Advances in Marine Biology, Volume 54

Advances in MARINE BIOLOGY Series Editor

DAVID W. SIMS Marine Biological Association of the United Kingdom, The Laboratory Citadel Hill, Plymouth, United Kingdom Editors Emeritus

LEE A. FUIMAN University of Texas at Austin

CRAIG M. YOUNG Oregon Institute of Marine Biology Advisory Editorial Board

ANDREW J. GOODAY Southampton Oceanography Centre

GRAEME C. HAYS University of Wales Swansea

SANDRA E. SHUMWAY University of Connecticut

ROBERT B. WHITLATCH University of Connecticut

Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands Linacre House, Jordan Hill, Oxford OX2 8DP, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA First edition 2008 Copyright # 2008 Elsevier Ltd. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher. Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://www.elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. ISBN: 978-0-12-374351-0 ISSN: 0065-2881 For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in UK 08 09 10 11 12

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CONTRIBUTORS TO VOLUME 54

Kenneth W. Able Marine Field Station, Institute of Marine and Coastal Sciences, Rutgers University, Tuckerton, New Jersey 08087 Christin Frieswyk DeJong Arboretum and Botany Department, University of Wisconsin-Madison, Madison, Wisconsin 53711 Bridget S. Green Marine Research Laboratory, Tasmanian Fisheries and Aquaculture Institute, University of Tasmania, Private Bag 49, Tasmania, 7001 Australia Charles H. Peterson Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557 Michael F. Piehler Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557 Charles A. Simenstad School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington 98195 David W. Sims Marine Biology and Ecology Research Centre, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United Kingdom Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, United Kingdom Victoria J. Wearmouth Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, United Kingdom Joy B. Zedler Arboretum and Botany Department, University of Wisconsin-Madison, Madison, Wisconsin 53711

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Volume 30, 1994. Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambshead, P. J. D., Pfannku¨che, O., Soltweddel, T. and Vanreusel, A. Meiobenthos of the deep Northeast Atlantic. pp. 1–88. Brown, A. C. and Odendaal, F. 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. Gardner, J. P. A. Hybridization in the sea. pp. 1–78. Egloff, D. A., Fofonoff, P. W. and Onbe´, T. Reproductive behaviour of marine cladocerans. pp. 79–167. Dower, J. F., Miller, T. J. and Leggett, W. C. The role of microscale turbulence in the feeding ecology of larval fish. pp. 169–220. Brown, B. E. Adaptations of reef corals to physical environmental stress. pp. 221–299. Richardson, K. Harmful or exceptional phytoplankton blooms in the marine ecosystem. pp. 301–385. Volume 32, 1997. Vinogradov, M. E. Some problems of vertical distribution of mesoand 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. 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. Goniatid 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. *The full list of contents for volumes 1–37 can be found in volume 38.

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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 pollock, Theragra chalcogramma. pp. 179–255. Volume 38, 2000. Blaxter, J. H. S. The enhancement of marine fish stocks. pp. 1–54. Bergstro¨m, B. I. The biology of Pandalus. pp. 55–245. Volume 39, 2001. Peterson, C. H. The ‘‘Exxon Valdez’’ oil spill in Alaska: acute indirect and chronic effects on the ecosystem. pp. 1–103. Johnson, W. S., Stevens, M. and Watling, L. Reproduction and development of marine peracaridans. pp. 105–260.

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Rodhouse, P. G., Elvidge, C. D. and Trathan, P. N. Remote sensing of the global light-fishing fleet: an analysis of interactions with oceanography, other fisheries and predators. pp. 261–303. Volume 40, 2001. Hemmingsen, W. and MacKenzie, K. The parasite fauna of the Atlantic cod, Gadus morhua L. pp. 1–80. Kathiresan, K. and Bingham, B. L. Biology of mangroves and mangrove ecosystems. pp. 81–251. Zaccone, G., Kapoor, B. G., Fasulo, S. and Ainis, L. Structural, histochemical and functional aspects of the epidermis of fishes. pp. 253–348. Volume 41, 2001. Whitfield, M. Interactions between phytoplankton and trace metals in the ocean. pp. 1–128. Hamel, J.-F., Conand, C., Pawson, D. L. and Mercier, A. The sea cucumber Holothuria scabra (Holothuroidea: Echinodermata): its biology and exploitation as beche-de-Mer. pp. 129–223. Volume 42, 2002. Zardus, J. D. Protobranch bivalves. pp. 1–65. Mikkelsen, P. M. Shelled opisthobranchs. pp. 67–136. Reynolds, P. D. The Scaphopoda. pp. 137–236. Harasewych, M. G. Pleurotomarioidean gastropods. pp. 237–294. Volume 43, 2002. Rohde, K. Ecology and biogeography of marine parasites. pp. 1–86. Ramirez Llodra, E. Fecundity and life-history strategies in marine invertebrates. pp. 87–170. Brierley, A. S. and Thomas, D. N. Ecology of southern ocean pack ice. pp. 171–276. Hedley, J. D. and Mumby, P. J. Biological and remote sensing perspectives of pigmentation in coral reef organisms. pp. 277–317. Volume 44, 2003. Hirst, A. G., Roff, J. C. and Lampitt, R. S. A synthesis of growth rates in epipelagic invertebrate zooplankton. pp. 3–142. Boletzky, S. von. Biology of early life stages in cephalopod molluscs. pp. 143–203. Pittman, S. J. and McAlpine, C. A. Movements of marine fish and decapod crustaceans: process, theory and application. pp. 205–294. Cutts, C. J. Culture of harpacticoid copepods: potential as live feed for rearing marine fish. pp. 295–315.

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Volume 45, 2003. Cumulative Taxonomic and Subject Index. Volume 46, 2003. Gooday, A. J. Benthic foraminifera (Protista) as tools in deep-water palaeoceanography: environmental influences on faunal characteristics. pp. 1–90. Subramoniam, T. and Gunamalai, V. Breeding biology of the intertidal sand crab, Emerita (Decapoda: Anomura). pp. 91–182 Coles, S. L. and Brown, B. E. Coral bleaching—capacity for acclimatization and adaptation. pp. 183–223. Dalsgaard J., St. John M., Kattner G., Mu¨ller-Navarra D. and Hagen W. Fatty acid trophic markers in the pelagic marine environment. pp. 225–340. Volume 47, 2004. Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M. A., Halliday, N. C., Harris, R. P., Leaper, R., Mieszkowska, N., Pingree, R. D., Richardson, A. J., Sims, D.W., Smith, T., Walne, A. W. and Hawkins, S. J. Long-term oceanographic and ecological research in the western English Channel. pp. 1–105. Queiroga, H. and Blanton, J. Interactions between behaviour and physical forcing in the control of horizontal transport of decapod crustacean larvae. pp. 107–214. Braithwaite, R. A. and McEvoy, L. A. Marine biofouling on fish farms and its remediation. pp. 215–252. Frangoulis, C., Christou, E. D. and Hecq, J. H. Comparison of marine copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen cycles. pp. 253–309. Volume 48, 2005. Canfield, D. E., Kristensen, E. and Thamdrup, B. Aquatic Geomicrobiology. pp. 1–599. Volume 49, 2005. Bell, J. D., Rothlisberg, P. C., Munro, J. L., Loneragan, N. R., Nash, W. J., Ward, R. D. and Andrew, N. L. Restocking and stock enhancement of marine invertebrate fisheries. pp. 1–358. Volume 50, 2006. Lewis, J. B. Biology and ecology of the hydrocoral Millepora on coral reefs. pp. 1–55.

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Harborne, A. R., Mumby, P. J., Micheli, F., Perry, C. T., Dahlgren, C. P., Holmes, K. E., and Brumbaugh, D. R. The functional value of Caribbean coral reef, seagrass and mangrove habitats to ecosystem processes. pp. 57–189. Collins, M. A. and Rodhouse, P. G. K. Southern ocean cephalopods. pp. 191–265. Tarasov, V. G. EVects of shallow-water hydrothermal venting on biological communities of coastal marine ecosystems of the western Pacific. pp. 267–410. Volume 51, 2006. Elena Guijarro Garcia. The fishery for Iceland scallop (Chlamys islandica) in the Northeast Atlantic. pp. 1–55. JeVrey, M. Leis. Are larvae of demersal fishes plankton or nekton? pp. 57–141. John C. Montgomery, Andrew Jeffs, Stephen D. Simpson, Mark Meekan and Chris Tindle. Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. pp. 143–196. Carolin E. Arndt and Kerrie M. Swadling. Crustacea in Arctic and Antarctic sea ice: Distribution, diet and life history strategies. pp. 197–315. Volume 52, 2007. Leys, S. P., Mackie, G. O. and Reiswig, H. M. The Biology of Glass Sponges. pp. 1–145. Garcia E. G. The Northern Shrimp (Pandalus borealis) Offshore Fishery in the Northeast Atlantic. pp. 147–266. Fraser K. P. P. and Rogers A. D. Protein Metabolism in Marine Animals: The underlying Mechanism of Growth. pp. 267–362. Volume 53, 2008. Dustin J. Marshall and Michael J. Keough. The Evolutionary Ecology of Offspring Size in Marine Invertebrates. pp. 1–60. Kerry A. Naish, Joseph E. Taylor III, Phillip S. Levin, Thomas P. Quinn, James R. Winton, Daniel Huppert, and Ray Hilborn. An Evaluation of the Effects of Conservation and Fishery Enhancement Hatcheries on Wild Populations of Salmon. pp. 61–194. Shannon Gowans, Bernd Wu¨rsig, and Leszek Karczmarski. The Social Structure and Strategies of Delphinids: Predictions Based on an Ecological Framework. pp. 195–294.

