radio telemetry to be lower along oiled shores in 1995-96, 1996--97 and 1997-98 (Esler et al., 2000). This survivorship problem is accompanied by evidence of induction of P450 1A detoxification enzyme in harlequins in 1998 (Trust et al., 2000). Winter counts of harlequin ducks in the western (oiled) region of Prince William Sound are still diverging from those in the eastern portion in an independent survey conducted from 1994-98 (Rosenberg and Petrula, 1998; Rosenberg, 1999). Consequently, this species of seaduck that is closely tied to shoreline habitats and resources for foraging appears to be experiencing long-term chronic impacts from the spill (Table 12). Some other groups of seaducks are abundant enough to allow analysis of oil impacts through the shoreline survey data. On oiled shores there was a big decline of the seaduck that feeds mostly on mussels, Barrow's goldeneye (Bishop et al. in Holland-Bartels et al., 1998). There was no evidence of recovery through the 1998 survey (Day et al., 1995, 1997a; Irons et al., 2000; Holland-Bartels et al., 1999). In addition, samples of Barrow's goldeneyes collected from oiled shores in Knight Island in December 1996 and February 1997 showed induction of P450 1A enzyme when compared with ducks from unoiled sites on Montague, indicating persistence of the detoxification induction (Trust et al., 2000). Other seaducks, such as the common goldeneye and the scoters (surf, black and white-winged), have shown no decline in abundance on oiled shores since the oil spill (Day et al., 1995, 1997a, b; Murphy et al., 1997; Irons et al., 2000). There is a possibility of persistent indirect effects of the oil spill acting through continued depression of abundances of forage fishes (Table 13), such as Pacific herring, which are of such widespread importance to many vertebrate consumers in this ecosystem (SAI, 1980; Hood and Zimmerman, 1986). Along oiled shores there were persistent reductions in abundance through at least 1998 in cormorants (particularly the pelagic: Phalacrocorax pelagicus Ridgway), mergansers (the common: Mergus merganser (L.); and red-breasted: Mergus serrator (L.)), black-legged kittiwake (Rissa tridactyla L.), murres (Uria spp.), and the pigeon

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Table 13 Effects of shoreline oiling and/or treatment on the guild of birds that consume forage fish prey from nearshore habitats.

Effect

Duration

Source(s)

Direct acute responses

Substantial numbers of dead oiled birds recovered on shore Shoreline surveys show statistically detectable declines in abundance of some groups on oiled shores in contrast to pre-spill expectations or to control shores

1989

Piatt et al., 1990

1989

Klosiewski and Laing, 1994; Day et al., 1995, 1997a: Murphy et al., 1997; Irons et al., 20OO

through at least 1998 (except for 1993 for loons)

Irons et al., 2000

1993-98

Oakley and Kuletz, 1996

Indirect or chronic delayed responses

Cormorants, black-legged kittiwake, murres, pigeon guillemot, mergansers and loons show continued depression in census counts on oiled shores vs. expectation Pigeon guillemot shows lower productivity of young, lighter fledgling weights with reduced proportions of high-lipid forage fishes in diets at oiled Naked Island complex

guillemot (Klosiewski and Laing, 1994; Day et al., 1995, 1997a; Murphy et al., 1997; Irons et al., 2000). These may be related to reduced abundance of forage fishes, at least partially in response to the oil spill. The pigeon guillemot appeared to be especially affected by the oil spill because of its restricted foraging to within only about 2--6 km of its shoreline nest and its use of shallow demersal fishes along with schooling forage fishes in the nearshore zone. Abundance of pigeon guillemots declined by 43% from the early 1980s to 1989 during nest attendance on the Naked Island complex, but some fraction of this decline can be associated with a regional decline over this time period (Oakley and Kuletz, 1996). The large decline in abundance and biomass of intertidal fishes (Barber et al., 1995) that persisted through 1990 and 1991 implies a reduction in prey abundance for pigeon guillemots. Ongoing research is successfully relating the productivity of young and consequent recovery dynamics of pigeon guillemot populations to availability of high-lipid forage fishes like herring, capelin and sand lance (Duffy, 1998). To the degree that these schooling forage fishes were or remained depressed in abundance by the

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oil spill, this represents a type of indirect effect, which incorporates delayed responses of consumer species through trophic interactions (Table 13). The evidence linking persistent declines in Pacific herring to the oil spill is not strong, so these important trophic effects on murres, kittiwakes and other unstudied vertebrate consumers of forage fishes may only partly be related to the oil spill (Duffy, 1998).

6. 6.1.

DISCUSSION Interaction webs

Analysis of food webs in ecology has a long history of providing insights about community processes (Elton, 1966; Pimm, 1982; Rafaelli and Hall, 1992). Food webs represent an essentially static accounting of the natural history and structure of trophic interactions that can suggest potentially important direct and indirect linkages between component species. By adding information about energy flow along the various pathways that link the species in a food web, the resulting energy flow webs summarize the consumption of food by source over some specified period of time in some explicit location. Such energy flow diagrams have been used to explain and even predict dynamics of changes that cascade through ecosystems, notably in pursuit of improved understanding of impacts on fishery production (ECOPATH of Christiansen and Pauly, 1992). Energy flow webs have also served as the basis for construction of dynamic models to evaluate the stability of alternative community structures (Pimm, 1991). Such uses of energy flow webs are risky because of many assumptions necessarily made about dynamics when using an approach based on static observations (Paine, 1980, 1988; Menge, 1995). A new form of dynamic modelling of trophic interactions (Waiters et al., 1997) is addressing some of the shortcomings of the ECOPATH approach, but this analysis is still based upon trophic interactions exclusively. What is truly needed is an approach based upon the complete suite of interactions that affect community and ecosystem dynamics, involving not only trophic interactions but also effects of biogenic habitat provision and physical (and chemical) habitat modification (Menge, 1995). A fundamental limitation to the use of interaction webs for understanding community and ecosystem dynamics is the need for information about interaction direction and strength for so many species and so many potential interactions of multiple types. Such information is best obtained by experimental manipulation, but for few communities is such experimentation even feasible. For this reason, it is important to take

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advantage of an event such as the "Exxon Valdez" oil spill to serve as an unplanned perturbation of the ecosystem that can illuminate important relationships and interactions. A limitation to strong inference about the role of both direct and indirect interactions in the ecosystem based on effects of an oil spill or some other perturbation is the absence of complete understanding of mechanism of interaction (Yodzis, 1988). However, this shortcoming applies generally to the scientific literature on indirect interactions (Fairweather, 1990), with only a small number of studies truly evaluating the mechanisms of indirect effects (Dungan, 1986; Schmitt, 1987; Wootton, 1992). We do not even know generally the degree to which an oil spill should be viewed as a pulse perturbation (Bender et al., 1984), with subsequent delayed recovery arising as a consequence of indirect effects from the initial injury, or, alternatively, a press perturbation, in which chronic exposure is still causing delayed recovery. However, the effects of the "Exxon Valdez" oil spill are here segregated into acute direct effects and indirect or chronic delayed effects (Tables 4-13). This provides a strong case for treating the "Exxon Valdez" oil spill and by implication other oil spills as both a pulse and a press perturbation because of the dramatic acute effects and the multitude of important chronic impacts. At the most descriptive level, the oiling of the intertidal zone and the contamination of shallow subtidal sediments acted as a marker to identify the many connections between the shoreline benthic habitat and important members of adjacent systems. So much past research in intertidal communities has focused on the plants and sessile animals that permanently reside on the shore that the open nature of shoreline systems is easily overlooked (Underwood and Denley, 1984). Not only does the shoreline form a triple interface between land, air and water as physical realms, but it also represents the locus of biological interaction and flows between realms (Polis and Hurd, 1996; Polis et al., 1997; Ben-David et al., 1998). The "Exxon Valdez" oil spill demonstrated the use of intertidal resources by terrestrial mammals, like bears and deer, that forage on intertidal food sources when land foods are unavailable. The significance of this interface for aerial consumers typically considered members of terrestrial ecosystems was made evident by oiling impacts. Bald eagles and northwestern crows forage and scavenge extensively along the shore, thereby allowing a further flow of energy from the marine to the terrestrial environment and establishing a pathway of functional connectivity. Similarly, fishes generally viewed as pelagic make important use of shoreline habitats for spawning, thereby linking the health of the marine pelagic ecosystem in part to the condition of shoreline habitats. This reproductive connection between the sea and the shore comes as no surprise when it involves anadromous

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fishes like salmon, but the importance of shoreline habitat to the most numerically and functionally significant forage fishes, Pacific herring, sand lance and capelin, receives new emphasis. The importance of shoreline haul-outs to marine mammals is already well appreciated. The oil spill highlights the importance of further interactions connecting intertidal resources, such as mussels and other shoreline invertebrates, and forage fishes that are themselves linked to shoreline habitats together with aquatic mammals like harbor seals and river otters. The high value of the shoreline habitats as productive foraging grounds for species from these other systems is made evident by reviewing the web of impacts of the oil spill. At a more dynamic level, the oil spill perturbation helped identify some important interactions emanating from shoreline impacts. Within the intertidal community itself, the reduction in herbivorous gastropods and loss of most of the perennial Fucus high on shore, together with fertilizer application as a bioremediation treatment, opened space and reduced herbivory, allowing colonization and expansion of more ephemeral, annual algae. This response appeared to be modest, more like the aftermath of the "Amoco Cadiz" than the greening of the shore seen after the "Torrey Canyon" and some other oil spills (Southward and Southward, 1978; Southward, 1982; Kingston et al., 1997). The modest greening response is somewhat surprising for the high intertidal rocky shore, where the dominant grazer, the limpet Tectura persona, was so dramatically removed by the oil and shoreline treatment. However, the greening by ephemeral algae may have been more evident had assessment studies in Prince William Sound been successful in 1989, the first summer after the spill. The replacement of the typically dominant balanoid barnacles by the normally competitively inferior Chthamalus dalli is consistent with our understanding of life histories and competitive dynamics between barnacles (Connell, 1961), but the magnitude of the response was a surprise. This explosion in abundance of Chthamalus dalli represents a likely consequence of three indirect interactions. First, space on the higher levels of the intertidal shore was opened up by loss of Fucus gardneri and balanoid barnacles. Second, reduction of grazing by loss of limpets, especially Tectura persona, high on shore, is likely to have enhanced survival of newly settled barnacles (Dayton, 1971). Third, the reduction in the barnacle's principal predator, the drill Nucella lamellosa (Ebert and Lees, 1996), doubtless reduced predation mortality on juvenile and older barnacles. The large effect of trophic stimulation, first of hydrocarbon-degrading microbes, then of oligochaetes, and other infaunal opportunists, especially several surface deposit-feeding polychaetes, is also consistent with our understanding of the enrichment response to injection of petroleum hydrocarbon (Spies and Desmarais,

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1983). This apparent cascade of effects through the food chain suggests, however, that a strong bottom-up interaction helps organize this sedimentary community. Interestingly, the taxa most sensitive to toxicity and that apparently suffered mortality from oil exposure in eelgrass habitat include important predatory seastars and a crab. Declines in these predators could have enhanced the stimulatory effect by providing a simultaneous release from top-down controls of abundances of sessile invertebrates, especially including the small mussel Musculus. This in turn may have attracted some demersal fishes, such as the juvenile Pacific cod, that feed on these benthic prey. The greater incidence of larger green sea urchins along northern Knight Island also implies operation of a top-down effect of removing the urchin's principal predator, the sea otter (Dean et al., 2000). The knowledge gained about interaction webs from the studies of the "Exxon Valdez" oil spill has a direct application to planning the responses to future oil spills. Because the aggressive treatment of oil on beaches caused so much mortality of intertidal plants and invertebrates, this approach has been criticized (Mearns, 1996). It was initially justified as a means to speed up the disappearance of the oil from the shore and the degradation of the oil by enhancing microbial oxidation processes. From our newly informed understanding of interaction webs, some conclusions about beach treatment seem justified. First, the aggressive treatments do seem to have speeded up the chemical degradation and transport of the oil off the beaches, although winter storms were more effective (Michel and Hayes, 1993; Gibeaut and Piper, 1997). Secondly, the concern over exposing birds and mammals to oil injury by leaving the beaches oiled seems well placed in that both terrestrial and marine mammals and birds experienced oiling and oil impacts through exposure on the shoreline. Chronic effects on some coastal birds and mammals continued after the initial acute mortality had ceased, so rapid removal of oil from the shoreline may be a means of reducing the level of chronic impacts. Yet, thirdly, the application of some treatments, notably pressurized hot-water wash, caused high mortality of shoreline invertebrates and plants that exceeded the direct effects of the oiling (Houghton et al., 1996b; Lees et al., 1996). Pressurized washing also displaced sediments down slope and thereby may have caused a long-term reduction in habitat function and value of intertidal sedimentary habitat for clams (Driskell et al., 1996). Fourthly, the failure to remove oil from under oiled mussel beds led to long-term contamination of mussels and likely exposure of their many predators. Fifthly, the intertidal community of rocky shore invertebrates and plants achieved substantial recovery after about 3 years, but in several ways the effects lingered. Sixthly, the subtidal sedimentary communities, where displaced oil came to reside in

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presumably higher amounts because of the intensive shoreline treatments, exhibited only some limited evidence of toxicity response at shallow depths and mostly showed trophic enrichment. Seventhly, the failure to direct treatment operations towards the oiled intertidal gravels of anadromous fish streams resulted in long-term chronic mortality of pink salmon eggs. From these conclusions, the following responses should be considered for future oil spills. Some directed treatment of shorelines seems justified wherever avian or mammalian use is frequent. In areas of little or no value to avian and mammalian consumers, shoreline treatment needs to be justified by some other consideration that must outweigh the likely injury to invertebrate and plant communities. A viable alternative to application of pressurized hot water should be pursued to avoid the most intense injury. Pressurized wash should not be applied to sedimentary shores at all because of risk of long-term habitat damage. Bioremediation seems a useful tool with likely benefits and no evident gross harm. Oiled mussel beds and other structural geological or biological habitat features that serve to armour the sediments from access by oxygenbearing water flows deserve special consideration and treatment, perhaps by the temporary removal of the overlying mussels (Babcock et al., 1997; Carls et al., 2000). Any beaches of importance for human uses such as subsistence or shellfishing, especially for suspension-feeding invertebrates that concentrate pollutants, need special attention. There should be full collaboration with the user groups to guarantee that information is exchanged and values to different stakeholders are considered in the response planning. Oiling of the banks of streams used by anadromous fishes represents such a severe risk of long-term injury to the fishes, such that some drastic measures may be called for to prevent oil from grounding at the mouths of those streams at all. Once oiled, removal of the oil without damaging the eggs of early life stages of the fishes seems an impossible mandate. Consequently, despite the toxicity of first generation oil-spill removers or dispersants (Smith, 1968; Southward and Southward, 1978), there is justification for limited use of better formulated dispersants on slicks that might encroach on habitats of anadromous fishes.

6.2.

Ecotoxicology vs. field assessment as approaches

There is growing use of risk assessment models both in environmental regulation and also in assessment of natural resource damages following environmental pollution events (NRC, 1993). For assessment of impacts of environmental pollution, the use of field assessments employing a

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rigorous design to permit inferences about impacts is a more reliable, but more costly, approach (NRC, 1981, 1993; Teal and Howarth, 1984; Gilbert, 1987). The results of the "Exxon Valdez" oil spill help underscore and illustrate the most important shortcomings of adoption of an ecotoxicity modelling approach to assessing natural resource damages. First, in modelling damages to biological resources from an oil spill, the ecotoxicity approach includes only a limited number of major process of impact, for example, the single mechanism of acute toxicity to dissolved PAHs for water column organisms (Neff and Stubblefield, 1995), rather than inclusion of the multiple mechanisms of injury and interactions among factors that are actually involved in nature (Cairns, 1983; Teal and Howarth, 1984; Southward, 1982; Hawkins and Southward, 1992). Secondly, this approach contemplates no indirect effects of induction of injury through trophic interactions, habitat loss and other dynamic processes important in natural systems (Elmgren et al., 1980; Underwood and Peterson, 1984; Kimball and Levin, 1985; Peterson, 1993; Suchanek, 1993; Clements and Kiffney, 1994). Finally, the chronic effects that occur over longer time periods are typically excluded (NRC, 1993; French et al., 1996). The grounds for exclusion of multiple interacting mechanisms, indirect effects and chronic impacts are based on the lack of information needed to incorporate them into the modelling and the high uncertainty involved in applying that information. The use of ecotoxicity modelling could conceivably be made complementary to field assessment by illuminating mechanisms, if a sufficient diversity of mechanisms were included in the toxicity assessments using the actual species of interest, and by applying knowledge of dose-response relationships to permit extrapolation of field conclusions. However, even this meshing of laboratory-based toxicity tests with field assessments would never provide mechanistic understanding of chronic, indirect, or delayed impacts. Ecotoxicology does play an important role in identifying the most sensitive species in advance of an oil spill, so that spill response may be based on protecting them and assessing injury to them. Many of the studies of impacts of oil spills serve to demonstrate important roles that multiple mortality factors can play in producing even the acute mortalities observed during the spill (NRC, 1985; Suchanek, 1993). The intertidal community includes organisms such as echinoderms, crabs and amphipods, that are sensitive to dissolved PAHs and other toxic components of petroleum hydrocarbons (Hyland and Schneider, 1976), but shoreline organisms are also at risk to many other processes beyond those revealed by standard toxicity tests. They suffer direct contact with masses of oil, which can enhance exposure to toxicants (Sanders et al., 1978). Layers of oil can kill intertidal animals by purely physical suffocation, even animals not sensitive to exposures to

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toxic compounds. Chemicals such as the dispersants used to treat oil spills can be toxic and interact with oil to enhance kills of intertidal animals (Smith, 1968; Malins and Collier, 1981; Southward, 1982) and invasive shoreline treatment can cause widespread mortality (Mearns, 1996). For some marine mammals, like sea otters, the loss of insulation efficiency through oiling of fur or the ingestion of oil from preening oiled fur is viewed as the major route of injury from spilled oil (Ballachey et al., 1994), but the studies of harbor seals following the "Exxon Valdez" oil spill revealed that mortality was induced by breathing toxic fumes from volatilized components of the oil (Frost et al., 1994). Complete models of direct acute mortality from oil spills must thus include a diversity of mechanisms to synthesize these direct effects. There is such great uncertainty associated with predicting the indirect effects of modifications to a community that oil spill impact models do not even attempt to incorporate the top-down trophic cascades and bottom-up effects of interactive dyaamics that are known to affect marine communities (Estes and Palmisano, 1974; Menge et al., 1994; Menge, 1995). The complexity of various interactions that are involved in creating important indirect effects in communities (Wootton, 1994; Menge, 1995) renders difficult even the interpretation of observed community dynamics. Nevertheless, this review of the chronic, indirect and delayed effects of the "Exxon Valdez" oil spill (Tables 4-13), when taken together with long-term evaluation of the "Torrey Canyon" oil spill (Hawkins and Southward, 1992), shows that any model of the impact of an oil spill or some other environmental perturbation would be grossly incomplete if only acute toxic effects were included. This review addresses only those effects of the "Exxon Valdez" oil spill that were induced by oiling and subsequent treatment of shoreline habitats, and there are additional demonstrations of chronic impacts of the spill that are not even discussed here. For example, the slow progression in date of initiation of breeding in common murre colonies of the Barren Islands and the time lags in initiating numerical recovery that are explained by recruitment failures for years after the spill when breeding was not initiated early enough (Rosenau et al., 1998, 1999) represent a compelling example of delayed effects unrelated to shoreline oiling. Thus, the indirect and chronic delayed effects identified in Tables 4-13 represent a subset of available examples. The synthesis of results of studying multiple individual species responses along with the trajectory of habitat changes following the "Exxon Valdez" oil spill illustrates the likely contributions of several indirect or chronic delayed effects (Tables 4-13). Most examples involve bottom-up effects moving up the food chain. These include the likely trophic stimulation of sedimentary invertebrate food chains by the

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petroleum hydrocarbon enrichment. Production of hydrocarbon-degrading bacteria was enhanced (Braddock et al., 1996), as was oligochaete abundance (Gilfillan et al., 1995a; Highsmith et al., 1996) and abundance of many deposit-feeding polychaetes in shallow subtidal sediments in protected embayments (Jewett et al., 1999). There was probably also some enhanced production of demersal fishes, crabs or shrimps at an even higher trophic level, but no study evaluated production of the appropriate species of these mobile consumers in shallow waters. Another likely indirect effect of the "Exxon Valdez" oil spill is the biological consequence of loss of fine sediments from the intertidal by flushing them down slope during pressurized water treatment of shorelines. The reduction in habitable sediments may explain the depressed recruitment and slow recovery of clams on oiled and treated shores (Driskell et al., 1996; Shigenaka et al., 1999). Potentially, the most important indirect bottom-up effect suggested by synthesis of the results of evaluation of the effects of the "Exxon Valdez" oil spill is the reduction of Pacific herring populations and perhaps also of other high-lipid forage fishes. The dynamics of marine mammal and seabird populations in the entire north Pacific region appear intimately related to availability of forage fish food sources (NRC, 1996), so depression of herring and other forage fishes is a tenable explanation for failure of harbor seal and pigeon guillemot populations to show recovery. Some undetermined fraction of the forage fish depression in Prince William Sound may be traceable to oil spill impacts, thereby establishing the indirect bottom-up linkage to impacts on some seabirds and marine mammals. Fewer top-down indirect effects are suggested by the post-spill studies (Tables 4-13). One of these, the increase in size of the green sea urchin along northern Knight Island, apparently in response to ongoing depression in local abundance of their principal predator, the sea otter, occurs early on in recovery, but may not develop further if sea otters return in greater numbers. The enhancement of annual algae on intertidal rocks a year and a half after the oil spill also represents a top-down effect, since removal of so many of the grazing limpets and periwinkles released those algae from herbivory. Other indirect and delayed effects observed in the intertidal benthic community are more readily related to release from competition, like the explosion of Chtharnalus dalli after removal of balanoid barnacle competitors. Competitive pre-emption of space is also the best explanation for the delay in return of red algae lower on rocky shores where Fucus gardneri had spread soon after the spill. Chronic impacts of oil spills are even less well appreciated than indirect effects emanating from species interactions (Boesch and Rabalais, 1987; Olsgard and Gray, 1995; Peterson et al., 1996). Chronic effects that influence population size and community composition act often through

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inducing reproductive impairment or by harming the health of exposed individuals sufficiently to shorten their life spans through interactions with disease or other stresses. Among the responses to the "Exxon Valdez" oil spill are some reproductive impacts in nearshore vertebrates best interpreted as chronic spill effects. The chronic effect that is best understood, and probably least anticipated, is the multi-year impact of oil tidally pumped from subsurface reservoirs along anadromous fish streams into the stream, where it chronically reduced egg survival of pink salmon (Heintz et al., 1999; Murphy et al., 2000). This process represents the imposition of chronic toxicity of weathered oil (the higher molecular weight PAHs) acting on fish eggs. Avoiding a similar chronic route of injury in a future spill that threatens anadromous fish streams poses a serious challenge to disaster planners. Another clearly demonstrated chronic effect is the impact of oiled prey on black oystercatchers, with consumption of contaminated mussels by chicks requiring more food to reach fledging size and delaying the date of fledging (Andres, 1996, 1997; Sharp et al., 1996). These chronic effects help explain the delay in recovery of black oystercatcher populations. The depression in overwinter survivorship of harlequin ducks that persists into the 1997-98 winter (Essler et al., 2000) may reflect a chronic impact of oil exposure. Other species such as Barrow's goldeneye may be suffering analogous chronic effects of the oil spill in the form of reduced survivorship or reproductive impairment. However, apart from evaluation of their detoxification enzyme system no direct study was made into the cause of their delayed recovery. Despite varying levels of uncertainty that necessarily accompany each individual example of an indirect or chronic delayed effect in the body of information produced following the "Exxon Valdez" oil spill, the examples when synthesized into a single set of responses (Tables 4-13) provide compelling support for concluding that use of an ecotoxicity modelling approach for assessing biological impacts of an oil spill would seriously underestimate the actual responses.

6.3. Understanding delayed recoveries It is quite clear that recovery did not uniformly begin immediately after the end of the acute mortality phase of the "Exxon Valdez" oil spill, but that many species suffered delays of several years before initiating recovery (Tables 4-13). Such delays are typical of indirect effects (Schoener, 1993) and of chronic impacts (Boesch and Rabalais, 1987). These two categories of response represent the biggest challenge to assessment of spill impacts because of their unpredictability, undefined but extended time frames, and the ambiguity and uncertainty in their

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assessment protocols. Perhaps the only way to evaluate these delayed effects is through intensive long-term study of multiple components of the ecosystem following an oil spill (Hawkins and Southward, 1992). Only the "Torrey Canyon" oil spill allows as much synthesis as can be obtained from review of the "Exxon Valdez" because of the scope, intensity and duration of the study effort. The persistence of subsurface pools of partially weathered oil in oiled mussel beds, banks of anadromous fish streams, and under boulder armour represents a likely link to many of the shoreline species that have exhibited delays in initiating recovery. During the process of shoreline treatment in summers of 1989, 1990 and 1991, the decision was made to avoid aggressive pressurized hot-water treatment of dense mussel beds because of concern about removing such an important prey resource (Mearns, 1996). Likewise, aggressive treatment of anadromous fish streams was avoided to prevent damage to salmon eggs and early life stages. Yet, the way that dense mussels shelter underlying sediments from access to oxygenated water flows and thus preserve high concentrations of very slowly weathering oil (Babcock et al., 1996; Boehm et al., 1996; Carls et al., 2000) came as a surprise. This oil continued to contaminate mussels locally in the oiled mussel beds for years after the oil spill (Harris et a l , 1996) and ultimately required special remediation (Babcock et al., 1997). Thus, for years these oiled mussel beds acted as a route of contamination of mussels and of predators that feed on mussels or in the dense mussel beds. In addition, the way that subsurface pools of weathered oil could be tidally pumped into anadromous fish streams and could still induce toxicity through impacts on fish eggs (Heintz et al., 1999; Murphy et aL., 2000) was unexpected. It is unclear to what degree various vertebrate consumers of mussels target their foraging towards dense mussel beds, which contain only a small fraction of all shoreline mussels (Boehm et al., 1996). Nevertheless, these oiled mussel beds occur in relatively sheltered sites and offer high mussel availability, so it is reasonable to expect them to represent preferred feeding sites for many vertebrate consumers. Because vertebrate consumers typically ingest the entire mussel along with shell and attached sediments, the route of chronic exposure includes a pathway not only through the tissues of the mussels but also through the surrounding abiotic medium, thus enhancing risk. The birds of this system whose diets contain most mussels are Barrow's goldeneye (95%), surfbird (75%), surf scoter (50%), and black oystercatcher (30%) (Bishop et al. in Holland-Bartels et al., 1998). The surfbird was not sufficiently abundant to be assessed adequately in shoreline surveys, but the Barrow's goldeneye and black oystercatcher represent two of the three avian consumers of shoreline invertebrates that have exhibited delays in initiating recovery (Day et al..

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1995, 1997a; Holland-Bartels et al., 1999; Irons et al., 2000). The surf scoter did not reveal any detectable effect of the oil spill on its abundance pattern (Day et al., 1995, 1997a, b; Irons et al., 2000), so it does not follow the pattern. The third species in this group of avian consumers of shoreline invertebrates that exhibited delayed recovery is the harlequin duck, which uses mussels for about 10% of its energy requirements, but also feeds on gastropods and other small shoreline invertebrates. The consumption of mussels does not represent the only pathway by which residual oil contamination may have entered the food chains leading to and potentially delaying recovery of shorebirds and seaducks. The lag in recovery of sea otters was caused at least initially by higher overwinter mortality of juvenile otters, the age class that is heavily dependent on mussels because of their ease of capture. Consequently, there is a link to mussels that may partially explain why some consumers of shoreline invertebrates did not initiate recovery immediately after the oil spill. The oil spill reduced populations of forage fishes, especially Pacific herring and perhaps also sand lance and capelin in the spill area. The resulting loss of a high-value food resource could explain delays in recovery of several fish-eating vertebrates of the coastal ecosystem. This hypothesis is made more attractive by recognizing that these piscivorous species that have suffered delays in recovery are species exhibiting long-term declines in the oil spill region, dating from a shift in the ocean physics in the late 1970s, namely harbor seals and pigeon guillemots. For species that are suffering food limitation already, any further reduction in abundance of high-value prey, such as a spill-related decline, would constitute a barrier to recovery of abundance to levels that would have been expected in the absence of the oil spill. However, the oil spill is probably not the major contributor to the crash in Pacific herring in 1993, so this bottom-up effect of prey limitation on forage fish eaters is only partly related to the oil spill. The importance of these persistent impacts of the oil spill, including the delayed recoveries through residual contamination of mussels, other invertebrates and shorelines, or through indirect effects on the prey base can easily be overlooked. This concern has led to the development of large multi-investigator research projects (Sound Ecosystem Assessment: Cooney, 1998; Nearshore Vertebrate Predators: Holland-Barrels et al., 1998, 1999; and Alaska Predator Ecosystem Experiment: Dully, 1998). However, despite the extensive research done after the "Exxon Valdez" oil spill, there still exists much uncertainty about the processes contributing to delays in recovery. Evaluating hypotheses to explain these delays involves taking a holistic view of the multiple interactions that drive the dynamics of the coastal ecosystem. Even in the most carefully planned experimental science, complete understanding and predictability will

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elude ecologists engaged in understanding the dynamics of ecosystems (Yodzis, 1988; Carpenter and Kitchell, 1993). Thus, the uncertainties still remaining after much study of the "Exxon Valdez" oil spill perturbation (Paine et al., 1996) are not unexpected. The insights into important processes that tie the coastal ecosystem to intertidal and shoreline habitats and their resources represent scientific progress in building the necessary components for constructing the interaction webs that characterize community and ecosystem dynamics of the northern Gulf of Alaska coastal ecosystem. A glimpse of where this information can lead comes from completion of preliminary models of ecosystem energetics for the spill ecosystem (Okey and Pauly, 1998). Subsequent work can go beyond energy flow webs to include important dynamic interactions suggested by the trajectory of the coastal ecosystem following the perturbation of the oil spill and thereby better approach the ideals of interaction webs to depict and model community and ecosystem dynamics.

7. S U M M A R Y AND CONCLUSIONS

Intense environmental perturbation was caused by oiling and subsequent treatments of shoreline habitats following the "Exxon Valdez" oil spill in 1989. Extensive field studies were made of impacts across a wide range of habitats and species. The data provide a unique opportunity to evaluate the direct and indirect linkages between shoreline habitats and the ecology of the coastal ecosystem of Prince William Sound and the northern Gulf of Alaska. The intertidal zone experienced both direct oiling and targeted treatments, such as pressurized application of hot water, resulting in great increases in bare space on rocks and large reductions in cover of a fucoid alga (Fucus gardneri), dominant grazing limpets and periwinkles, blue mussels and balanoid barnacles. Subsequent indirect effects included colonization of the upper shore by ephemeral algae and an opportunistic barnacle and, in some regions, spread of Fucus gardneri into the lower shore, where it inhibited return of the typically dominant red algae. The loss of biogenic canopy habitat normally provided by Fucus depressed its local reproductive success, slowing recovery on high shores, and suppressed abundances of associated shoreline invertebrates. On mixed sedimentary shores, infaunal abundance and densities of littleneck and butter clams were reduced directly. Their recovery was still incomplete by 1997 on oiled and treated shores where fine sediments had been washed down slope during pressurized water treatment. Impacts in shallow subtidal habitats were less intense than in the intertidal zone. Densities of kelps in three rocky habitats were apparently reduced in 1989, but density recovered rapidly through recolonization by 1990. Abundances of a

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dominant crab and seastar were reduced greatly, with recovery of the more mobile species, the crab, occurring by 1991. For about 4 years, eelgrass in shallow subtidal sedimentary habitats exhibited lower plant densities and thus reduced habitat for associated animals. Abundances of several toxin-sensitive amphipods declined dramatically and had not recovered by 1995, whereas the broader shallow subtidal community of infaunal invertebrates generally revealed enhanced densities, especially evident among oligochaetes and surface deposit-feeding polychaetes. The enhancement of oligochaetes and other surface deposit feeders probably reflects an indirect bottom-up trophic enrichment driven by the documented enhancement of production of hyrocarbon-degrading bacteria. Field sampling of the shallow subtidal rocky shore also indicated indirect effects. Along northern Knight Island, where sea otter populations had not recovered even by 1997 following the oil spill, the preferred otter prey, the green sea urchin, exhibited larger body sizes, as compared with unoiled shores of Montague Island. This initial response that might be expected from release of sea otter predation, could, if sustained, lead to additional cascades of indirect effects. Scavenging terrestrial birds, such as bald eagles and northwestern crows, suffered direct mortality as adults and reproductive losses, although recovery of eagles proceeded rapidly. Abundances of small benthic fishes of the intertidal zone were 40% lower on oiled than on unoiled shores in 1990, but convergence was well advanced by 1991. No impact on these small fishes was detected in the shallow subtidal zone when assessed in 1990. Nevertheless, exposure of small benthic fishes in eelgrass habitats to hydrocarbon contamination continued until at least 1996, as evidenced by hemosiderosis in liver tissues and P450 1A enzyme induction, reflecting the continuing sediment contamination. Oiling of intertidal spawning habitat had large effects on reproduction by herring and pink salmon, demonstrating an important linkage between the intertidal zone and the pelagic system through these species of importance to the food web. Pink salmon, as well as possibly two other salmonids, Dolly Varden char and cut-throat trout, also exhibited slower growth when foraging as older juveniles and adults along oiled shorelines, which for pink salmon implies lower survival. Two other forage fishes of great importance to vertebrate consumers because of their high lipid concentrations, sand lance and capelin, also use shallow sediments for spawning and, in sand lance, for shelter: no study assessed the possibility that the oil spill may have contributed to their historically low abundance. The colony of pigeon guillemots that suffered population-level impacts of the oil spill has shown reduced feeding on these high-value forage fishes, which may contribute to the failure of pigeon guillemots to initiate recovery from the spill. The analogous failure of harbor seal populations on oiled shores of Prince William Sound to exhibit convergence to numbers expected from

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concurrent changes on control sites may also be related to low post-spill availability of high-quality forage fish prey. Sea otters exhibited not only a direct mortality of perhaps 50% of the population in the spill area but also a continuing suppression of recovery for at least four winters after the spill, during which juvenile survival was depressed on oiled shores. Both black oystercatchers, a shorebird that consumes intertidal invertebrates, and also seaducks, including harlequins and goldeneyes, that also eat benthic invertebrates, exhibited reductions in abundance on oiled shores that persisted for years after the spill. The oystercatcher was shown to consume oiled mussels from beds where contamination by only partially weathered oil persisted until at least 1994, with a resulting impact on productivity of chicks. Harlequin ducks along oiled shores exhibited enhanced overwinter mortality among adults still in 1995-96, 1996-97 and 1997-98. Consequently, important avian and mammalian predators of both schooling forage fishes and shoreline invertebrates have experienced delays in recovery through chronic and indirect effects long after the initial acute impacts of the "Exxon Valdez" oil spill. Such delayed chronic and indirect effects of oil spills are not incorporated into risk assessment models: thus estimation of oil spill injury by such models will substantially underestimate the impacts of an oil spill. These impacts can be inferred more completely by direct field sampling approaches that are rigorous and extend long enough in time to observe the dynamics of recovery processes.

ACKNOWLEDGEMENTS Partial support for preparation of this review was provided by the "Exxon Valdez" Oil Spill Trustee Council and by the University of North Carolina. The views expressed in this paper are solely the author's and do not reflect opinions of the Trustee Council, My experiences with the NSF National Center for Ecological Analysis and Synthesis (NCEAS) in Santa Barbara, California helped encourage me to undertake this task. J. Fussell, III, J. C. Ingram and S. W. Jewett helped provide species authorities. I thank A. Gunther and C. Holba for help in assembling source documents. E Mundy and S. Senner provided guidance to important documents. W. B. Driskell and H. S. Lenihan helped with some figures. I owe the opportunity to reach some level of understanding of the ecosystem dynamics of the northern Gulf of Alaska to countless numbers of Alaskan friends and colleagues who have taught me with uncommon and undeserved patience. T. A. Dean, A. Gunther, A. J. Southward, R. Spies and an anonymous reviewer provided constructive comments.

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geographic map data. "Exxon Valdez" Oil Spill Trustee Council Symposium Abstracts (Anchorage, Alaska): 319. Short, J. W., Sale, D. M. and Gibeaut, J. C. (1996). Nearshore transport of hydrocarbons and sediments after the "Exxon Valdez" oil spill. American Fisheries Society Symposium 18, 40-60. Simenstad, C. A., Estes, J. A. and Kenyon, K. W. (1978). Aleuts, sea otters, and alternate stable state communities. Science 200, 403-411. Smith, J. E. (ed.) (1968) '"Torrey Canyon" pollution and marine life'. Cambridge University Press, Cambridge and London. Sousa, W. E (1979). Experimental investigations of disturbance and ecological succession in a rocky intertidal community. Ecological Monographs 49, 227254. Southward, A. J. (1982). An ecologist's view of the implications of the observed physiological and biochemical effects of petroleum compounds on marine organisms and ecosystems. Philosophical Transactions of the Royal Society of London B 297, 241-255. Southward, A. J. and Southward, E. C. (1978). Recolonization of rocky shores in Cornwall after the use of toxic dispersants to clean up the "Torrey Canyon" spill. Journal of the Fisheries Research Board of Canada 35, 682-706. Spies, R. B. and DesMarais, D. J. (1983). Natural isotope study of trophic enrichment of benthic communities by petroleum seepage. Marine Biology 73, 67-71. Spies, R. B., Rice, S. D., Wolfe, D. A. and Wright, B. A. (1996). The effects of the "Exxon Valdez" oil spill on the Alaskan coastal environment. American Fisheries Society Symposium 18, 1-16. Stekoll, M. S. and Deysher, L. (1996). Recolonization and restoration of upper intertidal Fucus gardneri (Fucales, Phaeophyta) following the "Exxon Valdez" oil spill. Hydrobiologia 326/327, 311-316. Stekoll, M. S., Deysher, L. and Dean, T. A. (1993). Seaweeds and the "Exxon Valdez" Oil Spill. Proc. In "1993 International Oil Spill Conference (Prevention, Preparedness, Response)", pp. 135-140. American Petroleum Institute Publication 4580, Washington, DC. Stekoll, M. S., Deysher, L., Highsmith, R. C., Saupe, S. M., Guo, Z., Erickson, W. E, McDonald, L. and Strickland, D. (1996). Coastal habitat injury assessment: intertidal communities and the "Exxon Valdez" oil spill. American Fisheries Society Symposium 18, 177-192. Stewart-Oaten, A., Murdoch, W. W. and Parker, K. R. (1986). Environmental impact assessment: pseudoreplication in time? Ecology 60, 1225-1240. Sturdevant, M. V., Wertheimer, A. C. and Lure, J. L. (1996). Diets of juvenile pink and chum salmon in oiled and non-oiled nearshore habitats in Prince William Sound, 1989 and 1990. American Fisheries Society Symposium 18, 578-592. Suchanek, T. H. (1985). Mussels and their role in structuring rocky shore communities. In "Ecology of rocky coasts: Chapter VI" (E G. Moore and R. Seed, eds), pp. 70-96. Hodder and Stoughton Educational Press, Kent. Suchanek, T. H. (1993). Oil impacts on marine invertebrate populations and communities. American Zoologist 33, 510-523. Swartz, R. C., Cole, E A., Schults, D. W. and Debea, W. A. (1986). Ecological changes in the Southern California Bight near a large sewage outfall: benthic conditions in 1980 and 1983. Marine Ecology Progress Series 31, 1-13. Teal, J. and Howarth, R. (1984). Oil spill studies: a review of ecological effects. Environmental Management 8, 27-44.