Professor Alan James Southward, B.Sc, Ph.D, D.Sc, F.L.S., 1928–2007

Photo credit: G. Braasch, with permission

Obituary Stephen Hawkins*,† and David Sims*,‡

With the death of Professor Alan Southward aged 79 on 27 October 2007, Advances in Marine Biology lost a greatly respected past editor of 20 years standing, and science lost one of the most influential British marine biologists of the past 50 years. Taking over as editor of Advances in Marine Biology in 1986 following the passing away of Founder Editor Sir Frederick S. Russell F.R.S., he brought an incredibly broad and deep knowledge of marine biology to his editorial role as well as the gift of a lucid writing style. This ensured the production of high-quality reviews of lasting importance and in so doing he helped a great many scientists along the way. Alan Southward was one of the leading marine biologists of the second half of the twentieth century. He conducted seminal research in many areas of marine ecology, principally studying how organisms are impacted by environmental changes such as climate and pollution, and how they are adapted to life on the rocky shore and in the deep sea. He was also a world expert on barnacle taxonomy. Most notably perhaps, between the 1950s and 1970s, when climate change research was still in its infancy, he demonstrated important links between climate and biological changes in the sea, work that laid the foundations for all subsequent studies worldwide.

Early years Alan was born in Liverpool on 17 April 1928. His father, a fitter, was involved in traditional Merseyside industries such as Cunard, eventually working at the Meccano factory. In his early teens he became profoundly deaf as a consequence of meningitis but had already become interested in marine organisms from excursions along the shores of the Mersey. He grew up during the war attending Liverpool Collegiate School before entering the University of Liverpool. Getting into University was a major * {

{

Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, United Kingdom College of Natural Sciences, Memorial Building, Bangor University, Gwynedd LL57 2UW, United Kingdom School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United Kingdom

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achievement for a deaf student, especially during times when there were fewer opportunities for people with disabilities. By the time Alan was in Part II and Honours he had a circle of friends who took notes for him whilst he concentrated on drawing the blackboard diagrams. Clearly this strategy worked: the University of Liverpool awarded him a First Class Honours degree in Zoology in 1948. During his undergraduate years at Liverpool he naturally attached himself to the school of marine biologists under Professor J. H. Orton F.R.S., and under his direction carried out vacation research on coelenterates. On the advice of Orton he submitted his first scientific paper on jellyfish feeding and excretory currents to Nature (Southward, 1949). Many were to follow. In total he produced over 220 publications, some 21 of which were in Nature, an unusually high number for an ecologist. Alan first encountered the University of Liverpool’s Marine Biological Station (then part of Zoology) at Port Erin whilst attending field courses. When he first went there electric light had not been installed. This did not put him off, however, and he returned for Ph.D. studies and then stayed for a University Post Doctoral Fellowship. His Ph.D. work on the intertidal ecology around the south of the Isle of Man was with the guidance of Professor Orton, including both rocky and depositing shores. The breadth and scope of his Ph.D. was impressive, introducing him to ideas of quantitative ecology, species interactions, geographical distribution, effects of climate change and time series studies. Whilst doing this work he managed to find time to add to records for the Isle of Man fauna. He also got seriously involved in photography—a life-long passion (e.g. Southward et al., 1976). Much of this early work was published in journals such as Transactions of the Liverpool Biological Society which denied it a wider audience (Southward, 1953a,b)—but it was an invaluable first step for scores of subsequent Ph.D. studies at Port Erin. These studies, along with those of Jones, Burrows and Lodge, were some of the first field experimental studies on rocky shores, pioneering an approach which has contributed hugely to ecological theory (reviewed in Southward, 1964a). Alan concentrated largely on rocky shores during his Fellowship. This involved biogeographic mapping of the major species of British and Irish shores, laboratory experiments on the causes of these patterns, completion and write up of Orton’s work on limpet reproduction and follow up work on the limpet removal experiments of the late 1940s at Port Erin. Much of the travel for this biogeographic fieldwork was done on a motorcycle balanced using sight cues only—intrepid as well as pioneering work. During this period a long-standing collaboration was started with Professor Dennis Crisp F.R.S. leading to some of the first papers on the influence of climate on the outcome of competitive interactions in barnacles. It was his discovery of the occurrence of the warm water barnacle Chthamalus in the Isle of Man (Southward, 1950) that triggered much of his later work, including

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broad surveys of distribution and studies of the effects of climate change that were very much ahead of their time (e.g. Southward, 1951; Southward and Crisp 1952, 1954; for an overview, see Southward et al., 1995). Indeed, the combination of field surveys, quantitative experiments and long-term studies, incorporating new methods and analyses were to typify his leading-edge research for the next 50 years. Whilst on the Isle of Man Alan met Eve Judges. Whether on a pillion of a motorcycle, on the shore or at sea, Eve has been a science collaborator and source of great support to Alan over the years. Theirs was an almost symbiotic relationship, as Eve was often Alan’s interface with the spoken word. She is also a fine scientist of international reputation in her own right, an expert on polychaetes, Pogonophora and an equal partner in the work on hydrothermal vents and chemosynthetic nutrition of animals (e.g. Southward and Southward, 1958, 1967, 1968; Southward et al., 1981, 2001).

Long-term studies at Plymouth Alan moved to Plymouth in 1953 when he took up a DSIR Fellowship at the Laboratory of the Marine Biological Association (MBA), marrying Eve soon after arriving. He remained working at the MBA for the rest of his life. Throughout the 1950s Alan consolidated his reputation in the ecology of shore animals, completing much of the biogeographic work (Southward and Crisp, 1956; Crisp and Southward, 1958), testing temperature tolerances (Southward, 1958a), undertaking laboratory studies of barnacle feeding behaviour (Southward, 1955a,b,c) and, in 1958, writing a highly influential review on zonation of rocky shores (Southward, 1958b). Under the stimulus of Sir Frederick Russell F.R.S. his energies were directed offshore: he took over responsibility for the zooplankton and young fish surveys as part of the MBA long-term study of the English Channel, which stretched back to the start of the twentieth century. He had realised the importance of climatic fluctuations as the most likely explanation for the inconsistency of the English Channel ecosystem, especially given that many species reached their biogeographic limits in the South and South-West of England (Southward, 1960, 1963). Within this programme he incorporated studies of intertidal barnacles as indicators of climate change (Southward, 1967). Interestingly, the barnacle biogeographic work carried out in the UK and overseas led to the discovery that there were two species of barnacles in Europe masquerading under the name of Chthamalus stellatus (Southward, 1964b, 1976), given to them by Darwin. He was awarded his D.Sc. from the University of Liverpool in the early 1960s. He gained much satisfaction from the presence on the platform of the degree ceremony of a former Dean, who a decade earlier had not been

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convinced about the wisdom of admitting a deaf student to the university. With a larger research ship at the MBA capable of working the continental slope, interests offshore and in deep water were developed in the 1950s and 1960s in liaison with Eve. It was the intention to study what appeared to be a barnacle zone at 1200 m close to cold-water reefs in the deep water of the Bay of Biscay. However, poor offshore position finding in those pre-GPS days resulted in many hauls of mud instead of the rock and coral expected. But in those hauls were the first pogonophoran tube-worms found in the Atlantic at the time (Southward, 1958c; Southward and Southward 1958). Together, they started working on the gutless pogonophoran worms that in the past had probably been thrown back over the side as ‘gubbins’. The very cold winter of 1962/63 and a switch back to colder conditions prompted continuation of long-term studies on the shore and helped maintain the impetus for the long-term offshore work (Crisp and Southward, 1964; Russell et al., 1971; Southward, 1974). A very influential review of the influence of limpet grazing (Southward 1964a) was written and a textbook on seashore ecology followed in 1965 (Southward, 1965). Although the work on shores was perhaps less prominent in Alan’s research by the late 1960s, it was reawakened with a crash when the Torrey Canyon oil spill contaminated most of the shores of western Cornwall in 1967. Serendipitously, the network of sites that Alan had established for long-term studies on climate effects on shore animals, came into its own as a baseline for assessing the aftermath of the spill and the recovery of the ecosystem. The research on the recovery of shores from oil and the massive use of dispersants became a much-cited classic (Southward and Southward 1978). The Southwards demonstrated that the chemicals used to disperse the oil were more toxic to the animals and plants than the oil itself. They showed that on shores where dispersants had been used some 10–15 years were needed for recovery of former conditions, whereas, in contrast, only 2–3 years were required on untreated, solely oil-laden shores. The work also gave valuable insights on the role of limpet grazing in structuring shore communities, in addition to elucidating mechanisms of succession. Alan’s innovative and patient research was hugely influential at the time and was, with other MBA research in the aftermath of the Torrey Canyon, largely responsible for governments and agencies abandoning the widespread use of toxic chemicals to tackle oil slicks. In the 1970s research was concentrated on describing the return of more northerly species to the English Channel and the work that followed became a seminal contribution (Russell et al., 1971; Southward, 1974; Southward et al., 1975). Alan Southward, together with colleagues, were essentially the first to discover, by documenting in hitherto unparalleled detail, how marine species respond to climate changes. In the western English Channel it was noticed that cold-water herrings and plankton, once common in the 1920s, had declined and were replaced by warm-water