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Testa, J. W., Holleman, D. E, Bowyer, R. T. and Faro, J. B. (1994). Estimating populations of marine river otters in Prince William Sound, Alaska using radiotracer implants. Journal of Mammology 75, 1021-1032. Thomas, M. L. H. (1973). Effects of bunker C oil on intertidal and lagoonal biota in Chedabucto Bay, Nova Scotia. Journal of the Fisheries Research Board of Canada 30, 83--90. Thomas, M. L. H. (1978). Comparison of oiled and unoiled communities in Chedabucto Bay, Nova Scotia. Journal of the Fisheries Research Board of Canada 35, 707-716. Trowbridge, C., Baker, T. T. and Johnson, J. D. (1998). Effects of hydrocarbons on bivalves following the "Exxon Valdez" oil spill. "Exxon Valdez" Oil Spill State/Federal Natural Resource Damage Assessment Final Report (Fish/Shellfish Study Number 13), Alaska Department of Fish and Game, Commercial Fisheries Management and Development Division, Anchorage, Alaska. Trust, K. A., Esler, D., Woodin, B. R. and Stegeman, J. J. (2000). Cytochrome P450 1A induction in sea ducks inhabiting nearshore areas of Prince William Sound, Alaska. Marine Pollution Bulletin 39 (in press). Underwood, A. J. and Denley, E. J. (1984). Paradigms, explanations and generalizations in models for the structure of intertidal communities on rocky shores. In "Ecological Communities: Conceptual Issues and the Evidence" (D. R. Strong, Jr., D. Simberloff, L. G. Abele and A. B. Thistle, eds), pp. 151-180. Princeton University Press, Princeton, New Jersey. Underwood, A. J. and Peterson, C. H. (1984). Towards an ecological framework for investigating pollution. Marine Ecology Progress Series 46, 227-234. Van Pelt, T. I., Piatt, J. E, Lance, B. K. and Roby, D. D. (1997). Proximate composition and energy density of some North Pacific forage fishes. Comparative Biochemistry and Physiology llSA, 1393-1398. van Tamelen, E G. and Stekoll, M. S. (1995). Recovery mechanisms of the brown alga, Fucus gardneri, following catastrophic disturbance: lessons from the "Exxon Valdez" oil spill. In "Proceedings of the third Glacier Bay science symposium" (D. R. Engstrom, ed.), pp. 221-228. US Department of Interior, National Park Service, Anchorage, Alaska. van Tamelen, P. G. and Stekoll, M. S. (1996a). Population response of the brown alga Fucus gardneri and other algae in Herring Bay, Prince William Sound, to the "Exxon Valdez" oil spill. American Fisheries Society Symposium 18, 193-211. van Tamelen, P. G. and Stekoll, M. S. (1996b). The role of barnacles in recruitment and subsequent survival of the brown alga, Fucus gardneri (Silva). Journal of Experimental Marine Biology and Ecology 208, 227-238. van Tamelen, P. G., Stekoll, M. S. and Deysher, L. (1997). Recovery processes of the brown alga, Fucus gardneri (Silva), following the "Exxon Valdez" oil spill: settlement and recruitment. Marine Ecology Progress Series 160, 265-277. Vermeer, K. (1981). Food and populations of surf scoters in British Columbia. Wildfowl 32, 107-116. Waiters, C., Christensen, V. and Pauly, D. (1997). Structuring dynamic models of exploited ecosystems from trophic mass-balance assessments. Reviews in Fish Biology and Fisheries 7, 139-172. Warwick, R. M. and Clarke, K. R. (1993). Comparing the severity of disturbance: a meta-analysis of marine macrobenthic community data. Marine Ecology Progress Series 92, 221-231.

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Wells, P. G., Butler, J. N. and Hughes, J. S. (1995). "Exxon Valdez" Oil Spill: Fate and Effects in Alaskan Waters. ASTM Publication 04-012190, American Society of Testing and Materials, Philadelphia, Pennsylvania. Wertheimer, A. C. and Celewycz, A. G. (1996). Abundance and growth of juvenile pink salmon in oiled and non-oiled locations of western Prince William Sound after the "Exxon Valdez" oil spill. American Fisheries Society Symposium 18, 518-532. White, C. M., Ritchie, R. J. and Cooper, B. A. (1995). Density and productivity of bald eagles in Prince William Sound, Alaska, after the "Exxon Valdez" oil spill. In '"Exxon Valdez" oil spill: fate and effects in Alaskan waters' (E G. Wells, J. N. Butler and J. S. Hughes, eds), pp. 762-779. ASTM STP 1219, American Society for Testing and Materials, Philadelphia, Pennsylvania. Wiens, J. A. (1995). Recovery of seabirds following the "Exxon Valdez" oil spill: an overview. In ' "Exxon Valdez" oil spill: fate and effects in Alaskan waters' (E G. Wells, J. N. Butler and J. S. Hughes, eds), pp. 854-893. ASTM STP 1219, American Society for Testing and Materials, Philadelphia, Pennsylvania. Wiens, J. A., Crist, T. O., Day, R. H., Murphy, S. M. and Hayward, G. D. (1996). Effects of the "Exxon Valdez" oil spill on marine bird communities in Prince William Sound, Alaska. Ecological Applications 6, 828-841. Willette, M. (1996). Impacts of the "Exxon Valdez" oil spill on the migration, growth, and survival of juvenile pink salmon in Prince William Sound. American Fisheries Society Symposium 18, 533-550. Willette, T. M., Cooney, R. T. and Hyer, K. (1999). Predator foraging-mode shifts affecting mortality of juvenile fishes during the sub-arctic spring bloom. Canadian Journal of Fisheries and Aquatic Sciences 56, 364-376. Wolfe, D. A., Hameedi, M. J., Gait, J. A., Watabayashi, G., Short, J., O'Clair, C., Rice, S., Michel, J., Payne, J. R., Braddock, J., Hanna, S. and Salel, V. (1994). The fate of the oil spilled from the "Exxon Valdez". Environmental Science and Technology 28, 561A-568A. Wolfe, D. A., Krahn, M. M., CasiUas, E., Sol, S., Thompson, T. A., Lunz, J. and Scott, K. J. (1996). Toxicity of intertidal and subtidal sediments contaminated by the "Exxon Valdez" oil spill. American Fisheries Society Symposium 18, 121-139. Woodin, B. R., Smolowitz, R. M. and Stegeman, J. J. (1997). Induction of cytochrome P450 1A in the intertidal fish A. purpurescens by Prudhoe Bay crude oil and environmental induction in fish from Prince William Sound. Environmental Science and Technology 31, 1198-1205. Wootton, J. T. (1992). Indirect effects, prey susceptibility, and habitat selection: impacts of birds on limpets and algae. Ecology 73, 981-991. Wootton, J. T. (1994). The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology and Systematics 2S, 443-466. Yodzis, E (1988). The indeterminacy of ecological interactions as perceived through perturbation experiments. Ecology 69, 508-515.

EFFECTS OF "EXXON VALDEZ" OIL SPILL

Appendix. Scientific names and authority for species quoted in the text by their common name. Common Name

Algae kelps

Scientific Name

rockweed

Nereocystis leutkeana Postels and Ruprecht Agarum clathratum Dumortier (previously A. cribrosum) Laminaria saccharina (L.) Lamouroux Laminaria bongardiana Postel and Ruprecht (previously L. groenlandica) Fucus gardneri Silva

Phaaerogams eelgrass rye grass

Zostera marina L. Elymus sp.

Mollusca blue mussel mussels scallop butter clam littleneck clam razor clam clams

cockle limpet periwinkles drill, whelk

Crustacea barnacles Dungeness crab helmet crab

Mytilus edulis L. Musculus sp. Mytilus trossulus Gould Chlamys rubida (Hinds) Saxidomus giganteus (Deshayes) Protothaca staminea (Conrad) Siliqua patula (Dixon) Humilaria kennerleyi Reeve Mya arenaria L. Serripes groenlandicus Brugui~re Macoma spp. Yoldia spp. Nuculana spp. Clinocardium nuttallii (Conrad) Tectura persona (Rathke) Littorina sitkana Philippi Littorina scutulata Gould Nucella lamellosa (Gmelin)

Balanus glandula Darwin Chthamalus dalli Pilsbry Semibalanus balanoides (L.) Cancer magister Dana Telmessus cheiragonus (Tilesius)

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Echinodermata

green sea urchin seastars sunflower star

Strongylocentrotus droebachiensis (O.E Mtiller) Dermasterias imbricata (Grube) Evasterias troschelii (Stimpson) Pycnopodia helianthoides (Brandt)

Fish

arctic shanny capelin crescent gunnel cut-throat trout Dolly Varden char flathead sole high cockscomb kelp greenling masked greenling Pacific cod Pacific herring pink salmon pricklebacks rock sole rockfishes sand lance walleye pollock yellowfin sole

Stichaeus punctatus (Fabricius) Mallotus viUosus (MUller) Pholis laeta (Cope) Oncorhynchus clarki (Richardson) Salvelinus malma (Walbaum) Hippoglossoides elassodon Jordan and Gilbert Anoplarchus purpurescens Gill Hexagrammos decagrammus (Pallas) Hexagrammos octogrammus (Pallas) Gadus macrocephalus "Nlesius Clupea pallasi Valenciennes Oncorhynchus gorbuscha (Walbaum) Stichaeus spp. Pleuronectes bilineatus (Ayres) Sebastes spp. Ammodytes hexapterus Pallas Theragra chalcogramma (Pallas) Pleuronectes asper Pallas

Birds

bald eagle Barrow's goldeneye black oystercatcher black turnstone black-legged kittiwake common goldeneye common merganser common murre glaucous-winged gull harlequin duck marsh wren mew gull northwestern crow oldsquaw pelagic cormorant pigeon guillemot red-breasted merganser red-winged blackbird ruddy turnstone seaside sparrow surf bird surf scoter

Haliaeetus leucocephalus (L.) Bucephala islandica (Gmelin) Haematopus bachmani Audubon Arenaria melanocephala (Vigors) Rissa tridactyla L. Bucephala clangula (L.) Mergus merganser (L.) Uria aalge (Pontoppidan) Laurus glaucescens (Naumann) Histrionicus histrionicus (L.) Cistothorus palustris (Wilson) Larus canus (L.) Corvus caurinus (Baird) Clangula hyemalis L. Phalacrocorax pelagicus Ridgway Cepphus columba Pallas Mergus serrator (L.) Agelaius phoeniceus (L.) Arenaria interpres (L.) Ammodramus maritimus (Wilson) Aphriza virgata (Gmelin) Melanitta perspicillata (L.)

EFFECTS OF "EXXON VALDEZ" OIL SPILL

Mammals black bear brown bear river otter sea otter Sitka black-tailed deer harbor seal SteUer's sea lion killer whale

Ursus americanus Pallas Ursus arctus L. Lutra canadensis Schreber Enhydra lutris (L.) Odocoileus hemionus sitkensis (Meriam) Phoca vitulina (L.) Eumetopias jubatus Schreber Orcinus orca L.

103

Reproduction and Development of Marine Peracaridans William

S. J o h n s o n , 1 M a r g a r e t

Stevens 2 and Les Watling s

1Department of Biological Sciences, Goucher College, Towson, MD 21204, USA 2Department of Biology, Ripon College, 300 Seward Street, Ripon, WI 54971, USA 3School of Marine Sciences, Darling Marine Center, University of Maine, Walpole, ME 04573, USA

1. Introduction 2. Sexual Reproduction, H e r m a p h r o d i t i s m and Sex D e t e r m i n a t i o n . . . . . . . . . . . . . . 2.1. Sex d e t e r m i n i n g h o r m o n e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Genetic d e t e r m i n a t i o n of s e x . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. E n v i r o n m e n t a l factors and s e x d e t e r m i n a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. H e r m a p h r o d i t i s m . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. A n a t o m y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Sexual d i m o r p h i s m and s e c o n d a r y sexual characteristics . . . . . . . . . . . . . . . . 3.2. A n a t o m y o f the r e p r o d u c t i v e system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. G a m e t o g e n e s i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. S p e r m a t o g e n e s i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Formation o f the s p e r m a t o p h o r e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. OOgenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. H o r m o n a l control o v e r g a m e t o g e n e s i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Reproductive Cycles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Life cycles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. R e p r o d u c t i v e timing and control o f g a m e t o g e n e s i s . . . . . . . . . . . . . . . . . . . . . . . 6. Reproductive b e h a v i o r . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6,1. Pairing and p r e c o p u l a t o r y b e h a v i o r . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. C o p u l a t i o n and fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7. D e v e l o p m e n t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Cleavage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Fate m a p p i n g , g a s t r u l a t i o n and g e r m layer f o r m a t i o n . . . . . . . . . . . . . . . . . . . . . 7.3. Differentiation o f m e s o d e r m . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4. O r g a n o g e n e s i s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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7.5. External differentiation 7.6. Larval stages and molting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. The Peracaridan Pattern of Marsupial Brooding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1. O6stegite and marsupial structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2. Internal brooding 8.3. Brooding behavior and brood care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.4, Release of the brood and parental care . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.5, Extramarsupial brooding 8.6. Brood mortality and brood parasitism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.7. Egg size, brood size and incubation time . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tabular S u m m a r y of Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Reproduction in peracarid crustaceans is characterized by direct development with the young carried by the female in a ventral brood pouch made from overlapping oOstegites. The major exception occurs in thermosbaenaceans where the young develop under a posterior extension of the carapace. Sexual reproduction is the norm, as is standard genetic development of males and females, but intersexes, males with unusual chromosome numbers and hermaphrodites occur in some species. General anatomy of the female reproductive tract is similar for all orders, differing only in the specific details. Asellote isopods develop a unique spermathecal duct for sperm storage. The male reproductive system is much more variable. In some orders it consists of paired tubes, and in others it is unpaired; sperm may be stored in the posterior region of the testes or in vas deferens; and the external genitalia may be located on the coxae or the sternites, with or without penes or other sperm transfer appendages. Sperm morphology has been considered a unifying trait for the Peracarida but, in fact, there are some significant differences among the orders. Peracaridan sperm are aflagellate. Most consist of a head piece and a rigid, non-motile, fibrillar tail of varying design by which the sperm are bundled in spermatophores. Tanaid sperm are round and tailless, and spermatophores are absent. Oi~genesis follows a common pattern in those peracarids that have been studied. A period of previtellogenic growth is followed by slow primary vitellogenesis with endogenous yolk synthesis. Prior to molting and fertilization, rapid secondary vitellogenesis, utilizing exogenous yolk synthesis, occurs. Life cycles in the more diverse peracaridan orders can be compared. Temperate species often have long overwintering generations interspersed with several shorter summer generations. Polar and deep-sea pericaridans have much longer generations whereas tropical species may produce broods year-round in rapid succession. Mating usually occurs when the mature oOstegites appear, with copulation occurring shortly after the female molts. Precopulatory pairing and mate guarding by males using specially modified

REPRODUCTION AND DEVELOPMENT IN PERACARIDANS

107

appendages is common, but some males cruise from one female to another. Sperm is generally deposited into the marsupium where fertilization occurs, but some isopods store sperm for later use. Development follows the general crustacean pattern o f superficial cleavage, with the details o f organ and appendage formation varying from order to order. Some special brood pouch structures exist, primarily in isopods, and in some tube-dwelling tanaids the young develop in the female's tube rather than in the marsupium. Peracarids generally hatch in the brood pouch as fully developed juveniles or as mancas (without the last pair o f thoracic legs). With a few exceptions, brood size is a function of female marsupial volume The trade-off between egg size and egg number varies with both habitat and, in some cases, with season. Since egg size affects incubation time, these complex interrelationships and the adaptive value of specific reproductive strategies are still unresolved.

1.

INTRODUCTION

The Peracarida, in the traditional sense, includes the orders Isopoda, Amphipoda, Mysidacea, Tanaidacea, Cumacea, Spelaeogriphacea, Mictacea and, often, the Thermosbaenacea. These diverse groups within the Malacostraca are united by their reproductive biology: all brood their young in a brood pouch or marsupium. The Mictacea is represented by but two genera, and little is known of their biology, although what are thought to be brood plates are present on some thoracic appendages (Sanders et al., 1985; Just and Poore, 1988). Thermosbaenacea, provisionally assigned to the Peracarida, also brood their young, but the marsupium is dorsal, under the carapace. Whether this represents a primitive condition or is the result of recent specialization is unknown. Although most authorities in recent decades have recognized the Peracarida as a natural grouping, the superorder has been subject to increasing debate (see summary in Hessler and Watling, 1999), and significant changes in peracaridan classification may be in the offing. Furthermore, relationships between the different peracarid orders are, at best, unclear (Watling, 1983, 1999). With the exception of the Mictacea, Spelaeogriphacea and Thermosbaenacea, all peracarid orders are widespread and abundant marine animals that exploit a variety of lifestyles and habitats ranging from the supralittoral to the abyssal. Most information comes from temperate shallow-water species, some of which have served as models for various aspects of crustacean reproductive biology. Increased exploration provides only an initial glimpse of the biology of the rich peracaridan fauna present

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

in the deep sea. Surprisingly, polar species are better studied than those in the tropics, although tropical research seems to be on the increase. Pelagic species are rather poorly known, with information from a few species that may, or may not, be representative. Our treatment is restricted to the free-living marine species with only occasional reference to freshwater, terrestrial or parasitic representatives. Despite their distinctive form of marsupial brooding, there are no recent reviews of either reproduction or development in Peracarida. Mauchline (1980) and Wittmann (1984) provide comprehensive reviews of reproduction in mysids, but similar treatments are lacking for the other orders. Various chapters in The Biology of Crustacea (Bliss and Mantel, 1982-1985) and in Crustacean Sexual Biology (Bauer and Martin, 1991) treat general aspects of crustacean reproduction that often apply to peracaridans plus some chapters devoted to work on gammarids or isopods that have served as models within the Crustacea. Wherever possible, we attempt to integrate information from all peracaridan orders and to note the similarities and differences among them. We have also made a conscious effort to incorporate and summarize some of the classic older works. Many are still the best - or only - sources in specific areas.

2.

SEXUAL REPRODUCTION, HERMAPHRODITISM AND SEX DETERMINATION

Sexual reproduction is the norm in all peracaridan groups, but geographic parthenogenetic reproduction is reported in amphipods of the genus Rhabdosorna (Sastry, 1983). Most species are not hermaphroditic, but some examples of sequential hermaphroditism are known, and intersexes have also been described. Sex determinism is primarily genetic, although in some species or populations sex is also influenced by environmental factors. Genetic and environmental factors probably exert their influence through hormonal secretions, the immediate determinants of sex. For a complete treatment, Charniaux-Cotton and Payen (1985) provide an excellent review with additional reviews by Charniaux-Cotton (1960, 1962, 1964, 1965, 1975) and Adiyodi (1985).

2.1. Sex determining hormones All genetic and environmental mechanisms of sex determination are believed to act through their influences on sex determining hormones. As is generally true in Crustacea, the two sources of sex determining

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hormones are the androgenic gland, associated with the male reproductive tract, and the ovary. Testes do not appear to play a role in sex determination. Although testicular development precedes the development of secondary or external male characteristics such as enlarged gnathopods and pleopods, this is probably because the products of the androgenic gland are transported by diffusion and therefore reach the nearby testes earlier. The androgenic gland is present in larvae of both sexes in rudimentary form but develops only in males. Its secretions are required for testicular development and function, for development and maintenance of primary and secondary male sex characteristics, and for male sexual behavior. The androgenic gland secretes androgenic gland hormone (AGH), which is active in males and causes development of male traits. A G H as isolated from androgenic glands of the terrestrial isopod, Armadillidium vulgare, consists of two major acidic proteins of similar primary structure and MW of 15 000-17 000 daltons (Hasegawa et al., 1987). In the absence of AGH, a sexually undifferentiated gonad will develop into an ovary, which, in turn, releases female hormones that mediate formation of female secondary sex characteristics such as the o6stegites. The roles of the androgenic gland and of the gonads have been analysed by removal of the androgenic gland from males and/or transplantation of the gland into females. In general, when an androgenic gland is transplanted into a female, oogenesis stops, and ovaries may change into sperm-producing testes. Circulating androgenic hormone can cause the formation of a new functional androgenic gland. In subsequent molts, other primary and secondary sex characteristics may also undergo masculinization. Species differ with respect to how late in development a sexual switch can take place and how complete the transformation will be. Females of some species can make this switch only if the transplantation takes place early in development, while others can change sex after sexual maturity has been reached. In a mature individual the ducts may be nonfunctional even though sperm are found in the gonad (Legrand et al., 1987). If the androgenic gland is removed from an adult male, the testes may degenerate or redifferentiate into ovaries, depending on the species. In the amphipod Orchestia gammarella, young males may undergo sex reversal after removal of the androgenic gland, but the gonad is unable to dedifferentiate from a testis into an ovary. Other species, such as O. montagui and Talitrus saltator, can undergo sex reversal much later (Charniaux-Cotton and Ginsburger-Vogel, 1962; Charniaux-Cotton, 1967; Hort-Legrand et al., 1974). For secretory activity, the androgenic gland requires secretions from the protocerebrum, optic lobe of the brain, or both. An isolated testis survives if co-cultured with a male brain or a female brain treated with A G H but

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degenerates if cultured with no brain or an untreated female brain. Therefore a neurosecretion required for maintenance of the testes is believed to be produced in the brain in response to secretion of androgenic hormones (Charniaux-Cotton and Payen, 1985). The hormonal control of gametogenesis is discussed in another section. Mature o6stegites appear only in the presence of a functional ovary, including one that differentiates from a testis or, in O. gammarellus, when an ovary is transplanted into a male from which the androgenic gland has been removed (Charniaux-Cotton and Payen, 1985). All indications, therefore, are that the androgenic gland and its secretions are necessary for differentiation of male reproductive structures, and that female structures differentiate in the absence of the androgenic gland and the presence of the ovary.

2.2.

Genetic determination of sex

Genetic factors that play a role in sex determination have been identified in isopods and amphipods. The review by Legrand et al. (1987), lists three methods currently used to address the subject: (1) cytological study of heterogametic species; (2) analysis of species that have sex-linked markers, especially those that influence body color; and (3) experimental reversal of sexual identity. In the latter method, manipulation of the androgenic gland to obtain sex reversal is followed by breeding of the affected individuals to determine the heterogametic sex. These analyses indicate that sex determination may require interaction of multiple genetic factors. Major sex factors, defined as those that have a large effect on sexual identity, are present in many species and may be associated with male or female heterogamy. Male heterogamy has been observed in the isopods Tecticeps japonicus, which have XO males and Anisogammarus anandalei, in which males are XY, and has been inferred from breeding of sex-reversed individuals of the terrestrial isopods Helleria brevicornis and Porcellio dilatatus dilatatus (Legrand et al., 1987). Sex-linked genes for color have been found to be linked to female heterogamy in the marine isopod Idotea balthica. Heterogamous females also are found in terrestrial isopods, the marine isopod Naesa (=Dynamene) bidentata, and in the superspecies Jaera albifrons, in which females are described as WWZ, in which females have two W chromosomes (the equivalent of X chromosomes of species in which females are homogametic), plus an unpaired Z chromosome (equivalent of a Y in a heterogametic male) (Legrand et al., 1987). Crosses between neo-males and normal females have demonstrated female homogamy in the amphipods Orchestia cavirnana and O. gammarella (Ginsburger-Vogel, 1972). For a more

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extensive treatment of sex inheritance in terrestrial species, consult Legrand et al. (1987). In a polygenic system of sex determination the same species may have both major and minor factors that interact to give unusual ratios of sexes. For instance sex inheritance in the isopod Idotea balthica basteri is determined primarily by female heterogamy (WZ). Color phenotypes such as albafusca (A), are specific to the W chromosome and can thus be used as a marker to identify sex-reversed individuals. A male exhibiting the A phenotype must have the W chromosome and be a W A Z neo-male. Test crosses between such males and normal females produce the expected color and sex ratio of 0.25 (1 Z Z male : 2 W A Z females : 1 WW female), indicating that WW females are viable. Individuals with the prevalent color type for the opposite sex appear regularly, indicating that polygenic mechanisms for sex determination are present in this species. Hybridizations between L b. basteri and L b. tricuspidata also give unusual combinations of color and sex that are best explained by polygenic influences over sex determination (Legrand et al., 1987). An unusual situation has been reported recently for the marine isopod Paracerceis sculpta, in which three types of male exist, distinguished by behavioral and physical characteristics (Shuster and Sassaman, 1997). Large alpha males have elongated posterior appendages modified for defence, used to guard harems of females against the other two morphs. Beta males resemble females and use subterfuge to invade the harems, while gamma males are small and gain access to females by stealth. The three morphs are genetically determined by separate alleles at a single autosomal locus designated Ams (alternative mating strategy). The alleles display a hierarchy of dominance, so that Ams ~ > Ams r > Ams ~. A locus closely linked to Ams displays typical Mendelian progeny ratios, whereas Ams departs from Mendelian inheritance patterns. Shuster and Sassaman (1997) interpret these aberrant ratios, plus the appearance of heterogeneous sex ratios within cross classes, as indicating the presence of additional factors influencing male phenotype. Their model supposes female homozygosity and two-way sex changes caused by an autosomal genetic locus designated Tfr (transformer) and an extrachromosomal factor.

2.3.

Environmental factors and sex determination

Environmental influences over sex determination, called epigenetic factors, occur in a number of terrestrial isopods and in marine and estuarine amphipods. These factors may assert their influence through their effects on the organs that produce sex determining hormones, especially the

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androgenic gland. However, the actual mechanisms by which they exert their effects have not been determined. Studies on terrestrial isopods are reviewed by Legrand et al. (1987) and will not be discussed here except as the information relates to work done on marine forms. Day length plays a major role in determining the sex of northern European populations of the amphipod Gammarus duebeni. Males outnumber females when days are longer than 14 hours, whereas females are more prevalent when days are shorter than 13 hours (Bulnheim, 1991). The environmental effects differ from one pair to another, indicating that genetic factors also are involved in sex determination. Populations from southern England are not sensitive to day length. Watt and Adams (1994) suggest that sensitivity to day length has a selective advantage for northern populations with a shorter growing season. They speculate that the reproductive potential of males, for which size is critical to reproductive success, is enhanced if they are born early in the growing season with its long day lengths. However, a long growing season is not as advantageous to females, which therefore are produced in high numbers later in the summer season when day lengths are shorter. In several genera of amphipods, parasites play a role in sex determination. This subject was reviewed by Legrand et al. (1987) and expanded by Bulnheim (1991). In these genera, thelygeny, defined as the regular occurrence of broods with a high proportion of females, occurs in some populations, while others display arrhenogeny, having broods that are all or mostly male. Mothers of thelygenous broods invariably are infected by feminizing microsporidean protozoan parasites. In both Orchestia garnmarella and Gammarus duebeni, males typically are not infected with parasites, whereas females are. Parasites live in the ovarian tissue, including eggs and follicle cells and are transmitted from mother to offspring via the cytoplasm of the egg. The progeny of infected females therefore all become daughters. Intersexes, displaying mixtures of male and female sex specific anatomy, exist in populations of both species and also are infected with parasites. However, there are significant differences related to interactions involving other environmental factors that warrant separate discussions of sex determination in the two species. In O. gammarella populations, thelygenous females and intersex males are infected by an intracellular protozoan, Paramarteilia orchestiae, at 15°C. Thelygeny and intersexuality are abolished by exposure of eggs or embryos, but not adults, to temperatures above 22°C. Thus, the parasites are eliminated from as yet sexually undetermined organisms by high temperatures, allowing the underlying genetic pattern to be followed. Some temperature-treated females are genetically amphogenous, producing equal numbers of males and females and no intersexes. Other treated females produce partial or total arrhenogeny. In this species, females are

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XX, while males are XY. Arrhenogeny is postulated to result from crosses of genetic males (XY or YY) that have been feminized by the parasite with normal XY males. For an XY to XY cross, most (75%) progeny will be male, while if the cross is YY to XY, all will have a Y chromosome and will therefore be male. There are also males that produce arrhenogeny and thelygeny. Crosses to YY females indicate that these males are XX. How such males are created is not known (Legrand et al., 1987). Sex determination in the amphipod subspecies G. duebeni duebeni involves complex interactions among parasitic infection, temperature and salinity, as well as effects of day length on genetic factors, described above. Two species of feminizing microsporidians, Octosporea effeminans and Thelohamia hereditaria, have been found in this amphipod. Parasites are found in ovarian tissue, including follicle cells and eggs. Infection is transmitted by tissue implants but not by feeding on food infected with parasites. The androgenic glands are reduced in size in infected individuals although no evidence of cellular damage has been found. Males are not infected (Legrand et al., 1987; Bulnheim, 1991). As both parasites are sensitive to low temperatures, amphipods cultured at temperatures less than 4°C do not display thelygeny or intersexuality, nor are their sexual organs infected with the parasites. For T. hereditaria, it is the initial infection of eggs by microsporidia that is sensitive to temperature, and once hosts are infected, exposure to low temperatures does not rid them of the parasites. If an androgenic gland is transplanted into males that have been sex reversed by T. hereditaria, they can be transformed into males, showing that the feminizing effects of the parasite must work through destruction of the androgenic gland and its hormones. Exposure to low temperatures will, however, eliminate parasites from amphipods already infected by Octosporea effeminans, and can result in sex reversal. An androgenic gland injected into hosts infected by this species effects a partial sex change, mainly involving the secondary sex characteristics, so the androgenic gland must be inhibited while this parasite is present (Bulnheim, 1991). Intersexes range from individuals that are normal males except for the presence of o6stegites, through intermediate forms that have both eggs and sperm in their gonads, to near-females displaying minor male secondary sex characteristics. The intermediate forms are sexually nonfunctional, but those on either end of the range can mate and produce offspring. Intersexes are caused by intermediate conditions between domination by androgenic gland hormone and ovarian hormones. Bulnheim (1991) attributes their conditions to changes in parasite load that occurred as individual hosts were developing. Temperature fluctuations and salinity fluctuations would be responsible for the changes in levels of parasitic infection (Bulnheim, 1991). If an embryo infected by

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O. effeminaus develops for a short interval at high salinity, for instance, it will be mostly feminized, whereas another embryo that develops at high salinity for a long period of time will be able to express the effects of day length and genetics and may be a male intersex (Bulnheim, 1991). 2.4.

Hermaphroditism

Hermaphroditism, while common in parasitic and terrestrial species, is unusual and relatively unstudied in free-living marine peracaridans~ Sequential hermaphroditism is more common and includes both protogyny and protandry whereas simultaneous hermaphroditism is known only in the tanaid Apseudes hermaphroditicus (Lang, 1953). Functional protogynous hermaphroditism is found in free-living tanaids and isopods. Conversion of a brooding female into a functional male can occur in a single molt, but often an intermediate form intervenes. The tanaid Heterotanais oerstedi has primary males that become sexually mature without passing through a female stage as well as secondary males that develop from females after brooding is complete. In the laboratory the presence of males prevents this conversion (Biickle-Ramfrez, 1965). Gonochoristic females, which never become males, also exist in the field (Sastry, 1983). Protogyny in isopods is best characterized in European populations of Cyathura carinata. Both primary males and secondary males are present. The former develop from the second-year class, which also includes brooding females and non-brooding females. The brooding second-year females lose their oostegites and become functional males during the third year. The nonbrooding second-year females become ovigerous during the third year, and then some transform into males during the fourth year while other females never undergo sex reversal (W/igele, 1979; K6hn and Sammour, 1990). Although protogynic development has not been described in North American populations of C carinata, sex reversal of females into secondary males has been suggested for another species, C. polita (Burbanck and Burbanck, 1974). Other protogynic isopods include Ptilanthura tenuis (Kensley, 1996) and Gnorimosphaeroma naktongense (Abe and Fukuhara, 1996). Protandrous hermaphroditism has been found only in the lysianassoidean amphipod genera Acontiostoma, Scolopostoma and Stomacontion (Lowry and Stoddart, 1983, 1986) and in the stegocephalid amphipod Stegocephalus inflatus (D. Steele, 1967), but in no other non-parasitic marine peracaridans. Its absence in free-living, marine isopods is notable considering that protandry is prevalent among parasitic and terrestrial isopods.

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3. ANATOMY 3.1.

Sexual dimorphism and secondary sexual characteristics

The degree of sexual dimorphism and the structures affected vary considerably among species of free-living marine Peracarida. Generally, females resemble the sexually undifferentiated juvenile stages, from which they are distinguished by the presence of o6stegites. These appendages develop from the coxae of various thoracic appendages and serve as a brood pouch for the developing embryos. Some female isopods have degenerate mouthparts or maxillipeds specially modified to circulate water through the brood pouch. These structures are described in the section on brooding. Male isopods, mysids and primitive amphipods are usually larger than the females. Among the more specialized amphipods, including the small burrowing gammarids (Bousfield, 1973) and the planktonic Phronimidae (Stephensen, 1929) the male may be smaller. Tanaid males are also usually smaller (Kiakenthal and Krumbach, 1927; Nierstrasz and Schuurmans Stekhoven, 1930; Lang, 1957), and cumacean males are more slender than the females (Foxon, 1936). Male cumaceans can also be smaller, especially in those species where the male does not swim but instead is adapted for grasping the female, e.g. members of the genus Lamprops (Sars, 1900). Veuille (1980) suggests that larger males thus result from competition for females and should be expected if: (1) only a small fraction of the females is receptive at any one time; and (2) females copulate at a discrete point in their reproductive cycle. Similar selective pressures may have produced the greatly enlarged gnathopods found on the males of many gammarids and carried to an extreme in caprellid amphipods. Males may possess specialized sensory organs and modifications to enhance swimming. Frequently, these structures appear only when the males become sexually mature and are often associated with a more errant lifestyle as they seek mates. In some species, males have significantly larger eyes. Adaptation for faster swimming occurs in a number of male isopods (Hessler, 1970), tanaids (Kukenthal and Krumbach, 1927; Nierstrasz and Schuurmans Stekhoven, 1930), cumaceans (Zimmer, 1941), hyperiids (Claus, 1872), and mysids (Nouvel, 1940). Bristles, calceoli, aesthetascs, flagella and other putative olfactory structures associated with the antennae or gnathopods are widespread in the Peracarida, and their use is discussed below in the section on mating. In some groups, mature males show reduced mandibles, maxillae and sometimes even maxillipeds (Gardiner, 1975; W~igele, 1981), suggesting that these terminal males do not feed.

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Male structures specifically modified to hold females during pairing or mating are common. Enlarged gnathopods with large spines or "thumbs" found in male caprellids and corophioid amphipods are adapted specifically for guarding females prior to mating (Conlan, 1989; Caine, 1991; Bousfield and Shih, 1994). Jassa marmorata is unusual in having two distinct forms of males: major males have a greatly enlarged propodus or "thumb" on rather large second gnathopods while smaller minor males lack these modifications (Clark, 1997). The male cumacean Pseudocuma longicorne employs the first and second pereiopods to hold females (Foxon, 1936), but other cumaceans use short, stout antennae as grasping structures. There are varying degrees of shortening of the antennae that seem to be correlated with the gradual loss of the swimming male stage, until, at last, the antennae have developed into fully grasping structures. This development has been seen in several of the cumacean families, especially Leuconidae and Lampropidae (Zimmer, 1941). Recent speculation suggests that male gammarids may also use their antennae to grasp females. Initially, the antennal calceoli found on adult males were thought to be chemosensory and capable of detecting female pheromones (Dahl et al., 1970), but no recent evidence supports this role. Moore and Wong (1996b) now suggest that calceoli may have adhesive properties that assist in holding females during mating. This, too, is problematic since Read and Williams (1990) found that removal of the antennular flagellum (and its associated calceoli) had no effect on amplexus. Most other structures known only in terminal males are species-specific and of unknown function.

3.2. Anatomy of the reproductive system The reproductive system of the Peracarida develops from a pair of mesodermal tubes, which consist of germ cells covered by an epithelium and surrounded and supported by a mesentery. The tubes run anteroposteriorly along the dorsal part of the thorax, ventrolateral to the pericardium and dorsolateral and parallel to the gut. Regional differentiation of the tubes varies according to species and sex. 3.2.1.

Female reproductive system

3.2.1.1. General anatomy of the female reproductive system. In the female, the original pair of tubes differentiates into the ovaries, which are often spindle-shaped (Gerstaecker and Ortmann, 1901; Zimmer, 1941) and prolonged at each end in a suspensory ligament (Dohrn, 1866; David, 1936). The size of the ovaries varies with the stage of oogenesis (Menzies,

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In°p° d.t.

Figure 1 Ventral presentation of the female reproductive system of the mysid Mesopodopsis orientalis. The triangular midpiece (m.p.) is the germinative region of the ovaries. Oocytes enter the smaller ventral tubes (v.t.) and then pass to the larger dorsal tubes (d.t.). Oviducts (ov) leave the dorsal tubes near their posterior extremity. Other peracaridean orders have a single set of paired tubes. (After Nair, 1939.)

1954; Pigeault, 1957; Peyrot and Trilles, 1964; Schmitz, 1967; Evans, 1968). Gravid ovaries occupy much of the space in the thoracic cavity and in some species may extend into the abdomen, as in the gammarid amphipods (Cussans, 1904) and sphaeromatid isopods (Pigeault, 1957). A lobulated appearance, resulting from pressure of growing oocytes against the ovary wall has been noted in amphipods (Cussans, 1904; Kunkel, 1918; Pirlot, 1930), mysids (Nair, 1939) and Thermosbaenacea (Barker, 1962). Ovaries of the mysid Mesopodopsis orientalis described by Nair (1939) have a unique structure (Figure 1) deserving special comment. Each ovary consists of two parallel longitudinal tubes located lateral to the gut. The larger dorsal tube is joined to the smaller ventral tube via a wide aperture at the anterior end. The two lower tubes are connected by a bridge of tissue. In other mysid species, such as Mysis oculata (Sars, 1900) and Neomysis japonica (Mauchline, 1980), the ovaries are similarly bridged, but each ovary consists of a single lateral tube. Ovaries of cumaceans are also bridged (Sars, 1990; Zimmer, 1941). The oviducts leave the ovary at the level of the fifth pereonite (sixth thoracic somite) as a pair of narrow tubes (Gerstaecker and Ortmann, 1901; Cussans, 1904; Forsman, 1944; Pigeault, 1957; Schmitz, 1967) except in mysids, in which they depart near the rear of the ovary (Zimmer, 1933; Nair, 1939). From their origin on the ventral side of the ovaries the

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oviducts pass more or less directly ventrolateraUy to the genital orifice, or oopore, on the sternite at the base of the fifth pereopod (amphipods [Cussans, 1904; David, 1936; Dunbar, 1946; Schmitz, 1967], isopods [Menzies, 1954; Pigeault, 1957; Wolfl~ 1962; Klapow, 1970], mysids [Zimmer, 1933], tanaids [Nierstrasz and Schuurmans Stekhoven, 1930], Thermosbaena mirabilis [Barker, 1962]). The genital orifice is located on the coxa of the fifth pereopod in isopods of the genera Columotelson and Idotea (Wilson, 1991). In cumaceans the oviducts leave the ovaries at their midpoint and open on the inner sides of the coxae of the third pereopods (sixth thoracopods) (Zimmer, 1941). The oviducts of some species of cumaceans appear for the first time in the molt prior to breeding and disappear between egg depositions. Early authors, baffled in their attempts to find the oviducts, suggested that the eggs were released into the body cavity, where they supposedly developed (Sars, 1900). This is now known to be incorrect (Zimmer, 1941). Specializations of the lower reproductive tract are involved in copulation and sperm storage. Typically insemination takes place through the oopore. The order Asellota (Isopoda) has evolved a unique structure called the cuticular organ, or spermathecal duct. This cuticle-lined tube connects to the spermatheca and serves as a copulatory passage (Menzies, 1954; Veuille, 1978; Lincoln, 1985a; Wilson, 1986a, b). Although the cuticular organ is found in all members of the order, its structure varies considerably between and even within genera (Figure 2). In the genera Asellus, Stenetrium and Pseudojaera, it is located ventrally, adjacent to the oopore. Pseudojaera investigatoris has a furrow on the ventral surface of the fifth pereonite into which the spermathecal duct opens. The oopore opens anterior to it in the same furrow, and a conical depression called the stylet receptacle is found between the two openings. This receptacle is present only in preovigerous females, as it is lost in the last molt in which o6stegites form (Poore and Just, 1990). In other genera such as Jaera, an external opening located on the dorsal surface of the fifth pereonite leads to a tube that runs ventrally to join the oviduct. In these genera copulation takes place through this dorsal opening, while oviposition occurs through the ventrally located oopore. The tube is lined with an epithelium that is continuous with the ectoderm and secretes cuticle. The organ is usually divided into an outer region with a thick, roughened cuticle and an inner region with smooth cuticle. Comparative studies of the cuticular organ have been published for the genus Jaera (Veuille, 1978) and for the entire order (Wilson, 1986a, 1991). In the genera Asellus, Pseudojaera and Stenetrium paired spermatheca, which are either specialized regions of the oviduct or diverticula of that organ, hold sperm until eggs are ready to be fertilized. They connect to the outside via spermathecal ducts, while a large opening on the anterolateral

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oviduct

s I ?

c

-64.Ll

: °

d.