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pilchards and plankton in the 1940s and 1950s. During the 1960s and 1970s boreal fish and plankton once again dominated. Relating these to fluctuations in the long-term sea temperature records and other physical data (Southward, 1960; Southward and Butler, 1972), Alan realised that the shifts in animal distribution and changes in abundance were closely linked with climate oscillations. The strength of this work was in its breadth and depth; he set about documenting changes in immense detail, from shore organisms to plankton and fish, and proposed several biological mechanisms. Later work using these data sets together with much older records from archived newspapers and diaries showed similar fluctuations in herring and pilchard fisheries occurring off Devon and Cornwall in relation to climate since at least the sixteenth century (Southward et al., 1988). The whole series of studies culminated in an excellent review and synthesis published in Nature in 1980—this described arguably the first large-scale study providing clear evidence of how ecosystems appear to shift between different and apparently stable states in relation to climate (Southward, 1980). This review also noted a breakdown in the relationship between sunspots as an index of solar heat flux and sea temperature, thereby making a contribution to emerging ideas about human driven climate change. The 1970s also marked the realisation that Darwin’s panglobal species Chthamalus stellatus was several species and that European C. stellatus consisted of two species: C. stellatus Poli and C. montagui Southward (Southward, 1976). Alan embraced new techniques in collaboration with Paul Dando to sort out these taxonomic problems, using gel electrophoresis of enzymes to identify cryptic species (e.g. Dando and Southward, 1980). Over the years Alan became the European taxonomic expert on barnacles, revising much of Darwin’s early work on barnacles as well as working on deep-sea stalked barnacles, culminating in Southward (2008).

Deep Sea discoveries The late 1970s saw the discovery of hydrothermal vents on the Galapagos Ridge in the Central Eastern Pacific. The Southward’s longstanding interest in Pogonophora became suddenly fashionable as closely related giant vestimentiferan worms were discovered by Alvin dives. Alan and Eve’s previous work had focused on how small pogonophores might obtain nutrition from dissolved organic compounds in the sediment (Southward and Southward 1968). But following the discovery by Colleen Cavanaugh of endosymbiotic sulphur-oxidising bacteria that supplied the giant vestimentiferan tubeworms with their nutrition by chemosynthesis, they quickly discovered that the small pogonophores of the Atlantic continental slope also contained endosymbiotic bacteria (Southward et al., 1981).

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They involved Paul Dando and David Dixon throughout the 1980s and 1990s in this exciting new endeavour (e.g. Southward and Dixon, 1980). Further work on the metabolism of the pogonophores’ symbionts benefitted greatly from the practical skills of the group in extracting minute amounts of bacteria from the worms for use in enzyme assays. Alan in particular showed a great ability for this highly dexterous and sustained work on research ships in often rough seas, presumably due in part to his enviable immunity to seasickness, a fortunate consequence of his deafness. However, despite much progress during several cruises in the Bay of Biscay, for example, identifying the chemosynthetic energy source for the slope pogonophores proved difficult. It was not until cruises in the Norwegian fjords that the discovery was made of two species of bivalves with endosymbiotic bacteria, living alongside the pogonophores, and the finding that all these organisms were capable of obtaining energy by ‘mining’ iron sulphides (Dando et al., 1986; Southward et al., 1986; Spiro et al., 1986). This opened up a new field of research of international importance since Alan and colleagues were able to demonstrate that organisms obtaining nutrition from endosymbiotic autotrophic bacteria were found in most reducing marine sediments from the intertidal to the deep sea.

‘Retirement’ years Alan was an unfortunate casualty of the re-organisation of the Marine Laboratories at Plymouth in 1986/1987; he had to retire at the age of 60 instead of 65 because of the new terms of employment offered to MBA staff. The 80-plus year old MBA time series was stopped in 1988—ironically just as detection of global warming and its impacts on marine ecosystems were becoming apparent. Characteristically, Alan bounced back. Leverhulme funding for a Senior Fellowship was secured providing salary and funding for another 3 years concentrating on chemosynthetic-driven systems, research conducted in equal partnership with Eve (Gebruk et al., 1997). As well as accepting time on research ship cruises in the Norwegian fjords, the North Sea and the Caribbean, studies were also pursued off the coast of British Columbia in Canada. He was awarded an Adjunct Professorship of Victoria University, British Columbia, collaborating with Verena Tunnicliffe and her group, and a house was purchased in Canada to be nearer to the vents. This freedom of action allowed successful applications to the UK Natural Environment Research Council (NERC) and the European Union for grants and there was not any hint of retirement. In 1989 Alan was made a Visiting Professor of Marine Biology at the University of Liverpool Port Erin Laboratory where his visits to teach and co-supervise students were

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always much appreciated. After 1987 in so-called retirement, he published well over 80 papers, books and book chapters. A bad fall in 1999 stopped work at sea and on the shore, so the focus of Alan’s work became barnacle taxonomy and advising on the re-start of long-term series on UK shores and in the Western English Channel between 1999 and 2006. He completed a Linnean Society Monograph on barnacles just before his death that was published in 2008 (Southward, 2008). Alan also led a major review of the long-term research conducted in the Western English Channel by the Plymouth laboratories for more than 100 years, and which appeared in 2005 in Advances in Marine Biology (Southward et al., 2005). Furthermore, without his presence at the MBA laboratory much of the long-term data would have become neglected, lost or deleted from old file formats. His data stewardship has led to a great many papers of relevance to climate change effects and fisheries (e.g. Sims et al., 2001, 2004; Genner et al., 2004). Some papers contributed to the recent report assembled by the Nobel-prize winning Intergovernmental Panel on Climate Change (IPCC). Alan graciously handed over the MBA time-series on rocky shore organisms, plankton and fish to younger generations as well as the editing of Advances in Marine Biology. He was an exquisite editor of Advances, with such great attention to detail and a real devotion to the task of helping to produce comprehensive reviews of exceptional clarity across a breathtaking array of subject areas, allowing both newcomers to a subject and seasoned experts a thorough understanding. His knowledge of marine biology was encyclopaedic and the expertise he brought to editing was equally impressive, not least his lucid writing style that was a pleasure to read (e.g. Southward and Roberts, 1987). Furthermore, the help he gave to authors, especially to those from overseas, was way beyond the call of scientific duty. He particularly welcomed reviews from outside Europe and the United States, and gave great help and encouragement to many of these scientists in making their work accessible to an international audience.

His science legacy Alan Southward mastered a wide range of disciplines and contributed seminal work in diverse areas of marine biology, from barnacle taxonomy to quantitative ecology, and from biogeographic surveys to climate change and long-term studies. Although he followed in the footsteps of the old naturalist scientists of the early part of the twentieth century, whose interests were often similarly broad, to say he was a marine naturalist in the older sense of the word is not sufficient. He was an extremely good marine naturalist but he was also prepared to use modern analytical and computing techniques to confirm his observations. Without doubt one of Alan’s most important contributions has

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been as a pioneer, steward and interpreter of long-term monitoring data sets to understand how marine organisms respond to environmental fluctuations (Southward, 1991). Throughout the 1990s it became clear that global climate change was occurring. There was a growing realisation of the human contribution via greenhouse gases; global warming progressed from speculation to a generally accepted view. The value of long-term data sets were belatedly seen as vital to help disentangle human driven global change from natural fluctuations (Southward, 1980) and local and regional impacts such as fishing (Southward, 1981a), pollution and habitat loss (Southward 1981b). Although scientists and politicians are now in general agreement that human activity is affecting Earth’s climate and the oceans, this was not always the case. Alan Southward realised very early that physical and biological variables measured frequently and over long periods would be vital for assessing the effects of climate change on marine ecosystems and he championed this method for over 50 years (Southward, 1995). Alan was not only instrumental in setting up new complementary time series of biological observations in the western English Channel and elsewhere during the 1950s and 1960s but was also responsible for invigorating the maintenance of established time series (dating from 1900) with his vision that this could lead to greater understanding of complex processes relevant to society. This he pursued at a time when the biological effects of climate and other external drivers in marine systems were very poorly understood and when this work was deemed unfashionable in science and funding for it was difficult to obtain. However, largely owing to his careful work and strength of character, these data sets are now reaching maturity and proving of crucial importance for helping to develop a fundamental understanding of the effects of climate-linked sea temperature changes on the distribution and abundance of marine animals and plants. Without Alan’s foresight these valuable timeseries data sets that he pioneered, helped motivate and later championed would not now be available to the marine science community. In this sense, he was a scientist very much ahead of his time. The impact of his research is both broad and long-lasting. Reference (citations) to his early work on climate impacts on marine animals and plants in particular continues to grow as a new generation of scientists re-discover its prescience. It is fair to say that his work laid the solid foundations for subsequent studies worldwide on the effects of climate fluctuations on marine species. Viewed from this perspective, his has been a singularly important legacy to marine science. In addition to his achieving great heights of scientific accomplishment, Alan, together with Eve, provided much hospitality, humour and support to the general marine biological community over the years—particularly to young scientists. The Southwards were always generous and unselfish collaborators and fine hosts. Alan and Eve were stalwarts at European Marine Biological Symposia (EMBS) meetings and Alan’s contribution to conferences was always marvellous: his talks were always stimulating and

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scholarly, whilst at the same time being amusing, and his questions and comments were always helpful and insightful. He was also an outspoken critic of short-termism in British Science, perhaps stemming from his vision for the need for long-term observations. Perhaps his breadth of interests also counted against him, coupled with his plain speaking, but it has been a surprise to many that there was not more formal recognition of his discoveries and contribution to science other than his honorary Fellowship of the Linnean Society, in which he took great pride. We all have fond and amusing memories and much admiration for Alan who was a true gentleman of science. He was an inspiration to all that met him and he leaves a great many friends and a rich scientific legacy.