Figure 2 General anatomy of the female reproductive system of female isopods, showing possible evolutionary changes in sites of sperm storage and copulatory passages. Dark arrows represent the sites in which sperm are held after copulation. (A) The ancestral condition as represented by the genus Limnoria. Terrestrial oniscoids (B) and Sphaeromatidae represented by Sphaeroma (C) have ventrally located internal brood pouches. (D) The condition in DynameneUa. The Asellidae (E) and Janiroidea (F) have evolved spermatheca within the oviduct. In the latter group a spermathecal duct connects the oviduct to the dorsal body surface and is used as a copulatory receptacle. (After Wilson, 1991.)

surface connects to the oviduct. The junctions have two layers of epithelium, an outer one that is continuous with the wall of the oviduct, and an inner one that is continuous with the wall of the spermathecal duct. The latter secretes a cuticular lining during the copulatory period (Veuille, 1978). Some suborders of Asellota have spermatheca with fleshy walls (Wilson, 1986a). The valviferan, Saduria entomon, has paired spermatheca that open into a single central fertilization chamber via muscular valves and are filled with sperm regardless of the reproductive state of the female. This species also has a pair of accessory glands filled with cells containing granular material. The fertilization chamber is connected to each oviduct by a tubular duct that also receives the secretions of the accessory gland. Eggs travelling down the oviduct must pass the point at

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which this common duct opens into the oviduct soon after they leave the ovary. Hryniewiecka-Szyfter and Tyczewska (1992) believe that eggs pass through this duct and into the fertilization chamber where they are fertilized by sperm released through the valves from the spermatheca. They would encounter secretions of the accessory gland as they pass back into the oviduct, propelled by contractions of the muscular wall of the fertilization chamber. Enlargements of the oviduct that serve to store sperm are also found in some amphipods (Gerstaecker and Ortmann, 1901). 3.2.1.2. Histology of the female reproductive system The ovarian wall is composed of columnar epithelium with a basal lamina and a thin tunica propria (Cussans, 1904). The region nearest the opening to the oviduct may also contain an interrupted layer of muscle cells (HryniewieckaSzyfter and Tyczewska, 1992). In cumaceans, tanaids and Thermosbaena mirabilis this wall is very convoluted so that each oocyte is surrounded by a follicular epithelium (Dohrn, 1869; Claus, 1887; Zimmer, 1941; Lang, 1953; Barker, 1962). The lumen is filled with oocytes, often in different stages of development (Dohrn, 1866; Meusy, 1968) and often aligned in rows. Single rows of large oocytes surrounded by smaller oocytes are reported in the ovaries of the amphipod Gammarus lacustris (Schmitz, 1967). The oocytes are also aligned in a single row in the ovaries of the mysid Mesopodopsis orientalis (Figure 1) where they start their growth in the lower tubes and travel anteriorly to enter the upper tube, through which they then move to the oviduct in single file (Nair, 1939). Double rows of oocytes are found in other species of amphipods (Gamroth, 1878; David, 1936; Sheader, 1981) and in cumaceans (Zimmer, 1941). Oocytes originate from a special region of the ovary wall called the germinal epithelium, germ layer or germinative zone. The germ layer consists of a mesodermal reticulum of flattened ceils surrounding the large gonia (Meusy, 1968) and is easily distinguished from the cylindrical somatic epithelium as a band along the length of the ovary. In S. entomon, the rosette-like germinative zone is located at the proximal end of the ovary and contains densely packed oogonia cells (Hryniewiecka-Szyfter and Tyczewska, 1992). In the isopod Ligia exotica, the germinal epithelium is located near the midline of the ovary (Kumari et al., 1993). In tanaids (Claus, 1887; Lang, 1953) and sphaeromatid isopods (Kinne, 1954a) it is on the inner side of the ovary, and in some amphipods on the outer side (Gerstaecker and Ortmann, 1901; Peyrot and Trilles, 1964). In other amphipods it may be localized along the dorsal side (Sheader, 1981) or at the anterior end of the ovary (Gamroth, 1878; Meusy, 1968). In mysids and possibly cumaceans (K0kenthal and Krumbach, 1927) the midpiece contains the germ layer. Nair (1939) describes the midpiece of

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M. orientalis as a triangular structure covered by a membrane. The apex of the triangle contains small, closely packed oogonia. The posterior margin consists of elongated, closely packed cells and gives rise to the germ cells. The oocytes are surrounded by follicle cells that do not appear to be involved in making R N A for export into the oocytes, as their nucleoli are much smaller than those of the oocytes (HryniewieckaSzyfter and Babula, 1995). They also do not seem to play a role in nutritive cycling, as they lack cytoplasmic alkaline phosphatase activity (Lane, 1980). The oviduct wall of the isopod S entomon is similar in structure to that of the ovary, consisting of a columnar epithelium and continuous muscle layer separated by a basal lamina. The apical surface is lined with a cuticle which is shed into the lumen during ecdysis (Hryniewiecka-Szyfter and Tyczewska, 1992). The amphipod oviduct is compressed and is lined with cuboidal epithelium supported by a basal lamina (Peyrot and Trilles, 1964). The general histology of this organ in other groups is probably similar. In the mysid M. orientalis, the distal region is swollen and glandular. A fine thread-like substance fills the lumen of the oviduct. Nair (1939) interprets this substance as a secretion of unknown function, which ceases when the eggs are deposited in the brood pouch. Another interpretation is that it is sperm. Shell-making regions are reported in the oviducts of some amphipods. A bright refractive substance localized in the widened distal end of the oviduct of the hyperiid Phronima appears to be involved in putting the shell on the egg (Gerstaecker and Ortmann, 1901). In Parathemisto gaudichaudi the oviducts have a thickened medial region identified as a shell gland by Kane (1963) that produces a membranous sac into which the ova are shed as they enter the marsupium (Sheader, 1981). Similar egg sacs also are found in mysids (Wittmann, 1981a). The external genitalia consist of the genital orifice and the o6stegites described in the section on brooding. 3.2.2.

Male reproductive structures

3.2.2.1. General anatomy The male reproductive system varies considerably from order to order and sometimes from species to species within an order. Generally it originates from paired tubes that run along the thorax on either side and dorsal to the gut. The tubes are usually regionally differentiated. The anterior-most region in each tube contains a localized sperm-producing tissue and is called the testis (Figure 3). Other specialized regions often present are seminal vesicles for storage of sperm and a muscular ejaculatory duct. Caution must be used when comparing descriptions from different authors, as some use the term vas deferens to refer to structures that are histologically identical to what others call the

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seminal vesicles. The androgenic gland, involved in development and maintenance of male secondary sex characteristics, is usually closely associated with the reproductive tract. In amphipods the tubes are unbranched, and their anterior ends become the testes (Gamroth, 1878; Nebeski, 1880; Cussans, 1904; Peyrot and Trilles, 1964; Schmitz, 1967; Lalitha et al., 1990). A similar situation exists in tanaids (Claus, 1887; Juchault, 1963), Thermosbaena mirabilis (Barker, 1956), and the isopod genera Limnoria (Menzies, 1954) and Paranthura (Gerstaecker and Ortmann, 1901). In other isopods and cumaceans, however, the testes consist of lobes extending from each tube, having originated from segmental lateral mesodermal cords that, in the female, differentiate into supportive ligaments. The lobes open separately into the central tube, called the vas deferens (Kumari et al., 1990) or seminal vesicle (Kinne, 1954b). Isopods have three testes on each side, whereas cumaceans have four (Sars, 1900; Zimmer, 1941; Fage, 1951; Juchault, 1963). Hermaphroditic species of tanaids such as Apseudes herrnaphroditicus may have a pair of ovotestes (Lang, 1958) or separate paired testes, consisting of two lobes which unite to form a single vas deferens (Lang, 1953).

v.tl.

Figure 3 Anatomy of the male reproductive system of the isopod Ligia exotica, illustrating anatomy typical of most isopods. Cumaceans have a similar anatomy, but have four lobes rather than three, while the testes of amphipods and tanaids are the anterior ends of unbranched tubes. The testes (t) consist of three pairs of fusiform follicles arising from the paired vas deferens (v.d.). The latter narrow before they open via genital apertures into the styliform appendages (s.a.) located on the seventh pereonites. (After Kumari et al., 1990.)

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I1.¥.

Figure 4 Anatomy of the male reproductive system of the mysid Praunus flexuosus. A. Lateral view. B. Ventral view. The testes (t) are paired ventral tubules connected to the dorsally located seminal vesicles (s.v.) by five pairs of swollen tubules called cysts (cys). (After Labat, 1961.)

Among mysids, several types of male reproductive systems have been described. The testes of Spelaeomysis are the anterior regions of simple, unbranched tubes (Nath et al., 1972). In Praunus flexuosus (Labat, 1961; Mauchline, 1980), Archeomysis grebnitzkii and Neomysis awatschensis (Kasaoka, 1974) the male reproductive system consists of two pairs of parallel tubes running longitudinally along the thorax on either side of the gut (Figure 4). The ventral pair is nearer the midline and contains the germinative area as a series of five or six swellings in each tube. These swellings are therefore considered to be the testes. The larger, more dorsally and laterally located pair function as seminal vesicles and contain mature sperm. The two seminal vesicles are connected anteriorly into a single U-shaped organ in A. grebnitzkii and N. awatschensis (Kasaoka, 1974). Each testicular swelling in the lower tube is connected separately to the seminal vesicle via a short duct which contains one or more swollen areas. In these swellings, referred to as cysts, meiosis and sperm differentiation take place (Labat, 1961; Kasaoka, 1974). The seminal vesicles of mysids, described above, are a separate pair of tubes. In other orders of Peracarida, sperm may be stored in the posterior region of the testes (Cussans, 1904; Nichols, 1909) or in separate seminal vesicles immediately posterior to the testes (Nebeski, 1880; David, 1936; Schmitz, 1967). Some species of amphipods store sperm in a distended region of the vas deferens (Gamroth, 1878; Cussans, 1904; David, 1936; Tuzet and Sanchez, 1952; Peyrot and Trilles, 1964; Evans, 1968). Tanaids may have a distended region in each vas deferens (Lang, 1953) or both vas deferens may empty into a single central seminal vesicle located in the last thoracic segment under the gut (Claus, 1887; Nierstrasz and Schuurmans Stekhoven, 1930; Lang, 1958).

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The vas deferens run laterally and ventrally as continuations of the seminal vesicles or testes. In isopods they form from the sixth pair of segmental mesentery cords and run ventrally perpendicular to the seminal vesicle (Pigeault, 1957) to an opening at or near the boundary of the last thoracic and first abdominal segments. In amphipods (Cussans, 1904; Schmitz, 1967), mysids (Nath et al., 1972), and cumaceans (Zimmer, 1941; Juchault, 1963) they open on the last thoracic segment. Bulbous muscular ejaculatory ducts occur as localized regions of the distal vas deferens in some mysids (Labat, 1961), tanaids (Claus, 1887; Gerstaecker and Ortmann, 1901) and amphipods (Claus, 1872; Nebeski, 1880). The external genitalia are usually located on the last thoracic segment, but may also be situated between it and the first abdominal segment. However, in Spelaeogriphacea and Mictacea they are located on the coxa of pereopod VII, which may be the ancestral position (Wilson, 1991). Genital openings are located at the tips of short conical chitinous papillae in most amphipods, mysids, cumaceans and tanaids. These projections are elongated into chitinous penes in some groups. Two genera of the mysid tribe Leptomysini, Mysidetes and Pseudomysidetes have long processes which extend forward as far as the mouth region (Nouvel, 1940; Tattersall and Tattersall, 1951). A similar process exists in the genus Mysidella of the Mysidellinae (Nouvel, 1940). The structure of the external male genitalia of isopods was reviewed by Wilson (1991). The genital orifices occur on papillae that may be elongated into penes and, in most species, are located on the sternum of the last thoracic segment. Only the freshwater phreatoicids have penes located in the ancestral position on the coxae, but some Asellota have an intermediate condition, with penes located between the coxae and the midline. In this group, sternal penes sometimes occupy a small plate derived from the coxa, separate from the sternite (Wilson, 1991). Penes may be paired, which is the ancestral condition (Naylor, 1955b), or fused into a cone-shaped ductus ejaculatorius (Menzies, 1954; Pigeault, 1957; Wilson, 1991). An evolutionary trend among the Valvifera, described by Sheppard (1957), has been for the openings to move posteriorly as the group evolved so that in the most derived species, they open on the pleotelson (Wilson, 1991). Also found on male isopods are the rod-like stylets, or appendices masculina. These movable, spinous structures arise from the endopodites of the second pleopods and are believed to act as extensions of the penes to aid in the transmission of sperm (Naylor, 1955b; Dearborn, 1967). Knobs and spines on the tip may play a role in species recognition (Wilson, 1991). Wilson describes another derived structure, the funnel, in the Asellota and Valvifera, as well as in terrestrial forms. Derived from the first and sometimes second pleopods, the funnel has a channel that

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probably helps to convey sperm from penis to stylet. The form is variable and, unlike the appendix masculina, which probably is monophytetic, funnels probably evolved separately in several isopod taxa. Finally, Wilson (1991) also describes a form of appendix masculina found in the Asellota, which he calls the "arm and hammer". In this type, the muscular exopod grasps the proximal region of the endopod, which is modified for sperm transport, and thrusts it into the body of the female. A medial copulatory spine has been described in the tanaid Apseudes latriellei (Claus, 1887; Kukenthal and Krumbach, 1927). Elongated movable penes on either side of the post-abdominal ring have been reported in caprellid amphipods (Dohrn, 1866). Penes originating from the coxa of the last pair of pereopods have been seen occasionally in cumaceans, including sporadically in genera where all other species are lacking penes (Watling and McCann, 1997). Such structures are therefore widespread among the orders of Peracarida and variable within the orders. The androgenic gland is not actually a part of the male reproductive system but is usually closely associated with some part of the system physically, and it has a prominent role in differentiation of the reproductive organs (see section on hormonal aspects of sex determination). The androgenic gland is associated most frequently with the vas deferens but has been found fused with the gonad wall in some cumacean and tanaidacean species (Juchault, 1963). In isopods it may consist of a single pair of structures or may be metameric in the fifth and sixth segments (Legrand and Juchault, 1960b, 1961). 3.2.2.2. Histology of the male reproductive organs Most of the histological work involving peracaridans has been carried out on terrestrial species, but the limited studies on marine species suggest that they are essentially similar. The gonads and reproductive tract have a wall containing either cuboidal or columnar epithelium, an underlying tunica propria and usually a thin muscular layer. The lumen is filled with spermatocytes and spermatozoa. The entire gonad is encased in a mesentery by which it is attached to the dorsal body wall or the dorsal organs such as the gut or pericardium. The anterior part of the testes is often elongated in a suspensory ligament in isopods (Pigeault, 1957) and amphipods (Pirlot, 1930; Peyrot and Trilles, 1964). In males of the amphipods Caprella albifrons and C. equilibra, Tuzet and Sanchez (1952) report that this ligament connects the testes to the digestive diverticulum and that a fine, epithelium-lined canal within the ligament connects the lumena of the two organs. The openings on each end are dilated and mobile, sometimes opening very wide. The authors postulate a direct exchange between the two glands. In the amphipods Orchestia cavimani and O. mediterranea (Charniaux-Cotton and Payen, 1985) and Talitrus

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saltator (David 1936; Fried-Montaufier, 1967), partial oogenesis occurs in the anterior region of the testes prior to initiation of spermatogenesis, sometimes continuing after sperm are being produced. However these oocytes never enter secondary vitellogenesis and eventually degenerate. The testes are lined with columnar (Nebeski, 1880; Gerstaecker and Ortmann, 1901; Schmitz, 1967) or cuboidal (Lalitha et al., 1990) epithelium except in the germ layer, where the spermatogonia originate. The location of the germ layer is specific to the taxonomic group. It is located in the testicular lobes of cumaceans and isopods, where it may be localized to an elongated cluster of cells running along the ventral surface of each testis (Hryniewiecka-Szyfter and Tyczewska, 1991). It is found in the swollen areas of the lower tubes of mysids (see general anatomy). In amphipods the germ area may be in almost any region of the testes depending on the species (Cussans, 1904; Nichols, 1909; Peyrot and Trilles, 1964). In the well-described species Orchestia gammareUus, it lies on the medial sides of the two gonads. In a pattern that seems to be typical of Peracarida, the primary gonia are embedded in a reticulum of separate somatic mesodermal cells associated with the gonad wall. These cells, variously referred to as supporting or nutritive (Kumari et al., 1990), accessory (HryniewieckaSzyfter and Tyczewska, 1991), or nurse cells (Brasiello, 1968; Reger and Fain-Maurel, 1973; Lane, 1980), are variable in shape and contain high levels of RNA (Brasiello, 1968; Lane, 1980; Hryniewiecka-Szyfter and Tyczewska, 1991), alkaline phosphatase and PAS-positive material (Lane, 1980; Lalitha et al., 1991). Lane (1980), working on several terrestrial isopod species, believes that the evidence supports a role for these cells in synthesis of microtubules rather than in nutrition. Periodically a population of primary spermatogonia emerge from the wall to undergo meiosis (Meusy, 1968). In the isopod Saduria entomon and possibly in other species, protrusions of the accessory cells surround the developing spermatocytes and spermatids (Hryniewiecka-Szyfter and Tyczewska, 1991). Germ cells are pushed further into the lumen as they mature, often resulting in a layering of germ cells by stage of development, with the more mature cells near the center of the lumen (see section on gametogenesis for details). In isopods, testes in the same male may differ with respect to the stages of spermatogenesis that are present (Hryniewiecka-Szyfter and Tyczewska, 1991). In some species, the posterior region of the testes is quite different from the germinal anterior end, containing cells secreting seminal fluid (David, 1936; Lalitha et al., 1990) and/or mucus (Pigeault, 1957). When a separate seminal vesicle adjoins the testis, its wall is similar to the non-germ layer region of the testes wall. In the mysid Praunus flexuosus, the wall of the seminal vesicle has a squamous epithelium with interspersed columnar cells that secret mucus and other products, possibly

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of a nutritional nature (Labat, 1961). Ripe sperm fill the lumen of the seminal vesicle, often distending it and creating a whitish translucent appearance. Sperm may be oriented randomly (Tattersall and Tattersall, 1951) or arranged in long thin threads, enclosed at first by thin membranes in bundles of about 12 sperm. Later the membrane breaks, but the sperm remain bound together by their tails (Zimmer, 1941; Forsman, 1944; Schmitz, 1967). The seminal vesicle walls of isopods contain two types of cells. The small prismatic ceils have fairly dense staining cytoplasm and are found in the vas deferens as well, while the aptly named giant cells (30-70/zm) are specific to the seminal vesicle region. The latter have been extensively studied in the terrestrial species Porcellio scaber, but are also described in the vas deferens of a marine species Bathynomus giganteus (Perry and Hinsch, 1991). They have heterochromatic nuclei, a prominent brush border, abundant rough endoplasmic reticulum with distended cisternae and numerous Golgi stacks (Newstead and Dornfield, 1965). These cells contain high levels of sulfated acid and neutral mucopolysaccharides and may be synthesizing PAS positive materials (Lane, 1980). The vas deferens may also contain sperm. It is lined with a cuboidal epithelium in amphipods (Pigeault, 1957; Schmitz, 1967), while the isopod Ligia exotica has a glandular columnar epithelium that probably produces mucopolysaccharides. Beneath the epithelium is a circular layer of muscle (Kumari et al., 1990). In tanaids the wall of the vas deferens is glandular and produces a sperm-binding substance (Juchault, 1963). In mysids, the glandular seminal vesicle fulfills the secretory role rather than the vas deferens (Labat, 1961). In the penis of the mysid Spelaemysis longipes the vas deferens is branched, the many canals giving a spongy effect (Nath et al., 1972). Ejaculatory areas containing circular, longitudinal and tangential muscles occur in the vas deferens of tanaids, amphipods (Claus, 1887; Nierstrasz and Schuurmans Stekhoven, 1930; Juchault, 1963), and in the isopod Saduria entomon (HryniewieckaSzyfter and Tyczewska, 1991). In Praunus flexuosus the ejaculatory bulb is merely an enlarged area near the penis, deriving its power from body wall contractions (Labat, 1961). The androgenic gland usually consists of a cord of cells either in a simple strand or folded upon itself to form a pyramid-shaped organ (Pigeault, 1957; Juchault, 1963; Peyrot and Trilles, 1964). The cells have prominent nuclei and nucleoli (Legrand and Juchault, 1960a, b, 1961) but are multinucleate and vacuolated in the amphipod Orchestia gammarellus (Charniaux-Cotton, 1962). They are rich in RNA in the mysid P. flexuosus (Legrand and Juchault, 1960b; Juchault, 1963) and terrestrial isopods (Lane, 1980). They also possess granules that may contain arginine-rich proteins. For this reason, Lane (1980) believes they secrete a proteinaceous product.

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GAMETOGENESIS

The gametes of both sexes originate from a specialized region in the wall of the gonads called the germ layer. The germ cells are enmeshed in a reticulum of non-syncytial mesodermal ceils. These cells, the primary gonia, are similar in males and females and divide by mitosis to produce new gonia. This division continues in adults of most Peracarida. Gonial division, once believed to be absent in mature mysid males, has been seen in male Archeomysis grebnitzkii and Neomysis awatschensis by Kasaoka (1974).

4.1.

Spermatogenesis

Spermatogenesis in peracaridans exhibits the normal pattern of mitotic proliferation of gonia, followed first by meiosis and finally by cytoplasmic differentiation, or spermiogenesis. The latter process has some unique aspects and is dependent on accessory cells that surround the differentiating spermatids, aid in their development and assist in packaging them into spermatophores. The special features of sperm differentiation are best appreciated in light of the unusual structure of the mature spermatozoon. 4.1.1.

Structure of the mature sperm

Peracaridan sperm are large: 0.9 mm long in the isopod genus Sphaeroma (Pigeault, 1957) and a full millimetre in the mysid Praunus inermis (Fain-Maurel, 1975a). Tuzet and Sanchez (1952) provide early detailed descriptions of amphipod sperm based on light microscopy. More recently, electron micrographs have appeared for spermatozoa of mysids (Labat, 1962; Fain-Maurel et al. 1975a, b; Craciun, 1987), isopods (Reger, 1964a, b; Fain-Maurel, 1970; Perry and Hinsch, 1991) and tanaids (Cotelli and Lora Lamia Donin, 1980). The sperm are aflagellate, consisting of a long, rigid tail connected to a flexible head via a mid-piece whose size and shape varies among species (Figure 5). The head and tail often join at an angle of considerably less than 90°, prompting many authors to liken the sperm to a whip or pennant, the rigid tail being the handle and the elongated, flexible head the lash or flag. This comparison is apt because the tail is non-motile, but the head can bend and change position with respect to the tail (Blanchard et al., 1961). While the whip-shaped sperm is most widespread, the sperm of some amphipods are straight and ribbon-like with no angle between the head and tail (Nichols, 1909). Tanaid sperm are

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_

/m

t

I

A

B

C

h

..

E

Figure 5 Overall structure of spermatozoa of selected peracaridans. Despite many differences, all have a long nonmotile tail, or "handle" (t) which consists of a membrane-bound proteinaceous rod. In the mid-region (m), the tail is attached at an acute angle to the head, or "lash" (h), which contains the nucleus, mitochondria and other organelles (A) The mysid Praunus flexuosus (after Labat, 1962). (B) The mysid Praunus inermis (after Fain-Maurel et al., 1975a). (C) The amphipod Caprella aequilibra (after Tuzet and Sanchez, 1952). D. The terrestrial isopod Anilocra physodes (after Fain-Maurel, 1966). E. A schematic isopod (after Craciun, 1987).

round, lack appendages, and have a large acrosome with scattered mitochondria (Cotelli and Lora Lamia Donin, 1980). As is true for most crustaceans, the tail of a peracaridan sperm lacks the characteristic 9 + 2 arrangement of microtubules found in flagella and does not originate from a centriole. The sperm is generally considered to be nonmotile, but Williamson (1951) reported slow, vermiform movements in the tails of sperm immediately after they were removed from the brood pouch of an ovipositing female Orchestia (Amphipoda). This movement did not resemble flagellar beating and ceased within one minute. Adiyodi (1985) speculates that the immotility of crustacean spermatozoa may be related to the need for long periods of storage in the female prior to fertilization, while Subramoniam (1993) suggests that immotility of crustacean sperm made packaging of sperm into spermatophores necessary.

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A

P

Figure 6 The mid-regions of peracaridan spermatozoa are the point of origin of the tails and therefore connect the tails to the heads. A. The mid-region of the mysid Praunus inermis contains a proteinaceous inclusion (p) that forms a grooved column, or "gutter" located along the side opposite the junction with the tail (t) and parallel to the nucleus (n) (after Fain-Maurel et al., 1975a); B. In the deep-sea isopod Bathynomus giganteus, the proteinaceous inclusion is a rod that extends parallel to the nucleus from a vesicle (v). The vesicle has been called an acrosome by several authors, n = nucleus, p -- proteinaceous rod of the midpiece, t = tail, v = vesicle of the midpiece (after Perry and Hinsch, 1991). Not to scale.

Ultrastructurally, the tail is a membrane-bound rod of fibrillar material with striations of species-specific periodicity (Blanchard et al., 1961; Reger, 1964a; Fain-Maurel, 1970; Craciun, 1987). The striations can be resolved into bands that are further based on components of 6A and 8A. This subunit structure indicates that the rod is composed of proteinaceous material which resembles collagen more closely than it does microtubular protein (Reger, 1964b). Often an electron-dense cortex surrounds an electron-transparent core, causing Reger (1964b) to suggest that the tail inclusion is hollow. The tail accounts for most of the length of the peracaridan sperm. The head, or lash, has three regions. The tail attaches to the head at a region designated the mid-region (Figure 6), or intermediate piece, characterized by proteinaceous supporting structures that are unique to the sperm of Peracarida. Adjacent to this region is the median segment containing the nucleus, centriole(s) and mitochondria. The extreme distal

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region of the head contains specialized cytoplasmic structures and is generally believed to contain the acrosome. The structure of the junction between head and tail differs from order to order. In mysids the proteinaceous supporting structure extends lengthwise along the head. As described by Fain-Maurel et al. (1975a), the proximal end of the tail lies in a U-shaped groove in the surface of the mid region. The extreme proximal end of the groove is roofed so that the proteinaceous inclusion entirely surrounds the proximal end of the tail. Instead of a groove, isopod sperm have a rounded vesicular formation at the junction of head and tail. Their midpieces also contain a proteinaceous inclusion similar to that found in the midpiece of mysid sperm (Pigeault, 1957; Fain-Maurel, 1970; Fain-Maurel et al., 1975a, b; Perry and Hinsch, 1991). Tanaid sperm heads are less specialized than those of mysids or isopods. The roughly spherical nucleus contains partially condensed chromatin and is surrounded by a nuclear envelope containing nuclear pores. At one pole is an acrosomal vesicle containing three different types of electron dense material organized into distinct zones. Electron dense sub-acrosomal material is present, associated with a rod-shaped "perforatorium" that protrudes into the acrosomal vesicle. Cytoplasm containing membranous cisternae and mitochondria is also present. These sperm lack either a traditional microtubular flagellum or the proteinaceous tail of isopods and mysids (Cotelli and Lora Lamia Donin, 1980). They also lack the modified centrioles that have been described in the spermatozoa of other peracarida. The mitochondria in the median part of the head vary in size, number and arrangement. Sperm of Archeomysis have large mitochondria, while those of Neomysis are small (Kasaoka, 1974). In mysid sperm the nucleus is greatly indented by numerous mitochondria and is surrounded by a multilamellar membrane of endoplasmic reticulum (Fain-Maurel et al., 1975a). The heads of Gammarus pulex sperm are described by Koster (1910) as having a single spiral mitochondrion covering the entire nuclear region. This report has not been confirmed with the electron microscope. Labat (1962) describes two centrioles in the mid-region of Praunus flexuosus, connected by a long desmosome, but Fain-Maurel and coworkers (1975a) were unable to find a second centriole in P. inermis sperm. The distal end of the "lash" is generally believed to be the acrosomal region, although Reger (1966) and Perry and Hinsch (1991) give this name to a vesicle in the mid-region. The distal cytoplasm is fairly abundant (Labat, 1962) and contains concentrically arranged multilamellar membranes (Fain-Maurel et al., 1975a). In isopods a granule originating from the Golgi apparatus at the free extremity is believed by Fain-Maurel (1970) to be analogous to an acrosome. Sugiyama (1933) and Reger (1966)

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describe a rod-like structure associated with the acrosome and located in the mid-region of the sperm head rather than the distal region. We suspect that these authors are calling the vesicle in the mid-region the acrosome and that the rod is actually the protein inclusion of the mid-region. The mature sperm are packaged into spermatophores in isopods (Nichols, 1909; Sugiyama, 1933), amphipods (Gerstaecker and Ortmann, 1901), mysids (Labat, 1962; Fain-Maurel et al., 1975a) and cumaceans (Zimmer, 1941). The bundle of sperm may be surrounded by an extracellular sheath (Nichols, 1909; Zimmer, 1941; Fain-Maurel, 1970). This sheath may be a mucous coating (Pigeault, 1957), a gelatinous sheath (Sheader, 1981), or a partition of steUate cell cytoplasm (Reger, 1964b). Sperm are held together by their tails and aligned head to head and tail to tail. Nuclei project from the bundle at irregular intervals in a roughly helical arrangement (Pigeault, 1957). Sperm bundles are generally present in the seminal vesicle, but may be dispersed in the lower genital tract. 4.1.2.

Origin of spermatogonia and meiosis

Primary gonia, still embedded in the mesodermal reticulum of the germ area, are 9-12/zm in diameter, with large nuclei (Tuzet and Sanchez, 1952). Many ribosomes and polysomes are in the cytoplasm, but the endoplasmic reticulum is poorly developed. A unique membrane connects the nucleolus to the internal nuclear membrane in gonia of Orehestia gammarellus (Meusy, 1968), but otherwise no structures peculiar to gonia are described. Periodically, a population of primary gonia migrates into the lumen or, in mysids, into the first set of pouches between the testes and the seminal vesicles where they become secondary gonia. These generally resemble primary gonia, but in O. gammarellus the membranous structure in the nucleus is lost (Meusy, 1968). The secondary spermatogonia multiply by mitosis prior to entering meiosis. As they enter prophase I, the primary spermatocytes become surrounded by a single layer of satellite, or follicle, cells, which arise from the lining of the testes or, in mysids, from the innermost epithelial layer of the wall of the pouches (Kasaoka, 1974). Meiosis and cytoplasmic differentiation of spermatids take place in close association with satellite cells. Cytoplasmic processes of the satellite cell completely surround the spermatocytes (Kasaoka, 1974). Normally four spermatids, the progeny of a single primary spermatocyte, are contained within one satellite cell, but the number varies from three to five, suggesting some loss and capture of spermatids by satellite cells (Labat, 1962). The resulting close association between sperm and satellite cell explains early reports of syncytial development of spermatids (Gilson, 1886; Sugiyama, 1933; Labat, 1962). Reger (1964b) and Kasaoka (1974) found no ultrastructural evidence for

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a syncytium, definite cell boundaries always existing among spermatids and between spermatids and satellite cells. The accessory cells are large secretory cells which may have lobed (Kasaoka, 1974) or large polyploid nuclei and multiple nucleoli (Montalenti et al., 1950). Their nuclear state reflects the state of spermatogenesis, as periods of intense RNA secretion in these cells are sometimes associated with lepto-zygotene and diakinesis-metaphase I of the spermatocyte (Montalenti et al., 1950). In Orchestia spp., the accessory cells do not undergo any cytological changes until diakinesis, when they grow and their nuclei swell. The function(s) of these cells is not well understood. They are active in protein synthesis during spermatogenesis in the freshwater isopod Asellus aquaticus (Brasiello, 1971) and in the marine valviferan isopod Saduria entomon (Hryniewiecka-Szyfler and Tyczewska, 1991). In Orchestia, they are believed to secrete the mucus sheath of the spermatozooids (Berreur-Bonnenfant, 1967; CharniauxCotton, 1965) (see section on spermatophores). They may also be involved in recycling, as Kasaoka (1974) has observed vesicles filled with electron dense material in the cytoplasm of follicle cells of the mysid genus Archeomysis and suggested that these vesicles might contain the remnants of the preceding generation of spermatids. The primary spermatocytes are fairly large cells with swollen nuclei and a coarse network of chromatin (Sugiyama, 1933; Tuzet and Sanchez, 1952; Menzies, 1954). The cytoplasm contains Golgi bodies and mitochondria (Tuzet and Bessiere, 1951; Labat, 1962). The nucleolus varies from species to species, as multiple nucleoli associated with the nuclear membrane are described for Orchestia (Nichols, 1909) and a single peripheral nucleolus, disappearing during meiosis, for Praunus flexuosus (Labat, 1962). No nucleolus was seen in primary spermatocytes of caprellid amphipods (Tuzet and Sanchez, 1952). During meiosis the cytoplasm remains relatively unchanged. In the nucleus, however, the chromatin filaments shorten and condense into chromosomes. As described for caprellid amphipods (Tuzet and Sanchez, 1952) and isopods (Tuzet and Bessiere, 1951), the chromosomes condense into spirenes that form loops at leptotene. Tetrads may or may not be visible in the numerous chromosomes. At metaphase II large, hemispheric Golgi bodies, bordered by mitochondria, are present in the cytoplasm. The first and second meiotic divisions occur quickly and in a normal manner. The young spermatid is small (5.5-7/~m diameter) and has a nucleus with chromatin condensed in a ring (Tuzet and Sanchez, 1952) or a hemispheric crescent (Labat, 1962) around its periphery. Two centrioles are located on one side of the nucleus, one near the nuclear membrane and the other near the plasma membrane. They are surrounded by mitochondria and give polarity to the cell (Tuzet and Sanchez, 1952).

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WILLIAM S. JOHNSON, MARGARET STEVENSAND LES WATLING

Sperm differentiation, or spermiogenesis

Within the cyst of spermatids, each cell changes from a roughly spherical cell to the whip-like sperm previously described. A number of competent studies have been made using light microscopy (Tuzet and Bessiere, 1951; Tuzet and Sanchez, 1952; Labat, 1962), but more recent studies have employed the electron microscope. Sperm differentiation was most recently reviewed by Fain-Maurel (1970). The considerable variation among orders, and even species, requires us to treat each part of the spermatozoon separately. The cell body of the spermatid undergoes elongation to become the head of the mature sperm. Differentiation is apparent in the acentric location of the centrioles. These separate early during spermiogenesis and move to opposite ends of the spermatid. One, designated the posterior centriole, then divides again into a proximal and distal centriole. The anterior centriole remains undivided. It will be associated with the cytoplasmic region of the head, while the two posterior centrioles are located in the region from which the tail arises. The two posterior centrioles are connected by a desmosome. The proximal one pushes further and further into the nucleus, eventually lying in a deep indentation of the cytoplasm extending into the nucleus but separated from it by the nuclear envelope (Tuzet and Sanchez, 1952). In Praunus inermis only one centriole, occupying the usual position of the proximal centriole, is present. Near this centriole, but not actually in contact with it, a hemispheric vesicle forms either in association with Golgi apparatus in mysids (Fain-Maurel et al., 1975b) or with the endoplasmic reticulum in isopods (Fain-Maurel, 1970). This vesicle, located near the posterior pole of the young spermatid, becomes the point of articulation between the head and the tail. Two inclusions appear in association with this vesicle. The first is the tail, which begins as an electron-dense cytoplasmic cone projecting outward from the vesicular region, pushing the plasma membrane ahead of it as it elongates. It continues to lengthen and, still bound by the plasma membrane, indents an adjacent satellite cell, but always remains separated from the satellite cytoplasm by its own and the satellite cell plasma membrane (Reger, 1964b). The intimate association of the developing tail with the satellite cell led early authors to believe that the tail was secreted separately from the rest of the sperm by the satellite cell and later united to it (Gilson, 1886). Sugiyama (1933) first reported that the tail developed from the sperm head, but incorrectly associated it with the centriole. In fact, it is never associated with the centriole, nor with a typical 9 + 2 pattern of microtubules. The repeating striations of electron dense and electron transparent material are present from the start (Reger, 1964b). The tails of all the spermatozoa associated

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with the same satellite cell become bundled together and are arranged around the nucleus of the satellite cell inside a pouch that projects into the cell's cytoplasm (Kasaoka, 1974). Originating from the same vesicle as the tail is another proteinaceous inclusion variously called the "cresta" in isopods (Fain-Maurel, 1970) or the "goutierre" ("gutter" or "trough") in mysids (Fain-Maurel et al., 1975b). The cresta of isopods emerges from the vesicle on the side opposite of the tail and then grows parallel to the nucleus. The cresta is proteinaceous and electron dense in both groups and may serve to support the delicate zone of articulation between head and tail. In isopod sperm, the cresta is sometimes connected to the centriole by microtubules (Fain-Maurel, 1970), but it also seems to be a product of the Golgi apparatus rather than of the centriole. The protective function of the mid-region is most pronounced in mysids, in which the vesicle elongates along with the tail and forms a groove enclosing the tail. The zone of articulation is thus buried deep within the body of the sperm head (Fain-Maurel et al., 1975a, b). Anterior to the vesicle and the posterior centriole(s) is the median region of the head, containing the nucleus and mitochondria. In the young spermatid, the nucleus is spheroidal and centrally located, but it elongates considerably during spermiogenesis. Its contents are reticular, bounded by a lining of heterochromatin, especially near the mid-piece vesicle. A large nucleolus is present (Fain-Maurel et al., 1975b). As the nucleus elongates the ring of heterochromatin becomes reticular and finally disappears (Koster, 1910). In mysid sperm, a multilamellar nuclear envelope forms from the endoplasmic reticulum (Fain-Maurel et al., 1975b) or from the Golgi (Kasaoka, 1974). The inner, or true, nuclear membrane has large pores, 6-7/~m in diameter with clear regions containing vesicles in the cytoplasm nearby (Fain-Maurel et al., 1975b). The proteins in the chromatin change from the lysine-rich histones found in early spermatocytes to arginine-rich histones. In the mature sperm, no histones remain. They are believed to have been replaced by protamines (Brasiello, 1971). In isopod sperm, a number of 150 ,~ tubules originate from the centriole and extend along the long axis of the nuclear region. These microtubules are similar to the manchette of mammalian sperm and may play a role in the elongation of the nucleus (Fain-Maurel, 1970). In early spermatids, mitochondria are associated with the nucleus in the mid-region, but their position changes as spermiogenesis proceeds. In fact, no mitochondria are present in mature sperm of the isopods Nerocula and Armadillidium, although they are present during differentiation (Idelman, 1967). In other isopods, they are present in mature sperm, arranged regularly along the cresta (Fain-Maurel, 1970). Mitochondria in

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young spermatids of caprellid amphipods are first clustered around the desmosome connecting the two centrioles, but in mature sperm the mitochondria are localized in the distal cytoplasm and absent from the mid-piece (Tuzet and Sanchez, 1952). As differentiation proceeds, the cytoplasm of the developing spermatid collects in the extreme distal region of the head anterior to the nucleus (Koster, 1910; Labat, 1962; Fain-Maurel et al., 1975b). This region usually contains dictyosomes which are often united into an idiosome (Idelman, 1967). Associated with them are the anterior centriole, mitochondria and endoplasmic reticulum, which in mysid sperm is elaborated into festooning lamellae (Fain-Maurel et al., 1975b). Any cytoplasm to be sloughed off the spermatozoon is also located in this region. The acrosomal granule is an electron dense inclusion in the distal region and is not membrane-bound in mysids. It may, however, have a membrane in isopod sperm (Idelman, 1967). The acrosomal contents are secreted by the idiosome (Tuzet and Bessiere, 1951; Fain-Maurel, 1966) or dictyosomes (Labat, 1962; Fain-Maurel et al., 1975b). The contents are chromophilic (Tuzet and Sanchez, 1952; Labat, 1962) and appear granular and fibrillar in electron micrographs, looking somewhat similar to ribosomes (Fain-Maurel et al., 1975b).

4.2.

Formation of the Spermatophore

Mature sperm of Peracarida are bundled into packages called spermatophores which contain 15-30 sperm and probably aid in transfer of the nonmotile sperm to the female reproductive tract (Reger and FainMaurel, 1973). Spermatophores seem to have very similar structure in isopods (Fain-Maurel, 1966; Reger and Fain-Maurel, 1973), mysids (Reger et al., 1970; Reger and Fain-Maurel, 1973; Kasaoka, 1974; Itaya, 1979), amphipods and cumaceans (Reger and Fain-Maurel, 1973). The sperm are oriented with their long axes running parallel to each other, tail in the center of the bundle, and head pointing outwards. The mid-regions at the junction of tail and head, called the acrosomes by some authors, are located at the apex of the bundle. A cone-shaped vestment of extracellular tubules which are 40--45 nm in diameter surrounds the apex of the spermatophore, extending forward beyond the spermatids and rearward to surround the nuclei. In the terrestrial genus Ligia, the tubules extend through the entire length of the spermatophore (Cotelli et al., 1976). The tubules are embedded in an electron-dense matrix, which is also found encircling the tails, where tubules are lacking (Itaya, 1979). Tubules with diameters ranging from 35-70 nm have been found in many Peracarida. The matrix is apparently secreted by the Golgi apparatus of the satellite

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cell. Hryniewiecka-Szyfter and Tyczewska (1991), studying the isopod S. entomon, found that the arrangement of spermatozoa within a spermatophore resembles the organized pattern imposed on the spermatid by the processes of accessory cells during spermiogenesis. They postulate that the extracellular tubules are synthesized by the cells of the proximal vas deferens following a pattern created by the accessory cells. Itaya (1979), and Reger and Fain-Maurel (1973), however, provide evidence that the accessory cells of A. vulgare and mysids secrete the tubules as well as the matrix. They have found extensive RER and dictyosomes associated with vesicles inside accessory cells that seemed to be transporting tubules to the extracellular channels surrounding the spermatids. Itaya also found extracellular tubules surrounding spermatids in the testes. The tubules persist in spermatophores of isopods even as they move down the vas deferens into the ejaculatory duct (Itaya, 1979), but in mysids the tubules disaggregate into filaments in the lower vas deferens (Reger et al.. 1970).

4.3. 06genesis O6genesis follows a common pattern in the species of Peracarida that have been studied, Primary o/3gonia originate from the germ layer in the wall of the ovary and remain embedded there. In reproductively active females, they divide by mitosis to produce secondary o/3gonia that are then pushed into the lumen of the ovary (Meusy, 1968; Zerbib, 1973). These cells enter first meiotic prophase and, as primary oocytes, undergo a period of previtellogenic growth during which no yolk is synthesized. Primary vitellogenesis follows, during which growth is relatively slow but yolk is being synthesized in the o/~cyte. An entire generation of o/~cytes that have completed primary vitellogenesis may accumulate. These oticytes displace an older generation of oocytes that move toward the center of the ovary and enter secondary vitellogenesis, which is a period of rapid growth and yolk deposition. Thus ovaries typically contain several generations of primary oocytes with o6cytes in the center growing most rapidly. When the older generation is full grown, mating and fertilization occur at the next molt. This initiates a round of mitosis among the primary o/~gonia to create a new generation of vitellogenic o/~cytes. 4.3.1. Pre-vitellogenic development Newly created oocytes are small cells, 15-20/xm in diameter in Orchestia gammarella (Zerbib, 1973) and 40--65/~m in isopods (Gerstaecker and

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Ortmann, 1901; Menzies, 1954; Kumari et al., 1993). They are arrested in pachytene (Montefaschi and Magaldi, 1953), zygotene (Lrcher, 1967), ordiakinesis (Charniaux-Cotton, 1985) until the completion of the cytoplasmic development of the oocyte. They have a nucleus 3-9/~m in diameter, with a single nucleolus and basophilic cytoplasm (Corey, 1969). Lampbrush chromosomes are present in some species (Nair, 1939; Lrcher, 1967). They do not appear to be active synthetically, having few ribosomes and dictyosomes and a poorly developed endoplasmic reticulum (Zerbib, 1973). During previtellogenic growth specialized structures appear. An egg nucleus, or "pseudonucleus", consisting of dense membrane-bound material containing chromatin appears early during previtellogenesis (Zimmer, 1941; Zerbib, 1973). A similar structure, described by Montefaschi and Magaldi (1953) as an accumulation of basic protein and DNA just outside the nuclear membrane, is present in young oocytes of Asellus aquaticus. It is acentric and associated with the nucleolus, which is large and may have "vacuoles" (Hryniewiecka-Szyfter and Babula, 1995). These do not appear to be actual vacuoles, but small areas, round in transverse section, and filled with material that is less electron dense than the surrounding nucleolar matrix. Possibly they contain the DNA of the nucleolar organizing region of the chromatin. O6cytes of mysids at least double their diameter during previtellogenic growth (Nair, 1939). In the amphipod Orchestia gammarella they grow from 20 to 160/~m in diameter (Zerbib, 1973). The nucleus also enlarges, reaching a diameter of 35 ~m (Nair, 1939). As they grow, the oocytes lose their basophily (Corey, 1969) and accumulate ribosomes, granular endoplasmic reticulum, mitochondria, Golgi apparatuses, and microtubules. The oocyte surface becomes covered with microvilli, 30-40/zm in length, which traverse the vitelline envelope to contact the follicle cells (Zerbib, 1973; Hryniewiecka-Szyfter and Babula, 1995).

4.3.2.

The ovarian cycle

Follicle cells have been described in isopods (Leichmann, 1891; Menzies, 1954; Souty, 1980), cumaceans (Zimmer, 1941) and amphipods (Charniaux-Cotton, 1965, 1974; Zerbib, 1973; Rateau and Zerbib, 1978). The origin of these cells has been identified as the ovarian wall (Van Beneden, 1869) or as the germ layer (Leichmann, 1891). A group of follicle ceils surrounds each oScyte early during previtellogenic growth, forming a follicle that remains with the oOcyte until it is released from the ovary. Charniaux-Cotton (1974) found that in Orchestia gammarella the number of follicle cells associated with a single orcyte increased from four or five surrounding a previteUogenic o0cyte to approximately 70

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surrounding an oOcyte in secondary vitellogenesis. The shape of the follicle cells changes from columnar to flattened as the follicle grows (Rateau and Zerbib, 1978). A similar shape change occurs in follicles of the isopod Idotea balthica basteri (Souty, 1980). Changes in the follicle cell ultrastructure provide evidence of increasing synthetic activity during oogenesis, as the cytoplasm accumulates mitochondria, Golgi apparatuses, rough endoplasmic reticula and ribosomes. Microvilli extend from the surface of follicle cells and cross the forming vitelline layer, contacting similar processes belonging to the oOcyte. The follicle cells adhere to each other and the basal lamina via tight junctions, desmosomes and hemidesmosomes (Rateau and Zerbib, 1978; Souty, 1980). These cells may contribute to oogenesis in some way, possibly by synthesizing a component of the vitelline layer (Zimmer, 1941). Hryniewiecka-Szyfter and Babula (1995), however, did not see evidence of synthetic activity in the follicle cells of Saduria entomon, a valviferan isopod, and concluded that the o6cyte synthesizes its own RNA. In O. gammarellus the follicle cells are believed to be the source of a hormone called vitellogenin-stimulating ovarian hormone (VSOH) that stimulates production of vitellogenin by the fat body. This process occurs only in the presence of an ovary in this species. However in the terrestrial isopod A. vulgare, no such ovarian hormone is involved, and vitellogenesis can proceed in the fat body in the absence of the ovary (Hasegawa et al., 1991). The fate of follicle cells that have participated in o6genesis may differ in amphipods and isopods. In amphipods the follicle cells leave the o6cyte prior to deposition and are recycled, joining other o6cytes which are about to enter vitellogenesis (Charniaux-Cotton, 1974). Souty (1980) found pycnotic follicle cells surrounding fully grown o6cytes in the isopod Idotea balthica basteri and believes that they degenerate after o6genesis is complete. 4.3.3.

Vitellogenes&

Rapid growth of the oOcyte results from accumulation of yolk and therefore is associated with vitellogenesis. Isopods and amphipods provide the primary modern studies of the ultrastructure involved in yolk deposition. We include some studies on terrestrial peracaridans that provide information as yet unavailable for marine species in which the basic process of vitellogenesis should be similar. It is generally agreed that there are two mechanisms of yolk synthesis, called endogenous and exogenous. These two processes take place at different stages of oOgenesis and make different products that eventually mix together in the same vesicles to form the yolk of the mature egg (Zerbib, 1977). oOcytes first enter primary vitellogenesis, characterized by endogenous yolk synthesis,

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which is restricted to this stage in some species (Bilinski, 1979). This process produces a granular product that is synthesized in the RER and accumulates in vesicles that arise directly from RER. This "primary yolk" is a glycoprotein (Zerbib, 1976), but appears to bypass the Golgi apparatus (Bilinski, 1979). It remains sequestered in vesicles of the ergastoplasmic reticulum until o6genesis is nearly complete. Exogenous yolk synthesis takes place during secondary vitellogenesis, which is characterized by rapid pinocytosis, as evidenced by rate of uptake of peroxidase (Zerbib, 1976, 1977). O6cytes enter secondary vitellogenesis at the beginning of the intermolt prior to the molt at which they will be fertilized. Although secondary vitellogenesis is of short duration, most o6cyte growth occurs during this stage. As an example, o6cytes of Orchestia gammarella grow from 200/~m to 800/zm in diameter (Zerbib, 1973). A cytoplasmic region surrounding the nucleus is connected to the peripheral cytoplasm at the surface by a network of cytoplasmic strands. Yolk granules are deposited between the strands and gradually hide them (McMurrich, 1895). Usually the nucleus is centrally located, but in the mysid Mesopodopsis orientalis yolk deposition occurs only on one side of the o6cyte, and the nucleus is pushed to the other side (Nair, 1939). As yolk accumulates, the o6cytes change in color from white to the color contributed by the yolk, which often matches the animal's habitat. Because many females are relatively unpigmented, this matching of yolk color to background coloration has obvious survival value (Wittmann, 1981a). The product of exogenous yolk synthesis in oniscoid isopods is a glycolipoprotein containing carotenoid pigment and called viteUin (Zerbib, 1977). The chemical makeup is similar but not identical from species to species. Yolk protein is synthesized outside the ovary in the fat body (Croiselle and Jun6ra, 1980; Picaud and Souty, 1980) in the form of higher molecular weight precursors collectively called vitellogenin (Souty and Picaud, 1981; Suzuki et al., 1989) and then transported to the ovary via the haemolymph (CroiseUe et al., 1974; Suzuki, 1987; Suzuki et al., 1989). In ovaries of Idotea balthica basteri intercellular spaces appear between the follicle cells during secondary vitellogenesis. These spaces provide a route by which vitellogenin can reach the surface of the o6cyte (Souty, 1980). O6cytes in secondary vitellogenesis have microvilli, which greatly expand their surface area. They actively pinocytose vitellin or its precursor and incorporate it into coated vesicles (Zerbib, 1977; Souty, 1980). These vesicles fuse with thin-walled tubular structures called microcanaliculi, which are continuous with the endoplasmic reticulum and contain the primary yolk (Zerbib, 1977). The processing of vitellogenin into vitellin decreases the molecular weight, while conserving immunological identity (Suzuki, 1987). For this reason it is believed to involve proteolytic

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cleavage of the molecule (Suzuki, 1987; Suzuki et al., 1989). Whether this cleavage occurs before or after pinocytosis has not been determined. This area has been reviewed for malacostracans in general by CharniauxCotton (1985). Cortical granules appear in the o0cytes of Orchestia gammarella after the oOcytes have been extruded into the brood pouch. These granules are oval and membrane-bound with a dozen or so concentric lamellae of differing electron densities. They are 0.1-0.2/~m in diameter and are closely associated with the plasma membrane (Zerbib, 1975).

4.4.

Hormonal control over gametogenesis

Gametogenesis is controlled in several ways. First, the onset of gametogenesis must be controlled so that the organism is large enough to support gametogenesis. This form of control has not yet been studied in peracaridans. Secondly, the environment must provide clues that control seasonal and possibly diurnal manifestations of reproductive cycles. Finally, the various structures involved in reproductive activity must be coordinated so that they all operate on the same timetable. Because the body must coordinate the function of many organs, which must respond to external events, it should not be surprising that reproductive processes are coordinated internally by chemicals synthesized in response to the activity of the nervous system. Both the external control mechanisms and the ultimate adaptive value of specific life cycle traits represent areas of active research. The role of environmental factors in influencing the timing of gametogenesis is discussed in the section on reproductive cycles. Internal controls over gametogenesis are believed to be hormonal, involving chemicals that are produced in specific organs and reach their target(s) via the hemolymph or by diffusion. Payen (1991) has reviewed control over gametogenesis in male crustaceans. The androgenic gland (AG) controls maintenance of the germinal zone and spermatogenesis in the testes of amphipods and isopods. In organisms that breed seasonally, the size of the AG fluctuates, enlarging during the breeding season. In Orchestia gammarella the supraoesophageal ganglion of males, but not of females, liberates a hormone that helps to maintain the genital tract. When a protandric hermaphrodite changes from male to female, production of this hormone ceases (Charniaux-Cotton and Payen, 1985). AG function is downregulated by three different products of neurosecretory cells. A secretion of the optic lobe and/or protocerebrum of the brain controls AG formation. A secretion of neurosecretory cells scattered throughout the entire nervous system inhibits synthesis of AGH, and yet another

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generalized neurosecretion controls its release into the hemolymph (Payen, 1991). Studies of hormonal control in female peracaridan species have centered around control over o/Scyte maturation, reviewed most recently by Meusy and Payen (1988) and vitellogenesis, reviewed by Adiyodi (1985), Charniaux Cotton and Payen (1985), Charniaux-Cotton (1985) and Hasegawa et al. (1993). The germinal zone of the ovary does not depend on secretions from any other organs for maintenance, but production of secondary follicles requires a secretion of the protocerebrum (CharniauxCotton and Payen, 1985). The major site of yolk protein synthesis is the fat body, which synthesizes 60 times more vitellogenin than the ovary (Suzuki et al., 1989). The fat body of amphipods, but not of isopods, is stimulated by vitellogenin stimulating ovarian hormone (VSOH) produced in the ovary, probably by the follicle cells. The fat bodies may also be stimulated by ecdysteroids, or molting hormones. In terrestrial isopods, ecdysteroids produced by the Y organ are present at much higher levels (5x) in females than in males, and in each molting cycle ecdysteroid production peaks during the period of vitellogenesis (Suzuki et al., 1996). Extirpation of the Y organ, which is the site of production of the ecdysteroids, causes a decrease in vitellogenin synthesis and therefore in the rate of oOcyte growth. For these reasons ecdysteroids are believed to stimulate vitellogenesis. However, at least in isopods, ecdysteroid hormones are produced in about the same concentrations in both breeding and nonbreeding females (Suzuki et al., 1996), which suggests that the role of Y organ secretions in regulation of reproductive cycles needs to be examined more closely. Because reproductive activities such as mating and formation of o6stegites are dependent on molting, it is not surprising to find that molting hormones play a role in regulation of o6genesis. Neurosecretions may stimulate or inhibit vitellogenesis. In the mysid Siriella arrnatai destruction of the eyestalk prevents the completion of secondary vitellogenesis and results in degeneration of o(icytes. I t is unknown whether this effect is because of the presence of a hormone that acts directly on the fat body or ovary or indirectly via the Y organ and production of ecdysteroids (Cuzin-Roudy and Saleuddin, 1989). As previously stated, a protocerebral factor is required for secondary vitellogenesis in the amphipod Orchestia gammarella (Charniaux-Cotton and Payen, 1985). A hormone that inhibits uptake of vitellogenin (Vitellogenin Inhibiting Hormone, VIH) has been found in the medial part of the protocerebrum of isopods. In amphipods VIH is present, but is produced in another part of the brain. VIH may act through inhibition of vitellogenin synthesis by the fat body and/or uptake of vitellogenin by the ovary (Hasegawa et al., 1993).

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5. 5.1.

143

REPRODUCTIVE CYCLES Life cycles

Reproductive patterns are best known for temperate littoral and coastal gammarids, isopods and mysids (Figure 7). Only a few caprellid, hyperiid, cumacean and tanaidaeean life cycles have been established, and nothing at all is known for thermosbaenaceans, spelaeogriphaceans or mictaceans. Mauchline's comprehensive review (1980) of mysid biology remains the most complete treatment for life cycles in that group while gammarids were extensively reviewed by Sainte-Marie (1991). Important earlier contributions by Morino (1978), Nelson (1980), Van Dolah and Bird (1980) and Wildish (1988) provide additional perspectives on gammarid life cycles. Gammarids typically have one overwintering generation and one or more spring-summer generations. The number of generations per year and the number of successive broods per female decrease with latitude as reproductive output is increasingly concentrated in the warmer months. Rapid growth rates and smaller size at first reproduction, coupled with short incubation times for the smaller eggs all contribute to shorter summer generations. Boreal and polar species are more likely to be large and have a single large, well-timed brood. In contrast, warm temperate species tend to be small in size, produce many small broods, and have several generations a year (D. Steele and Steele, 1975c). Reproductive cycles in the tropics can be much faster. Melita zeylandica from brackish lakes in India matures in less than 30 days and can produce up to 22 broods per year at intervals of only 8 days (Krishnan and John, 1974). Even within an amphipod species, there is some plasticity of life cycles owing, in part, to differences in food availability. Leonardsson et al. (1988) observed that populations of Pontoporeia from different depths in the Gulf of Bothnia reached maturity after 2, 3 or 4 years. They suggest that reproduction occurs when females reach a certain "threshold size" and that differential growth rates result in variation in maturation time. Gamrnarus salinus produces two generations per year in the Baltic and one in Limfjord (Kolding and Fenchel, 1981). However, Franz (1989) noted that multiple cohorts should be particularly advantageous in unpredictable environments such as rocky intertidal areas where space is sporadically available or where predation is high (Wilson and Parker, 1996). Still, there is little evidence of multiple cohorts being commonly associated with any specific habitat type. Life cycles for temperate mysids are consistent with this gammarid pattern. For example, Antarctomysis ohlini had generation times of 3 to

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12 Figure 7 Schematic representations of typical peracarid life cycles. Small arrows directed inward indicate release of a brood. A. An annual cycle with a single brood per female (Cyathura carinata). B. Discrete summer and winter generations, with the former giving rise to multiple broods (Orchestiagammar~lla). C. Multiple overlapping generations (Idotea viridis). All data from Arcachon, France. (After Amanieu, 1970.)

5 years (Ward, 1985). In contrast, temperate isopods and cumaceans tend to have longer life spans and usually lack the discrete summer and overwintering generations displayed by mysids and gammarids. In general, cumacean life cycles end with terminal males and females, with most females producing only a single brood before they die (Corey, 1981). However, some estuarine cumaceans like Almyrocuma proximoculi do have multiple broods with smaller summer generations (Duncan, 1984). Sporadic data on tanaidaceans and caprellid and hyperiid amphipods reveal no definitive pattern in their life cycles. Data available for deep-sea amphipods and isopods and for mesopelagic mysids suggest rather long life spans with late maturity and lengthy incubation times. For example, the deep-sea/polar lysianassoid amphipod Eurythenes gryllus (Ingram and Hessler, 1987) lives at least 13 years, and other abyssal species may live even longer.

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5.2.

145

Reproductive timing and control of gametogenesis

Despite numerous studies, the interplay between environmental cues and endogenous rhythms in controlling reproductive timing remains obscure. Specific environmental factors can limit reproduction in a given situation, but most natural cycles result from seasonal fluctuations in temperature, photoperiod or food availability. Early experiments on Orchestia gammarella (Charniaux-Cotton, 1957) provided strong evidence that temperature alone regulates this supralittoral gammarid's reproductive cycle, and these early findings are supported by Moore (1983), Moore and Francis (1986), and Morritt and Stevenson (1993). In other gammarids, photoperiod is clearly involved (Segerstr~ile, 1967, 1970, 1971a, b; D. Steele and Steele, 1975c), and several different aspects of photoperiod have been implicated. Talitrus saltator, also from a supralittoral habitat, reproduces when photoperiod reaches a "critical day length" (Williams, 1985). In contrast, controlled laboratory experiments suggested that changes in photoperiod rather than any specific day length triggers reproduction in Garnrnarus setosus (Steele et al., 1977). Reproductive cycles in polar marine animals often coincide with seasonal productivity peaks (Dunbar, 1957; Bone, 1972; Thurston, 1979). D. Steele and Steele (1975c) and Kolding (1981) emphasize that release of the brood is timed to match the availability of small filamentous algae eaten by newly liberated Gammarus. Even in the deep sea, isopods (Harrison, 1988), cumaceans (Bishop and Shalla, 1994), and amphipods (Powell, 1992) have seasonal reproductive peaks coincident with seasonal detrital deposition (Powell, 1992). In these cases, it is unlikely that food availability triggers gametogenesis. It is more probable that the phylogenetic history of the taxon (Eckelbarger and Watling, 1995) serves as the master governing variable, ensuring that gametogenesis occurs on a schedule such that the young are released when ample food is available.

6. REPRODUCTIVE BEHAVIOR As a rule, mating takes place when the fully developed o6stegites of the marsupium appear at the females' ovigerous molt. Ovulation and then fertilization in the brood pouch or oviducts follows promptly. The timing of these three steps would seem to (1) ease passage of the large, yolky eggs through the gonopores while the cuticle is soft, (2) facilitate the act of copulation by having it occur before the marsupium is fully formed and

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

hardened (at least in some species); and (3) maximize the chances of fertilization by depositing the eggs promptly after mating while the sperm are fresh and before they are washed from the marsupium.

6.1.

Pairing and precopulatory behavior

Since fertilization is possible for only a brief period after the female's ovigerous molt, recognition between males and conspecific females that are approaching their reproductive molt is crucial. The mechanisms facilitating pair recognition are still the subject of both controversy and, rather belatedly, renewed investigation. Holmes (1903) failed to detect any sign of either visual or olfactory recognition by Hyalella dentata (=azteca) males that attempted to amplex virtually all other amphipods they encountered including immature females and other males Males and juvenile females violently resisted such improper advances, but ripe females remained quiescent. Female Orchestia palustris that could not be separated from males by force were readily released when the female was prodded and began to struggle on her own (Smallwood, 1905). These early observations suggest that males recognize receptive females by their passiveness alone. More recent observations on the caprellid Caprella laeviuscula (Caine, 1991) and the isopods Cymodetta gambosa (Bowman and Ktihne, 1974) and Idotea neglecta (Sheader, 1977a) support this interpretation of pair recognition based entirely on physical cues. 6.1.1.

Chemical recognition

Despite several decades of controversy (Dunham and Hurshman, 1991) and the inability to isolate and characterize the chemicals involved, accumulating evidence now strongly suggests chemical cues acting at a distance, or upon contact, facilitate pairing. Increased activity or directional orientation in males when in close proximity of females nearing their ovigerous molt has been reported in gammarids (Williamson, 1951; Kinne, 1953; Ducruet, 1973; Borowsky, 1984b; 1985), mysids (Nouvel, 1940; Clutter and Theilacker, 1971; Wittmann, 1982) and tanaids (Johnson and Attramadal, 1982). Lyes (1979) showed that female Gammarus duebeni release a pheromone in their urine that is received by the male second antennae. Identification of the specific antennal structures responsible for pheromone reception has not been achieved in this case or for any peracarid. Dahl et al. (1970) showed that ripe female Gammarus duebeni treated with tritium attracted a congregation of males who had quantities of radio-label on the calceoli of their second antennae. More

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recent investigations failed to detect any innervation to calceoli (Lincoln, 1985b; Godfrey et al., 1988; Read and Williams, 1990) thus casting doubt on a chemosensory role for these structures (Moore and Wong, 1996b). Other structures on the antennae including male-specific sensory aesthetascs on some isopods (Heiman, 1984) and sensory sensilla on male mysids (Johanssen and Hallberg, 1992; Johanssen et al., 1996) may be used to detect female pheromones, but experimental confirmation is needed. Stanhope et al. (1992) discovered that female Eogammarus confervicolus produce a pheromone only recognized by males of the same race, and their breeding experiments confirmed that race recognition has a genetic component. The pheromones seem to be small, polar molecules, but they have not been fully characterized. In this case, pheromones acting as pre-zygotic isolating mechanisms may have important implications for speciation in Eogammarus and perhaps in other peracaridans as well. Once the female has been located, she is usually grasped by the male and then examined by repeated contact or palpation with antennae and other appendages (Heinze, 1932; Dunham et al., 1986). It seems as if some specific stimulus is required before the next stages of mating can commence (Dick and Elwood, 1992; Borowsky, 1984a, b). After each examination, the female may be released, held in precopula, or immediately mated if she has already molted. The stimulus involved may be a "contact pheromone" (Michel, 1986; Borowsky and Borowsky, 1987) where the chemical is on the surface of the female rather than in solution. Such species-specific chemicals have long been associated with settling barnacle cyprids where they are apparently recognized by physical means involving special sensory setae (Crisp and Meadows, 1962, 1963). In peracaridans, the specific cues and the mechanism of their reception have not been identified, although a number of specialized sensory structures appear on the antennae of mature males. Dunham (1986) found that the male's decision to retain or release a female can be influenced by the contents of her marsupium, but whether this evaluation involves chemical cues or some other means of recognition remains uninvestigated. Clearly, chemical cues are involved in pairing, but the nature of the chemicals themselves and the precise mode of their reception need further exploration. Williamson's observations (1951) illustrate the subtle interplay of both behavioral and chemical cues at distinct periods in the mating process. Female Orchestia gammarella, if unmated, remain attractive and capable of successful mating for several days after the reproductive molt. These females are usually passive when contacted by males before mating. Once mated, females remain attractive to males for only about an hour after first copulation but resist violently if approached by males during this postcoital period. Thus the act of copulation promotes an immediate behavioral

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

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Figure 8 Pairing and mating in Pericarida. A. The amphipod Gammarus duebeni in amplexus prior to mating (B). C. Praunusflexuosus (Mysidacea) pairing (C) and mating (D) in the water column. A pair of cumaceans, Lamprops fasciata in one of several different riding positions reported for this group (E). E the tanaidaceans (Heterotanais oerstedi) mating in their tube. G. Transverse section of the isopod Jaera albifrons during copulation showing the position of the male's

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change to prevent further matings until chemical signals can be switched. Again, attempts to identify the specific chemicals involved have been inconclusive (Hartnoll and Smith, 1980). Modem molecular techniques might yield real insights into the mechanisms responsible for this behavior in Crustacea and the nature of its control. 6.1.2.

Precopulatory pairing

Pairing may involve lengthy periods where males hold and often guard females prior to mating. Other peracarids pair and mate during brief nocturnal liaisons, and still others mate in tubes. These different modes of pairing seem related to habitat and lifestyle, since each is seen in a number of peracarid groups. 6.1.2.1. Protracted pairing and mate guarding Lengthy precopulatory pairing, or precopula, is seen in some isopods and is common in benthic gammarid and caprellid amphipods, and in cumaceans. Here we outline a general example of precopulatory pairing as exhibited by gammarid amphipods from shallow subtidal or intertidal habitats. The reproductive molt is preceded by a period of precopulatory pairing of several days to several weeks during which the male assumes a "riding" or "carrying" position superior to the female (Figure 8A and 8E). The male maintains a firm hold on the female by fastening his second gnathopods to the exposed margins of the female's anterior thoracic segments. This grip, often facilitated by special notches in the female's coxal plates, may be so tenacious that the pair cannot be separated without injury (SmaUwood, 1905; Blegvad, 1922). While in "precopula" the paired animals may still have some ambulatory or swimming capability, generally provided by the larger male. Actually, different gammarid families show an amazing variety of precopulatory positions (figured in Bousfield and Shih, 1994). Similar descriptions of precopula are available for caprellids (Lewbel, 1978; Caine, 1991; Aoki, 1996), isopods (Kjennerud, 1952; Moreira, 1973b; Jormalainen and Merilaita, 1993), and cumaceans (Sars, 1900; Foxon, 1936; Fage, 1951; Gnewuch and Croker, 1973; Duncan, 1983). Mate guarding during precopula is particularly widespread among gammarid and capreUid amphipods where sexual pairing is often a time of

copulatory operculum (op) inserted into the female's oviduct (od). The sperm storage receptacle (sr) lies between the oviduct and the ovary (ov). (A and B after Kinne, 1954b; C and D after Nouvel, 1937; E after Sars, 1900; F after BtickleRamfrez, 1965; G from Forsman, 1944.)

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

intense competition between males. Conlan (1989, 1991) attributes this behavior to high population densities typical of these "colonial" living species, the short period of receptivity in females, the polygynous habits of males, and to asynchronous and continuous reproduction. Larger males frequently dislodge smaller rivals in precopula or evict smaller males from tubes shared with reproductive females This may be a powerful selective force favoring larger males or males with larger gnathopods that are found only in mate-guarding groups. Jassa marmorata males attempt to remove other males from receptive females' tubes or proximity by engaging in contests or displays. The cruising male J. marmorata approach rivals with their huge second gnathopods spread wide (Clark, 1997). Interestingly, these displays seldom involve direct contact. In contrast, caprellids often engage in violent contests that may result in death. Caprella gorgonia hold females with their fifth pereopods, which frees their greatly enlarged second gnathopods, armed with a poison-bearing tooth, for serious conflict (Caine, 1979). Precopula as described above, while common, is not yet reported in several specific groups. Tube-dwelling gammarids (Forsman, 1956; Moore, 1981a), supralittoral beach hoppers (Williamson, 1951; Sameoto, 1969a) and most polar species examined thus far (Bregazzi, 1972) typically lack precopula. In addition, lengthy precopulatory pairing has not been reported for mysids, for hyperiid amphipods, or for many gammarids that mate in the water column (Bousfield, 1973). These exceptions suggest that lengthy pairing may well be disadvantageous under certain circumstances. The amplexed pair faces potential difficulties in locomotion: swimming, crawling and burying are all impaired. In most circumstances, this would increase vulnerability to predation. In fact, Strong (1973) documented specific differences in both the length of precopula and its frequency in the amphipod Hyalella azteca correlated with levels of fish predation. Increased risk of predation would also apply to those tubicolous species where the tubes do not accommodate the amplexed pair. The risk of predation is probably the foremost disadvantage of precopula, but an additional handicap is that one or both of the pair may forego feeding for the duration of precopula (isopods: Johnson, 1976; Sheader, 1977a; Shuster, 1991a, b; Wong and Moore, 1996; cumaceans: Duncan, 1983). This would affect growth (Robinson and Doyle, 1985) and possibly future reproduction. Precopula seems most prevalent in situations where these potential disadvantages are minimized. 6.1.2.2. Cruising and non-cruising males A number of amphipods and tanaids build individual tubes where they reside for their entire lives. An alternative form of precopulatory pairing is typical of these tube-dwelling species. Only the adult males leave their tubes and then only to search for

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reproductive females. The male joins the female in her tube until she molts. Copulation occurs, and the male then departs in search of other females. Although these "cruising males" (Borowsky, 1983a) are at considerable risk while in the water column, pairing and mating, as well as brooding, take place in the comparative safety of the tube. This pattern has been described for gammarids in the genera Microdeutopus (Borowsky, 1980b), Lembos (Shillaker and Moore, 1987b), Corophium (Nair and Anger, 1979), Jassa and Ampithoe (Borowsky, 1983b), and in the tanaid genera Tanais (Johnson and Attramadal, 1982; Borowsky, 1983b) and Heterotanais (Bfickle-Ramirez, 1965). In some tanaids these "swimming males" may represent a terminal stage specially modified for swimming and mate location. Most peracaridans pair only prior to mating and are separate during non-reproductive periods. In contrast, Myers (1971) reports a more permanent pairing in the amphipod. Microdeutopus gryUotalpa, where mated pairs share the same tube over a period of months with up to 11 successive mating and brooding periods. Similarly the wood-boring isopod Lirnnoria tripunctata and the kelp-boring gammarid Peramphithoe stypotrupetes usually have one male and one female per burrow for extended periods which may include multiple broods (Menzies, 1954; Conlan and Chess, 1992, respectively). In order to compare this mating strategy with the short-term pairings typical of tubicolous peracarids it would help to know (1) just how and at what stage the initial pairing takes place and (2) what happens if the male of the pair is removed from the burrow. 6.1.2.3. Planktonic pairing Planktonic mating seems the norm for mysids and is well documented. Mysids pair and mate during brief nocturnal meetings, without the lengthy preliminaries (Nouvel, 1937; Nair, 1939; Wittmann, 1982) often associated with marked breeding aggregations (Samter and Weltner, 1904; Mauchline, 1971e). Nouvel (1937) observed that Praunus flexuosus males were only attracted to females within 12 hours of their molt. Since male P. flexuosus were also attracted to, and attempted to copulate with, recently mated males, he suggested that a chemical attractant was passed from female to male during mating. Clutter (1969) reported that male Metamysidopsis elongata began a "searching behavior" when within 5 cm of a recently molted female. Apparently the attractant was species-specific, because males responded only to females of the same species when two species were breeding simultaneously in the same tank. For the more benthic peracaridan groups, excursions into the plankton are common (Tully and O'C6idigh, 1987) and are frequently associated with reproductive activities. A number of benthic isopods (Baan and

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

Holthius, 1969; Champalbert and Macquart-Moulin, 1970; Jones, 1970), amphipods (Williams, 1972), and cumaceans (Fage, 1923; Fish, 1925; Foxon, 1936; Zimmer, 1941) are found in the surface plankton at night. Corophium lacustre and other gammarids peak in the North Carolina plankton only on the flood of spring tides (Williams, 1972). Nocturnal swarms of the cumaceans Mancocuma stellifera (Gnewuch and Croker, 1973) and Dimorphostylis asiatica (Akiyama and Yoshida, 1990) are also strongly correlated with tidal or lunar cycles, and this may be true of other groups as well. Highly synchronized emergence would maximize population density and thus the chances of finding mates and minimize time spent in the plankton (Borowsky, 1983b). Macquart-Moulin provides experimental studies (1972, 1973, 1980) on the exogenous and endogenous control of these swimming rhythms. Males are often more common in the plankton than females. Aesthetascs and other specialized sensory adaptations are found only in the terminal planktonic stage of many male gammarids (Conlan, 1991; Bousfield and Shih, 1994) and isopods (Kensley, 1982) commonly found in the plankton. This suggests that these males are in the plankton primarily to search for females. According to Zimmer (1941), the adult males of Diastylis rathkei swim in the surface plankton awaiting the arrival of females who only leave the substratum when ripe. The females are paired soon after reaching the swarm of males. Since the adult females are rarely caught in the surface plankton (Zimmer, 1941; Akiyama and Yoshida, 1990) mating probably takes place at or near the substratum. While Hager and Coker (1979) observed Amphiporeia virginica pairing freely in the water, the case for gammarids actual mating in the plankton as suggested by Watkin (1941) and Mills (1967) is largely circumstantial. After planktonic pairing, mating may take place on the bottom. Alternatively, some of the male gammarids in the plankton may be the "cruising males" (Borowsky, 1980b, 1983b) of tubicolous species who must emerge from their tubes to find new mates. Here, both pairing and mating may actually take place in or near the female's tube rather than in the plankton where both the females and the mating pair would seem more at risk (Shillaker and Moore, 1987b). 6.1.3.

Complex mating systems

As a rule, peracarid mating involves pairings of a single male with one female as outlined above. Some Sphaeroma rugicauda broods show evidence of shared parentage produced by multiple matings involving two or more males (Heath et al., 1990), but such multiple matings are seldom observed in free-living marine species outside of the janiroidean isopods.

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Further application of molecular techniques may reveal more widespread polyandry. Presumably, these multiple matings result from separate encounters with individual males. More recently, complex social structures and mating systems among isopods have emerged. Upton (1987) noted harem formation in the saltmarsh isopod Paragnathia formica. However, Shuster's account (1987) of the mating habits of Paracerceis sculpta in the oscula of sponges in the intertidal zone of the Gulf of California details the most involved and unusual mating system known in peracarids - or any crustaceans. The sponges serve only as a reproductive habitat. Mature females are attracted to and enter spongocoels already occupied by elaborate "alpha" males. A single spongocoel may contain a single alpha male and a harem of 1 to 11 reproductive females plus beta and gamma males. These latter are sexually mature and distinctive male morphs. The three male morphs do not represent stages in a developmental sequence and are seemingly irreversible. All three can sire viable offspring.

6.2.

Copulation and fertilization

Typically, males transfer sperm to the marsupium, and the act of mating results in ovulation. Fertilization occurs as the eggs pass through the oviducts or shortly after they are deposited in the marsupium. Different taxonomic groupings display individual variations on this basic theme. Furthermore, a few genera exhibit specific modifications for sperm storage and internal fertilization. 6.2.1.

Sperm transfer into the marsupium

Males ordinarily deposit their sperm or spermatophores in the marsupium close to, or into, the openings of the oviducts. In species having copulatory appendages, these are inserted into the marsupium in a series of convulsive abdominal jerks over a span of only a few seconds. This process may be repeated several times at intervals of a few minutes. Each group of peracarids has its own typical form of positioning while mating as shown for amphipods and mysids in Figures 8B and 8D. Most tanaid and cumacean males are equipped with short genital cones rather than well developed copulatory appendages (Gardiner, 1975; Duncan, 1983) and thus often deposit their sperm near the females' genital openings or ovisacs before the marsupium is fully formed (Johnson and Attramadal, 1982; Duncan, 1983). Btickle-Ramirez (1965) describes Heterotanais oerstedi females holding their o6stegites open as sperm are

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

deposited in the marsupium (Figure 8E), a singular observation for Peracarida. Also unusual is the use of uropods or modified pereopods to transfer sperm as seen in the hyperiid Parathemisto gaudichaudi (Sheader, 1977b) and the isopod Cymodetta gambosa (Bowman and K~ihne, 1974) respectively. Isopods characteristically molt the posterior half of the cuticle before the anterior half; and males usually copulate with females in the half-molted condition before the anterior part of the marsupium is fully formed (Forsman, 1956; Kjennerud, 1952). For more detailed descriptions see for gammarids: Della Valle (1893), Sexton and Matthews (1913), Blegvad (1922), Sexton (1928), Heinze (1932), Williamson (1951), Kinne (1953), Nagata (1966), Lim and Williams (1970) and Moore (1981a); for hyperiids: Sheader (1977b); for caprellids: Lewbel (1978) and Caine (1991); for isopods: Kjennerud (1952), Bowman and Ktihne (1974) and Wilson (1991); for mysids: Nair (1939), Nouvel (1937, 1940) and Labat (1954); for cumaceans: Dohrn (1869), Sars (1900) and Forsman (1938). 6.2.2.