ACKNOWLEDGEMENTS We are grateful to many colleagues, and in particular to Gerald Boalch and Paul Dando, for allowing us to draw on their written accounts of their scientific work with Alan. We also thank Linda Noble and the staff of the National Marine Biological Library at the MBA for preparing a full bibliography of Alan’s published work from which the selected references given here were taken.

REFERENCES Southward, A. J. (1949). Ciliary mechanisms in Aurelia aurita. Nature 163, 536. Southward, A. J. (1950). Occurrence of Chthamalus stellatus in the Isle of Man. Nature 165, 408–409. Southward, A. J. (1951). Distribution of Chthamalus stellatus in the Irish Sea. Nature 167, 410–411. Southward, A. J., and Crisp, D. J. (1952). Changes in the distribution of the intertidal barnacles in relation to the environment. Nature 170, 416–417. Southward, A. J. (1953a). The ecology of some rocky shores in the south of the Isle of Man. Proc. Trans. Liverpool Biol. Soc. 59, 1–50. Southward, A. J. (1953b). The fauna of some sandy and muddy shores in the south of the Isle of Man. Proc. Trans. Liverpool Biol. Soc. 59, 51–71. Southward, A. J., and Crisp, D. J. (1954). Recent changes in the distribution of the intertidal barnacles Chthamalus stellatus Poli and Balanus balanoides L. in the British Isles. J. Anim. Ecol. 23, 163–177. Southward, A. J. (1955a). Feeding of barnacles. Nature 175, 1124–1125. Southward, A. J. (1955b). On the behaviour of barnacles. I. The relation of cirral and other activities to temperature. J. Mar. Biol. Assoc. UK 34, 403–422. Southward, A. J. (1955c). On the behaviour of barnacles. II. The influence of habitat and tide-level on cirral activity. J. Mar. Biol. Assoc. UK 34, 423–433. Southward, A. J., and Crisp, D. J. (1956). Fluctuations in the distribution and abundance of intertidal barnacles. J. Mar. Biol. Assoc. UK 35, 211–229. Crisp, D. J., and Southward, A. J. (1958). The distribution of intertidal organisms along the coasts of the English Channel. J. Mar. Biol. Assoc. UK 37, 157–208. Southward, A. J. (1958a). Note on the temperature tolerances of some intertidal animals in relation to environmental temperatures and geographical distribution. J. Mar. Biol. Assoc. UK 37, 49–66.

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Southward, A. J. (1958b). The zonation of plants and animals on rocky sea shores. Biol. Rev. 33, 137–177. Southward, A. J. (1958c). Abundance of Pogonophora. Nature 182, 272. Southward, A. J., and Southward, E. C. (1958). Pogonophora from the Atlantic. Nature 181, 1607. Southward, A. J. (1960). On changes of sea temperature in the English Channel. J. Mar. Biol. Assoc. UK 39, 449–458. Southward, A. J. (1963). The distribution of some plankton animals in the English Channel and approaches. III. Theories about long-term biological changes, including fish. J. Mar. Biol. Assoc. UK 43, 1–29. Southward, A. J. (1964a). Limpet grazing and the control of vegetation on rocky shores. In ‘‘Grazing in terrestrial and marine environments’’ (D. J. Crisp, ed.), pp. 265–273. British Ecological Society Symposium No.4, Oxford Blackwell Science Publishers. Southward, A. J. (1964b). On the European species of Chthamalus (Cirripedia). Crustaceana 6, 241–254. Crisp, D. J., and Southward, A. J. (1964). Effects of the cold winter of 1962–63. South and South-west coasts. J. Anim. Ecol. 33, 179–183. Southward, A. J. (1965). Life on the Sea-Shore. p. 153. Heinemann, London. Southward, A. J. (1967). Recent changes in abundance of intertidal barnacles in South-West England: a possible effect of climatic deterioration. J. Mar. Biol. Assoc. UK 47, 81–95. Southward, E. C., and Southward, A. J. (1967). The distribution of Pogonophora in the Atlantic Ocean. Symp. Zool. Soc. Lond. 19, 145–158. Southward, A. J., and Southward, E. C. (1968). Uptake and incorporation of labelled glycine by Pogonophores. Nature 218, 875–876. Russell, F. S., Southward, A. J., Boalch, G. T., and Butler, E. I. (1971). Changes in biological conditions in the English Channel off Plymouth during the last half century. Nature 234, 468–470. Southward, A. J., and Butler, E. I. (1972). A note on further changes of sea temperature in the Plymouth area. J. Mar. Biol. Assoc. UK 52, 931–937. Southward, A. J. (1974). Changes in the plankton community of the western English Channel. Nature 249, 180–181. Southward, A. J., Butler, E. I., and Pennycuick, L. (1975). Recent cyclic changes in climate and in abundance of marine life. Nature 253, 714–717. Southward, A. J. (1976). On the taxonomic status and distribution of Chthamalus stellatus (Cirripedia) in the north-east Atlantic region: with a key to the common intertidal barnacles of Britain. J. Mar. Biol. Assoc. UK 56, 1007–1028. Southward, A. J., Robinson, S. G., Nicholson, D., and Perry, T. J. (1976). An improved stereocamera and control system for close-up photography of the fauna of the continental slope and outer shelf. J. Mar. Biol. Assoc. UK 56, 247–257. Southward, A. J., and Southward, E. C. (1978). Recolonization of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. J. Fish. Res. Bd. Can. 35, 682–705. Dando, P. R., and Southward, A. J. (1980). A new species of Chthamalus (Crustacea: Cirripedia) characterized by enzyme electrophoresis and shell morphology: with a revision of other species of Chthamalus from the western shores of the Atlantic Ocean. J. Mar. Biol. Assoc. UK 60, 787–831. Southward, A. J. (1980). The western English Channel—an inconstant ecosystem? Nature 285, 361–366. Southward, A. J., and Dixon, D. R. (1980). A note on the free amino acids in some small species of Pogonophora. J. Mar. Biol. Assoc. UK 60, 171–174. Southward, A. J. (1981a). Overfishing: is there a solution? Nature 291, 449–450. Southward, A. J. (1981b). Life on an oily wave. Nature 294, 215–216.