Sperm storage

A markedly different pattern of mating and reproduction is found in the asellote isopods. Mating in this group has been most thoroughly examined in the genus Jaera, which shows notable differences between closely related species. McMurrich (1895) first noted that female Jaera marina have sperm storage receptacles, but their importance in the animal's reproduction was not fully revealed for almost 50 years. Forsman (1944) showed that Jaera albifrons first mate well before the female reaches sexual maturity. Females usually mate and thus refill their sperm receptacles at each ovigerous molt thereafter. However, once mated as juveniles, isolated females can use the sperm stored in their receptacles to fertilize successive broods. Such sperm storage is common in terrestrial isopods (Vandel, 1937) but has yet to be reported for other marine isopod groups or for any other peracaridan. In the Jaera "albifrons" group mating also differs from the normal isopod pattern. According to Forsman (1944), the male faces the female's posterior during the brief precopulatory pairing. While copulating, the male moves his abdomen slightly to one side and applies the pleotelson to the region of the female's copulatory opening (Figure 8F). Sperm are transferred from penes to sperm grooves on the second pleopods which lead to stylets on each outer margin (Veuille, 1978; Wilson, 1986a; Poore and Just, 1990). It is not certain whether or not the stylet projects into the genital aperture (see Jones and Fordy, 1971, for anatomical details). The male fills the left sperm receptacle first, then the right. Fertilization apparently occurs during ovulation in the oviduct near its junction with the sperm receptacle and not in the ovary itself (McMurrich, 1895;

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Forsman, 1944). Eggs are laid 2-10 hours after the female's molt. Veuille (1980) suggests that the unusual reproductive biology of the Atlantic Jaera species has resulted in a pattern of sexual dimorphism where females are significantly larger than males, whereas the pattern is reversed in the Mediterranean species J. italica and J. nordani. Reproductive organs and seminal receptacles in deep-sea haploniscids (Lincoln, 1985a) and other deep-water Asellota (Wilson, 1986a, b) make internal fertilization likely, but little is yet known about their mating habits. Another peculiarity of the superfamily Janiroidea is that a secondary opening to the female's reproductive system and to the spermatheca, the "cuticular organ" opens on the dorsal surface of most species (Wilson, 1986b; see also section 3 on reproductive anatomy). This may allow mating regardless of the female's molt status which would be a benefit to deep-sea species with long intermolt periods and low population densities. Franke (1993) describes yet another reproductive aberration in the Janiroidea involving both sperm storage and continued female receptivity. The commensal isopod Jaera hopeana females first mate just days after leaving the marsupium, long before sexual maturity. Adult males attempt to amplex with any manca I juveniles and are apparently unable to distinguish between males and females at this stage. Males carry the much smaller mancas ventrally using their fourth pereopods to clasp them while waiting for the female's first post-marsupial molt. Newly molted manca II females mate and store sperm for future use. Female J. hopeana are continuously receptive to mating thereafter without regard to their reproductive status or molt stage, but these subsequent matings occur rapidly without the precopulatory pairing typical of juvenile matings. These diminutive isopods (2-2.5 mm) live ectocommensally on the ventral surface of another isopod, Sphaeroma serratum, and it is possible that these unusual breeding habits are related to their symbiotic lifestyle as parasitic groups are well known to exhibit a number of reproductive anomalies. At least some male aseUotes from the deep sea also sequester manca stage females (Hessler and Str6mberg, 1989), and information on mating habits from this fauna would be most welcome. The only other report of sperm storage and internal fertilization in marine peracaridans is in Excirolana chiltoni where copulation occurs prior to the ovigerous molt (Klapow, 1970). Here the sperm are stored briefly in enlargements of the oviducts. This arrangement seems a necessary adaptation associated with internal brooding where the eggs are never deposited in the rudimentary marsupium. Similar copulatory adaptations may yet be found in those sphaeromatid isopods with small or missing o6stegites (Table 1). Internal fertilization is also likely for members of the order Thermosbaenacea (e.g. Halosbaena acanthura) since they lack a ventral marsupium. Internal fertilization and sperm storage in

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

seminal receptacles have been confirmed for Thermosbaena mirabilis from thermal haline springs (Barker, 1962), but we know nothing of mating in marine species. 6.2.3. Ovulation and fertilization In cases of external fertilization where sperm storage is not involved, ovulation follows soon after the last copulation, and mating itself seems to stimulate ovulation. In the absence of males, female isopods (Borowsky, 1987) and gammarids (Williamson, 1951) can delay ovulation for up to several days after molting. If a male appears, ovulation follows promptly after mating. If no male appears, the eggs are either resorbed by the ovary (Sexton, 1924; Forsman, 1956) or deposited in the marsupium where they fail to develop and are lost within a few days (Nouvel, 1940; Wittmann, 1981a). Williamson (1951) reports the only major departure from this sequence. He observed that the semi-terrestrial beach hopper Talitrus saltator ovulated 4 days after the ovigerous molt regardless of the time of mating which could occur at any time over the 4 days. If these observations are confirmed, several questions arise. How are the sperm stored so that they remain viable, and where does fertilization occur? Amphipods and mysids deposit eggs from each ovary into the brood pouch in a gelatinous matrix (Moore, 1981a), which is itself enclosed briefly in a membranous envelope secreted by glands associated with the ovaries (Della Valle, 1893; Le Roux-Legueux, 1928; Sheader and Chia, 1970; Moore, 1981a). Kinne (1955) suggested that the envelopes trap sperm in the marsupium and prevent them from being washed away before fertilization. The envelopes may also keep the brood intact in the marsupium until the newly formed oOstegites are in place (Sheader and Chia, 1970). Such structures have been described in gammarids (Sheader and Chia, 1970), hyperiids (Sheader, 1977b), caprellids (Lewbel, 1978) and mysids (Kinne, 1955; Wittmann, 1981a) and may well be more widespread within these groups but overlooked due to their delicate and transitory nature. Existence of these marsupial envelopes in other peracarid groups is unknown. The more robust oOstegites common in those orders may make egg envelopes unnecessary or obscure their presence. 7.

DEVELOPMENT

The embryology of Peracarida follows the general crustacean pattern of superficial cleavage, gastrulation by ingression and epiboly and teloblastic formation of the post-naupliar region. The peculiar feature of peraearidan embryology is that the young are brooded within the marsupium

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

throughout the period corresponding to larval development in other Crustacea and are released as miniature adults. For this reason, development is more or less direct, with greatly modified larval stages.

7.1. Cleavage In all peracaridan orders except the amphipods, cleavage follows a superficial pattern in which the nuclei divide without an accompanying cytoplasmic division. The nuclei remain in contact via strands of cytoplasm (Richardson, 1904; Scholl, 1963; StrOmberg, 1972) and, as further divisions occur, migrate to the surface of the embryo, which they reach as early as the 8-cell stage in some isopods (Nair, 1956) and tanaids (SchoU, 1963) or as late as the 128-cell stage in a mysid (Nair, 1939). Nuclear emergence at the 16 or 32-cell stage is common (McMurrich, 1895; Gerstaecker and Ortmann, 1901; Korschelt and Heider, 1902; Manton, 1928; Str6mberg, 1965, 1972). Reports of discoidal cleavage in isopods (reviewed by McMurrich, 1895, and Hewitt, 1907), mysids and cumaceans (reviewed by Korschelt and Heider, 1902) are now known to be erroneous. These reports may have arisen because in some species the nuclei emerge at one pole of the egg and, as nuclear division proceeds, migrate to the opposite pole (Nair, 1956). Division of the cytoplasm, derived from the formative yolk plus the cytoplasm that surrounds each nucleus, usually follows shortly after the nuclei reach the surface. The yolk-laden central part of the egg does not divide. Cleavage thus results in a central undivided yolk mass surrounded by a cellular blastoderm. This blastoderm often becomes thickened ventrally into a germ disc as a result of increased cell division (Richardson, 1904; L~inge, 1958; SehoU, 1963; Str6mberg, 1967) or cell migration (Nusbaum, 1891; Nair, 1939; Kajishima, 1952). The germ disc is the future site of gastrulation and differentiation of the embryo. In cleaving amphipod eggs the entire egg divides, but the result is a similar centrolecithal blastula. After four or five divisions have occurred, the nuclei and cytoplasm migrate to the surface of their respective blastomeres, leaving the yolk in the center. The blastomeres then undergo a cytoplasmic division parallel to the surface of the embryo, cutting off the nutritive yolk from the nucleus and cytoplasm. Plasma membranes separating the central parts of the blastomeres then disintegrate, leaving a ring of cells around a central undivided yolk mass (Rappaport, 1960). This type of cleavage is believed by Weygoldt (1958) to be secondary to amphipods, because superficial cleavage is universal in the Malacostraca, and the amphipods are unique among Peracarida in having a holoblastic cleavage.

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7.2. Fate mapping, gastrulation and germ layer formation Fate mapping is complicated by the internal position of the nuclei and, except in amphipods, the late division of the cytoplasm. In the isopods, a group of four cells marks the future site of the blastopore. These cells, called vitellophages, remain syncytial after cell boundaries elsewhere are well defined in Jaera marina (McMurrich, 1895). The vitellophages are surrounded by 12 mesentodermal cells, with 16 ectodermal cells scattered over the remainder of the embryo's surface. Because the viteUophages are large compared with the surrounding cells, they provide a landmark whereby a fate map can be made of the surface of the blastodisc, particularly in mysids (Manton, 1928; Nair, 1939). Fate mapping in amphipods is often possible because early cleavages are unequal, producing large macromeres and smaller micromeres. In some species the germ layer anlage, or blastodisc, arises from both macromeres and micromeres (Gerstaecker and Ortmann, 1901), while in other species it arises from macromeres alone (Rappaport, 1960). Gastrulation begins with the ingression of individual cells at the blastopore to create a plug of cells inside (Manton, 1928; Nair, 1939, 1956; Weygoldt, 1960; Str/~mberg, 1967). An actual blastopore opening seldom exists, although its location may be indicated by a depression in the surface of the blastodisc (Manton, 1928; Kajishima, 1952; Str6mberg, 1972). Ingression also occurs in other regions of the blastodisc in isopods (Nusbaum, 1891; L/inge, 1958; Weygoldt, 1958). Reports of delamination of cell layers are old and probably incorrect. The first cells to enter the blastopore are the vitellophages. These cells migrate into the nutritive yolk and begin to absorb it (Liinge, 1958; Weygoldt, 1960; Scholl, 1963; Str6mberg, 1965, 1967, 1972). They are followed into the embryo's interior by cells of the genital rudiment and the mesentoderm (Manton, 1928). Some authors have been able to identify separate endoderm and mesoderm prior to ingression (Langenbeck, 1898; Manton, 1928; Zimmer, 1941), while others describe the mesentoderm as undifferentiated until after ingression has taken place (McMurrich, 1895; Weygoldt, 1958). Gastrulation is completed by an epibolic process whereby a row of cells situated just anterior to the blastopore grows over the blastopore region, ending ingression (L~nge, 1958; Weygoldt, 1960; Scholl, 1963; Str6mberg, 1967; Dohle, 1970). Confusion over the identity of vitellophages and of the separation of endo- and mesoderm is evident. The mesentoderm apparently proliferates under the blastopore, forming a plug of cells which extends into the yolk (Nair, 1939; Weygoldt, 1958, 1960). The endoderm and mesoderm then relocate so that mesoderm is lateral (Nusbaum, 1891; Cussans, 1904) or anterior to endoderm (Hewitt, 1907). The endoderm is identified by most

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

authors as a non-epithelial layer of cells which spread out on the surface of the yolk and eventually form the digestive glands of the embryo (L/inge, 1958). Reports that the endoderm sinks into the yolk as separate cells and absorbs it apparently refer to the vitellophages (Uljanin, 1881; Gerstaecker and Ortmann, 1901; Grschebin, 1910; Zimmer, 1941).

7.3. Differentiation of mesoderm

Mesoderm has three sources. Preantennular mesoderm derives from a small number of cells originating from the head ectoderm that ingress separately from the mesentoderm anterior to the blastopore (Manton, 1928; Nair, 1939, 1956; Weygoldt, 1958, 1960; Petriconi, 1968; Strtimberg, 1972). Preantennular mesoderm is absent in tanaids (SchoU, 1963) but contributes to the mesoderm of the stomadeum in other groups. The mesoderm of the first three segments, or naupliar mesoderm, forms from mesentoderm cells that migrate forward from the blastopore on either side of the germ area, forming a horseshoe-shaped thickening under the ectoderm. The paired anterior ends develop into the cephalic lobes or presumptive eyes. Behind the cephalic lobes the primordia of the three naupliar appendages appear as paired thickenings of the lateral mesodermal bands, representing the future head region of the adult. This region corresponds to the nauplius larva of those Crustacea that have a free-living naupliar stage. Mesoderm of all segments posterior to the first three originates from the mesoteloblasts. The origin and fate of cells forming the postnaupliar segments has been studied extensively in mysids by Scholtz (1984), tanaids and cumaceans by Dohle (1972, 1976), amphipods by Scholtz (1990), and isopods by Hahnenkamp (1974) and discussed in relation to other malacostracans by Dohle and Scholtz (1988). Most post-naupliar segments originate from the teloblasts, which are rows of cells that form anterior to the blastopore in most groups and run transversely across the embryo. In cumaceans these cells form behind the blastopore and migrate anteriorly on each side to line up in front of it. The maxillary segments and anterior part of the first thoracic segment in isopods and cumaceans are also non-teloblastic (Dohle, 1976; Dohle and Scholtz, 1988). There are two types of teloblasts, the internally located mesoteloblasts that give rise to the mesoderm, and the superficially located ectoteloblasts that are the source of the ectoderm. Mesoteloblasts are present in all embryonic Peracarida, but ectoteloblasts are absent in amphipods, in which postnaupliar ectoderm originates from cells of the germ disc (Dohle and Scholtz, 1988; Scholtz, 1990). In the other orders, both rows of teloblasts divide mitotically in a precise pattern that is highly predictable for each segment, resulting in rows of cells

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oriented perpendicular to the antero-posterior axis. Although amphipods lack ectoteloblasts, cells from the germ band organize themselves similarly and undergo similar patterns of cell division. In fact, segments can differ substantially in their early patterns of cell division and still achieve the same end result. In general, waves of mitotic divisions begin anteromedially and proceed posteriorly and laterally until the entire postnaupliar region has undergone mitosis. The resulting rows of cells divide several times to create bands four cells wide. In the mesoderm, each band gives rise to the mesoderm of a single segment, but in the ectoderm, the descendants of a single band of teloblasts form the posterior half of one segment plus the anterior half of the next segment. The appendages show a similar pattern of origin, each developing from the posterior part of one teloblast band and the anterior part of the next (Dohle and Scholtz, 1988). Studies using three species of amphipods, Gamrnarus pulex, G. roeselii and Orchestia cavimana (Scholtz et al., 1994), have shown that a gene homologous to the engrailed (en) locus of Drosophila, which is highly conserved in arthropods, is expressed in the anterior rows of cells within each ectoteloblastic band. Expression first occurs in a single row of cells in each segment. When these cells divide their progeny express en, as do cells recruited from the cell row just posterior to the expressing cells. Since these cells are found in the anterior part of the ectoteloblast band, they are in the posterior part of their respective segments, which is the pattern of expression found in other arthropods. The naupliar mesoderm does not undergo segmentation until late, resulting in a very reduced coelomic cavity or none at all (Nair, 1939; Weygoldt, 1958). The metanaupliar region formed from the teloblasts is arranged in definite somites, one pair per segment. Segmental formation and differentiation is similar for the mesoderm of both regions. Each somite divides into a medial, dorso-lateral and ventro-lateral section (Nair, 1939; Str6mberg, 1967). The medial section forms the longitudinal ventral muscles, while the ventro-lateral part forms the muscles of the limb bud (Richardson, 1904; Scholl, 1963; Strtimberg, 1965, 1967). The dorso-lateral section may have a transitory (Manton, 1928; Weygoldt, 1958; Scholl, 1963; Str6mberg, 1967) or irregular coelom (Zimmer, 1941; Weygoldt, 1958).

7.4. Organogenesis During early embryonic stages, several organs, variously called dorsal, dorsomedial, or dorsolateral organs depending on location, appear in the dorsal region (Needham, 1937; Weygoldt, 1960; Str6mberg,

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

1965, 1972). These organs consist of disc-shaped ectodermal thickenings containing cavities communicating with the extraembryonic space (Cussans, 1904; StrSmberg, 1972). Both types of organs exist only during embryonic development, persisting either until loss of the egg membranes (Gerstaecker and Ortmann, 1901; Grschebin, 1910; Lalitha et al., 1989), the postnaupliar molt (Dohrn, 1870), or emergence from the brood pouch (Gambardella et al., 1996). Because they connect to the yolk the dorsolateral organs of isopods and the dorsal organs of mysids have been postulated to function in yolk absorption (Manton, 1928; StrOmberg, 1965). They are secretory and are physically and chronologically connected to the larval cuticle and molting process, suggesting they may also be involved in secretion of the larval cuticle (Manton, 1928; Doyle et al., 1959; Str0mberg, 1967). Meschenmoser (1989) found the dorsal organ of the terrestrial amphipod Orchestia cavimana (Figure 9) to be located between the ectoderm and endoderm. Dorsal organs have a central extracellular region containing electron-dense material and continuous with the periembryonic space. Bottle-shaped cells are arranged in a circle around this material. Their apical plasma membranes have microvilli and canaliculi that greatly increase surface area. The canaliculi contain material similar to that found in the extracellular space. These cells also contain numerous mitochondria and granules composed of calcium, magnesium, phosphate, and chloride. Immediately before hatching the number of granules in the cells decreases, just at the time that the embryo swells to approximately twice its former size. Meanwhile, similar granules in the periembryonic space increase in number. Meschenmoser (1989) suggests that the dorsal organ actively transports ions into the periembryonic space and might play a role in osmoregulation and in molting in terrestrial species. The dorsal organ does not appear to be involved in osmoregulation in marine organisms, and its time of appearance differs among species. However, it is always present before the embryonic molt. Its function(s) are still not well understood and may differ with environment, but its invariable appearance at the time of molting suggests that it plays a role in this process. The gut of peracaridans differentiates primarily from two ectodermal invaginations of the external body wall that push into the body toward each other. The proctodeum is much longer than the stomadeum, extending throughout the entire length of the abdomen and far into the thorax (Zimmer, 1941). It develops into the intestine, while the stomodeum becomes the gastric mill, stomach and esophagus (Goodrich, 1939; Zimmer, 1941). Evaginations of the stomodeum become salivary glands (Nusbaum, 1891). If endoderm contributes to the gut, it is as a short piece of midgut where proctodeum and stomodeum meet (McMur-

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Figure 9 Morphology of the dorsal organ of the amphipod, Orchestia cavirnana, after the embryonic moult. The organ is partially enclosed by the

embryonic envelope (eE) and ectodermal cells (eC). The proximal surface is bounded by a basal lamina (bl) and rests upon the endodermal cells (enC), which contain yolk granules (Y). The organ consists of two layers of cells surrounding a central cone (C) of electron dense extracellular material and capped by a plug (p) consisting of another type of extracellular material. Bottle-shaped ceils form most of the organ and border the central cone. The basal region (bl) of these cells contain calcium granules, while the neck region (neR) has a cup-shaped cavity. An inner layer of central cells (cCe) lacks these features. (After Meschenmoser, 1989.)

rich, 1895; Goodrich, 1939; Nair, 1956; Scholl, 1963; Strtimberg, 1965, 1967, 1972). Most authors agree that two tissues originate from endoderm, the viteUophages and the anlage of the mid-gut caecum. The amoeboid vitellophages migrate into the yolk at gastrulation (Grschebin, 1910; Nair, 1956) and in isopods form a sac that surrounds the yolk and is called the yolk epithelium (Str6mberg, 1967). A similar sac in amphipods forms from yolk cells, which may originate from viteUophages (Manton, 1928). Eventually, the vitellophages and yolk epithelium are resorbed by the midgut and its caecum or disintegrate as the yolk disappears during development (Nusbaum, 1891; Nair, 1939, 1956; Str6mberg, 1965, 1967). McMurrich's suggestion (1895) that they become blood cells is no longer tenable. The midgut caecum is the only endodermal structure of any size that survives embryonic development. The midgut caecum "anlage" and, if one exists, a midgut of non-vitellophage origin, come from the mesentoderm. In amphipod embryos the hepatic caeca have a similar origin (Cussans, 1904; Doyle et al., 1959) and are therefore believed to be homologous to the midgut caecum anlage of other orders. The circulatory system and the inner part of the excretory system

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develop from mesoderm. According to Nair's description (1956), the dorsally located heart forms from tissue strands originating from the segmental mesodermal blocks. They attach to the dorsal body wall to form a haemocoelic space roofed with ectoderm. In Ligia exotica, the heart is originally tubular, with a wall composed of a single layer of spirally orientated muscle cells (Yamagishi and Hirose, 1997). During late embryonic development the heart begins to contract rhythmically. This contractility is myogenic, and there is no localized pacemaker region, as the entire organ has an innate rhythmic contractility, and the cells are electrically coupled. After emergence from the brood pouch, control of the heartbeat is taken over by the cardiac ganglion (Yamagishi and Hirose, 1997). Blood corpuscles originate from cells of segmental mesoderm that spread posteriorly into the thorax between the yolk sac and the ectoderm (Manton, 1928; L~nge, 1958; Weygoldt, 1960). They multiply and invade the intercellular spaces, which become the haemocoels. The primary excretory organ, the maxillary organ, has a dual origin; the duct being ectodermal, while the part containing the nephridia is mesodermal (Needham, 1937). The segmental ganglia of the central nervous system arise as ventral ectodermal thickenings, usually paired and connected to each other via ectodermal bands (Cussans, 1904; Zimmer, 1941; Doyle et al., 1959; Dohle, 1976). Particularly in the cephalic region, fusion of ganglia takes place to form the "brain" as has been described in isopods (McMurrich, 1895; Richardson, 1904; Hewitt, 1907), amphipods (Cussans, 1904; Weygoldt, 1958) and tanaids (Scholl, 1963). The eyes originate as paired ectodermal thickenings of the hypodermis, which become retinas (Korschelt and Heider, 1902; Cussans, 1904; Schatz, 1929). The eyes begin as paired structures. In cumaceans they move nearer to each other as development proceeds and eventually fuse (Zimmer, 1941).

7.5.

External differentiation

The naupliar region begins to differentiate while the embryo is still contained within the fertilization membrane and/or chorion (Figure 10). Anterior segments differentiate first. The naupliar appendages arise as ectodermal tubes projecting from the body which are later invaded by the head mesoderm (Nair, 1939). Before the embryo hatches from the egg membranes all five pairs of head appendages are present, arranged in two parallel rows down the length of the embryo's ventral side, still held close to the embryo by the membrane. Postnaupliar segments appear along with their appendages by teloblastic growth followed by constriction of the intersegmental regions (Gamroth, 1878; Zimmer, 1941; StrSmberg, 1967).

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REPRODUCTION AND DEVELOPMENT IN PERACARIDANS

As further segments differentiate the germ area elongates, curving around most of the egg. In isopods, mysids, cumaceans and tanaids, a deepening cleft, the dorsal furca, appears in the dorsal surface and represents the boundary between thorax and abdomen (Sars, 1900; Gerstaecker and Ortmann, 1901; Grschebin, 1910; Zimmer, 1941; Forsman, 1944; Str6mberg, 1965, 1967, 1972; Holdich, 1968; Jones and Naylor, 1971). The furca deepens until it reaches midway to the ventral surface, dividing the yolk into a large cephalic part and a small caudal part. The embryos thus

A

pr

c

B 'VIII

d

~

5

o

E ~

VIII

ch+v cl

liru liru

L/mnorfa

liru

Figure 10 Embryonic stages of the isopod Limnoria lignorum. Stages A and B are still within the chorion (ch) and vitelline membrane (vm). Stage C has moulted from these membranes, but is still enclosed within the embryonic membrane (em). Stage D is released from the embryonic membrane, freeing the appendages. The position of the dorsal organ (do) is indicated in (B). Roman numerals represent the numbers of thoracic segments, and arabic numerals denote abdominal segments~ (cl, cephalic lobe; liru, liver rudiment; pr, proctodeum, st, stomodeum; ys, yolk sac. (E) Comparison of an embryo of the amphipod Parathemisto gaudichaudi at the same stage as (B) demonstrates the dorsal curvature of isopod embryos and the ventral curvature of amphipods. (A-D modified after Str6mberg, 1967; E modified after Kane, 1963.)

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WILLIAM S. JOHNSON, MARGARET STEVENSAND LES WATLING

develop a dorsal curvature, and appendages develop on the outer surface of the embryo. In the amphipod embryo a ventral caudal furca forms instead, and the embryo has a ventral curvature (Gamroth, 1878; Gerstaecker and Ortmann, 1901; Steele and Steele, 1969; Fish, 1975).

7.6. Larval stages and molting Loss of the fertilization membrane/chorion is considered analogous to hatching in species with a free-swimming nauplius according to Manton (1928), Nair (1939), Kane (1963) and Green (1970). Unfortunately, this term has also been used to refer to later molts occurring within the brood pouch (Grschebin, 1910; Berrill, 1969; Sheader and Chia, 1970) or even to release from the brood pouch (Forsman, 1944). We will restrict the use of this term to loss of the egg membranes. Although internal development of peracaridan embryos is continuous, only at molting can the external body shape change. Three molts occur while the embryos are still in the brood pouch in isopods (Scmme, 1941; Needham, 1942; Naylor, 1955a; Str6mberg, 1967; Holdich, 1968; S. Fish, 1970; Jones and Naylor, 1971), amphipods (Kane, 1963; Gra£ 1972), and the mysid Mysidium columbiae (Davis, 1966). The three molts include hatching from the egg membranes, a postnaupliar molt, and a larval ecdysis just prior to release from the brood pouch. Only two molts are described for embryos of other species of mysids (Manton, 1928; Nair, 1939; Berrill, 1969). However, Nair (1939) describes a molt occurring just after release which may be the equivalent of the pre-manca molt of the other orders. Four molts are described for cumacean development (Zimmer, 1941), the extra one being a postnaupliar molt. In Gammarus pulex, embryonic development is said to occur entirely within the egg membrane (Weygoldt, 1960). Similarly, hatching from the egg membrane and embryonic cuticle is said to occur simultaneously in Bathyporeia pilosa and B. pelagica (Fish, 1975). Hatching takes place via rapid uptake of water by the yolk, causing the embryo to swell (Manton, 1928, Nair, 1939; Davis, 1966; Str6mberg, 1967). The membrane splits, and the embryo emerges already encased in the naupliar or embryonic cuticle. This cuticle is believed to be formed by the blastoderm cells (Dohrn, 1870; Gra£ 1972) or by the dorsal organ of isopods (Gerstaecker and Ortmann, 1901). In the newly hatched embryo, the first three pairs of appendages are separately encased in the naupliar cuticle and can project away from the body (Sars, 1900; Manton, 1928; Jepsen, 1965; StrOmberg, 1967). Other appendages are less differentiated and held against the body wall by the naupliar exoskeleton. Isopods have five pairs of cephalic and six pairs of thoracic appendages

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at this stage, the anterior being developmentally more advanced than the more posteriorly located ones (Hewitt, 1907; SOmme, 1941). All cephalic and thoracic appendages and four pairs of abdominal appendages are present in mysid embryos at this stage (Nair, 1939). Appendages continue to develop during the naupliar intermolt, lengthening and, in the case of the anterior pairs, undergoing segmentation via constriction of the joint regions (Str6mberg, 1967). Also the naupliar cuticle stretches to allow the embryo to elongate and straighten, although a strong dorsal curvature still exists (Kjennerud, 1952; Davis, 1966; Str6mberg, 1967; Holdich, 1968). The end of the naupliar stage is signaled by loss of the embryonic cuticle. Molting requires muscular body movements (Somme, 1941; Fish, 1975) and/or limb movements (Grschebin, 1910; Fish, 1975), including twisting of the body (Strtimberg, 1967) or wriggling (Fish, 1970). Spines also help to tear the membranes (Fish, 1975). The molt frees the rest of the appendages and allows the embryo to straighten further. At this stage it becomes possible to distinguish between embryos of the different orders. Isopod embryos straighten as the larval membrane stretches (Forsman, 1944). The head, very large in proportion to the rest of the body, becomes relatively smaller as yolk is absorbed (Needham, 1937). The eyes are fully pigmented, and the heart can be seen beating through the larval cuticle (Forsman, 1944; Holdich, 1968). By the end of the pre-manca stage the yolk has been totally resorbed (Forsman, 1944). Based on early (and the only) detailed descriptions (Gerstaecker and Ortmann, 1901; Korschelt and Heider, 1902), tanaid development seems similar to that of isopods. As in isopods and tanaids, mysids (Nair, 1939) and cumaceans display strong dorsal curvature up to the postnaupliar molt, but cumacean larvae eventually turn and curve ventrally instead (Sars, 1900; Zimmer, 1941). The unsegmented thorax and differentiation of a lateral carapace fold in the region of the maxillae (referred to as a branchiostegal fold; see Watling, 1999 for details) distinguish cumaceans from isopods at this stage (Zimmer, 1941). In contrast, amphipod larvae display ventral curvature throughout development, but it becomes less pronounced in later stages (Kane, 1963). The post-naupliar molt in isopods (Hewitt, 1907; Kjennerud, 1952; Nair, 1956; Str6mberg, 1967), tanaids (Gerstaecker and Ortmann, 1901; Korschelt and Heider, 1902), and cumaceans (Zimmer, 1941) results in a "manca", a miniature adult except for the missing seventh pair of thoracic appendages. In contrast, amphipods (Gamroth, 1878; Cussans, 1904; Weygoldt, 1958), spelaeogriphaceans (Watling, unpublished observations), and mysids (Kukenthal and Krumbach, 1927) are released from the embryonic cuticle and from the brood pouch with a full complement of appendages and thus lack a manca stage.

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

THE PERACARIDAN PATTERN OF MARSUPIAL BROODING

Most marine invertebrates, including most crustaceans, liberate their young as larvae with subsequent development taking place in the plankton. Peracaridans are an exception, the only large crustacean group where brooding is the rule. Many potential advantages supposedly favor brooding. The young receive a measure of protection from their mother, and they are liberated at an advanced stage that is presumably less vulnerable to predation and perhaps better able to exploit food sources. However, the trade-offs are significant: brooding requires a huge energetic investment per offspring at the expense of overall fecundity. Furthermore, the time spent brooding limits the number of potential broods per season for iteroparous species. Most young remain in the vicinity of their parents which would both restrict gene flow and encourage competition between adults and juveniles. Clearly, the advantages must have offset these liabilities. Despite rampant speculation, there is still no satisfactory explanation regarding the specific selective pressures that led to brooding in this group - or whether brooding arose independently in the different peracaridan lines (Watling, 1999). Although there are notable exceptions, a basic characteristic of the Peracarida is development of the young within a ventral brood pouch or marsupium. Several pairs of oOstegites - flattened, overlapping extensions of the coxae - form this external incubatory chamber. Large, yolky eggs are deposited into the marsupium through openings on the sixth thoracic segment. Since the bulky eggs only pass through the small oopores when the cuticle is soft (Della Valle, 1893; Blegvad, 1922; Forsman, 1938; Barnard, 1969), egg deposition occurs during or shortly after the ovigerous molt. The brood develops in the space between the ventral thoracic cuticle and the overlapping oOstegites with no maternal nutrition other than the yolk contained in the egg, although advanced young may feed while still in the mother's brood pouch. Young depart the female's marsupium as fully developed juveniles (gammarid amphipods) or as mancas which closely resemble the adults but lack the last pair of thoracic appendages. Brooding, as described above, is typical of all orders of free-living marine Peracarida except thermosbaenaceans, but each group has its own peculiar marsupial structure and mode of brooding (Figures 11 and 12). Thermosbaenaceans brood their young in a dorsal brood chamber formed from a posterior expansion of the carapace rather than a ventral marsupium. Barker (1962) provides particulars of brooding in Therrnosbaena from inland thermal springs, but details of reproduction in euhaline subterranean forms are not yet available, although Stock (1976) describes females with posteriorly expanded carapaces.

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8.1. 06stegite and marsupial structure The o6stegites are usually associated with the thoracic walking legs (pereopods), but small o(istegites form at the base of the maxillipeds 2 and 3 in Cumacea and on the maxiUipeds of some isopods. The number and arrangement of the o6stegites is surprisingly variable in isopods, tanaids and mysids (Table 1) and may reflect taxonomic divergence among separate evolutionary lines. Watling (1999) showed that there were at least two modes of formation of oOstegites: in a small bag or pouch attached to the inside of the coxa (as in amphipods); or as a sheet of cells that proliferates under the sternites, becoming a free brood plate when the female molts (as in cumaceans and some isopods). As a result, he questioned the assumption that all o6stegites were homologous. The o~stegites themselves consist of two outer epidermal layers connected by cytoplasmic bridges and tonofibrillae (De Luca, 1965). Except in gammarids, the o6stegites are broad, flattened plates that overlap to enclose the brood beneath the ventral body wall (Figure l l A B). In contrast, most gammarid o6stegites are rather slender but equipped with long marginal setae (lacking in hyperiids and caprellids) which interlock or intermesh to hold the brood (Figure l l C - D ) . Actually, within the gammarids there is a progression from the primitive broad o6stegites without setae to the more common narrow form with long setae that Steele (1991) associates with increasing egg size. Here, the brood chamber is essentially an open mesh structure that would enhance gas exchange for the larger eggs. Often female peracaridans go through one or more "preparatory" molts during which o/Sstegites first appear as small ventral protrusions or buds on the coxal plates that become fully formed only at the ovigerous molt. Gardiner (1975) noted that the new mature o~stegites come encased in small cuticular envelopes, soon lost as the o~stegites unfold to their full size. He likens this process in tanaids to the unfolding wings of emerging insects, an analogy supported by Moers-Messmer's suggestion (1936) that "blood" pressure effects this expansion. Many mysids and amphipods produce successive broods at each molt after maturity with no change in marsupial structure, but some gammarids have a resting stage of one or more molts between broods when the o6stegites remain, but the long marginal setae are reduced (Verway, 1929; V. Steele, 1967). Isopods and cumaceans usually have one or more intermolt periods between broods in which oOstegites are reduced or lacking (Lang, 1953; Forsman, 1956) to be formed anew if there are subsequent broods. While the ventral marsupium is usually a single chamber formed by a series of overlapping o6stegites, some mysids and tanaids have two separate lateral brood pouches formed from one or two pairs of otistegites

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

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Figure 11 Typical arrangement of o/Sstegites and marsupial structure in isopods and gammarid amphipods. (A) The flat platelike oSstegites overlap in the midline of isopods. (B) The marsupial cavity between the oSstegites and the ventral body wall (vbw) shown in transverse section with the dorsal blood vessel (dbv) in the midline. (C) Successive stages of oSstegite development in the gammarid Corophium volutator showing the narrow o~)stegites and (D) transverse section through a gammarid showing the position of the oOstegites and young beneath the ventral body wall (vbw). (A from Holdich, 1968; C after Watkin, 1941; D from Kunkel, 1918.)

REPRODUCTION AND DEVELOPMENT IN PERACARIDANS

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Figure 12 Lateral views of brooding in the mysid Anchialina typica (A), the caprellid Phtisica marina (B), the tanaidacean Pseudotanais forcipes (C) and the cumacean Hemilamprops californica (D) showing the typical pericaridan ventral marsupium. Thermosbaenacea (E) are unusual in brooding their young dorsally as shown here in Halosbaena acanthura, one of the few species where ovigerous females are described. (A from Zimmer, 1927, after Sars, 1877; B from Stephensen, 1929; C from Zimmer, 1927; after Sars, 1900; D from Zimmer, 1936; E from Stock, 1976.)

(Table 1). When this occurs in mysids, the two last pairs of o6stegites do not overlap. Instead they fold inward toward themselves to form two more-or-less separate marsupia (Nouvel, 1940). In some tanaids (Tanaidae) the paired ventral brood pouches or "ovisacs" (Lang, 1960) are elaborate structures, each fashioned from a single o6stegite (Figure 13). Johnson and Attramadal (1982) suggest that these unusual brood chambers may have evolved as an adaptation to reduce osmotic shock in tidepool-dwelling tanaids.

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

F

G

Figure 13 Ovisac development in the tanaidacean Tanais dulongi. All views are lateral except (D) which is medial. (A-D) Progressive increase in o6stegite size at successive preparatory moults. D. Developed ovisac with genital slit through which sperm are transferred. No further moults occur during the marsupial development (D-G). (From Johnson and Attramadal, 1982.)

8.2.

Internal brooding

Modifications to the basic peracaridan pattern of marsupial brooding are found in several different (non-parasitic) isopod groups and at least one hyperiid amphipod, which have developed special internal brood chambers or ventral pockets not made of oOstegites. Extensive surveys by Hansen (1905) and Harrison (1984) of brooding among the Sphaeromatidae (Isopoda) reveal two distinct modes of brooding in addition to typical marsupial brooding and a number of interesting intermediates. At least a dozen sphaeromatid genera lack o6stegites and brood their young in two large ventral pockets - one fore and one aft that arise as extensions or flaps of the ventral body wall (Figure 14A). These pockets have transverse openings to the outside through which the young presumably exit. Unfortunately, we lack descriptions of brooding in these species, and one should wonder how the brood gets into these pockets initially. Bathycopea and Campecopea have anterior oOstegites plus a large posterior pocket, but the role of either or both of these in brooding is unclear. Even by sphaeromatid standards the related genera Cymodocella and Ischyromene are exceptional. They have an anterior marsupium of o6stegites plus a large posterior pocket as above. However, neither is used for brooding. Instead the brood develops embedded in the

177

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ventral cuticle. Brooding in this fashion may be the evolutionary precursor to later formation of internal sacs described below. Leichmann (1891) first noted that Sphaeroma rugicauda eggs develop not in the marsupium itself, but rather in four pairs of internal sacs (Figure 14B). These sacs are thin finger-like invaginations of the ventral epidermis which open to the outside via transverse slits in the body wall. It appears that the eggs are shed directly into the marsupium and then pass through the external slits into the brood sacs. Movement of eggs into the pouches must occur immediately after the eggs are laid while the cuticle is soft, for animals with eggs in the marsupium are almost never encountered (Leichmann, 1891; Hansen, 1905). Kinne (1954a) suggests that when the female rolls into a ball (common behavior in sphaeromatids) the resulting pressure on the brood opens the slits and forces the brood inside, but this was not observed by Daguere de Hureaux (1966). Regardless of how they get there, the eggs are evenly apportioned among the eight internal sacs

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

that stretch to fill the maternal peritoneal space (Kinne, 1954a). Following their internal incubation, the young isopods leave the brood sacs to reside in the empty marsupium for several days before their departure (Kinne, 1954a; Leichmann, 1891). Exceptions occur in certain species in the genus Sphaeroma where o(istegite reduction is associated with burrowing or boring lifestyles (Harrison and Holdich, 1984). External openings of the oviducts have not been found, nor have eggs or brood been observed in the marsupium. Klapow (1970) described an entirely internal mode of incubation for Excirolana. The eggs apparently pass directly from the oviducts into a pair of internal brooding sacs or "uteri". When development is complete, external openings to the uteri appear between the fourth and fifth pereopods, and the young emerge passively, posterior end foremost. Their expulsion may be aided by a sudden increase in hydrostatic pressure from the coelomic fluid at the time of release. After parturition the uteri are resorbed and must be reformed for subsequent broods. An additional example of internal brooding in isopods is Sheppard's (1957) account of the Edotea oculata brood being almost surrounded by the tissue from the body wall. Brusca (1981) provides the only evidence for internal brooding in free living amphipods with a description of an internal brood sac formed "as a deep invagination on the ventral side of the thorax between the second pereopods" in the giant hyperiid Cystisoma (Figure 15). Brusca speculates that either the long pereopods or the posterior o0stegites assist the eggs from the gonopores to the ventral openings of the brood sac. Since he found only developing eggs and embryos in the brood sac, fertilization must occur in the oviduct or as the eggs are in transit. Speculation on the biological significance of internal brooding abounds. Kinne (1954a) suggested that brooding in a normal marsupium would interfere with the ability of Sphaeroma to roll up and thai internal brooding alleviates the problem. Charmantier and Charmantier-Daures (1994) showed that S. serratum embryos were buffered from osmotic shock while in the internal pouches, and this could be a significant benefit in estuarine or intertidal habitats with wide and rapid salinity variations. For most species, the benefit may simply be increased physical protection for the brood, for these adaptations have not yet been associated with any changes in either brood nutrition or mode of development. Klapow (1970) feels that internal brooding in Excirolana and Eurydice serves as an adaptation for life on wave-swept beaches by affording better physical protection for the brood. Similarly, Sheppard (1957) surmised that the marsupial modifications found in Edotea are aids to brooding in a "dirty" environment. Harrison (1984) concurs and states that sphaeromids with internal brooding are typical of either turbid shallow areas or unsheltered habitats in the intertidal zone.

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179

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Figure 15 Internal brooding in the large deep-water gammarid Cystisoma. The single brood sac (bs) lies just posterior to the digestive caecum (c) at the anterior end of the digestive tract (dr) and opens ventrally between the second pereopods. Small o6stegites are also visible. (After Brusca, 1981.)(B) Transverse section of the brood sac shows its bilobed structure with a median groove through which the ventral nerve cord (vnc) and caecal duct (cd) pass. 8.3.

Brooding behavior and brood care

In most cases, marsupial incubation involves a minimum of direct care from the brooding female. She may seek a protected habitat or minimize her exposure to predation by altering feeding patterns or even by foregoing food for the duration of incubation. B e y o n d the protection afforded by brooding and limited manipulation of the eggs or young with

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

their pereopods (Lewbel, 1978; Wittmann, 1981a; Johnson and Attramadal, 1982) or occasionally replacing some that fall out (Croker, 1968; Wittmann, 1978; Borowsky, 1983c; Shillaker and Moore, 1987a; Sheader, 1996), the female's care seems limited to providing adequate ventilation for the developing embryos. Regular ventilatory movements of the o/Jstegites in all major groups enhance water circulation in the tightly packed marsupium. A posterior-to-anterior water current through the marsupium of some isopod families (Table 1) is produced by specially modified maxillipeds ("Wasserstrudelapparat") that appear only at the ovigerous molt (Hansen, 1905; Emden, 1922; Harrison, 1984). The rather small anterior o~stegites found in some tanaids (on chelipeds), cumaceans (maxillipeds) and mysids do not usually hold the brood, but aid water flow (Forsman, 1938). The specially modified coxa I of stenetriid isopods may serve the same function (Wilson, 1980). Even in those species with internal brooding, nutrition of the developing brood comes from the yolk supplied in the egg without further maternal contribution. To this rule, Johnson and Attramadal (1982) provide a singular exception. Just before release of young at the manca II stage, Tanais dulongi females inject a large deposit of "yolk" through the gonopores upon which the brood feed just before they depart the marsupium. This direct sacrifice of nutritional resources of future broods to feed the current crop of offspring is unique among peracarids and perhaps Crustacea. Brooding female isopods and tanaids may feed little if at all. The volume of the growing embryos compresses the female's internal organs, including the gut, which would hinder food intake (Figure 1). In addition, mouthparts are so reduced or modified in some brooding females (Table 1) that they cannot feed. Since the incubation period may last several months, the problem of maternal nutrition could be severe. Many isopods remain quiescent while brooding which would help conserve energy. Even so, Holdich (1971) found that Naesa bidentata females show considerable degeneration of muscle tissue while brooding. Apparently, protein is their primary source of nourishment since most of their lipid reserves are incorporated into the o/Scytes prior to ovulation. Most mysid and amphipod females continue to feed while brooding, but the carnivorous amphipod Cheirimedon femoratus and deep-sea lysianassoids stop feeding altogether during the latter stages of incubation (Bregazzi, 1972).