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Southward, A. J., Southward, E. C., Dando, P. R., Rau, G. H., Felbeck, H., and Flugel, H. (1981). Bacterial symbionts and low 13C/12C ratios in tissues of Pogonophora indicate unusual nutrition and metabolism. Nature 293, 616–617. Dando, P. R., Southward, A. J., and Southward, E. C. (1986). Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proc. R. Soc. B 227, 227–247. Southward, A. J., Southward, E. C., Dando, P. R., Barrett, R. L., and Ling, R. (1986). Chemoautotrophic function of bacterial symbionts in small Pogonophora. J. Mar. Biol. Assoc. UK 66, 415–437. Spiro, B., Greenwood, P. B., Southward, A. J., and Dando, P. R. (1986). 13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 28, 233–240. Southward, A. J., and Roberts, E. K. (1987). One hundred years of marine research at Plymouth. J. Mar. Biol. Assoc. UK 67, 465–506. Southward, A. J., Boalch, G. T., and Maddock, L. (1988). Fluctuations in the herring and pilchard fisheries of Devon and Cornwall linked to change in climate since the 16th century. J. Mar. Biol. Assoc. UK 68, 423–445. Southward, A. J. (1991). Forty years of changes in species composition and population density of barnacles on a rocky shore near Plymouth. J. Mar. Biol. Assoc. UK 71, 495–513. Southward, A. J. (1995). The importance of long time-series in understanding the variability of natural systems. Helgolander Meeresuntersuchungen 49, 329–333. Southward, A. J., Hawkins, S. J., and Burrows, M. T. (1995). Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. J. Therm. Biol. 20, 127–155. Southward, E. C., Gebruk, A., Kennedy, H., Southward, A. J., and Chevaldonne, P. (2001). Different energy sources for three symbiont-dependent bivalve molluscs at the Lagatchve hydrothermal site (Mid-Atlantic Ridge). J. Mar. Biol. Assoc. UK 81(4), 655–661. Gebruk, A. V., Galkin, S. V., Vereshchaka, A. L., Moskalev, L. I., and Southward, A. J. (1997). Ecology and biogeography of the hydrothermal vent fauna of the Mid-Atlantic Ridge. Adv. Mar. Biol. 32, 93–144. Sims, D. W., Genner, M. J., Southward, A. J., and Hawkins, S. J. (2001). Timing of squid migration reflects North Atlantic climate variability. Proc. R. Soc. B 268, 2607–2611. Sims, D. W., Wearmouth, V. J., Genner, M. J., Southward, A. J., and Hawkins, S. J. (2004). Low-temperature-driven early spawning migration in a temperate marine fish. J. Anim. Ecol. 73, 333–341. Genner, M. J., Sims, D. W., Wearmouth, V. J., Southall, E. J., Southward, A. J., Henderson, P. A., and Hawkins, S. J. (2004). Regional climatic warming drives longterm community changes of British marine fish. Proc. R. Soc. B 271, 655–661. Southward, A. J., Langmead, O., Hardman-Mountford, N. J., Aiken, J., Boalch, G. T., Dando, P. R., Genner, M. J., Joint, I., Kendall, M., Halliday, N. C., Harris, R. P., Leaper, R., Mieszkowska, N., Pingree, R. D., Richardson, A. J., Sims, D. W., Smith, T., Walne, A. W., and Hawkins, S. J. (2005). Long-term oceanographic and ecological research in the western English Channel. Adv. Mar. Biol. 47, 1–104. Southward, A. J. (2008). Barnacles: Keys and Notes for the Identification of British Species, p. 140. Field Studies Council Publications, ShrewsburySyn. British Fauna, New Series Vol. 57.

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Maternal Effects in Fish Populations Bridget S. Green Contents 1. Introduction 1.1. Definition of maternal effects 1.2. Maternal effects in fisheries and aquaculture 1.3. Scope of review 1.4. Fishes and aquatic systems compared to other ecosystems and taxa 1.5. Review overview 2. Pathways and Evidence of Maternal Effects 2.1. Reproductive mode 2.2. Maternal environment 2.3. Maternal attributes 2.4. Summary of evidence of maternal effects 3. Offspring Traits Affected 3.1. Response variable selection 3.2. Trade-off between offspring size and number 3.3. Time course of effects (traits and ontogeny) 3.4. Difficulties in studying maternal effects and environment 4. Summary Acknowledgements References

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Abstract Recently, the importance of the female to population dynamics—especially her non-genetic contribution to offspring fitness or maternal effect—has received much attention in studies of a diverse collection of animal and plant taxa. Of particular interest to fisheries scientists and managers is the role of the demographic structure of the adult component of fish populations in the formation of future year classes. Traditionally, fisheries managers tended to assess whole populations without regard to variation between the individuals within the population. In doing so, they overlooked the variation in spawning production Marine Research Laboratory, Tasmanian Fisheries and Aquaculture Institute, University of Tasmania, Private Bag 49, Tasmania, 7001 Australia Advances in Marine Biology, Volume 54 ISSN 0065-2881, DOI: 10.1016/S0065-2881(08)00001-1

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2008 Elsevier Ltd. All rights reserved.

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between individual females as a source of variation to recruitment magnitude and fluctuation. Indeed, intensive and/or selective harvesting of larger and older females, those that may produce more—and higher quality—offspring, has been implicated in the collapse of a number of important fish stocks. In a fisheries resource management context, whether capture fisheries or aquaculture, female demographics and inter-female differences warrant serious consideration in developing harvesting and breeding strategies, and in understanding general population dynamics. Here I review the range of female traits and environmental conditions females encounter which may influence the number or quality of their offspring via a maternal effect.

1. Introduction For almost a century, fisheries biologists have searched for a unifying theory on recruitment variation and the source of year-class strength in fisheries populations. Commencing with Hjort in 1914, environmental factors such as advection and starvation were identified as potential sources of recruitment variation. A progression of Hjort’s pioneering work suggested a link between egg size, timing of spawning and food availability (Bagenal, 1971). Numerous advancements on these theories describe variable year-class strength and the dynamics of larval survival as potential sources of recruitment variation, with each development building on the theory and evidence from previous hypotheses: match–mismatch (Cushing, 1972), stable oceans (Lasker, 1975), bigger is better (Miller et al., 1988) and stage-duration (Leggett and Deblois, 1994). Subsequently, predation, competition and larval supply were incorporated into the theoretical framework (Hoey and McCormick, 2004; Miller et al., 1995; Paris and Cowen, 2004). The evolution from a population-based, single factor approach to a multivariate approach, exploring variations between individuals within a population as well as variation between populations has identified numerous environmental and biotic factors as important sources. Amongst these are what are commonly referred to as maternal effects, which are the nongenetic contribution of a female to the phenotype of her offspring. While the link between size variation of larvae at hatching and strength of recruitment still remains largely theoretical for most populations, it is theory that is gaining increasing support through laboratory and field experiments (Bergenius et al., 2002; Meekan and Fortier, 1996; Wright and Gibb, 2005). Though the concept of the value of larger, older or better condition females to a spawning population has been around since the 1960s (Nikolskii, 1962), this field of study has only developed and entered

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mainstream fisheries science in recent years. To advance the field, streamline ideas and synthesise the importance of maternal effects on offspring variation—these advancements require further collation of the most up-to-date findings. The purpose of this paper is to fill this need by reviewing the occurrence of maternal effects in fish populations.

1.1. Definition of maternal effects ‘Maternal effects’ has multiple definitions, uses and misuses, and the most appropriate depends on the context in which it is used. The definitions of maternal effects that are the broadest and most applicable to this review are that maternal effects are the non-genetic contribution of the female to offspring condition (Reznick, 1991); or any influence of the parent on offspring, not caused by shared DNA (Reinhold, 2002); or phenotypic variation in offspring that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff, 1998). The broadest misuse of the term occurs when offspring variation is attributed to any trait of the female without accounting for maternal genetics. Such variation would be more precisely referred to as ‘female influence’, which does not imply a separation of genetic and non-genetic effects. See Box 1.1 for further definitions to be used throughout this review. The non-genetic sources of variation in offspring can be from either parent, but as it is the female that provisions the egg with nutrients, hormones and cytoplasm and generally chooses where to deposit them, she is a more likely Box 1.1 Glossary of terms used

Additive genetic variance: Phenotypic variance due to different genotypes, and is the numerator in the heritability ratio. Broad-sense heritability: The proportion of total phenotypic variability (H2) due to all genetic effects. The sum of additive variance þ dominance variance þ epistatic variance is the total genetic variance and heritability in the broad sense is the ratio Genetic variance/phenotypic variance. Dam: Female parent. Ecological fallacy: Inferences about the nature of individuals are based solely upon aggregate statistics collected for the group to which those individuals belong. Gametogenesis: Gametogenesis is the production of haploid gametes by diploid multicellular organisms through the process of meiosis. Gonochoristic: In a sexually reproducing species where there are at least two distinct sexes.

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Box 1.1 (continued )

Heterosis: The biological phenomenon in which an F1 hybrid of two genetically dissimilar parents shows increased vigor at least over the mid-parent value (P1+P2/2). Maternal effects are a type of heterosis. Heritability: Additive genetic variance/phenotypic variance. Heritability is a ratio that describes the amount of phenotypic variation that can be attributed to the differences in the ‘additive genetic merit’ of individuals in a population. Differences in additive genetic merit exist if individuals have different alleles at loci that contribute to measurable differences in performance. So, to understand heritability, one must first understand additive genetic merit. Iteroparity: The repeated production of offspring throughout the life cycle. Maternal effects: Phenotypic variation in offspring, that is a consequence of the mother’s phenotype rather than the genetic constitution of the offspring (Roff, 1998), inherited environmental effects. Maternal influence: An effect derived from the female that may be genetic or phenotypic. Matrotrophy: Provisioning of young with nutrients in excess of those supplied through the yolk. Narrow-sense heritability: The proportion of phenotypic variance that can be attributed to additive genetic variance. Oogenesis: The production of female gametes (ova). Oocyte: A female germ cell in the process of developing. Oocytes give rise to the ovum or egg. Oviparity: Expulsion of underdeveloped eggs rather than live young. Oviviparity: The eggs are hatched in the oviduct of the female. The embryos develop in the uterus until fully grown. Phenotypic plasticity: The different phenotypic expressions of a genotype in response to ranging environmental conditions. Quantitative genetics: The quantification of inherited continuous traits responsible for phenotypic differences. Reaction norm: The range of phenotypes an organism can express in response to environmental variation (Riska, 1991). Semelparity: A single reproductive season before death, also referred as ‘big bang’ reproduction. Sequential hermaphrodite: Where a single organism can be sexually functional as a male and as a female, and the expression (primary and secondary sexual characteristics) and function of one gender is followed by the other, that is, both sexes do not operate at the same time.

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Sire: Male parent. Trait: A measurable quality or characteristic. Transgenerational adaptive plasticity: If the parental environment is predictive of future environment, then it is advantageous to produce offspring adapted to the environment in which they are reared (Mousseau and Fox, 1998); females use current environmental cues to adjust their offspring investment to future environmental conditions and is a strategy to increase offspring fitness (Plaistow et al., 2004). Vitellogenesis: The process of yolk deposition, the process of nutrients being deposited into the oocytes—usually initiated after the first meiotic division. Viviparity: The embryo is nourished inside of the female by a placenta, and females give birth to live young. source of variation, at least in the initial stages. The bulk of this review will focus on the female component of non-genetic input into offspring variation. The male influence will be only briefly discussed in this review (see Section 2.2.7).

1.2. Maternal effects in fisheries and aquaculture 1.2.1. Fisheries Traditionally, fisheries managers tended to assess whole population dynamics without regard to variation between the individuals within the population. In doing so, they overlooked females, and more so, the variation in spawning production between individual females, as a source of variation to recruitment magnitude and fluctuation. There is now consensus in management of many heavily exploited stocks—though not yet universally incorporated into broad-scale fisheries modelling—that spawning stocks are not single entities with respect to sizes, but are composed of individuals of a range of sizes and ages that may contribute differently to spawning and recruitment (Marshall et al., 1998; Marteinsdottir and Thorarinsson, 1998; Scott et al., 1999). In this review, the argument will be explored that the variation in attributes of quality between individuals is critical to consider in the stock recruitment relationship (Scott et al., 1999; Vallin and Nissling, 2000). Traditional models assume that egg production is directly related to spawner biomass or spawning stock biomass (SSB) when considered across a whole population and the two factors are interchangeable in predictive models. The resulting assumption is that many small individuals will produce as many offspring as a few large individuals. Where this is not true, models of stock productivity, and the subsequent fisheries management decisions, may critically underestimate the contribution of different female size classes to recruitment variation in fish stocks. In reality, when individual stocks are assessed, spawner biomass is often

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not related to total egg production (Marshall et al., 1998). To quote Marshall et al. (2003), ‘The lack of proportionality between SSB [spawning stock biomass] and egg production means that biomass reference points should be regarded as being inherently uncertain’ (p. 185). Given isometric scaling laws, which purport that volume = length3, a female’s capacity to store eggs increases as a cube of her body length. Longer females theoretically can produce significantly more eggs than shorter females. In fact, some fishes have a greater reproductive capacity than ascribed even by these body-size scaling laws. In Atlantic cod, Gadus morhua, the smallest fish can produce approximately 300 eggs g1 compared with large cod which can produce approximately 500 eggs g1 (Marshall et al., 1998). The inclusion of size, quality and quantity of spawners in a fisheries population or stock would lead to more accurate SSB estimates. Furthermore, the influence of these factors on offspring quality and the manner in which this feeds into year-class strength need to be incorporated into a basic stock assessment. Maternal effects are a major source of phenotypic variation within a population. Numerous studies have described how a truncation of the age or size of a fishing population can directly affect the quality of offspring and recruitment (Longhurst, 2002; Scott et al., 2006), and many have inferred an effect (Berkeley et al., 2004a). If there was generality in the influence of a maternal effect on recruitment, then maternal effects would be a key pathway through which fisheries regulation could manage recruitment mechanisms (Solemdal, 1997). For maternal effects to be usefully incorporated in to stock–recruitment (S/R) relationships there must be a strong and consistent or at least predictable relationship between offspring quality and attributes of the parent within a species, and this relationship would become more effective if it existed between species (Ouellet et al., 2001) or higher level taxonomic or life history grouping. This review will examine some of the generalities published as maternal effects. When variation in reproductive output between females is incorporated into estimates of SSB, accurately predicting recruitment or year-class strength is difficult because of high variability and uncertainty in the relationship between the numbers of eggs spawned and juveniles surviving to recruit (Marshall et al., 2003). This relationship between egg quality and offspring survival is moderated by environmental conditions. Quantifying recruitment variation due to maternal effects is potentially very important in estimating recruitment from SSB if larger or more experienced fish produce more viable offspring with higher likelihood of surviving a range of environmental conditions. While there are instances where a relationship between SSB or S/R relationships and the number of eggs produced has been demonstrated through meta-analysis (Myers and Barrowman, 1996), there is so much uncertainty in most fisheries models that many attempts to manage stocks have failed, resulting in further stock declines, or reduction in age and size classes (Pauly et al., 2002). The most common explanation for a lack of S/R

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relationship is high mortality in the larval period, estimated at 99.9% (Ferron and Leggett, 1994). If selectivity of larval mortality could be estimated via assessment of female quality then better estimates of the S/R relationships may result. Recruitment models which incorporate female traits such as variable SSB between years, egg production, and amount of liver lipid are better predictors of recruitment variation than models that simply rely on SSB (Marshall et al., 2003). Although a maternal component was stipulated in one of the early models predicting a relationship between SSB and egg production (Beverton and Holt, 1957), for example, ‘survival of fry hatched from large eggs may be better than from small ones’, this caveat was generally overlooked for the following four decades. As fishing pressure increases, and the large end of the size distribution of a targeted population is depleted,1 the relative contribution of each female size class to spawning output shifts also. Smaller females contribute proportionally more to stock spawning output under this scenario. While a decrease in size and age at maturity are common responses to increased fishing pressure, this is unlikely to compensate for the contribution of larger or higher quality females. 1.2.2. Aquaculture The importance of female size and other attributes of female quality on the production of offspring also have implications for another aquatic harvest, the aquaculture industry, where fish are cultured in artificial systems rather than harvested from wild populations. As this industry is based on the production of stock in captivity to supply the food fish requirements of growing human populations, optimising production and streamlining effort is the primary goal of most farms. Reproductive output per unit of female fish is probably the most critical performance measure in this industry, and consequently the main goal of aquaculturists, as with most animal and plantbreeders, is to improve the performance of their production stock, in terms of growth, vigour, disease resistance or environmental tolerance (Lutz, 1997). Traditional aquaculture used selective breeding to select from desirable phenotypes, and even with current genetic engineering, the performance of the fish is governed by its genetic potential and immediate environmental conditions (Pickering, 1993). The potential for larger females to produce better quality and more numerous offspring has focused research attention onto the identification of maternal effects on a few key aquaculture species, for example, Atlantic salmon (Refstie and Steine, 1978), rainbow trout (Nagler et al., 2000; Refstie, 1980) and rabbitfish (Ayson and Lam, 1993) for which there is high quality information. 1

This truncation of larger fish is typical of traditional industrial fishing practices, however, this is changing as the demographic of export markets shifts and many fisheries supply the Asian market which pays premium price for plate-sized fish.

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The existence of maternal effects can have both positive and negative implications for the aquaculture industry. By enhancing a female’s environment, production in terms of numbers and quality can be enhanced. Development of fish stocks with enhanced resistance to commonly encountered fish pathogens would be highly advantageous ( Johnson et al., 2003). The disadvantages are that when tailoring a breeding programme to enhance specific genetic traits, or increase heterosis (see Box 1.1 for definitions), the variation due to maternal effects can interfere with the phenotype under selection (Falconer, 1981). It is in selective breeding programmes that maternal effects were first seen as experimental noise (Falconer, 1981). Aquaculture studies more commonly partition sire and dam components of variance in offspring traits (Blanc et al., 2005) in attempts to maximise production and therefore offer a more rigorous approach to the study of maternal effects. However, the results from studies of maternal effects in aquaculture are not always directly applicable to natural resource management as, for instance, the hatchery environment reduces initial size differences (Einum and Fleming, 1999).

1.3. Scope of review Previously, maternal effects have been viewed in many different ways including as experimental noise (Falconer, 1981), genetic divergence (Hendry, 2001) and natural variation (Heath and Blouw, 1998), and as phenotypic plasticity to deal with a variable environment and local adaptation of characters (Mousseau and Fox, 1998). Each approach confers a slightly different perspective on how maternal effects operate both within the confines of a genotype and the environment. One of the difficulties in producing this review was to contain the content to a manageable amount without excluding themes, papers or species of central importance to the overall understanding of how maternal effects might operate in fishes. Each component of maternal effects reviewed has lead to annals on related topics, which could not be included. For instance, I only briefly review the tradeoff between egg size and number (see Section 3.2), as this topic is comprehensively reviewed elsewhere (Hendry et al., 2001; Smith and Fretwell, 1974; Stearns and Koella, 1986). The present review focuses mainly on fish and any kind of maternal influence where there is a direct link between mothers and offspring, and it refers back to many other organisms that lend themselves to experimental manipulation and therefore offer a comprehensive approach to partitioning out variance due to maternal effects. There are many female-offspring relationships that have been described under the general catalogue of ‘maternal effects’ particularly in the fish and fisheries literature, however many do not strictly adhere to the definition of maternal effects adopted here, but rather should be considered maternal