8.4.

Release of the brood and parental care

The juvenile or manca stage of the free-living species can crawl and/or swim on their o w n at the end of brooding. Indeed, this is the usual means

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of exodus from the marsupium or internal pouch at the end of juvenile development. Some mysid, amphipod and tanaid females actively assist their young out of the marsupium with their pereopods (Skogsberg and Vansell, 1928; Harrison, 1940; Wittmann, 1978) or urosome (Sheader, 1977b), or by opening the o6stegites (Nair, 1939; B0ckle-Ramirez, 1965; Bregazzi, 1972). Sheader (1977b) was able to reinitiate release behavior of female Parathemisto by placing a living copepod in the empty marsupium after the brood had departed. In other cases, some of the fully developed brood may remain in the marsupium until the o0stegites are lost at the next molt. For Tanais dulongi, escape from the enclosed ovisacs (Figure 13) could present more of a problem than exit from a typical marsupium made of o6stegites, but the sacs disintegrate completely within seconds after the supplemental yolk (see above) enters from the oviducts. Johnson and Attramadal (1982) suggest that enzymatic action dissolves the ovisac, but it is unclear whether this comes from the female, from the yolk itself, or from the young once they have eaten the yolk. In most cases the newly released mancas leave their mothers and are on their own, but extended parental care occurs in some peracaridans. A few gammarids (McCloskey, 1970; Kanneworff and Nicolaisen, 1973; Thiel et al., 1997) and isopods (Sars, 1899; Svavarsson and Davidsdotir, 1995) may literally cling to their mothers who carry young attached to their antennae for up to several weeks. Caprellids are the only peracaridans (excluding the special cases described below) known to provide active maternal care for the newly released brood (Harrison, 1940; Lim and Alexander, 1986; Aoki and Kikuchi, 1991; Thiel, 1997a, b). Juvenile Caprella monoceros remain in the immediate vicinity of their mothers for several weeks. Aoki and Kikuchi (1991) noted that, when disturbed, the mother would vigorously wave her antennae as a signal for the young to gather. She then assisted them as they climbed onto her body where they clung while she moved to another location. When approached by other caprellids, she used her gnathopods to defend her offspring. These females did not molt while caring for their broods. However, when the brood was removed, they molted and produced eggs within days.

8.5. Extramarsupial brooding 8.5.1. Brooding in tubes Many amphipods and tanaids construct tubes to live in. Both display similar and remarkable alterations in their brooding behavior associated with this lifestyle. Once the young leave the marsupium, sometimes a little earlier than usual, they complete their development in the tube. In effect,

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

this extends the protection afforded by brooding itself. Some gammarids remain in the tubes with their mothers. For example, Leptocheirus pinguis females produce up to three consecutive broods, and several different clutches remain in the tube with them (Thiel et aL, 1997; Thiel, 1997c). Each young L. pinguis makes an individual tube inside the mother's larger tube. Females pump water through the burrow, and the young apparently feed on the suspended particles. Juveniles leave their mother's burrow when they are about half grown. Tanaids show even more parental care. Females partition off a brood chamber by stringing a mesh across either end of the tube using sticky threads or secretions from glands that exit at the tips of pereopods (Siewing, 1954; Gardiner, 1975). Young that stray within the tube may be fastened to the tube wall with these strings. Kudinova-Pasternak (1969) observed the deep-sea Typhlotanais magnificus young roaming free around the mother in her tube rather than inside her rudimentary brood pouch. She surmised that this extramarsupial brooding was related to the great fecundity of Typhlotanais. The only other reported instance of such external brooding in free-living Peracarida occurs in tubicolous hyssurid isopods, which lack oOstegites altogether (W/igele, 1981). Thiel (1999) suggests that juvenile Leucothoe spinicarpa remaining inside ascidians with their mothers may represent an initial stage in the development of extramarsupial brooding in gammarids. At this stage, there is no evidence of early release of the brood or of direct parental care beyond the females' allowing the brood to remain within the parental abode. 8.5.2.

Brooding in gelatinous zooplankton (hyperiid amphipods)

The nature of the relationship between hyperiids and gelatinous zooplankton varies from genus to genus and from juvenile to adult, precluding clear distinctions between parasitic and non-parasitic forms (Harbison et al., 1977; Madin and Harbison, 1977; Laval, 1980). In fact, many hyperiids might be more properly termed predators than parasites. Regardless, species-specific associations with siphonophores, medusae and salps have resulted in some unusual forms of brooding. Relatively normal development resulting in release of fully developed and independent offspring is found in Parathemisto (Kane, 1963; Sheader, 1977b) and Hyperoche (Westernhagen, 1976). However, many hyperiids liberate their young from the marsupium at a much earlier (pre-manca) stage than do other amphipods (Laval, 1965; Metz, 1967; White and Bone, 1972), and these young use their hosts for food or habitat prior to entering the plankton (Dahl, 1959; Laval, 1965, 1968, 1972). According to Diebel (1988) and Richter (1978), Phronima removes the living tissue from its salp or pyrosome prey to make hollowed barrels that serve as both home

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183

and brood chamber. Laval (1963, 1972) uses the term "demarsupation" to describe this extra-marsupial development within the tunicate. A peculiarity of phronimids is their habit of depositing eggs into the marsupium in discrete batches separated by several days (Woltereck, 1904; Dudich, 1926; Shih, 1969). This results in young of different stages occupying the same marsupium and in a staggered release of young. Contrary to earlier speculation, these larvae do not feed on the tunicates as they develop (Shih, 1969; Richter, 1978). In contrast, the young Hyperia, Vibilia and Lycaea are dearly parasitic. The female Hyperia galba remove young from the marsupium one by one, and place each in small holes she makes in the host tissue (Dittrich, 1987). Similar individual placement of young in salps occurs in Vibilia (Laval, 1963). Lastly, BovaUius (1890) and Schellenberg (1933) report an aberrant female form of Rhabdosoma (=Xiphocephalus) whitei. The minute o6stegites are too small to form a marsupium, and the large thoracic gills make a type of brood chamber where the embryos develop. Clearly, the pelagic hyperiids represent a diverse assemblage and one of the least studies. Further reproductive exceptions and oddities are likely.

8.6.

Brood mortality and brood parasitism

Development within the confines of the marsupium or internal brood pouches provides a measure of protection from predation and an adequate food supply until development is virtually completed. Thus, if the mother survives, the brood should have an excellent chance to survive until its release. In many species mortality during marsupial development is negligible, but there are notable exceptions. Some species routinely exhibit progressive mortality of broods at successively later developmental states, sometimes approaching 40% mortality. Causes of this brood mortality are poorly understood. The great increase in the volume of the embryos during development could result in expulsion or crushing of some individuals (Jancke, 1926), but there is no indication that this is a widespread phenomenon. Likewise, isolated observations of brood cannibalism in mysids (Wittmann, 1984) and in female Gammarus duebeni with inadequate diets (Sheader, 1983) provide no general explanation for the numerous reports of high brood mortality. The great variability in brood mortality rates reported for the same species may be due to environmental factors (Heath and Khazaeli, 1985). Overall, the developing broods of euryhaline species show remarkable tolerance of salinity changes not exhibited by stenohaline forms. The vitelline membrane itself has very low permeability to both water and salts, but the brood pouch may provide osmotic control, at least in some species. McLusky and Heard (1971) provide evidence for osmotic regula-

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

tion within the brood pouch of the euryhaline mysid, Praunus flexuosus. The beach fleas Orchestia and Mysticotalitrus secrete urine isosmotic with the haemolymph directly into the marsupium via cuticular channels (Morritt and Spicer, 1996, 1999; Morritt and Richardson, 1998) to buffer the developing embryos from low salinities until the hatchlings develop their own osmoregulatory capacities. Nevertheless, Sheader (1983) showed that the extremes of temperature or salinity encountered by Gammarus duebeni in tide pools sometimes result in a loss of the entire brood. Laboratory studies on isolated mysid eggs also show mortality attributable to severe salinities (Vlasblom and Elgershuizen, 1977; Greenwood et al., 1989). Fungus (Plectospira) or parasitic isopods (Clypeoniscus and Ancyananiscus) (Holdich, 1968; Salemaa, 1986) in the marsupium can destroy the brood. On the other hand, Schultz and Allen (1982) described another parasitic isopod, Prodajus bigelowiensis, as an obligatory parasite in the marsupium of Americamysis bigelowi but found no discernible impact on either development or survival. Between these two extremes, Just (1978) describes a fascinating interplay between the Arctic amphipods Acanthonotozoma spp. and the parasitic copepod Sphaeronella. Both males and female copepods are found on some species of Acanthonotozoma and not on others at the same location. The adult female copepods are found only in the marsupium of female amphipods, although male and juvenile female Sphaeronella are found on male amphipods. The parasites attach to female hosts before the oOstegites are completely developed. At this point amphipod gonadal development is halted. The o6stegites, however, continue to develop into a complete marsupium for the exclusive use of the parasite and its developing ovisacs. Since she found a number of parasitized amphipods with a fully developed marsupium at a size notably smaller than usual, Just suggested that "the full development of marsupial plates is induced, even prematurely, by the parasite". These observations raise interesting questions about the control mechanisms involved in o6stegite development and their relationship to gonadal maturation. Recently, Moore and Wong (1996a) and Beare and Moore (1998a) found a similar situation with Sphaeronella in brood pouches of two different gammarid species off Scotland where a single female copepod occupied the marsupium.

8.7.

Egg size, brood size and incubation time

Reproductive cycles, brood size, egg size and incubation time are related to each other and to environmental variables (Mauchline 1973, 1980). Most data (Table 3) come from North Atlantic coastal species, primarily

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gammarids (see reviews by Nelson, 1980; Van Dolah and Bird, 1980; Sainte-Marie, 1991), isopods and mysids~ Enough polar and deep-sea Peracarida have been studied to indicate specific reproductive adaptations to these environments. Other adaptations are unique to particular families and may be products of previous evolutionary constraints rather than current conditions. Nevertheless, a few trends have emerged. 8.7.1.

Egg size

Egg diameter within the peracaridans is, with rare exceptions, speciesspecific and varies over two orders of magnitude (Table 2). The majority have eggs falling between 0.3 and 0.8 mm with most eggs above 2.0 mm belonging to polar or deep-water species (Table 3). The smallest eggs reported are 0.12-0.15mm (diameter) in Cumacea, Tanaidacea and Isopoda and 0.21 mm in gammarids, perhaps reflecting a minimum practical size for the eggs considering the peracaridan mode of development. At the other extreme, the 10-12 mm eggs of the isopod Bathynomus giganteus are exceptional even among the deep-sea species and are the largest known within the Peracarida. Comparison of egg diameter within each group shows cumacean and caprellid eggs fall within a narrow diameter range regardless of female size. In contrast gammarids, isopods and mysids exhibit a marked linear increase in egg diameter with average female length for different species (Figure 16), and the limited data suggest a similar trend for Tanaidacea and hyperiid amphipods. Thus fecundity for each species is fairly predictable within each peracaridan order based on female size - with a few notable gammarid exceptions (Table 3). For example, the semi-terrestrial Talitrus saltator eggs are among the largest gammarid eggs, but Orchestia platensis from the same habitat carries surprisingly small eggs for its size. Members of the genus Gammarus (except G. mucronatus) tend to have rather small eggs for their size. Egg size is usually consistent for a given species or population, but seasonal differences in egg size are known. Larger eggs in winter may be a general trend in gammarids (Steele and Steele, 1975c; Van Dolah and Bird, 1980; Moore, 1986) where eggs up to 36% larger (volume) occur in cold months (Bell and Fish, 1996; Sheader, 1996; PoweU, 1992). In contrast, overwintering Idotea spp. females produced many small eggs, but later summer generations carried fewer eggs with 23% greater volume (Kroer, 1989). Seasonal differences of this magnitude may be common since the differences in egg diameters would be less than 10% and thus easily overlooked. Interestingly, the seasonal differences reported for two gammarids with elliptical eggs by Beare and Moore (1998b) seem primarily due to changes in width while length was virtually unchanged.

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Brood size

Peracaridan brood size ranges from 1 to over 1000, but 10-75 is more typical (Table 2, Table 3). As expected, larger species, with greater

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marsupial volume, tend to have larger broods (Figure 17). Accordingly, many of the most fecund peracaridans are large polar or bathypelagic species, e.g. the amphipod Gammaracanthus, and the isopod Glyptonotus (Table 3). Exceptions to this rule occur in some large deep-sea isopods with unusually large eggs. The huge Bathynomus giganteus (18--29 cm) carries only about 30 10-12 mm eggs. This may represent a singular case, but the deep-sea serolids show the same trend, albeit to a more modest degree. Within a species, the general trend for brood size to increase with the size of females is almost universal, although the exact relationship is species dependent. Typically, seasonal variation in brood size simply reflects differences in the sizes of females present at different seasons. There are, however, cases where fecundity for females of the same size differs significantly at different seasons, with larger broods generally associated with smaller individual egg size (Figure 18). Such brood size variations have been noted for mysids (Mauchline, 1980; Wittmann, 1984; Wooldridge, 1986; Astthorsson, 1987; Johnston and Northcote, 1989; Fenton, 1994), gammarids (Kolding and Fenchel, 1981; Moore, 1981b; Sheader, 1983; Hiwatari and Kajihara, 1984; Skadsheim, 1984b; Elka'fm et al., 1985; Dauvin, 1988c; Powell, 1992; Beare and Moore, 1998b), and isopods (Kroer, 1989), although there is no agreement on which of the seasonal generations has the larger broods. Allen (1984) also noted lowered brood size for Mysidopsis at the end of the reproductive season.

8.7.3.

Duration of brooding

Temperature, egg diameter and salinity all affect incubation time. Temperature accounts for much of the latitudinal and seasonal variation reported in brood time which ranges from 96 h in Mesopodopsis orientalis from tropical waters to well over a year for many polar or deep-water species (Table 2). Development time at a given temperature also increases with egg size (Steele and Steele, 1973b, 1975d; Van Dolah and Bird, 1980; Wittmann, 1981b, 1984).

8.7.4.

Direct effects of temperature and salinity on incubation time, egg size and brood survival

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sheim (1989) on Gammarus indicate increased yolk deposition at lower temperatures resulting in larger eggs and may explain the seasonal differences in egg size found in some species. Whether the larger eggs of polar and deep-sea species results from similar direct physiological effects or from more subtle evolutionary factors cannot yet be answered. Salinity effects are most pronounced at the extremes of the salinity range for each species and may have an impact on the numbers of females reproducing (Mills and Fish, 1980), survival of embryos (Shyamasundari, 1976; Vlasblom and Elgerhuizen, 1977; Lalitha et al., 1989-90; McKenney, 1996), incubation time (Shyamasundari, 1976) (Figure 19) and sometimes brood size (Pinkster and Broodbakker, 1980; Steele and Steele, 1991; MeKenney, 1996). Vlasbloom and Boiler (1971) noted swelling of eggs at

190

WILLIAM

S. JOHNSON,

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low salinities, but the cellular mechanisms associated with adverse salinity effects are unstudied. Many estuarine peracaridans experience a variety of temperature and salinity combinations throughout the year. McKenney (1996) found significant salinity-temperature interactions for most reproductive functions in Mysidopsis, with effects most pronounced at low temperatures (Figure 20). 8.7.5. Evolutionary trends Wittmann (1984) and Mauchline (1980) both noted the ratio of brood volume or weight to that of the female in mysids is relatively constant, so that overall reproductive output is similar but with major differences in how reproductive energy is packaged (Nelson, 1980; Corey, 1981; Mauchline, 1988). Overall, both fecundity and egg size increase with female size in peracarids, but the much larger deep-sea and polar species put more of the increased total brood volume into individual egg size and less into increasing brood number. Increased egg size is at the expense of fecundity, and it could limit the number of broods for iteroparous species owing to increased incubation times associated with larger eggs. Wittmann (1984) suggested using the average number of broods per

191

REPRODUCTION AND DEVELOPMENT IN PERACARIDANS

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incubatory day as a means of comparing reproductive output and asserted that for mysids this ratio is relatively constant over a broad range of habitats from polar to tropical and from littoral to deep sea. Figure 21 shows that mysids, and indeed most peracarid orders, have a ratio close to one. Smaller tropical species produce smaller broods but at more rapid intervals compared with species in colder areas in all groups~ Similar constraints associated with the peracaridan mode of brooding affect all groups. Despite the many differences among the orders and individual species, this similarity in reproductive output may indicate that the evolutionary trade-offs between egg size, incubation time and brood size result in a common set of reproductive adaptations. There has been much discussion of the trade-offs between egg size and brood size in specific habitats (Mauchline, 1973, 1980, 1988; Kolding and Fenchel, 1981; Fenwick, 1984; Wittmann, 1984; Ingram and Hessler, 1987; Sainte-Marie, 1991), but both consensus and convincing evidence are rare. The exceptionally large eggs found in polar and deep-sea species may be related to cold water, although no direct connection has been established. Clarke (1982) asserts that polar species have had ample time to evolve physiological mechanisms to compensate for temperature and that larger eggs are an adaptation to low food availability rather than to temperature

192

WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

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per se. Since both polar and deep benthic habitats are suspected to have

uncertain food supplies, larger young might be at an advantage in securing food. Species with high risk of adult mortality should benefit from higher fecundity and earlier reproduction. Extensive comparisons of temperate gammarids by Nelson (1980) and Van Dolah and Bird (1980) show that for a given size, infaunal haustoriids have both a greater total brood volume and a smaller egg size than epifaunal gammarids and ampeliscids, resulting in greater fecundity. Similarly, littoral and coastal cumaceans showed somewhat larger broods than those from deeper water habitats (Corey, 1981). In both cases, increased fecundity was suggested as a means to offset higher predation. Van Dolah and Bird (1980) further argue that the shorter incubation time of smaller eggs increases the chance that females survive to release each brood, although the smaller young might be at some disadvantage. While predation is the most common explanation for higher fecundity and faster development times, other selective pressures may be involved. In the sand beach isopod Pseudolana towrae, Dexter (1985) found increased brood size coincident with greater exposure to wave action. Hyperiid amphipods also release an unusually large number

193

REPRODUCTION AND DEVELOPMENT IN PERACARIDANS

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of young that emerge from the marsupium at an earlier stage and immediately begin feeding on their gelatinous zooplankton "host". High fecundity here might offset the challenge of finding a particular host or prey species in the water column. No one has offered an explanation for the unusually high fecundity of sphaeromids and idoteids compared with other isopods of similar size. While these trade-offs between, egg size, brood size and incubation time continue to invite speculation, generalizations still seem premature.

ACKNOWLEDGEMENTS

We thank Dennis M. Allen, Valerie Chase, G. D. F. Wilson and K. J. Eckelbarger for reading early versions of this manuscript and encouraging its completion. Special appreciation goes to Donald P. Abbott, Arthur C.

194

WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

Giese and Welton Lee for their inspiration, example and mentorship in the explorations of marine invertebrate biology. M. S. was supported in this endeavour by a Ripon College Faculty Development Grant and L. W. by NSF/PEET grant DEB-952173.

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WILLIAM S. JOHNSON, MARGARET STEVENS AND LES WATLING

REFERENCES

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Journal of Experimental Marine Biology and Ecology 196, 239-250. Wittmann, K. J. (1978). Adoption, replacement and identification of young in marine Mysidacea (Crustacea). Journal of Experimental Marine Biology and Ecology 32, 259--274. Wittmann, K. J. (1981a). Comparative biology and morphology of marsupial development in Leptomysis and other Mediterranean Mysidacea (Crustacea). Journal of Experimental Marine Biology and Ecology 52, 243-270. Wittmann, K. J. (1981b). On the breeding biology and physiology of marsupial development in Mediterranean Leptomysis (Mysidacea: Crustacea) with special reference to the effects of temperature and egg size. Journal of Experimental Marine Biology and Ecology 53, 261-279. Wittmann, K. J. (1982). Untersuchungen zur Sexualbiologie einer mediterranen Mysidacee (Crustacea), Leptomysis lingvura G. O. Sars. Zoologischer Anzeiger 209, 362-375. Wittmann, K. J. (1984). Ecophysiology of marsupial development and reproduction in Mysidacea (Crustacea). Oceanography and Marine Biology, Annual Review 22, 393-428. Wittmann, K. J. (1985). Freilanduntersuchungen zur Lebensweise von Pyroleptomysis rubra einer neuen bentho-pelagischer mysidacee aus dem Mittelmeer und dem Roten Meet. Crustaceana 48, 153-166. Wolff, T. (1962). The systematics and biology of bathyal and abyssal Isopoda Asellota. Galathea Reports 6, 1-320. Woltereck, R. (1904). Zweite Mitteilung tiber die Hyperiden der Deutschen Tiefsee-Expedition. "Physosoma", ein neuer pelagischer Larventypus; nebst Bererkungen zur Biologie von Thaumatops and Phronima. Zoologischer Anzeiger 27, 553-563. Wong, Y. M. and Moore, E G. (1996). Observations on the activity and life history of the scavenging isopod Natatolana borealis Lilljeborg (Isopoda: Cirolanidae) from Loch Fyne, Scotland. Estuarine, Coastal, and Shelf Science 41, 247-262. Wooldridge, T. H. (1986). Distribution, population dynamics and estimates of production for the estuarine mysid, Rhopalophthalmus terranatalis. Estuarine and Coastal Shelf Science 23, 205-223. Yamagishi, H. and Hirose, E. (1997). Transfer of the heart pacemaker during juvenile development in the isopod crustacean Ligia exotica. Journal of Experimental Biology 200, 2393-2404. Zerbib, C. (1973). Contribution h l'6tude ultrastructurale de l'ovocyte chez le Crustac6 Amphipode Orchestia gammarellus Pallas. Comptes Rendus de l'Academie des Sciences de Paris, s6ries D, 277, 1209-1212. Zerbib, C. (1975). PremiEre observation de granules corticaux dans l'ovocyte d'un Crustac6, l'Amphipode Orchestia garnrnarellus (Pallas). Comptes Rendus de l'Academie des Sciences de Paris, s6ries D, 281, 1345-1347. Zerbib, C. (1976). Nature chimique des enclaves vitellines de l'ovocyte du Crustac6 Amphipode Orchestia gammareUus (Pallas). Annales d'Histochimie 21, 279295. Zerbib, C. (1977). Endocytose ovocytaire chez le Crustac6 Amphipode Orchestia gammarellus (Pallas). D6monstration par la peroxydase. Comptes Rendus de l'Academie des Sciences de Paris, s6ries D, 284, 757-759. Zimmer, C. (1927). Ordnung der "Reihe Peracarida" der Crustacea Malacostraca: 8. Mysidacea, 9. Cumacea, 10. Tanaidacea, 11. Isopoda. In "Handbuch der Zoologie" (W. Ktikenthal and T. Krumbach, eds), pp. 605-766. Walter de Gruyter & Co., Berlin, Germany.

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Zimmer, C. (1933). Mysidacea. Die Tierwelt der Nord- und Ostsee Lfg. 23 (Teil Xg. 3), 29-69. Zimmer, C. (1936). California Crustacea of the order Cumacea. Proceedings of the United States National Museum 83, 423-439. Zimmer, C. (1941). Cumacea. Bronn's Klassen und Ordnungen der Tierreichs 5 (Part 1), No. 41-222. Zirwas, C. (1911). Die Isopoden der Nordsee. Kieler Meeresforschungen, Abt. Kiel. N.E 12, 73-118.

Remote Sensing of the Global Light-Fishing Fleet: An Analysis of Interactions with Oceanography, other Fisheries and Predators R G. R o d h o u s e , 1 C. D. E l v i d g e , 2 a n d P. N. T r a t h a n 1

1British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK Tel: 01223 221612; Fax: 01223 362616: E-mail: [email protected]; p. [email protected], uk 2 Office of the Director, NOAA National Geophysical Data Center, 325 Broadway, Boulder, CO 80303, USA Tel: 303-497-6121; Fax: 303-497-6513; E-mail: [email protected]

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Description and Interpretation of the Global Cephalopod Light Fisheries Imaged with the DMSP OLS: Interactions with Oceanography . . . . . . . . . . . . . . . 2.1. DMSP-OLS images . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Other squid fisheries and unspecified species . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Unexploited squid stocks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Interactions with Other Fisheries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Kuroshio Current . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. China Sea Shelf . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Sunda-Arafura Shelves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. New Zealand . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. California Current . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. H u m b o l d t Current . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7. Southwest Atlantic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Cephalopod Fisheries that do not use Lights . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Interactions between the Light Fisheries and Predators of the Target Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Analysis of predator diets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Predators of species exploited by light fisheries . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Use of predator data to identify new fisheries . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Implications for precautionary measures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Discrepancy between global, and regional, estimates of predator consumption of cephalopods and fisheries yield . . . . . . . . . . . . . . . . . . . . . . . .

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Acknowledgements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Appendix. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Overfishing is causing changes in global marine ecosystems including a downward shift in the mean trophic level o f exploited species. As groundfish landings have decreased, landings o f cephalopods, which are short-lived trophic opportunists, have increased in some fisheries suggesting overfishing of their predators and, or, competitors may have positively affected cephalopod population~ These changes in marine ecosystems emphasize the need for methods analogous to satellite remote sensing o f land use in agriculture. The cephalopod fisheries, which are implicated in change, use powerful incandescent lights. We used archived data from the United States Defence Meteorological Satellite Program (DMSP) Operational Linescan System (OLS) to formulate a detailed description and interpretation of the global light fishery in relation to physical and biological oceanography. The extent of interaction between the exploited squid and groundfish stocks, and between the target species of the fisheries and higher predators, was then assessed. Globally, the highest concentration of light fishing is in the Kuroshio Current, the China Sea Shelves and Sunda-Arafura Shelves Provinces of east Asia. Other major light fisheries are pursued around New Zealand, in the California and Humboldt Currents and in the southwest Atlantic. A n analysis of the world squid catch based on FAO data revealed that 63-89% of the total catch is caught with lights that can be visualized with DMSP-OLS imagery. In three o f the provinces where concentrations of light-fishing vessels were located, increasing cephalopod catches have coincided with overexploitation o f groundfish stocks. In two of these the squid catch is dominated by loliginids. Evidence that over-exploitation of groundfish is implicated in the expansion o f ommastrephid fisheries is less clear, except perhaps in New Zealand. The other ommastrephid fisheries are either in areas dominated by pelagic fisheries or are off-shelf. Given the extent o f light fishing in several of the ocean's ecological provinces, and the potential for expansion into ecologically sensitive areas such as the Antarctic, it is important to know what their direct and indirect effects are on the functioning o f marine ecosystems.

1.

INTRODUCTION

Global fisheries have generally reached the limits of production and in some notable examples have declined dramatically (FAO, 1994). There is

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little prospect of a substantial increase in fish production from wild stocks and production may not even be sustainable at current levels. As well as damaging populations of target species, overfishing is also causing changes in global marine ecosystems. One fundamental change has been a downward shift in the mean trophic level of species exploited by fisheries over the last four decades (Pauly, 1998). This has been reflected in a transition from predominantly long-lived, high trophic level piscivorous fish to short-lived, low trophic level invertebrates and planktivores. In particular, a recent study has shown that as groundfish landings have decreased in some fisheries, landings of cephalopods have increased. Cephalopods are short-lived trophic opportunists and overfishing may have positively affected their populations (Caddy and Rodhouse, 1998). World cephalopod fisheries have increased from - 2 million tonnes in 1987 to > 3 million tonnes in 1996, and for this reason synoptic information might provide insights into these ecological changes in the world's oceans. Analysis of global fisheries generally relies on statistics collected by national governments and reported to FAO. These data are low resolution and there is delay before they become available for scientific use. Given the global nature of change in fisheries there is a need for methods analogous to satellite remote sensing of land use in agriculture for marine systems. Cephalopod fisheries provide such an opportunity. Many of these fisheries are pursued by concentrating the target species with powerful incandescent lights. Large fleets of vessels, mostly from east Asia, operate using lights in various parts of the world's oceans. The recent availability of archived data from the United States Defence Meteorological Satellite Program (DMSP) Operational Linescan System (OLS) provides a novel means of monitoring the activities of whole fleets of light-fishing vessels in near real time (Cho et al., 1999). The OLS has the unique capability to detect low levels of visible and near infra-red radiance at night. Elvidge et al. (1997a, b) have developed algorithms to identify and geolocate VNIR emission sources in night time imagery and have compiled an inventory of light sources present at the Earth's surface. The OLS sensor is an oscillating scan radiometer designed for cloud imaging with a swath width of about 3000 km. The sensor has two spectral bands: the VIS band spans the visible and very near-infrared (VNIR) part of the spectrum (0.5 to 0.9/~m) and the thermal band (10.5 to 12.6/zm). DMSP platforms are stabilized using four gyroscopes providing three axis stabilization. Orientation is adjusted using a star mapper, an earth limb sensor and a solar detector. The wide swath allows global coverage four times per day at dawn, day, dusk and night. Satellites F-10 to F-14 overpass at - 2 0 : 3 0 to 21:30 local time. The sensors measure radiance in the VIS band down to 10-9W cm-2sr -1/~m -1, which is more

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than four orders of magnitude more sensitive than the VNIR bands of other sensors used for oceanographic applications such as the NOAA AVHRR. Originally collected for military use, DMSP data were declassified in 1972 but they have only been archived in digital form since 1992 at the NOAA National Geophysical Data Center. Light-fishing vessels are mostly jiggers which catch squid with jigs (lures armed with an array of barbless hooks) and fished in series on lines using automatic machines (Suzuki, 1990) (Plate la). Squid are attracted to the jigs with an array of metal halide, incandescent lights (Plate lb). Small artisanal vessels may deploy a single lamp. Large, industrial vessels operate offshore and use an average of about 150 lamps. Typical lamps are 2 kW but they range from 1-3 kW. The lamps are usually white with a small number of green lamps interspersed (Inada and Ogura, 1988). The principal lamps are suspended above water but on industrial vessels two additional underwater lamps are sometimes used. These are 2-5 kW each, depending on whether they are green or white. A typical east Asian "far seas" squid jigger of 70 m overall length operating in the southwest Atlantic would operate 150 lamps giving a total light power of 300 kW. It would also operate 110 jig lines carrying 25 jigs per line (total 2750 jigs) and would expect to catch 25-30 t of squid (exceptionally 100 t) per night with a crew of 20 persons. Experiments using sonar to detect squid attracted to fishing lamps have shown that in water of optical type "oceanic III" (Jerlov, 1964) squid (Todarodes pacificus) are concentrated in a depth layer between 30 and 70 m in spectral irradiance levels (at 510 nm) of 1.8 × 10 -2 to 5.4 × 10 -5/xWcm-2nm -1 (Arakawa et al., 1998). Combining DMSP-OLS images of the global distribution of light fishing with other spatial data, using a marine Geographical Information System (GIS) developed at The British Antarctic Survey (BAS) (Trathan et al., 1993), enabled the formulation here of a detailed description of the geographical extent of the global light fishery and interpretation of the relationship of the species they are targeting, with the bathymetry and physical and biological oceanography of the regions where they operate. An assessment of the extent of interaction between the stocks of squid exploited by these light fisheries and the groundfish stocks of the continental shelves in their vicinity is presented. Interactions between the target species of the fisheries and higher predators are also examined. The spatial resolution provided by the DMSP-OLS data on the global squid fisheries facilitates relating their distribution to specific ecological provinces (Longhurst, 1998) rather than to the much larger-scale, and less ecologically meaningful, FAO statistical areas. Longhurst (1998) provides a scheme based on physical oceanography and the seasonal response of planktonic algae to seasonal forcing by physical processes as determined from remotely sensed ocean colour data. FAO data are the only global

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data on fisheries production; they were used for the analysis of global cephalopod fisheries by Caddy and Rodhouse (1998) and are used in this review for comparison of global catches with the distribution of lightfishing fleets (see FAO Yearbook, 1996b which covers the period 19871996).

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2.1.

DESCRIPTION AND INTERPRETATION OF THE GLOBAL CEPHALOPOD LIGHT FISHERIES IMAGED WITH THE DMSP OLS: INTERACTIONS WITH OCEANOGRAPHY DMSP-OLS images

The images presented here illustrate the geographical distribution of fishing lights over the 6 month period between October 1994 and March 1995 as detected in cloud-free conditions during the dark half of each lunar cycle (see Appendix). They show where lights have been detected at least once during that period. Where fishing fleets shifted their location during that time the same lights will appear in different places on several occasions. On the other hand the images provide a conservative estimate of area fished with light during the period because there may have been areas that were exploited by the fleet during periods of cloud cover that are not included. The images thus quantify the minimum area exploited by light-fishing vessels between October 1994 and March 1995, but cannot be used to quantify fishing effort. Squid fishers generally expect better catch rates during overcast weather and during the dark part of the lunar cycle (PGR, personal observation). The far seas fleets of large vessels from East Asia continue fishing in all conditions of cloud and moonlight but it is possible that small inshore vessels may vary effort according to the prevailing conditions. Because the composite images are based on cloud-free images from satellite passes during the dark half of the lunar cycle it is expected that the coverage of small inshore vessels might be biased. However, the argument still holds that the images provide a conservative estimate of the geographical area fished with light. 2.1.1.

Kuroshio Current

In the waters of the Kuroshio Current and seas to the northeast of Taiwan, fishing lights are more numerous and denser than anywhere else in the world's oceans. They are clearly visible in the Tsushima Strait between the Korean Peninsula and Japan, throughout the southern part of the Sea of

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Table 1 Squid catch identified to genera or species in seven ecological provinces where DMSP-OLS imagery reveals light-fishing activity.

Province Kuroshio Current China Sea Shelf Sunda-Arafura Shelves New Zealand California Current Humboldt Current Southwest Atlantic

FAO statistical area(s) in which Province lies 61

Species

Todarodes pacificus Ommastrephes bartrami 61 Loligo spp. (L. chinensis + others) 57 and 71 Loligo spp. 81 Nototodarus sloanii N. gouldi 77 Loligo opalescens 87 Dosidicus g i g a s 41 lllex argentinus Martialia hyadesi Loligo gahi

Catch (103 t.y -1)

% of world squid catch in 1996

1228--716(1987/96) 4248-378(1985/90)

29 5-3

117-24 (1987/96)

**-1

q37-195 (1987/96) ~29-83 (1987/96) 31-39 (1979-93) 278 (1977) 10.3-195(1987/96) 1157-401(1987/96) 10.2-24(1987/96) 144--89 (1987/96)

**7 2 -1 3 6 17 <1 *2

Sources: 1FAO, 1996; 2de Luca, pers. comm, 1998; 3Gibson, 1995; 4Murata and Nakamura, 1998; 5based on Nagasawa et al.'s (1998) estimate of 70 x 103 t in 1994. *not caught using lights; **unknown proportion caught using lights

Japan, and in the Pacific Ocean to the west of Japan off northern Honshu and Hokkaido (Plate 2). These lights represent the largest squid fishery in the world. It is largely pursued by Japanese, Korean and Taiwanese vessels mainly targeting the Japanese flying squid, Todarodes pacificus (Table 1). Catches have fluctuated from high levels in the 1960s to low levels in the 1980s but have increased again over the last - 1 0 years. These changes are apparently part of a regime shift associated with decadal changes in sea temperature (Minobe, 1997; Sakura et al., 2000). To the east of Japan, in oceanic waters, the fishery also targets the neon flying squid, Ommastrephes bartrami. Catches of this species peaked at nearly 400 × 103ty -1 in the 1980s (Murata and Nakamura, 1998). This was during the driftnet fishery that was subsequently banned by a UN moratorium in 1991 because of unacceptable by-catches of seabirds, marine mammals and other nontarget species. Since then the fishery has been re-established as a light fishery with Japanese jiggers catching - 7 0 x 103 t y -1 in the mid-1990s (Nagasawa et al., 1998) and Chinese and Taiwanese vessels catching another --80 x 103 t y-1 (A. Yatsu, pers. comm.) The Kuroshio Current, where these fisheries are located, is the western boundary current of the north Pacific (Longhurst, 1998). It originates off

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the east coast of the Philippines at about 15°N, flows northwards to 35--40°N, where an eddy field is created at the confluence with the cold southward flowing Oyashio Current, and where both currents are deflected eastward. This is an area of strongly seasonal primary production with maxima in spring (Saijo et al., 1970) and it is here that the O. bartrami fishery operates. There is also a torchlight net fishery for Pacific saury (Cololabis saira) in this area which operates between August to midNovember (Anon., 1995) so some of these lights may be included in the October-March composite image (Figure 2). A branch of the Kuroshio, the Tsushima Current, flows through the Tsushima Strait to the east of Honshu into the deep basin of the Sea of Japan. Within the Sea of Japan there is a gyre-like cyclonic flow which generates many warm- and cold-core mesoscale eddies. The most intense light fishing for squid takes place for Todarodes pacificus in the Tsushima Current (Figure 2). The continental Shelf in the Sea of Japan is narrow and strong phytoplankton blooms, supporting large zooplankton concentrations, are initiated by upwelling caused by eddy vorticity along the shelf edge and in the margins of warm core rings (Yamamoto and Nishizawa, 1986). The western part of the Sea of Japan is part of the China Sea Coastal Province (Longhurst, 1998). This area is characterized by the southwards flow of cold, subarctic, water from the Sea of Okhotsk which forms major cyclonic eddies. Off eastern Korea this current meets the northward flowing Kuroshio and forms a permanent thermal front across the shelf. These dynamic processes are associated with very high densities of light-fishing vessels that are targetting Todarodes pacificus.

2.1.2.

China Sea Shelf

This is another area of extensive light fishing extending along the whole shelf from the Yellow Sea in the north to the coast of Vietnam in the south (Plate 3). Greatest numbers of lights are visible in the southern and central part of the Yellow Sea, near the shelf edge to the northeast of Taiwan, off the north coast of Taiwan, around the Peng-Hu islands (Pescadores) to the west of Taiwan and in shelf waters to the west of Hainan. Substantial quantities of "common squid" (Loligo) as well as unspecified "cuttlefish" and "cephalopods", are reported to FAO by Taiwan (Table 1). The cephalopod fauna of this region, which includes the Exclusive Economic Zones (EEZs) of China, Taiwan, Vietnam and Korea, has been documented recently (Kubodera and Yamada, 1998; Lu, 1998). Cephalopod catches by Vietnam are relatively small at <10.103 t y-1 (Nguen Xuan Duc, pers. comm., 1996). The most abundant species in catches from the region

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P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

is Loligo chinensis (Wu et al., 1989; Dong 1991). In the Yellow Sea there is probably some light fishing with purse seine nets for finfish such as small clupeids (A. Yatsu, pers. comm., 1999) and these lights probably contribute to the fleet visible in Plate 3. The China Sea Coastal Province (Longhurst, 1998) includes an area of continental shelf that extends from the Yellow Sea in the north to the southern East China Sea in the south together with the narrow shelf area of the western Sea of Japan. This is one of the largest areas of shallow shelf in the world and is characterized by the discharge of freshwater and sediments by the Yellow and Yangtse Rivers. This high sediment load is consistent with the presence of myposid squid which, because they possess a corneal membrane, are adapted to the presence of high concentrations of suspended particles. No ommastrephid catches are reported to FAO by China or Vietnam. The Province is bordered to the east by the shelf edge and the flow of the Kuroshio Current. The Kuroshio flows around the south of Taiwan and onto the East China Sea shelf generating a northwards drift of warm water over the shelf which retroflects in an area of intense light fishing in the DMSP-OLS image. There is a return flow of coastal water southwards from the western Yellow Sea which is reinforced by freshwater discharging from the Yellow and Yangtse Rivers, and is associated with a persistent mesoscale eddy about 150 km south of Cheju Island. Along the margin of the continental shelf off China the Kuroshio meanders, generating mesoscale eddies. Cool streamers advect cold shelf water seawards and warm eddies move in across the shelf and are propagated northwards. There is upwelling near the Peng-Hu Islands where the squid fishery is located and off the northeast coast of Taiwan which are both areas of intense light-fishing activity which have been documented (Lu et al., 1987; C. C. Lu, pers. comm., 1999). There is also upwelling off Shanghai and in the eddy system south of Cheju Island but these are not areas of particularly high light-fishing activity, probably because of the low salinity and high sediment load of the Yellow and Yangtse Rivers. Chlorophyll levels are elevated in the vicinity of persistent upwelling features and also at the mouths of the major rivers but the latter are not areas of light fishing.