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influences. Disentangling these female influences from true maternal effects is a laborious task, which can often only be achieved experimentally. This looser description of female influences encompasses any relationship between the female and her offspring, including those that are genetic, or specifically related to the size and/or age of a female and are therefore a byproduct of stage-specific growth rather than an effect of the maternal environment directly on offspring phenotypic plasticity. In terms of a fisheries population, female age and/or size and the looser definition of ‘female influence’ are equally as important sources of variation to offspring traits as are the more traditional and tightly defined ‘maternal effects’. The results are still pertinent to understanding the source of phenotypic variation in young fishes that might lead to recruitment variability in wild fisheries or different phenotypes (performance measures) in an aquaculture setting. This review will provide an overview of both maternal effects and influences. Studies of maternal effects and the broader maternal influences in fishes have addressed a few key hypotheses and generalities including 1. Size of female is related to the number of eggs produced and therefore will affect reproductive potential (Marshall et al., 1998). 2. Qualitative changes in eggs and larvae are due to age and size variation in female (Solemdal, 1997). 3. Size of egg is related to size of hatchling (Chambers et al., 1989). 4. There is a ‘broad brush’ of relationship between recruitment and quality and number of female within a population (i.e., stock level correlation recruitment dynamics). 5. There is a trade-off between the egg size and number, and a general increase in one results in a decrease in the other (Hendry et al., 2001; Smith and Fretwell, 1974). These generalities are not universal in fishes and exceptions will be discussed throughout this review. One general thesis to arise from the study of maternal effects in other organisms, both plant and animals, is that bigger females produce better quality and/or more abundant offspring, and therefore size and age variation in parent fishes increases variation in offspring traits that are important to recruitment. While there are exceptions to this general trend, it is generally well-supported in the fields of quantitative genetic analysis, plant-breeding and avian population biology. This literature will be referred to throughout this review to provide context for the fish, fisheries and aquaculture examples. In marine systems I have not yet encountered a single example where the influence of female size has been tracked from parent sources to the success of the next generation in wild populations. The focus of this review will be on the early life stages of fishes as this is when maternal effects are expected to be most evident due to the nature of their transmission.

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1.4. Fishes and aquatic systems compared to other ecosystems and taxa Fishes and aquatic ecosystems have many unique features compared with other ecosystems and taxa that influence how maternal effects are manifested and consequently interpreted. Fishes are epitomised by their diversity in morphology, habitat associations, reproductive and general biology. Of the vertebrates, fishes are the most abundant and speciose group, comprising an estimated 24,000 species (Nelson, 1994), and they show the widest variety of adaptive responses to their environment. They are unique amongst the vertebrates in having indeterminate growth. Furthermore, they have the most diverse range of reproductive strategies of the vertebrates, demonstrating every kind of reproductive strategy that occurs in vertebrates (outlined in Table 1.4, Section 2.1 and also in Berglund, 1997). Numerous species within the Perciformes are sequential hermaphrodites, another unique feature among the vertebrates. Fishes have colonised a large range of habitats spanning a 46  C temperature range, and from 3812 m above sea level to 7000 m below it, and a range of salinities from 0 to 35% (Nelson, 1976). A pelagic larval phase found in most teleosts, coupled with small size and often cryptic appearance of the larvae, make it difficult to close the link between maternal quality and condition and the strength of recruitment. Due to the diversity in both fish reproduction and ecosystem usage, no single approach can characterise population biology. In general, fish reproduction is more similar to invertebrates such as insects, characterised by the release of thousands of gametes, most of which will die in the very early stages. Unlike insects though, there are many limitations in breeding fishes because of the requirement for an aquatic environment and the large proportional change in size in the early life stages.

1.5. Review overview The purpose of this present review is to describe the range of sources, responses and expressions of maternal effect described in fishes. Firstly, the evidence of maternal effects associated with the maternal environment will be described; secondly, the evidence of maternal effects and their link to maternal attributes; thirdly, the traits affected, time course of effects, and patterns of expression of maternal effects will be summarised; and finally I will synthesise information about when maternal effects would be most likely to occur and review the difficulty in studying maternal effects in fishes, with suggestions as to why maternal effects may not be detected.

2. Pathways and Evidence of Maternal Effects Maternal effects occur in a wide range of fishes and are expressed in a variety of offspring traits. The identification of maternal effects and their pathways varies across species and within species (e.g., see discussion on cod,

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G. morhua; Ouellet et al., 2001). There are many pathways through which a female’s phenotype can influence the phenotype of her offspring. Some of these pathways are unique to fishes while others either do not occur or have not been examined in fishes. Pathways include female physiology, timing of spawning within a season, egg provisioning, cytoplasmic inheritance, egg composition (hormones; McCormick, 1999), toxins (Hammerschmidt et al., 1999), carotenoids, for example, birds (Blount et al., 2003), and immunoglobin, for example, birds (Gasparini et al., 2001, cited in Gorman and Nager, 2004), incubation temperature (birds, citations in Gorman and Nager, 2004), and behaviour, including spawning and nesting site choice, and parental care. The latter also includes post-hatching parental feeding, as displayed in many mammals and birds, which is also a pathway for a paternal effect in brooding fish with paternal care (Green and McCormick, 2005b).

2.1. Reproductive mode The reproductive mode of a fish will influence the pathway of maternal effects, and the amount of variability in offspring traits. Of the vertebrates, fish have the widest variety of reproductive strategies, and uniquely, they exhibit all of the known vertebrate reproductive modes. Reproductive modes in fishes include: internal or external fertilisation; broadcast or substrate spawning; oviparity, oviviparity and viviparity; matrotrophy, semelparity and iteroparity; and parental care or no parental care (Table 1.1; see Box 1.1 for definitions). Reproduction in any species will include a combination of these components. For example, guppies (Poecilia reticulata) have internal fertilisation, are viviparous and semelparous; Atlantic salmon (Salmo salar) have external fertilisation, ovivipary, and spawn on the substrate with no parental care; and Atlantic cod (G. morhua) are broadcast spawners with external fertilisation and no parental care. The diversity and possible permutations of reproductive strategies in fishes makes the study of maternal effects in fishes both complex and multifarious. Within these reproductive strategies are also differences in the level of female investment to each clutch relative to lifetime fecundity. Some fishes, for example, Pacific salmon (genus Oncorhynchus, including chinook, chum, coho, pink and sockeye salmon), invest everything in to one pre-terminal reproductive bout (referred to as semelparity). They migrate as far as 1600 km to their natal stream to lay eggs in the gravel, allowing fertilisation by multiple males. Another strategy is to reproduce only once per year, but over multiple years in a lifetime (iteroparity). For example, winter flounder, Pseudopleuronectes americanus, migrate from deep offshore waters to shallow inshore estuarine areas and pair-spawn to produce negatively buoyant adhesive eggs in mid-winter. Other fish ‘hedge their bets’ (bet-hedging) by reproducing repeatedly on a daily,

Table 1.1 Summary of the range of reproductive features found in fishes Life history feature

Feature sub-category

Reproductive mode (sp)

External fertilisation Internal fertilisation Ovipary Ovivipary Vivipary Semelparous Iteroparous Single batch Multiple batches Winter Spring-summer Fall Aseasonal Early season Mid season Late season Lunar <1 d Multiple days Pelagic, open water Benthic Inshore Reef crest (fish spawn on edge of reef into water column in big currents) Group spawning Paired spawning Harem Broadcast, separate, buoyant Broadcast, grouped, buoyant Negatively buoyant Adhesive Benthic attached Nest building, tending Mouth brooding Feeding of offspring Defense of offspring Offspring disinfection Mouth brooding Pouch brooding One age class versus multiple age classes Allocation of parental products Dispersive Non-dispersive

Parity (sp)

Spawning frequency (sp) Spawning periodicity (sp) Seasonality of spawning (sp)

Timing of spawning (ind)

Duration of spawning (ind) Location of spawning (sp)

Mating behaviour (sp)

Attribute of eggs (sp) Attributes of egg placement (sp)

Maternal care (sp)

Paternal care

Dispersal of offspring

sp ¼ expressed across the species; ind ¼ varies among individuals.