2.1.3.

Sunda-Arafura Shelves

Fishing lights are visible in large concentrations in the Gulf of Thailand, the Andaman Sea and in coastal waters of the Philippines (Plate 4). There are no published data about the cephalopod fisheries of the Philippines but substantial catches of unspecified "common squid" (Loligo) are reported to FAO in the "cephalopods" category (Table 1). The annual

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269

catch of Loligo spp. reported to FAO approximately doubled in the Philippines between 1987 and 1996. However, some of the lights appearing in the coastal waters of the Philippines may also be vessels exploiting finfish. The Thai fisheries for cephalopods in both the Andaman Sea and the Gulf of Thailand have been documented by Chotiyaputta (1993). A mixed fleet of light-fishing vessels, trawlers etc. catch loliginid squid, cuttlefish and octopuses. Although light fishing is the most effective means of catching squid (Loligo chinensis and L. duvauceli), a proportion of the light fishery also catches pelagic fish. These fisheries are located in the tropical Sunda-Arafura Shelves Province which includes the shelf areas of the South China Sea, Sulu Sea, Gulf of Thailand and Andaman Sea (Longhurst, 1998). Taken together this is the largest shelf area in the world ocean. It is unusually shallow and has complex tidal dynamics and high sediment input from rivers. The dominant oceanographic influence is the reversal of flow between the Pacific and Indian Oceans driven by the seasonally reversing monsoon winds. DMSP-OLS imagery has potential for analysing the spatial changes in light-fishing activity in response to this ocean cycle.

2.1.4. New Zealand Fishing lights are present on the shelf around New Zealand and are distributed off the west coasts of North and South Island extending into the Taranaki Bight between the two islands and off the southeast coast of South Island (Plate 5). The fishery targets two ommastrephid squid species, the Wellington flying squid, Nototodarus sloanii, which is the major species in the New Zealand fishery, and Gould's arrow squid, Nototodarus gouldi (Table 1). These are very similar species which can only be separated on the basis of hectocotylus morphology in males, sucker counts and molecular genetic markers (Smith et al., 1981; Smith, 1985; Smith et al., 1987). They also differ with respect to parasite load (Smith et al., 1981). The fishery for both species is well documented by Gibson (1995) and Uozumi (1998); N. gouldi is a subtropical species which occurs in Australian and New Zealand waters to the north of the Subtropical Convergence Zone (SCZ) and N. sloani is distributed in cooler New Zealand waters to the south of the SCZ. The fishery is located in the New Zealand Coastal Province (Longhurst, 1998). The shelf is widest around North Island and off the southeastern part of South Island including the area of shelf around the Snares Islands. New Zealand lies in the latitude of the Subtropical Convergence and the sub-Antarctic Front. The regional oceanography is complex. The West Auckland and East Auckland Currents flow southwards along the shelf on

270

P. G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

the west and east side of North Island respectively and there are three major eddies off the shelf on the east of the Island. Off the west coast of South Island the gyral circulation of the Tasman Sea bifurcates at about 44°S. The southern branch flows south along the coast, rounds the south of the Island and then forms the inshore component of the northward flowing Southland Current off the east coast of South Island. The northern branch, the Westland Current, flows northwards to the west coast of North Island. The D'Urville Current flows into Taranaki Bight through Cook Strait, which separates North and South Island. Surface chlorophyll is especially enhanced over the shallow bathymetry off southern New Zealand. The N. sloanii fishery is concentrated along the southeast coast of South Island and all over the Snares Shelf in the Southland Current system. There is also a trawl fishery on the Auckland Islands Shelt~ The species is caught in both Subtropical Front and sub-Antarctic water at temperatures of -<13°C and the squid fishery is associated with elevated chlorophyll levels. In the mainland/Snares shelf area the fishery mostly occurs over water depths of 40-140 m but there is some fishing beyond the 200 m iso-bath. The fishery usually begins in February and the length of the season is partly determined by the relative value of the catch and the catch rate in the N. gouldi fishery. The N. gouldi fishery is pursued around the northwest coast of South Island and the southwest coast of North Island over a broad area of shelf in subtropical water (-18°C) of the Westland/D'Urville Current system. The fishery starts in December in the southern part of the area and moves slowly northward into the Taranaki Bight and further north by April. Only jiggers using lights target this species and most fishing is over water depths of 80-180 m. The distribution of paralarvae and juveniles of both species of Nototodarus is similar to that of the adults and spawning probably takes place over the continental shelf (Uozumi, 1998). Hatching occurs mainly from April to June. 2.1.5.

California Current

The large-scale image in Plate 6 shows small groups of fishing lights operating close inshore around the Channel Islands off the coast of Southern California. This fishery exclusively targets Loligo opalescens (Table 1) which is caught on the spawning grounds along much of the Californian coast from central to southern California in the California Current Province (Longhurst, 1998). The fishery differs from most other squid fisheries using lights in that a single "lightboat" attracts and concentrates the squid, allowing one or more purse seiners to catch them using lampara nets.

REMOTE SENSING OF LIGHT FISHING

271

The California Current is the eastern boundary current in the Northeast Pacific, arising in the north from the bifurcation of the eastwards flow of the north Pacific and it flows south to the convergent front at the root of the North Equatorial Current off the southern tip of Baja California (Longhurst, 1998). The shelf is narrow and characterized by upwelling fronts and fronts associated with meanders in the coastal jet and cyclonic eddies. As in the Humboldt system, ENSO events occur when the northwesterly trade wind stress relaxes. The coastal upwelling system is complex and the enhanced productivity supports a low diversity diatom/copepod pelagic system (Mann and Lazier, 1991). The highly variable fishery for L. opalescens is linked to ENSO events in the California current (Mclnnis and Broenkow, 1978). 2.1.6.

Humboldt Current

Fishing lights are visible in large concentrations off the Peruvian Shelf extending from northern Peru at about 4°S (south) to about 9°S (Plate 7). The fishery is well documented (Yamashiro et al., 1998) and the jigging vessels are exclusively targeting the jumbo flying squid, Dosidicus gigas (Table 1), the largest member of the family Ommastrephidae, which was virtually unexploited until recently (FAO, 1994). Until 1990 catches had been low and limited to the Peruvian artisanal fleet, apart from some activity by Soviet Union trawlers in the late 1980s. In 1990 Japan and the Korean Republic entered the fishery. Catches peaked in 1994 and thereafter declined, apparently in response to cold (La Nifia) conditions. After this, many of the vessels moved their activities further north, to the vicinity of the Costa Rica Dome and by 1996 catches there had increased from <1% of the catch off Peru in 1994 to about 300%. Fishing effort and catches in the Peruvian fishery are greatest between June and December and the fishery is pursued largely by jiggers that also fish in the southwest Atlantic largely between February and May. The Humboldt Current Coastal Province in which the fishery is located is the eastern boundary current of the southeastern Pacific (Longhurst, 1998). This Province is characterized by a very narrow continental shelf, extensive and productive coastal upwelling features and periodic ENSO events. Distribution of D. gigas is mostly off the shelf edge in areas of high but not maximum primary production (Nesis, 1983). 2.1.7.

Southwest Atlantic

Fishing lights extend in a line closely following the Patagonian Shelf edge from about 40°S southwards to the Falkland Islands (Malvinas) and spread

272

P. G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

widely over the southern part of the shelf to the north of the Islands (Plate 8). This fishery is primarily targeting the winter spawning stock of the ommastrephid squid Illex argentinus, but it also catches variable amounts of another ommastrephid, Martialia hyadesi (Table 1). The fishery biology of the genus Illex in the Atlantic has recently been reviewed (Rodhouse et al., 1998) and the fisheries for I. argentinus and M. hyadesi are well documented (Rodhouse, 1997; Haimovici et al., 1998). The fishery began in the early 1980s when east Asian squid jiggers shifted their effort from the north Atlantic, following the collapse of the I. illecebrosus fishery off eastern Canada. Catches in the Southwest Atlantic are variable and linked to annual recruitment, which is driven by oceanographic factors (Waluda et al., 1999). The fishery operates from December-June with peak catches from March-May. In 1995 there was a large catch of M. hyadesi in the fishery that was targeted in May by numerous vessels that clustered on the shelf break front to the north of the Falkland Islands (Plate 9). Analysis of positions of fishing vessels reported to the Falkland Island Government Fisheries Department showed that vessels were fishing in a region where a mesoscale feature, possibly a cold streamer flowing in over the shelf edge, could be observed in A V H R R imagery (Gonz~ilez et al., 1997). There is also a large fishery for another species of squid, Loligo gahi in this Province (Table 1), largely over the shelf to the south and east of the Falkland Islands (Hatfield et al., 1990). Since 1987 annual catch rates have been between 44 and 89 × 103 t but this is caught entirely by trawlers that do not use lights and are not visible in the DMSP-OLS image. The I. argentinus and M. hyadesi fisheries are associated with the Southwest Atlantic western boundary current system of the Southwest Atlantic Shelves Province which includes the Patagonian Shelf and Falklands Plateau, one of the widest and flattest areas of continental shelf in the world's oceans (Longhurst, 1998). Circulation here is very complex; a shelf break front extends almost the entire length of the shelf and separates the sub-Antarctic water of the northwards-flowing Falkland (Malvinas) Current (which is part of the Antarctic Circumpolar Current) from shelf water (Glorioso and Flather, 1995). It is this front where much of the light fishing visible in Figure 7 is concentrated. To the north of the province is the confluence of the Falkland (Malvinas) Current and the Brazil Current. At the confluence, the Falkland (Malvinas) Current is retroflected back southwards and the Brazil Current separates from the shelf and is deflected into the oceanic interior (Olson et al., 1988). The confluence is characterized by a zone of intermediate surface water filled with eddies where the winter spawning stock of I. argentinus spawn (Haimovici et al., 1998). The latitude of the confluence is variable and

REMOTE SENSING OF LIGHT FISHING

273

determined by the relative strength of flow of the two currents. The shelf break front is characterized by the consistent presence of chlorophyll, associated with dynamic eddying at the front, and there is also a strong chlorophyll feature associated with tidal mixing in shallow water over the inner shelf and around the Falkland Islands where the I. argentinus fishery spreads widely across the shelf.

2.2.

Other squid fisheries and unspecified species

About 28% of the world squid catch in 1996 is unaccounted for in Table 1. Less than 6% of this is caught by fisheries in other FAO statistical areas where there are no lights in the DMSP-OLS images (Table 2). The rest is accounted for by squid catches that are not identified to species or genus (squids, nei) within the FAO statistical areas where the light fisheries operate (Table 3). Ommastrephes bartrami is probably included in both Tables 1 and 3 as the catch given in Table 1 was taken from a source independent of FAO and is probably also accounted for by FAO as "squids, nei". Approximately 100% of the world squid catch is therefore accounted for in Tables 1, 2 and 3. Between 62 and 70% of the squid catch in Table 1 is caught with lights. Summing the percentages of total world squid catch in 1996, given in Tables 1 and 3 (less 3% for O. bartrami which is accounted for twice), shows that - 9 6 % of the world squid catch is either known to be caught with lights or taken in FAO areas where lights are detected with DMSP-OLS. Because of the uncertainties, the best estimate that can be made of squid caught by light fisheries therefore lies between a minimum of 62-70% and up to some value <96% of the global squid catch. Most of the uncertainty in these estimates is associated with the identity of the species reported as "squids, nei" in Table 3. The bulk of the catch in Table 3 is from areas 41 and 61 and probably includes a large proportion of ommastrephids (Illex argentinus in area 41 and Todarodes pacificus in area 61) caught using lights. However, it is known that there are catches made by other gears in these areas, especially in area 61 where, for instance, some 22 to 27 × 10 3 t y-1 of the gonatid Berryteuthis magister are presently caught, largely as a by-catch of trawl fisheries (Nesis, 1997).

2.3.

Unexploited squid stocks

Most of the world's shelf and near-shelf stocks of squid are probably fully exploited or are approaching full exploitation so variations in catch rate, evident in catch data reported to FAO over the last decade, are mostly environmentally driven. Several oceanic stocks that are currently unex-

274

P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

Table 2 Squid catches reported to F A O from statistical areas where lights do not appear in DMSP-OLS images. FAO statistical area 21 27

31

34 37

47 51

67

Province(s)

Species

Northwest Atlantic Shelf Loligo pealei Illex illecebrosus Squids, nei Northeast Atlantic Shelf Loligo spp. (*L. forbesi and L. vulgaris) lllex illecebrosus and I. coindetii Todarodes sagittatus Squids, nei Caribbean/Guianas Loligo spp. Coastal (*L. pealei, L. plei and Loliguncula brevis) lllex illecebrosus Squids, nei Eastern Canary and Loligo spp. Guinea Current (*L. vulgaris) Coastal Squids, nei Mediterranean Loligo spp. ( *L. vulgaris) Todarodes sagittatus Squids, nei East African Coastal Loligo reynaudi Squids, nei East African Loligo spp. Coastal/Northwestern ( *L. duvauceli, Arabian L. singhalensis, UpweUing/Western Sepioteuthis lessoniana others?) India Coastal Squids, nei North Pacific Squids, nei Epicontinental Sea, Alaska Downwelling Coastal, Pacific Subarctic Gyre (East)

% of world Catch squid catch (103 tonnes) in 1996 11.7-23.0 2.0-28.2 0.04-1.3 3.5-5.7

0.5 0.7 <0.1 0.2

2.1-6.2

0.1

0.0-3.9 4.2-9.9 0.9-3.9

<0.1 0.3 <0.1

5.9-30.5 0.06-3.1 3.0-6.5

1.2 <0.1 0.1

8.8-23.6 7.8-10.6

0.9 0.3

4.9-11.3 0.3-0.9 2.7-10.7 0.4-16.1 0.0-4.6

0.2 <0.1 0.3 <0.1 <0.1

0.3-4.2 0.2-55.6

0.2 <0.1

*Based on Roper et al. (1984).

p l o i t e d , o r o n l y lightly e x p l o i t e d , h a v e b e e n i d e n t i f i e d as h a v i n g p o t e n t i a l f o r e x p l o i t a t i o n ( O k u t a n i , 1998). O f these, t h e s p e c i e s with m o s t p o t e n t i a l a r e p r o b a b l y t h o s e such as t h e o m m a s t r e p h i d s Sthenoteuthis oualaniensis in t h e I n d o - P a c i f i c a n d O m m a s t r e p h e s bartrami in s u b t r o p i c a l / w a r m t e m p e r a t e w a t e r s o f all t h e oceans. Martialia hyadesi in t h e A n t a r c t i c P o l a r F r o n t a l Z o n e ( A P F ) has b e e n i d e n t i f i e d as h a v i n g p o t e n t i a l c o m m e r c i a l v a l u e ( R o d h o u s e , 1990) a n d v a r i o u s g o n a t i d s p e c i e s in t h e S u b a r c t i c N o r t h Pacific (Nesis, 1997), t h e S u b a r c t i c N o r t h A t l a n t i c a n d t h e S o u t h e r n O c e a n

275

REMOTE SENSING OF LIGHT FISHING

Table 3 Squid catch reported by FAO that is not identified to genera or species (squids, nei) in FAO statistical areas that include the seven ecological provinces where DMSP-OLS imagery reveals light-fishing activity.

FAO statistical area(s) in which Province lies

Province included in area(s) where light fishing occurs

Catch (103 tonnes) (1987/96)

% of world squid catch in 1996

61

Kuroshio Current/ China Sea Shelf Sunda-Arafura Shelves

218.9-405.5

13.5

10.9-18.5 9.7-27.8 23.0--53.0 30.5-79.0 0.07-28.8 208.4--428.3

0.6 1.0 1.0 3.2 0.01 10.0

57 and 71 81 77 87 41

New Zealand California Current Humboldt Current Southwest Atlantic

(Wiborg, 1979; Kristensen, 1983) are also of potential fishery value. Many of these squid, especially the oceanic ommastrephids (Rodhouse, 1990, 1998; Dunning, 1998; Yamashiro et al., 1998; Yatsu et al., 1998; Young and Hirota, 1998) prey on planktonic crustaceans and mesopelagic fishes (e. g. myctophids) of the deep scattering layer. Both the Indian Ocean and APE where some of these stocks exist, are regions known to support high density aggregations of mesopelagic fish (Mann, 1984). Any new fisheries for squid stocks feeding on mesopelagic fish would have unknown implications, given the current state of knowledge of the ecology of the deep scattering layer and its dependent species, and would pose new challenges for sustainable management.

3. 3.1.

INTERACTIONS WITH OTHER FISHERIES Kuroshio Current

Total fishery landings in this Province are among the highest in the world. Pelagic fish, including Pacific herring and saury, Japanese pilchard, chub mackerel, anchovy and jack mackerel, are very productive but fluctuate widely and dominance, in terms of catch volume, shifts between species. Variability is generally accepted to be driven by the environment rather than fishery effects (FAO, 1994). The core flow of the Kuroshio is characterized by annual and decadal shifts which drive variability in the fisheries. One particular feature of these regime shifts has been the inverse relationship between the abundance of different pelagic species including

276

P. G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

sardine Sardinops melanostictus (Kawasaki and Omori, 1995) and squid (Murata, 1990). Given that the finfish fisheries in this region are primarily targeting pelagics and that most of the T. pacificus and all the O. bartrami fisheries take place off shelf, there is probably little interaction between the squid and groundfish stocks in this province. 3.2.

China Sea Shelf

Groundfish stocks in the East China Sea and Yellow Sea are extensively overfished and have been estimated to be at levels of 0.1 to 0.2 of unexploited levels (Yu, 1991). In addition, Pacific herring were fished out in the Yellow Sea in the 1980s (Sherman and Alexander, 1989). Other coastal pelagics in the area are very productive but subject to environmentally driven variability. Overfishing in the area may be compounded by use of very fine nets in coastal areas catching pre-recruits (FAO, 1994). Here cephalopod populations may have responded to changes in the groundfish stocks. In the decade 1987-96, catches of squid reported to FAO by China and Hong Kong, all of which can be assumed to be loliginids caught on the shelf, have increased substantially. However, catches of loliginids, reported by Taiwan, have remained relatively stable suggesting that if there has been a response to overfishing of groundfish stocks it has not been homogeneous across the China Sea Shelf, possibly because of confounding effects of political, social and economic conditions in the region. 3.3.

Sunda-Arafura Shelves

This is another area of intense fishing historically where there is good evidence of overfishing (FAO, 1994). Groundfish in this province are overexploited, especially in the Gulf of Thailand and Malacca Straits. Pelagic species are heavily exploited in the Malacca Straits, Java Sea, Gulf of Thailand and the shelf around the Philippines. The Gulf of Thailand is one of the best examples of an ecosystem where overexploitation of groundfish has been accompanied by expansion of cephalopod populations (Caddy and Rodhouse, 1998) and the increased catch of Loligo spp. in the Philippines is indicative of a similar trend. 3.4.

New Zealand

The major groundfish stocks in the New Zealand province are fully exploited (Baird, 1992; Annala, 1993). Blue grenadier, snapper and orange

REMOTE SENSING OF LIGHT FISHING

277

roughy are overfished and it is possible that the squid fishery may have benefited from reductions in these stocks.

3.5.

California Current

The finfish fisheries in the California Current province resemble those of the Humboldt system. Upwelling areas support important fisheries for small pelagics, notably the Californian sardine, Sardinops sagax caeruleus, and the northern Pacific anchovy, Engraulis mordax, which are highly variable and also under the influence of ENSO events. The finfish exploited in this region are predominantly pelagics so there is probably little interaction between groundfish exploitation and the squid fisheries in this Province.

3.6.

Humboldt Current

The finfish fisheries in this province are dominated by small pelagics, especially anchoveta (Engraulis spp.), which vary with ENSO events but are not considered to be overexploited (FAO, 1994). Demersal stocks caught over the narrow continental shelf are fully exploited or overexploited but there is probably no interaction between groundfish and D. gigas which does not occur over the shelf. The off-shelf distribution of this species precludes any interaction with groundfish stocks.

3.7. Southwest Atlantic

Fish catches in this province are dominated by hoki (Macruronus rnagellanicus) two species of hake, Merluccius hubbsi and M. australis, which are fully exploited (FAO, 1994). The other fisheries, e. g. southern blue whiting, Micromesistius australis, are moderately to fully exploited. This is apparently an anomalous area where there is naturally a high ratio of cephalopods to groundfish and where groundfish exploitation has had little to do with the expansion of the squid fishery (Caddy and Rodhouse, 1998).

4.

CEPHALOPOD FISHERIES THAT DO NOT USE LIGHTS

The analysis presented by Caddy and Rodhouse (1998) considered all cephalopod fisheries whether exploited by light fshing or other methods

278

P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

such as trawling. Although the present analysis identifies those squid stocks that are fished with lights, it should be emphasized that other cephalopod stocks, such as Octopus vulgaris on the Saharan Bank, that support large-scale industrial fisheries implicated in ecological change (Caddy, 1983) are caught by other methods, especially bottom trawl.

5.

INTERACTIONS BETWEEN THE LIGHT FISHERIES AND PREDATORS OF THE TARGET SPECIES

The role of cephalopods in the diet of higher predators (seabirds, seals, cetaceans and fishes) throughout the world's oceans has been dealt with in detail by Croxall and Prince (1996), Klages (1996), Clarke (1996b) and Smale (1996). Here we focus on the interactions between the air breathing predators and the squid species targeted by the global light-fishing fleet.

5.1. Analysis of predator diets Although most cephalopods are soft bodied, the remains of their mandibles (beaks) are commonly found in the gut contents of predators. The beaks are composed primarily of chitin (Dilly and Nixon, 1976) and are very resistant to digestion. The beaks can usually be identified to family, or genus, and often to species level (Clarke, 1986) so the accumulations in predators' guts can provide a great deal of information about the species and size of their prey. Over the last three decades numerous studies of cephalopod predation, especially by seabirds, seals, cetaceans and fishes, have been carried out in all the world's oceans (Clarke, 1996a). It is therefore possible to make a preliminary assessment of the interactions between the major world light fisheries for squid and the predators dependent on these exploited stocks. The squid stocks exploited by light fisheries, and the dependent predators that have been identified, are given in Table 4.

5.2. 5.2.1.

Predators of species exploited by light fisheries Todarodes pacificus

Although this has been historically the largest squid fishery in the world there are few data on predators of the species. Only one study, on short-finned pilot whales (Table 4), records it as prey for a higher

O

Plate 2 Kuroshio Province: a) DMSP-OLS composite image of fishing lights for the period October 1994 - March 1995 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and, b) direction of associated winter surface currents (surface current data from Wyrtki (1961), Inoue (1981), Sugimioto and Tameishi (1992), Fang et al. (1998)).

Plate 3 China Sea Shelf Province: a) DMSP-OLS composite image of fishing lights for the period October 1994 - March 1995 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and b) direction of associated winter surface currents (surface current data from Wyrtki (1961), Inoue (1975) and Fang et al. (1998).

Plate 4 Sunda-Arafura Shelves Province: a) DMSP-OLS composite image of fishing lights for the period October 1994 March 1995 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and b) direction of associated winter surface currents (surface current data from Wyrtki (1961)).

Plate 5 New Zealand Province: a) DMSP-OLS composite

image of fishing lights for the period October 1994 - March 1995 (200 m and 1000 m bathymetfic contours shown in blue; area lit by fishing lights shown in yellow with red outline) and b) direction of associated surface currents with area covered by a} indicated with a broken outline (surface current data from Carter et al. (1998)).

Plate 6 California Current Province: 8} DMSP-OLS composite image of fishing lights from March 1996/January February 1997 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and b) direction of associated surface currents with area covered by a) indicated with a from broken outline (surface current data from Wyrtki (1966)).

Plate 7 Humboldt Current Province: a) DMSP-OLS composite image of fishing lights for the period October 1994 - March 1995 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and, b) direction of associated surface currents with area covered by a) indicated with a broken outline (surface current data from Anon, 1987)).

Plate 8 Southwest Atlantic Province: a) DMSP-OLS composite image of fishing lights for the period October 1994 - March 1995 (200 m and 1000 m bathymetric contours shown in blue; area lit by fishing lights shown in yellow with red outline) and b) direction of associated surface currents with area covered by a) indicated with a broken outline (surface current data from: Peterson and Stramrna (1991), Peterson and Whitworth (1989), Peterson (1992)).

Plate 9 DMSP-OLS single night sample of the Southwest Atlantic 23 May 1995.

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282

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predator. However, given the substantial consumption of ommastrephids inhabiting shelf regions elsewhere, the lack of data probably reflects limited research. 5.2.2.

Ommastrephes bartrami

This oceanic squid is found in the diet of sperm whales and short-finned pilot whales in the Kuroshio Current Province (Table 4) and elsewhere (Clarke and Roeleveld, 1998). It is probably also consumed by other predators in this Province. Elsewhere in the Pacific it is the prey of sharks (Dunning et al., 1993; Seki, 1993); Parkinson's petrel, Procellaria parkinsoni (Imber, 1976) and some seabirds breeding in the Hawaiian Islands (Harrison et al., 1983). 5.2.3.

Loligo spp.

Despite the extensive fishery for loliginids throughout the east and southeast Asian ecological provinces there appear to be no studies that reveal their presence in the diet of predators. This almost certainly reflects the lack of research on the subject in this area. Judging by the importance of a loliginid species (L. opalescens) in an area (the California Current) where detailed predator/prey studies have been carried out, then there are probably numerous predators of loliginids off south and southeast Asia, as well as elsewhere in the world's oceans. 5.2.4.

Nototodarus sloanii and N. gouldi

The beaks of these species from predator gut contents are indistinguishable and where they have been identified in the litereature it is on the basis of known distribution. Each year several hundred Hooker's sea lions are caught incidentally by trawlers targeting Nototodarus sloanii around the Auckland Islands off New Zealand and it is assumed they are preying on the squid in this area (Reijnders et al., 1993). However, there appears to be no interaction between the sea lions and the light fishery operating in the New Zealand Province. A Nototodarus sp. identified as sloanii is also consumed by fiordland and yellow-eyed penguins in New Zealand waters (van Heezik, 1989, 1990a, b). Elsewhere, in Australian waters, Nototodarus gouldi are preyed on by the Australian fur seal, Arctocephalus pusillus (Gales et al., 1993), the little penguin Eudyptula minor (Montague and Cullen, 1988; Gales and Pemberton, 1990; Cullen et al., 1992) and the short-tailed shearwater (Skira, 1986).

REMOTE SENSING OF LIGHT FISHING

5.2.5.

283

Dosidicus gigas

By far the greatest estimated consumption of a commercially exploited species by a predator is that of Dosidicus gigas by the sperm whale in the Humboldt Current. R. Clarke et al. (1988) estimated that, when sperm whales were at, or below, the level of maximum sustainable yield, between 1959 and 1961, the minimum consumption of this squid was 6.7 m t y-1 and could have been as high as 20.1 m t y-l, or at last 34 times the highest annual catch recorded in the Peruvian fishery since the start of industrial fishing in 1991 (Yamashiro et al., 1998). R. Clarke et al. argued that D. gigas is almost the only prey of sperm whales in the Humboldt Current. In view of the huge consumption of D. gigas by sperm whales it is notable that, although the diet of sperm whales has been analysed in the South Atlantic (Clarke, 1980), New Zealand (Clarke and Roper, 1998) and the Kuroshio Current (Okutani et al., 1976; Okutani and Stake, 1978) there are no records of consumption by the whales of the target species of the light fisheries in these areas. Todarodes pacificus, Nototodarus sloanii, N. gouldi and lllex argentinus are smaller than D. gigas and O. bartrami and, probably more importantly, they generally inhabit shallower water where sperm whales do not regularly feed. However, it is not obvious why Martialia hyadesi, which is a larger species that generally occurs off shelf, is not eaten by sperm whales in the South Atlantic although it is taken by other predators and by fisheries.

5.2.6.

Illex argentinus

In spite of the importance of the Illex argentinus fishery in the South Atlantic there has been relatively little research on the role of this species in predators' diets and no attempt to quantify consumption by predators. An analysis of fish, seabird and marine mammal stomachs has shown that I. argentinus is important in the diet of Thunnus obesus, Xiphius gladius and Polyprion americanus (Santos, 1992) and L. B. Prenska (unpubl. data cited by Haimovici et al., 1998) has estimated that it comprises about 38% of food of fish on the Southern Patagonian Shelf. There is a complex trophic system in the region (Angelescu and Prenski, 1987): L argentinus and hake, Merluccius hubbsi, feed on anchovy, the squid prey on young pelagic hake and older hake feed on all sizes of the squid. Hake are therefore competitors and prey of L argentinus as well as an apparently important predator. It is, however, surprising that, in spite of the dominant role of squid, and L argentinus in particular, in the fisheries of the Southwest Atlantic they are not apparently more important in the diet of air breathing seabirds and marine mammals.

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5.2.7. Martialia hyadesi Although the ommastrephid Martialia hyadesi is only occasionally caught in substantial numbers in the Patagonian Shelf fishery, its importance in the diet of Antarctic seabirds and marine mammals, and the fact that there has been exploratory fishing for the species in Antarctic waters (FAO statistical subarea 48.3), has meant that special attention has been given to assessing its role in the diet of these predators. It has been known since the earliest days of marine biology in the South Atlantic that squid are an important component of the Southern Ocean ecosystem although in the early years they were impossible to catch with the scientific sampling tools available. Harrison-Matthews (1929) wrote: "The squid are certainly there, and at times, if not always, near the surface, though no naturalist has yet invented gear which will catch them and prove their presence directly". Later research on predator diets in the Scotia Sea (Clarke, 1980; Clarke et al., 1981; Clarke and Prince, 1981; Clarke and McLeod, 1982a, b) added considerably to knowledge of the squid fauna of the region and once new net, and jig, caught material from the fishery around the Falkland Islands was available (Rodhouse and Yeatman, 1990) a major species in the diet of albatrosses, white chinned petrels, king penguins and southern elephant seals at South Georgia (Rodhouse et al., 1987, 1990, 1992b; Rodhouse and Prince, 1993; Croxall and Prince, 1994; Croxall et al., 1995; Rodhouse et al., 1998) was identified to be Martialia hyadesi, an ommastrephid with the potential to support commercial fisheries in Antarctic waters. M. hyadesi is a circumpolar species largely associated with the Antarctic Polar Frontal Zone (APFZ) (Piatkowski et al., 1991; Xavier et al., 1999), which in the South Atlantic forms a broad loop linking the ecosystems of South Georgia and the north Scotia Arc with the Patagonian Shelf edge (Figure 8). The species occupies the ecological niche of epipelagic fish in this area (Rodhouse and White, 1995) where it feeds on mesopelagic fish and crustaceans (Rodhouse et al., 1992c) in a community dominated by tunicates, crustaceans, fish and coelenterates as well as other squid species: Gonatus antarcticus, Moroteuthis knipovitchi, Galiteuthis glacialis, Histioteuthis eltaninae and Brachioteuthis ?picta (Piatkowski et al., 1994; Rodhouse et al., 1994, 1996; PagEs et al., 1996). M. hyadesi is associated with meso-scale oceanographic features in the APFZ (Rodhouse, 1997) where satellite tagging experiments with seabirds indicate that this is where these predators forage for them (Rodhouse et al., 1996, 1998b). The squid occasionally invades the Patagonian Shelf edge where it is caught by the light-fishing fleet primarily targeting Illex argentinus (Rodhouse, 1991; Gonzfilez et al., 1997; Ivanovic et al., 1998; Anderson and Rodhouse, in

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press). Small juveniles caught near the shelf edge around the Falkland Islands indicate that the species spawns in this area (Rodhouse et al., 1992a) but the life cycle is poorly understood.

5.3.

Use of predator data to identify new fisheries

Most of the world's finfish resources (with the major exception of the oceanic mesopelagics) are exploited to some extent and many are either fully, or over-exploited (FAO, 1994). On the other hand there are undoubtedly cephalopod stocks that still remain relatively unexploited (Okutani, 1998) and others that are as yet unexploited by humans but which are abundant in the diet of predators (Clarke, 1996c). These include members of the family Ommastrephidae not presently exploited, and other families that are so far unexploited including the Alloposidae, Architeuthidae, Octopoteuthidae, Lepidoteuthidae, Pholidoteuthidae, Cycloteuthidae, Cranchiidae, Thysanoteuthidae, Onychoteuthidae, Histioteuthidae and Gonatidae. The members of some of these families are unpalatable because of the texture of the flesh, or because the tissues contain high concentrations of ammonium as an adaptation for buoyancy (Denton, 1974) but others, including the Thysanoteuthidae, Gonatidae and possibly the Pholidoteuthidae, would be suitable for human consumption. In the past, new fisheries for Dosidicus gigas and Martialia hyadesi have been anticipated on the basis of data from higher predators (R. Clarke et al., 1988; Rodhouse, 1990). In a further instance, evidence for the large stock of Loligo gahi in the South Atlantic was present in the gut contents of finfish analysed by Polish scientists in the 1970s, but this was overlooked until the stock was discovered independently during fishing trials (Z. Karnicki, Marski Institute Rybacki, pers. comm.). In the future data from predators may provide the information to guide exploratory fishing and to make estimates of stock size of unexploited, but potentially commercial species. More importantly these data should also provide the basis for rational fishing with regard to dependent predators in particular and the whole marine ecosystem in general.

5.4.

Implications for precautionary measures

Because of the importance of squid in the diet of higher predators in the Antarctic, and because of the philosophy of ecosystem management in the area under the Convention for the Conservation of Antarctic Marine Living Resources (CCAMLR, 1995) and the precautionary approach more

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generally (FAO, 1996), this region has been the first where precautionary measures have been developed for squid fisheries in the context of the dependent predators. In the South Atlantic, commercial interest in the stock of Martialia hyadesi varies with the abundance of Illex argentinus on the Patagonian Shel£ In the late-1980s and again in the mid-1990s, exploratory fishing by Japanese and Korean light vessels in the Scotia Sea near South Georgia and the Polar Frontal Zone (CCAMLR area 48.3) focused attention on the need for a preliminary assessment of the size of the stock and for precautionary measures to be put in place prior to the establishment of a fishery. A preliminary assessment of predator consumption was made by Rodhouse et al. (1993) who estimated that between 326000 and 382 000 t y-~ of M. hyadesi is consumed by seabirds, seals and whales in the Scotia Sea. This was later revised to between 245000 and 550000 t y -1 (Rodhouse, 1997), the lower estimate being conservative; the upper included best estimates of odontocete consumption, which are unreliable because of uncertainties about diet and population size. It was proposed that the timing and total removals by the fishery should be highly conservative and set taking into account the timing of breeding and consumption rates of the most sensitive of the dependent species, which is the grey-headed albatross, Thalassarche chrysostoma. The proposal was implemented in CCAMLR Conservation Measure 99/XV in 1997 to the extent that the TAC was set at 25000ty -~, or about 1% of the most conservative estimate of predator consumption (CCAMLR, 1997).

5.5.

Discrepancy between global and regional estimates of predator consumption of cephalopods and fisheries yield

Data on cephalopod consumption by higher predators have been combined with estimated feeding rates and population size to produce estimates of global and regional consumption. Clarke (1977, 1980) estimates that about 100 M t y-1 are consumed by sperm whales and in the Antarctic all predators (whales, seals and seabirds) were estimated to consume about 34 M t y-1 (Clarke, 1983). Voss (1973) extrapolated, on the basis of conservative estimates of predator consumption, that some 100 to 300M t y -1 of cephalopods could be available for capture by fisheries world-wide and that the actual potential was probably as high as 500 M t y-1. A further estimate of the global standing stock biomass of cephalopods given by Rodhouse and NigmatuUin (1996) lies between 193 to 375 M t. These are very large volumes compared with the total world

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catch of about 100 M t y-1 and total world cephalopod catch of about 3.0 M t y-1 ( F A t , 1996a). TMs raises the question of whether the global estimates of predation, and subsequent extrapolations of potential catches are realistic or whether there are biases involved in the estimates that need to be considered. Cephalopods are short-lived, most have a life span of about 1 y, and so the biomass of a single cohort increases from that of the eggs spawned by one generation to a short-lived peak of biomass later in the year and then declines to zero by the end of one year of life. In a model of the lifetime energetics of a cohort of Illex argentinus, cohort biomass peaks at about 9 months and then declines towards the spawning season (Rodhouse and Nigmatullin, 1996). If this reflects reality then for much of the year the biomass of an entire species may be relatively low although the total turnover of biomass may be quite large. The extent to which a predator population, or fishery, can exploit the production of a cephalopod population will depend on the timing of removal; so, too, will estimates of population biomass based on predator consumption. If predators tend to consume cephalopods only when cohort biomass is close to maximum then average biomass of cephalopod populations will be overestimated. Conversely, predation on cohorts at times when biomass is less than maximum will tend to underestimate biomass and potential for exploitation by fisheries. Although much thought has been given to the problem of retention times of cephalopod beaks in predator stomachs (Clarke, 1980) this is still a potential source of bias. The lining of seal stomachs, for instance, is very convoluted and tends to retain squid indigestible beaks whereas fish bones are more easily digested and pass more rapidly through the alimentary tract. Retention of beaks will tend to cause overestimates of cephalopod consumption unless this is accounted for in making the calculations. The greatest errors in estimating fishery potential from data on predation probably arise from the fact that there are whole families of squid that are unsuitable for exploitation, either because of their unpalatable flavour or texture or because their behaviour makes them unsuitable for fisheries using currently available gear. Rodhouse (1990) concluded that although a total cephalopod biomass of 3.7 M t y -1 is consumed by predators in the Scotia Sea (Croxall et al., 1985), only one species out of a total of 12 consumed by predators was likely to be of interest to commercial fisheries in the short to medium term. The conclusion to be drawn is that cephalopod biomass in the world's oceans is undoubtedly large relative to commercial fisheries but there are enough questions about the estimates based on predators to require more observational science to derive independent estimates. Conventional scientific sampling gear was inadequate for the task a quarter of a

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P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

century ago (Clarke, 1977) and remains so today. Initiatives to quantify the biota of the world's oceans (Ausubel, 1999) will require that new technologies be developed that will match natural predators' and commercial fishers' abilities to catch cephalopods whilst doing so in a way that enables this group to be adequately quantified. The huge biomass of the mesopelagic community of the deep scattering layer (Mann, 1984) upon which many of the cephalopods of the open oceans depend mean that there are undoubtedly important new discoveries to be made about the extent and functioning of this system. Despite the extensive use of artificial light for catching cephalopods commercially, it has only found limited use for scientific sampling (Clarke and Pascoe, 1985). Future efforts to improve scientific sampling should give this discrepancy more attention.

6.

INTERACTIONS WITH PREY

The prey of the target squid species of the major world light fisheries, where known, are given in Table 5. Squid, and cephalopods in general, are ecological opportunists feeding on a wide range of prey types and sizes (Rodhouse and Nigmatullin, 1996). They generally prey on crustaceans when small and shift, to a greater or lesser extent, to fish as they grow. This shifting pattern of diet largely reflects the taxonomic basis of the pelagic biomass spectrum which the squids exploit as they track their optimum prey size during growth (Rodhouse et al., 1994; Rodhouse and Piatkowski, 1995). When preying on fish the squid of the continental shelves prey on both pelagic and demersal fish while the off-shelf species prey largely on mesopelagics such as myctophids (see sections 2.3 and 5.5 above). The on-shelf species such as Illex argentinus, Todarodes pacificus, the Nototodarus spp. and the loliginids are therefore more likely to interact with groundfish stocks as predators than the more oceanic squids: Dosidicus gigas, Ommastrephes bartrarni and Martialia hyadesi. The close trophic relationship between members of the Illex genus and the hakes (Caddy and Rodhouse, 1998) means that the recruitment of each is likely to be influenced by the relative abundance of the other. In the Gulf of California Dosidicus gigas has been demonstrated to have a substantial impact on the abundance of California sardine when there are large migrations of the squid into the Gulf (Ehrhardt, 1991). The interrelationships between groundfish stocks, the squid stocks targeted by light fisheries and their prey deserve closer attention, especially in those areas where the interactions appear to be driving changes in ecosystem structure.

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DISCUSSION

Use of DMSP-OLS data has enabled the precise location of the distribution of the global light-fishing fleet over a 6 month period in relation to the large and general mesoscale oceanography of the ecological provinces where they occur. The squid catch in these light fisheries can be identified to genera or species in seven ecological provinces where DMSP-OLS imagery reveals light-fishing activities. In one instance, in the Southwest Atlantic, the location of vessels on one night could be determined in relation to the surface signature of a specific mesoscale feature on the Patagonian Shelf edge. The data provide a unique insight into the relations between oceanography and the squid fisheries and, by implication, the distribution of the target species under exploitation. Furthermore the DMSP-OLS data provide the information needed to review the relationship between the squid fisheries using lights and other fisheries for finfish with better spatial resolution than has been previously possible using data for FAO statistical areas alone (Caddy and Rodhouse, 1998). It is shown here that 62-70%, and possibly up to something <96%, of the world squid catch can be accounted for in the light fisheries identified in the images. This has provided the opportunity to be more specific about possible interactions between cephalopod fisheries and declining groundfish stocks and has allowed the hypothesis about the inverse relationship between the trends in these fisheries to be explored in more detail. The relationship between oceanography and the distribution of squid stocks, inferred from distribution of light-fishing fleets, differs between the squid families exploited by the fisheries. The light fisheries for ommastrephid squid are related to large-scale ocean current and upwelling systems. These are the high energy western boundary current systems of the North Pacific and South Atlantic in the case of T. pacificus and L argentinus, the equally high energy Antarctic Circumpolar Current system in the case of the Nototodarus spp. on the New Zealand Shelf and the low energy but very productive Peruvian coastal upwelling system in the case of D. gigas. In each situation the fisheries are generally associated with areas of high mesoscale activity that is generated by the interactions between the current systems and local bathymetry. The ommastrephid squid are powerful swimmers which exploit mesoscale oceanographic features such as eddies, core rings and streamers that are presumably areas of high prey availability (Sugimoto and Tameishi, 1992; Rodhouse et al., 1996a). Loliginid squid dominate many of the light fisheries in the DMSP-OLS images over continental shelves. They are therefore not generally related to the major geostrophic flow of the deep oceans but are nevertheless

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mostly linked to specific hydrographic features such as coastal upwelling systems off the California coast, and off the north coast of Taiwan and the Peng-Hu Islands. There is also a large light fishery on the shelf to the northeast of Taiwan where the Kuroshio Current flows in over the shelf and then loops back to the shelf edge (Figure 2). Three of the six ecological provinces where major concentrations of light-fishing vessels are located with DMSP-OLS imagery are areas where increasing catches of cephalopods have apparently coincided with overexploitation of groundfish stocks. In two of these Provinces the squid catch is dominated by loliginid squid, which are myopsids adapted for coastal/shelf ecosystems. Evidence that overexploitation of groundfish is implicated in the expansion of ommastrephid fisheries is less clear except in New Zealand where the fisheries for Nototodarus spp. are located over the shelf in areas where groundfish fisheries are also pursued and have been heavily exploited. The other ommastrephid fisheries are either located in areas dominated by fisheries for pelagic fish or are pursued off the shelf edge. Future research on possible interactions between cephalopod fisheries and finfish stocks might be most profitably pursued in the East China Sea, Sunda-Arafura Shelves and possibly New Zealand, areas identified here using DMSP-OLS data where the spatial distribution of the different fisheries overlap. It should be emphasized here that light-fishing vessels largely target squid and DMSP-OLS imagery does not locate net and trap fisheries for other cephalopods (cuttlefish and octopus) that may also be implicated in ecological change associated with overexploitation of groundfish stocks. The ability to visualize the spatial distribution of fishing fleets and their movements over time with DMSP-OLS data has implications for the assessment and management of the exploited squid stocks. Reports of catches by vessels according to statistical squares provides relatively low resolution spatial data which may obscure important detail such as whether vessels are targeting unusually high concentrations of squid at certain times as illustrated in Figure 8. Sampling on concentrations at migratory choke points, where migration routes narrow, or on spawning aggregations may cause assessments to be biased and fishing in these areas may have a disproportionate impact on the stock. DMSP-OLS images might in future provide the information needed to formulate special measures to regulate fishing at critical times and locations. Future collaborative research by the authors will use nightly images for detailed analysis of patterns and trends in light fisheries for squid. The DMSP-OLS images presented here raise questions about the effects of intensive light fishing on marine ecosystems. The impact of the global light fishery might be at least twofold. First, the effects of removals of the target species on predators and prey and the direct effect of the

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P.G. RODHOUSE, C. D. ELVIDGE AND R N. TRATHAN

lights themselves. In other respects jigging with lights is probably an "ecologically friendly" fishing method as there is virtually no by-catch and, by adjusting jig size, a specific size range of the target species can be selected. There is probably an approximately linear relationship between CPUE and stock size as the jiggers rely on lights to attract their quarry. This is in contrast to other pelagic fishing methods, such as purse seining, which allow high CPUE to be maintained with declining stock size because of the ability to search for and target individual shoals (Yatsu, pers. comm., 1999). In contrast to longliners there also seems to be little interaction between squid jiggers and seabirds (Gonzfilez and Rodhouse, 1998) although birds may be attracted to the fishing lights in foggy conditions. Finally, jigging with lights has no physical impact on the seabed in the way that bottom trawling does. The effects of removals by light fishing are probably no different from those in any other fishery except that, as mentioned above, by-catch of other, non-target, species is generally minimal. Given the reliance of some populations of squid predators, especially in high latitudes of the southern hemisphere, on the squid populations there is a continuing need to manage new fisheries in the context of the whole marine ecosystem. There are probably unique effects of light fishing on marine ecosystems caused by the lights themselves. Dense concentrations of high power fishing lights over extensive areas probably affect the behaviour of larvae, juveniles and adults of other forms of nekton including fish and unexploited species of cephalopod, zooplankton, and perhaps phytoplankton, as well as the larval, juvenile and pre-recruit phases of the cephalopod species under exploitation. It seems important to know what these effects might have on the functioning of marine ecosystems where light fishing takes place.

ACKNOWLEDGEMENTS We thank Prot~ C. C. Lu (Dept Zoology, National Chung Hsing University, Taichung, Taiwan) for interpreting the Chinese language papers cited here, Nguen Xuan Duc (Institute of Ecology and Biological Resources, National Centre for Natural Science and Technology, Nghiado, Tuliem, Hanoi, Vietnam) for information about the Vietnamese cephalopod fishery and Dr Akihiko Yatsu (National Research Institute of Fisheries Science Fisheries Agency of Japan, Fukuura 2-12, Kanazawa-ku, Yokohama 236-8648, Japan) for many helpful comments. We dedicate this review to the memory of Peter Prince and Martin White whose untimely deaths, in 1998 and 1999 respectively, brought a

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tragic end to 15 years of some of the most exciting collaborative research in marine biology. REFERENCES

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APPENDIX METHODS USED IN ANALYSIS AND INTERPRETATION OF DMSP-OLS DATA 1. Types of data and Images The analysis presented here uses three groups of DMSP-OLS data. The first is a single night sample in the South Atlantic collected on the 23 May 1995. In this image the fishing lights appear as white areas against a dark background. The second group of data is taken from a global composite image of fishing lights for the 6 month period October 1994-March 1995 collected during the dark half of each lunar cycle. To generate this composite, lights in cloud-free portions of each satellite pass were tallied in a grid. These counts were then divided by the total number of cloud-free observations in the grid cell and multiplied by 100. Depending on the area as many as 94 images and as few as 10 images were used depending on cloud cover. The 6 months of OLS data were thus compiled into one global image of lights where pixel's value represented the frequency of occurrence of a light in cloud-free imagery for that pixel. This global image was cropped at 6% to remove most of the noise and ephemeral light sources. Areas of light fishing activity were then manually "cut" from the global image. The final group of data was used to visualize

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small groups of fishing lights off Southern California, and comprised a world average radiance calibrated image generated by combining world individual radiance calibrated images from March 1996, and JanuaryFebruary 1997. Each pixel contained a DN value between 0 and 255. Values between 0 and 254 were converted to radiance values with the equation: Radiance

= D N (3/2) 1 0 - 1 ° W

cm -2 sr -1

~m -1.

The value 255 signified that no unsaturated pixels were found over that location for the duration of the reduced gain experiment.

2.

Use of a Geographical Information System (GIS)

Positional information and light values from the DMSP-OLS images were loaded into a marine Geographic Information System (GIS) established using Arc/Info 7.2 (ESRI) software (Trathan et al., 1993). The GIS included digital bathymetric contours (200 m and 1000 m) taken from the General Bathymetric Chart of the Oceans (GEBCO) Digital Atlas (Anon., 1997). DMSP images were loaded from binary files and established with a geographic coordinate system. The images were subsequently converted to a Mercator coordinate system for display and plotting. For plotting purposes, light values from the DMSP-OLS composite images were converted to a binary scale, that is, either no lights present (0), or some lights present (1). In these images the area lit by fishing lights is shown in yellow with a red outline so that small areas appear as red only.

Taxonomic Index

Acanthohaustorius miUsi 195 Acanthonotozoma 184 Acontiostoma 114 Aeginina longicornis 206 Agarum clathratum 40 Agelaius phoeniceus (red-winged blackbird) 45

Akerogammarus knipowitschi 195 Alaria 24, 26 Alicella gigantea 195 Almyracuma proximoculi 144, 217 Amathillina cristata 195 Amathillina spinosa 195 Amathimysis cherados 213 Amathimysis polita 213 Americamysis almyra 213, 215 Americamysis bahia 192, 213 Americamysis bigelowi 184, 213 Ammodramus maritimus (sea sparrow) 45

Ammodytes hexapterus 52, 56-7, 70, 72, 80

Ampelisca Ampelisca Ampelisca Ampelisca Ampelisca Ampelisca Ampelisca Ampelisca Ampelisca

abdita 195 araucana 195 brevicornis 195 diadema 195 macrocephala 195 sarsi 195 tenuicornis 195 typica 195 vadorum 195

Ampharetidae 36 Amphictenidae 36 Amphipoda 107, 157, 195-205 caprellids 157, 186, 187, 189, 206 gammarids 157, 186, 187, 189, 193, 195-205 hyperiids 157, 186, 187, 189, 207 Amphiporeia lawrenciana 196

Amphiporeia virginiana 152, 196 Amphithoe 151 Amphithoe lacertosa 196 Amphithoe longimana 196 Amphithoe rubricata 196 Amphithoe vaillante 196 Anaplopoma fimbria 279 Anatanais 160 Anchialina typica 175 Ancyananiscus 184 Angliera phreaticola 208 Anilocra physodes 129 Anisogammarus anandalei 110 Anonyx nugax 196 Anonyx sarsi 196 Anoplarchrus purpurescens (high cockscomb) 50

Antarctomysis maxima 213 Antarctomysis ohlini 143-4, 213 Antarcturus polaris 208 Antias unioramea 208 Antias uniramus 159 Anuropidae 157

Aphriza virgata (surf bird) 15, 64, 66, 68, 80

Apseudes 159 Apseudes hermaphroditicus 114, 122 Apseudes latreillei 125, 219 Apseudomorpha 159

Arachnomysis 161 Archeomysis 131,133 Archeomysis grebnitzki 123, 128 Arctic shanny see Stichaeus punctatus Arctocephalus forsteri 279 Arctocephalus gazella 281 Arctocephalus pusillus 282 Arctocephalus tropicalis 281 Arcturella sawayae 159, 208

306 Arcturidae 159 Arcturus 159 Arcturus longicornis 208 Arenaria interpres (ruddy turnstone) 66-7 Arenaria melanocephala (black tumstone) 15, 64, 66 Armadillidium 135 Armadillidium vulgate 109, 137, 139 Arrhis phyllonyx 196 AseUota 118, 119 AseUus 118 Asellus aquaticus 133, 138 Astacilla 159 Astacilla ceaca 159 Atyloella magellanica 196 Austrosignum maltinii 208

Bagatus algicola 208 Balanus glandula 26, 29 Balanus-Semibalanus spp. 18 bald eagle see Haliaetus leucocephalus barnacle see Balanus; Chthalamus Barrow's goldeneye see Bucephala islandica Bathycopea 176 Bathynomus 157 Bathynomus giganteus 127, 130, 185, 188, 208 Bathyporeia guilliamsoniana 196 Bathyporeia pelagica 170, 196 Bathyporeia pilosa 170, 196 Bathyporeia sarsi 196 bears see Ursus spp. Berryteuthis magister 273 black bear see Ursus americanus black oystercatcher see Haematopus bachmani black turnstone see Arenaria melanocephala black-legged kittiwake see Rissa tridactyla Bodotria scorpioides 217 Boreomysinae 160 Boreomysis arctica 213 Boreomysis nobilis 213 Bovallia gigantea 196 Bowmaniella floridana 213 Brachydiastylis resima 217 Brachyscelus crusculum 207 Brasilomysis casyroi 214

TAXONOMIC INDEX

brown algae see Fucus gardneri brown bear see Ursus arctus Bucephala 15, 17 Bucephala clangula (common goldeneye) 68 Bucephala islandica (Barrow's golden eye) 64-5, 68, 78, 80 Bumeralius buchalius 196 butter clam see Saxidomus giganteus Byblis japonicus 196 Caecidae 36 Calliopius laeviusculus 196, 197 Callorhinus ursinus 280 Campecopea 176 Campecopea hirsuta 208 Cancer magister (Dungeness crab) 17 capelin see Mallotus villosus Capitellidae 36 Caprella 206 Caprella advena 206 Caprella albifrons 125 Caprella bidentata 206 Caprella bispinosa 206 CapreUa christibrachium 206 Caprella danilevskii 206 Caprella decipiens 206 Caprella equilibra 125, 129 Caprella gorgonia 150, 206 Caprella kroyeri 206 Caprella laeviuscula 146, 206 Caprella monoceros 181, 206 Caprella mutica 206 Caprella okadai 206 Caprella penantis 206 Caprellidae 36 Caprellidea 157, 186, 187, 189, 206 Cardiophilus baeri 197 Casco bigelowi 197 Cepphus columba (pigeon guillemot) 57, 69-70, 77, 80 Ceratoseralis trilobitoides 208 Cerorhinca monocerata 280 Chaetogammarus hyrcanus 197 Chaetogammarus ischnus 197 Chaetogammarus marinus 197 Chaetogammarus palcidas 197 Chaetogammarus pauxillus 197 Chaetogammarus stoerensis 197 Chaetogammarus warpachowskyi 197 Cheirimedon femoratus 180, 197

TAXONOMIC INDEX

Cheirimedon fougneri 197 Chelura terebrans 197 Chiridotea 158 Chlamys rubida (scallop) 39 Chthalamus dalli (barnacle) 18, 24, 26, 29, 72, 78 Cirolana 157 Cirolana harfordi 208 Cirolana imposita 208 Cirolana parva 208 Cirolanidae 157 Cistothorus palustris (marsh wren) 45 Citharichthys stigmaeus 279 clam see Humilaria; Macoma; Mya; Protothaca; Saxidomus; Serripes; Yoldia Clangula hyemalis 15 Clinocardium nuttallii (cockle) 15 Clupea pallasi 52-4, 56-7, 68-70, 72, 77, 80 Clypeoniscus 184 cockle see Clinocardium nuttalii cod see Gadus macrocephalus Colidotea rostrata 208 Cololabis saira 267 Columotelson 118 cormorant see Phalacrocorax Corophiidae 36 Corophium 151 Corophium acherusicum 197 Corophium arenarium 197 Corophium bonnellii 197 Corophium chelicorne 197 Corophium curvispinum 197 Corophium insidiosum 197 Corophium lacustre 152, 197 Corophium nobile 197 Corophium robostum 197 Corophium triaenonyx 191 Corophium volulator 174, 197 Corvus caurinus (northwestern crow) 45, 46, 47-8, 71 crescent gunnels see Pholis laeta crow, northwestern see Corvus caurinus Cryptocope 160 Cuclopoapsuedes 159 Cumacea 107, 161, 186, 187, 189, 193, 217-19 Cumopsis goodsiri 217 cut-throat trout see Oncorhynchus

307

clarki Cyathura carinata 114, 144, 208 Cyathura polita 114 Cymodetta gambosa 146, 154 CymodoceUa 176 CymodoceUa acuta 208 Cymodocella tubicauda 208 Cymudasa compta 198 Cystisoma 157, 179 deer, Sitka black-tailed see Odocoileus

hemionus sitkensis Dermasterias imbricata (seastar) 32, 38, 41, 42 Deutella californica 206 Deutella penantis 206 Dexamine spinosa 198 Diastylis laevis 217 Diastylis lucifera 217 Diastylis polita 217 Diastylis quadrispinosa 217 Diastylis rathkei 152, 161, 217 Diastylis sculpta 217-18 Diastylis tumida 218 Diastyloides biplicata 218 Dikerogammarus aralensis 198 Dikerogammarus caspius 198 Dikerogammarus haemobaphes 198 Dikonophora 160 Dimorphostylis asiatica 152 Diogodias littoralis 198 Diomeda exulans 281 Dogielinotus loquax 198 Dolly Varden char see Salvelinus malma Dosidicus gigas 271, 277, 280, 283, 285, 288-9 drill see Nucella lameUosa Drosophila 165 Dungeness crab see Cancer magister Dyopedos monacanthus 198 Echinogammarus pirloti 198 Edotia 178 Edotia oclopetiolata 158 Edotia oculata 158, 178 Elasmopus levis 198 Elymus 43 Engraulis mordax 277 Enhydra lutris (sea otter) 15-17, 41-3, 60-2, 73, 76-7, 80, 280

308 Eogammarus confervicolus 147, 198 Eopsetta jordani 279 Erythrops serrata 214 Eucopia 160 Eucopia grimaldii 214 Eudorella emarginata 218 Eudorella pusiUa 218 EudoreUa truncatuta 218 Eudyptes chrysolophus 281 Eudyptes pachyrhynchus 279 Eudyptula minor (little penguin) 282 Eulimnogammarus obtusatus 198 Eumetopias jubatus (Steller sea lion) 62 Eunoyx chelatus 198 Eurycoipidae 159 Eurycope brevirostris 208 Eurycope cornuta 209 Eurydice 157, 178 Eurydice af-finis 157, 209 Eurydice longicornis 209 Eurydice natalensis 209 Eurydice pulchra 209 Eurymera monticulosa 198 Eurythenes gryllus 144, 157, 198 Eurythenes obesus 198 Eusirus perdentatus 198 Evasterias 42 Evasterias troschelii (seastar) 41 Excirolana 157, 178 Excirolana braziliensis 209 Excirolana chiltoni 155, 209 Excirolana japonica 157, 209 Excirolana kumari 157 Exoediceroides maculosus 199 Exoediceros fossor 199 Exosphaeroma truncatitelson 209 Flabellifera 157-8 flathead sole see Hippoglossoides elassodon Fucus gardneri 17-19, 23, 25, 26, 44, 72, 78 Fucus spp. 18-24, 28-9, 43, 52, 72 Fulmaris glacialis 280

Gadus macrocephalus (Pacific cod) 17, 49, 50, 53, 73 Galiteuthis glacialis 284 Gammaracanthus 188 Gammaracanthus caspius 199

TAXONOMIC INDEX

Gammaracanthus loricatus 199 Gammaridea 157, 186, 187, 189, 193, 195-205 Gammaropsis nitida 190, 199 Gammarus 145, 185, 188 Gammarus aequicauda 199 Gammarus angulosus 199 Gammarus chevreuxi 199 Gammarus crinicornis 199 Gammarus duebeni 112, 146, 148, 183, 199 Gammarus duebeni duebeni 113 Gammarus finmarchicus 199 Gammarus inaequicauda 199 Gammarus insensibilus 199 Gammarus lacustris 120 Gammarus lawrencianus 199 Gammarus locusta 199 Gammarus mucronatus 199-200 Gammarus obtusatus 200 Gammarus oceanicus 200 Gammarus olivii 200 Gammarus palustris 200 Gammarus pulex 131, 165, 170 Gammarus roeselii 165 Gammarus salinus 143, 200 Gammarus setosus 145, 200 Gammarus squamosa 200 Gammarus subtypicus 200 Gammarus tigrinus 200 Gammarus wilkitzii 200 Gammarus zaddachi 200 Gastrosaccinae 161 Gastrosaccus 161 Gastrosaccus lobatus 214 Gastrosaccus psammodytes 214 Gastrosaccus vulgaris 214 Gavia arctica 279 Genyonemus lineatus 279 glaucous gull see Larus glaucescens Globicephala macrorhynchus 279 Globicephala melaena 280--1,281 Gloiopeltis furcatis 18 Glyptonotus 188 Glyptonotus acutus 209 Glyptonotus antarcticus 158, 209 Gmelina brachyura 201 Gmelinopsis tuberculata 201 Gnathophausia 160 Gnathophausia gracilis 214 Gnathophausia ingens 214

TAXONOMIC INDEX

Gnathophausia longispina 214 Gnathophausia zoea 214 Gnorimosphaeroma insulare 209 Gnorimosphaeroma naktongense 114 Gnorimosphaeroma noblei 209 goldeneye see Bucephala Gonatus antarcticus 284 Gould's arrow squid see Nototodarus gouldi green sea urchin see Strongylocentrotus droebachiensis guillemot see Uria aalge gulls see Larus spp. Haematopus bachmani (black oystercatcher) 15-17, 64--6, 78, 80 hake see Merluccius hubbsi Haliaetus leucocephalus (bald eagle) 17, 45, 46, 71 Halosbaena acanthura 155, 175 Haplocope angusta 219 Haplomesus quadrispinosus 159, 209 harbour seal see Phoca vitulina Hargeria rapax 219 harlequin duck see Histrionicus histrionicus Haustoriodes japonicus 201 Haustorius arenarius 201 Haustorius canadensis 201 Haustorius saginatus 201 Helleria brevicornis 110 helmet crab see Telmessus cheiragonus Hemilamprops calfornica 175 Hemilamprops rosea 218 Hemimysis lamornae 214 herring see Clupea pallasi Heteromysis 160 Heteromysis armoricana 214 Heteromysis beetoni 214 Heteromysis filitelsona 214 Heteromysis formosa 214 Heteromysis tuberculospina 214 Heterotanais 151, 160 Heterotanais oerstedi 114, 148, 153-4, 219 Hexagrammos deeagrammus (kelp greenling) 48-9 Hexagrammos octogrammus (masked

309

greenling) 49 high cockscomb see Anoplarchrus purpurescens Hippoglossoides elassodon (flathead sole) 60 Hippoglossus stenolepsis 279 Hippomedon propinquus 201 Hippomedon whero 201 Hirondella gigas 201 Histioteuthis eltaninae 284 Histrionicus histrionicus (harlequin duck) 15, 17, 64-5, 67-8, 78, 80 Holmesimysis eostata 214 Humilaria kennerleyi (clam) 39 Hyale barbicornis 201 Hyale nilssoni 201 Hyale pugettensis 201 Hyalella azteca 150 Hyalella dentata 146 Hyperia galba 207 Hyperiidea 157, 186, 187, 189, 207 Hyperoche 182 Hyperoche medusarum 207 Hyperoodon planifrons 281 Iais pubescens 209 Idotea 29, 118, 185, 210 Idotea baltica 110, 158, 20%10 Idotea baltiea baltica 210 Idotea baltiea basteri 111, 139-40, 210 Idotea baltica tricuspidata 111 Idotea chelipes 210 Idotea granulosa 210 Idotea marginata 158 Idotea neglecta 146, 158, 210 Idotea ochotensis 210 Idotea pelagica 210 Idotea resecata 210 Idotea viridis 144, 158 Idoteidae 158 Illex argentinus 272-3, 280, 283-4, 286-9 Illex coindetii 274 Illex iUecebrosus 273-4 Indomysis annandalei 214 Iphigenella andrussowi 201 Iphinoe serrata 218 Iphinoe tenella 218 Iphinoe trispinosa 218 Isaeidae 36 Ischyromene 176

310 Isopoda 107, 157--60, 186, 187, 189, 193, 208-13 flabelliferids 157 valviferids 158 Istiophoridae 281 lsurus oxyrhincus 281

Jaera 29, 118, 154-5, 159 Jaera albifrons 110, 148, 154, 210 Jaera hopeana 155 Jaera ischiosetosa 210-11 Jaera italica 155 Jaera marina 154, 163, 211 Jaera nordmani 155, 211 Janira gracilis 211 Janira maculosa 211 Jassa 151 Jassa falcata 201 Jassa marmorata 116, 150, 201 KaUiapseudes 159 kelp greenling see Hexagrammos decagrammos killer whale see Orcinus Kogia breviceps 281 Lacunidae 36 Lagenorhynchus obliquidens 280 Laminaria bongardiana 40 Laminaria saccharina 40 Lampropidae 116 Lamprops 115 Lamprops fasciata 148, 218 Lamprops quadrispinosa 218 Larus 17 Larus californicus 280 Larus canus (mew gull) 47, 280 Larus glaucescens (glaucous gull) 47, 64, 67, 280 Larus heermanni 280 Lembos 151 Lembos websteri 190, 201 Lepidactylus dytiscus 201 Lepidepecreum cingulatum 202 Lepidomysidae 160 Leptocheirus pilosus 202 Leptocheirus pinguis 182 Leptochelia dubia 219 Leptochelia savigngi 219 Leptognathia brevimanus 219 Leptognathia breviremis 219

TAXONOMIC INDEX

Leptomysis apiops 214 Leptomysis gracilis 214 Leptomysis lingvura 214 Leptostylis longimana 218 Leucon jonesi 161, 218 Leucon nasica 218 Leucon profundus 218 Leuconidae 116 Leucothoe spinicarpa 182 Leuroleberis zeylandica 202 Ligia 136 Ligia exotica 120, 122, 127, 168 Limnoria lignorum 169 Limnoria 119, 122, 157 Limnoria andrewsi 211 Limnoria lignorum 157, 169, 211 Limnoria tripunctata 151, 211 Limnoriidae 157 limpet see Tectura persona littleneck clam see Protothaca staminea Littorina scutulata 18, 28 Littorina sitkana 18, 24, 28 Loligo (squid) 267-8, 274, 276, 279, 282, 289 Loligo chinensis 267, 269, 279, 289 Loligo duvauceli 269, 274 Loligo forbesi 274 Loligo gahi 272, 285 Loligo opalescens 270-1, 279, 289 Loligo pealei 274 Loligo plei 274 Loligo reynaudi 274 Loligo singhalensis 274 Loligo vulgaris 274 Loliguncula brevis 274 Lophogaster 160 Lophogaster typicus 214-5 Lophogastrida 160 Lumbrineridae 36 Lutra canadensis (river otter) 17, 61-2, 72 Lyaea pulex 207 Macoma (clam) 39 Macronectes giganteus 281 Macronectes halli 281 Maldanidae 36 Mallotus villosus (capelin) 52, 70, 72, 80 Mancocuma stellifera 152, 218

TAXONOMIC INDEX

Marinogammarus marinus 202 Marinogammarus obtusatus 202 Marinogammarus stoerensis 202 marsh wren see Cistothorus palustris Martialia hyadesi 272, 274, 283-6, 288-9 masked greenling see Hexagrammos octogrammus Megadyptes antipodes 279 Melanitta perspicillata (surf scoter) 15, 17, 64, 80 Melanitta (scoter) 15 Melita appendiculata 202 Melita nitida 202 Melita palmata 202 Melita pellucida 202 Melita zeylandica 143, 202 merganser see Mergus Mergus merganser (merganser) 69 Mergus serrator (red-breasted merganser) 69 Merluccius hubbsi (hake) 277, 280, 283 Merluccius polylepis 277 Mesidotea entomon 211 Mesopodopsis orientalis 117, 120--1, 140, 188, 215 Mesopodopsis slabberi 215 Metaleptamphopus pectinatus 202 Metamysidopsis elongata 151, 215 Metamysidopsis swifti 215 Metapseudes 159 mew gull see Larus canus Microdeutopus 151 Microdeutopus danmoniensis 202 Microdeutopus gryllotalpa 151, 202 Micromesistius australis 277 Mictacea 107 Mirounga angustirostris 280 Mirounga leonina 281 Monoculodes edwardsi 202 Monoculodes gibbosus 202 Monoculodes packardi 203 Moroteuthis knipovitchi 284 Munnopsis typica 211 Munnopsurus atlanticus 211 murre see Uria aalge Musculus 32, 37, 49, 52-3, 73 mussel see Musculus; Mytilus Mya arenaria (clam) 39 Mysida 160, 213-17

311

Mysidacea 107, 160-1, 186 Mysidae 160 Mysidella 124 Mysidetes posthon 215 Mysidium columbiae 170, 215 Mysidium integrum 215 Mysidopsis 161, 188, 190 Mysidopsis didelphys 215 Mysidopsis gibbosa 215 Mysinae 160 Mysis litoralis 215 Mysis mixta 215 Mysis oculata 117 Mysis relicta 215 Mysis stenolepis 215 Mysticotalitrus 184, 190 Mytilidae 36 Mytilus edulis (blue mussel) 13, 18, 29 Mytilus trossulus (west coast mussel) 13, 15, 18

Naesa bicentata 110, 180, 211 Neasticilla 159 Neohaustorius biarticulatus 203 Neohaustorius schmitzi 203 Neomysis 131 Neomysis awatschensis 123, 128 Neomysis integer 215, 216 Neomysis japonica 117 neon flying squid see Ommastrephes bartrami Neotanais 160 Nereidae 36 Nereocystis 52 Nereocystis (kelp) 52 Nereocystis leutkeana 40 Nerocula 135 Niphargoides derzhavini 203 Niphargoides grimmi 203 Nototodarus 270, 279, 288 Nototodarus gouldi (Gould's arrow squid) 269-70, 279, 282-3, 289 Nototodarus sloanii (Wellington flying squid) 269-70, 279, 282, 283, 289 Nototropis guttatus 203 Nucella lamellosa 24, 274, 30, 73 Nuculana 39 Octopus vulgaris 278 Octosporea effeminaus 113-14

312

Odocoileus hemionus sitkensis (Sitka black-tailed deer) 17, 43--4 Oediceros saginatus 203 oldsquaw see Clangula hyemalis Olividae 36 Ommastrephes bartrami (neon flying squid) 266-7, 273--4, 276, 279, 282-3, 288-9 Oncorhynchus clarki (cut-throat trout) 17, 59 Oncorhynchus gorbuscha (pink salmon) 17, 52, 55-7, 58-9, 74, 78 Oncorhynchus keta (chum salmon) 58 Oncorhynchus kisutch (coho salmon) 279 Oncorhynchus tshawytscha (Chinook salmon) 279 Onsimus lotoralis 203 Opheliidae 36 Ophiuroidea 36 Opiodon elongatus 279 Orchestia 129, 147, 184, 190 Orchestia bottae 203 Orchestia cavimana 110, 125, 165-7 Orchestia gamrnarella 109-10, 112, 126-7, 132, 137-42, 144-5, 147, 203 Orchestia mediterranea 125 Orchestia montagui 109 Orchestia platensis 146, 185, 203 Orchestia scutigerula 203 Orchomene cavimanus 203 Orchomene gerulicorbis 203 Orchomene nanus 203 Orchomene plebs 203 Orchomene rossi 203 Orchomenella minuta 203 Orchomenella pinguis 203 Orchomenella proxima 204 Orcinus orca (killer whale) 63 otter see Enhydra lutris; Lutra canadensis Oxyurostylis smithi 218 oystercatcher see Haematopus bachmani Pacific cod see Gadus macrocephalus Pacific herring see Clupea pallasi Pacific saury see Cololabis saira Pagirapseudes largoensis 219

TAXONOMIC INDEX

Pagrus pagrus 280 Pallasiella quadrispinosa 204 Pancolus 160 Pandalus (shrimp) 17 Paracerceis sculpta 111, 153, 212 Paragnathia formica 153 Parahaustorius longimerus 204 Paraleptosphaeroma glynii 212 Paramarteilia orchestiae 112 Paramesopodopsis rufa 216 Paramoera mohri 204 Paramoera walkeri 204 Pararnysis arenosa 216 Pararnysis bacescoi 216 Pararnysis bahamensis 216 Paramysis nouveli 216 Paranthura 122 Parapseudes 159 Parasellota 159 Parathemisto 181, 182 Parathemisto gaudichaudi 121, 154, 169, 207 Parathemisto gracilipes 207 Parathemisto japonica 207 Parathemisto pacifica 207 Parharpinia rotundifrons 204 Parhyalella basrensis 204 Parhyalella roperi 204 Parvimysis bahamensis 161 Patuki roperi 204 Pectenogammarus longimanus 204 Pectenogammarus planicrurus 204 Pendanthura tanaiformis 212 Pentidotea 158 Peracarida 105-260 Peramphithoe stypotrupetes 151 Perioculodes longimanus 204 periwinkles see Littorina spp. Petalophthalmidae 160 Phalacrocorax pelagicus (cormorant) 69 Phalocrocorax pencillatus 279 Phobetria palpebrata 281 Phoca vitulina 60-3, 72, 76-7, 80 Phocaena phocaena 280 Phocarctos hookeri 279 Pholis laeta 48-9 Phoxocephalidae 36 Phronima 121, 182-3 Phronima atlantica 207 Phronima sedentaria 207

TAXONOMIC INDEX

Phthisica marina 175 Physeter catodon 280, 281 Physeter macrocephalus 281 pigeon guillemot see Cepphus columba Plectospira 184 Pleuronechthys decurrens 279 Pleuronectes asper (yellowfin sole) 58--60 Pleuronectes bilineatus (rock sole) 58-60 Pleuroprion 159 Polychaeta 36 Polycheria antarctica 204 Polynoidae 36 Polyprion americanus 280, 283 Pomatomus saltatrix 280 Pontocrates altamarinus 204 Pontocrates arcticus 204 Pontocrates arenarius 204 Pontogammarus crassus 204 Pontogammarus maeoticus 204 Pontogammarus robustoides 204 Pontogammarus subnudus 204 Pontogeloides latipes 212 Pontogeneia inermis 204 Pontogeniella brevicornis 204 Pontoporeia 143 Pontoporeia affinis 204 Pontoporeia femorata 204 Pontoporeia microphthalma 205 Porcellio dilatatus dilatatus 110 Porcellio scaber 127 Porichthys notatus 279 Praunus flexuosus 123, 126-7, 129, 131, 133, 148, 151, 184, 190, 216 Praunus inermis 128-31, 134, 190, 216 prickleback see Stichaeus Primno abyssalis 207 Primno evansi 207 Primno johnsoni 207 Prionace glauca 279 Procellaria aequinoctialis 281 Procellaria parkinsoni (Parkinson's petrel) 282 Prodajus bigelowiensis 184 Proleptomysis rubra 216 Prostebbingia gracilis 205 Protohaustorius deichmannae 205 Protophoxus australis 205

313

Protothaca staminea (littleneck clam) 15, 31-2, 39 Psammokalliapseudes 159 Psammonyx nobilis 205 Psammonyx terranovae 205 Pseudidothea bonneri 158 Pseudidothea scultatus 158 Pseudinciola obliquua 205 Pseudocuma longicorne 116 Pseudocuma longicornis 218 Pseudojaera 118 Pseudojaera investigatoris 118 Pseudolana cocinna 212 Pseudolana towrae 193, 212 Pseudorchestoidea brasiliensis 205 Pseudotanais 160 Pseudotanais forcipes 175 Ptilanthura tenuis 114 Puffinus creatopus 280 Puffinus griseus 279 Puffinus tenuirostrus 280 Pycnopodia helianthoides (sunflower star) 38, 41 razor clam see Siliqua patula red-breasted merganser see Mergus serrator red-winged blackbird see Agelaius phoeniceus Rhabdosoma 108, 157 Rhabdosoma brevicaudatum 207 Rhabdosoma whitei 183, 207 Rhepoxynius abronius 205 Rhopalophthalmus terranatalis 216 Rissa tridactyla (black-legged kittiwake) 69-70, 280 river otter see Lutra canadensis rock sole see Pleuronectes bilineatus rockfish see Sebastes ruddy turnstone see Arenaria interpres rye grass see Elymus Sabellidae 36 Saduria entomon 119, 120-1,126-7, 133, 136-7, 139, 158, 212 salmon Chinook see Oncorhynchus tshawytscha chum see Oncorhynchus keta coho see Oncorhynchus kisutch pink see Oncorhynchus gorbuscha

314 Salvelinus malma (Dolly Varden char) 17, 58-9, 59 sand hopper see Talitrus saltator sand lance see Ammodytes hexapterus Sardinops melanostitictus 276 Sardinops sagax caeruleus 277 saury see Cololabis saira Saxidomus giganteus (butter clam) 15, 31-2, 39 scallop see Chlamys rubida Schistomysis kervillei 187, 216 Schistomysis ornata 216 Schistomysis spiritus 216 Scolopostoma 114 scorer see Melanitta sea otter see Enhydra lutris seal, harbour see Phoca vitulina seaside sparrow see Ammodramus maritimus seastar see Dermasterias; Evasterias Sebastes (rock fish) 17, 279 Semibalanus balanoides 26, 29 Septioteuthis lessoniana 274 Serolidae 158 Serolis cornuta 212 Serolis polita 212 Serolis tropica 212 Serripes groenlandicus (clam) 39 shrimp see Pandalus Sigalionidae 36 Siliqua patula (razor clam) 15 Siriella armatai 142 SirieUa chierchiae 217 Siriella clausii 217 Sitka black-tailed deer see Odocoileus hemionus sitkensis sole see Hippoglossoides; Pleuronectes Spartina 43 Spelaemysis longipes 127 Spelaeogriphacea 107, 171 Sphaeroma 119, 128, 178 Sphaeroma hookera 212 Sphaeroma quadridentatum 213 Sphaeroma rugicauda 152, 177, 212 Sphaeroma serratum 155, 178, 213 Sphaeromatidae 158 Sphaeronella 184 Spheniscus magellanicus 281 Sphyrapus 159 Sphyrna lewini 280

TAXONOMIC INDEX

Spilocuma salomani 218 Spilocuma watlingi 218 Spionidae 36 Spirobidae 36 squid see Loligo; Nototodarus; Ommastrephes Stegocephaloides christianiensis 205 Stegocephalus inflatus 114, 205 Steller sea lion see Eumetopias jubatus Stenetrium 118 Stenogammarus compressus 205 Stenogammarus kereuschui 205 Stenogammarus macrurus 205 Stenogammarus similis 205 Sthenoteuthis oualaniensis 274 Stichaeus (prickleback) 48-9 Stichaeus punctatus (Arctic shanny) 49-51 Stomacontion 114 Storthyngura birsteini 213 Strongylocentrotus droebachiensis 41, 73, 77 Stygiomysidae 160 sunflower star see Pycnopodia helianthoides surf bird see Aphriza virgata surf scoter see Melanitta perspicillata Syllidae 36 Synapseudes 159 Talitrus saltator (sand hopper) 109, 125-6, 145, 156, 185, 205 Talorchestia margaritae 205 Talorchestia martensii 205 Tanaidacea 107, 159, 186, 187, 189, 193, 219 Tanais 151, 160 Tanais dulongi 176, 180-1 Tecticeps ]aponicus 110 Tectura persona (limpet) 24, 26, 72 Tellinidae 36 Telmessus 32, 41, 42, 49, 52 Telmessus cheiragonus (helmet crab) 37, 37-8, 41 Tenagomysis macropsis 217 Tenagomysis tasmaniae 217 Thalassarche chrysostoma 281,286 Thalassarche melanophrys 281 Thelohamia hereditaria 113

315

TAXONOMIC INDEX

Theragra chalcogramma (walleye pollock) 60 Thermosbaena 172 Thermosbaena mirabilis 118, 120, 122, 156 Thermosbaenacea 107, 161 Tholozodium ocellatum 213 Thunnus alalunga 281 Thunnus albacares 280, 281 Thunnus obesus 280, 281, 283 Tmetonyx 205 Todarodes pacificus 264, 267, 273, 276, 279, 283, 288-9 Todarodes sagittatus 274 Trichiurus lepturus 280 Trichophoxus epistomus 205 Trochidae 36 Tryphosella kergueleni 205 Typhlotanais 160, 182 Typhlotanais brevicornis 219 Typhlotanais magnifica 160, 182, 219 Uhlorchestia spartinophila 205 Uria 69-70 Uria aalge (murre) 76, 280 Urohaustorius metungi 205 Urothoe brevicornis 205 Ursus americanus (black bear) 15, 17, 43-4

Ursus arctus (brown bear) 15, 17, 43-4 Valvifera 158 Vibalia armata 207 Vibalia propinqua 207 walleye pollock see Theragra chalcogramma Wellington flying squid see Notodarus sloanii west coast mussel see Mytilus trossulus Westwoodilla caecula 205 whale killer whale see Orcinus sperm whale see Physeter catodon whelk see Nucella lamellosa Xenarcturus 159 Xiphius gladius 281, 283 Xiphocephalus whitei 183, 207 yellowfin sole see Pleuronectes asper Yoldia 39 Zalophus californianus 280 Zernovia volgens& 205 Zostera marina 34-5