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weekly, monthly or lunar cycle within a breeding season (usually seasonally defined) and over multiple years throughout their lifetime (repeat iteroparity). For example, coral trout Plectropomus leopardus are protogynous sequential hermaphrodites that spawn in groups after aggregating, releasing positively buoyant pelagic eggs 3–4 nights on a new moon for 3–4 summer months (Samoilys, 1997). The duration and frequency of gamete release differs in each of these strategies, resulting in opportunities for the expression of maternal effects over a range of scales: within and between batches (Chambers and Waiwood, 1996), season (Rideout et al., 2005b) and years (Manning and Crim, 1998). Changes in gender in the case of sequential hermaphrodites, and age and size with time, can result in further differences in the expression of maternal effects within an individual fish. The likelihood that a female trait such as body size influences the quality of the egg incubation environment depends on the type of reproductive behaviour and the level of female involvement. Different levels of female investment provide a range of opportunities for environmental influences to affect the quality of gametes the female produces. Demersally spawning fishes are expected to exhibit more variation in offspring traits as the selection of spawning and larval habitat are influenced by the maternal phenotype (Einum and Fleming, 2002; Hendry et al., 2001), offering more pathways for a maternal influence or effect. Hendry et al. (2001) predicted a gradient of the expression of maternal effects in Canadian freshwater fishes according to reproductive investment, and found relationships occurred between egg size and female size in fishes with the most active role in nest site selection and egg care. The authors concluded that in an environment where oxygen (or another critical environmental variable) is limiting for the propagules, being of a large size for the female could be an advantage in gaining the best territories, tending the nest and choosing these same qualities in a mate. 2.1.1. Intervention to eggs or clutches to assess maternal effects There are three commonly used tools in manipulating eggs or clutches to partition out the effects of genes, environment, parental care and maternal effects. These include food supplements to the female, cross-fostering, egg or nest manipulation. Food supplementation has been covered in the section on prey abundance and quality (Section 2.2.5). Here, I will briefly discuss techniques used for manipulating eggs and nests. 2.1.1.1. Egg manipulation When the life cycle of the study organism is too long to allow for controlled genetic crossing to explicitly isolate maternal effects from genetic influences, techniques such as egg manipulation may be useful (reviewed by Bernardo, 1991). Micro-manipulating yolk quantities is a tool to alter maternal allocation without interfering with the genetic bequest, and can partition out the pathways for maternal allocation

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and the resulting trade-off in egg size and number. This technique was pioneered in lizards and has been coined ‘allometric engineering’ (Sinervo, 1990; Sinervo and Huey, 1990). Egg manipulation allows for the detection of co-varying factors that would remain undetected in typical correlative studies. These are difficult to perform in fishes as expertise in microsurgery is required to penetrate the chorion and remove measured aliquots of yolk without disrupting developmental processes; however, it has been successfully employed in a few species. Yolk-reduced eggs generally produce smaller hatchlings in zebrafish Danio rerio ( Jardine and Litvak, 2003), herring Clupea harengus (Morley et al., 1999) and lizards (Sinervo, 1990; Sinervo and Huey, 1990); in the case of the lizard, yolk reduced eggs also resulted in a reduced sprint speed in hatchlings (Sinervo, 1990; Sinervo and Huey, 1990). The reduction in yolk is designed to duplicate reduced maternal aliquot to the egg. Egg size can also be manipulated indirectly, by manipulating the size of the follicles during vitellogenesis. Again in lizards, large eggs were produced when the number of follicles is reduced, and conversely when extra follicle growth was stimulated, smaller eggs were produced (Sinervo and Licht, 1991). Hormonal injection of female spawners can influence allocation to eggs. Larvae from female rabbitfish (Signaus guttatus) injected with thyroxine (T4) were longer and higher survival compared to larvae from sham-injected females (Ayson and Lam, 1993). Post-fertilisation exposure of eggs to cortisol in a tropical damselfish Pomacentrus amboinensis resulted in shorter larvae, and exposure to testosterone decreased yolk utilisation rate (McCormick, 1999). All three kinds of manipulations serve as surrogates for partitioning maternal effects on offspring from genetic effects, by using controlled testing to measure relationships such as egg aliquot and larval size, and hormone profiles and offspring size, without variation in maternal genetics. 2.1.1.2. Nest manipulations: Cross-fostering In animals with nest-care, the care the offspring receive whilst in the nest can introduce phenotypic variation through the quality of parental care, or the incubation environment (Green et al., 2006). This source of parental effects can be separated from pre-oviposition parental effects through cross-fostering. Cross-fostering involves switching eggs or clutches of eggs from the natal parents to another set of nesting parents to provide incubation. Cross-fostering has been successfully used in birds (Gorman and Nager, 2004; Saino et al., 2002a) and reptiles (Crespi and Lessig, 2004). Fishes tend not to accept step-parenthood as readily, and will cannibalise cross-fostered young (Amphiprion melanopus, Green, personal observation; Gasterosteus aculeatus, Frommen et al., 2007). This technique needs development before it is a useful tool for partitioning maternal effects in fishes.

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2.2. Maternal environment One of the broader definitions of maternal effects, as ‘inherited environmental variation’, includes the maternal environment as an integral source of maternal effects. There are multiple pathways through which the environment can influence maternally mediated offspring traits. Firstly, the environment can act directly on the female and influence her condition or physiology during oogenesis, which then acts to influence propagule condition. Secondly, the environment can act directly on the eggs in the female-selected nesting location. Finally, maternally mediated offspring traits can interact with the offspring’s environment, after it is liberated from the female. Environmental factors fluctuate daily, seasonally and randomly, and all types of environmental shift have the potential to influence maternal and offspring condition. The physical parameters of aquatic environments differ markedly from terrestrial environments. Oxygen is rarely limiting in terrestrial environments; however, due to low solubility of oxygen in water (water contains 0.03% of the amount of oxygen in air), it can be limiting in aquatic systems, particularly in shallow, still freshwater and lentic habitats (discussed in Wootton, 1990). In contrast, the dramatic temperature fluctuations that shape some terrestrial environments are rare in aquatic habitats as water acts as a thermal buffer reducing the extremes. Nevertheless, temperature does fluctuate on a diel and annual basis in aquatic environments, and can interact with a maternal effect to influence offspring quality (e.g., anemonefish, Green and McCormick, 2005a). Fishes contend with these and other variables including predator fields, contamination, flow regimes, salinity and temperature gradients, stress from competitors and complex habitat structure. Environmental parameters unique to the aquatic environment influence spawning and mating behaviour as well as quality of nest or egg release environment, all of which can be sources of maternal effects. Flow regime can influence oviposition choice, pertinent in substrate-laying species like salmon whereby a high flow can wash eggs away and low flow can restrict the amount of oxygen available to the eggs (Hendry et al., 2001). The number of ideal egg incubating environments is limited in some aquatic systems, and so female size and experience can increase their ability to access the best spawning habitat. Water turbidity influences mate choice in gobies by reducing visibility and assessment of potential mates which can lead to a reduction in offspring quality (Jarvenpaa and Lindstrom, 2004; Seehausen et al., 1997). The maternal environment can affect offspring traits via its effect on the physiology of the female. For example, if the female is exposed to a toxic environment then often this toxicity is passed directly onto the offspring through the cytoplasm. An environment that is socially stressful to the female through aggressive encounters with conspecifics can increase her cortisol levels which can act to reduce the size of larvae at hatching, as has

16

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been shown for fish (McCormick, 2006) and birds (Saino et al., 2005), and can bias the sex ratio of offspring in the case of birds (Love et al., 2005). There are also indirect effects of the maternal environment. Ideal propagule size and subsequent survival will vary with the environment the propagule encounters. Growth advantages at hatching may be transient or may even be negative in a harsh environment. In salamanders, larvae from large eggs had a survival advantage in ponds with constant water level, but were at a disadvantage in seasonally drying ponds (Semlitsch and Gibbons, 1990). 2.2.1. Location of spawning Spawning site location acts as habitat for developing embryos in benthic spawning species (Blanchfield and Ridgway, 2005), and provides entry into circulation patterns critical for transport to suitable recruitment sites in pelagic spawning species (Paris et al., 2005). Whether the fish is a benthic or pelagic spawner, the parental choice of spawning site can be critical to the initial survival of the offspring. Larval transport pathways from spawning aggregation sites can be a critical link in recruitment magnitude (Paris et al., 2005). Within a population, herring (C. harengus) spawning site selection is critical to larval retention and subsequent year class strength (Iles and Sinclair, 1982). There is some evidence of spawning ground location influencing growth in Atlantic salmon, as size and age at first spawning increase with the distance to spawning grounds and river harshness (Schaffer and Elson, 1975). A more detailed discussion on nest-site selection for benthic spawning fishes is given in Section 2.3.6.2. 2.2.2. Season of spawning Seasonal environmental changes characterise high latitude and temperate aquatic ecosystems, and within these ecosystems, most organisms reproduce seasonally (Bye, 1990). The length of the breeding season varies within species along latitudinal gradients (e.g., Fundulus heteroclitus, Schultz et al., 1996); with age of the individuals (e.g., Atlantic cod, G. morhua, Comeau et al., 2002) and between species. In a number of species that show a seasonal migration to spawning grounds, larger, older females arrive first (and in territorial species gain access to the best territories), for example, brook trout, Salvelinus fontinalis (Blanchfield and Ridgway, 2005), and spawn first. Early spawning within a season can provide an extended growing season to the offspring, and greater access to seasonal food production. Within individual females, seasonal changes may influence egg quality during oogenesis. Many iteroparous fishes show a change in the quality or quantity of eggs produced throughout a spawning season, generally related to the water temperature, or depletion of female reserves. Chambers (1997) offers a broader discussion of seasonal trends in variation of offspring traits, particularly egg size, and rather than repeat the discussion from that volume, I will report on the main trends that were described. Spring/summer spawning

Maternal Effects in Fish Populations

17

species (referred to as spring spawners) have smaller eggs than autumn/winter spawners. For many serial spawners (spring spawners), the egg diameter tapers off as the spawning season advances, for example, haddock Melanogrammus aeglefinus (Rideout et al., 2005b; Trippel and Neil, 2004), walleye Pollock Theragra chalcogramma (Hinckley, 1990), turbot Scopthalmus maximus (McEvoy and McEvoy, 1991), Atlantic cod G. morhua (Chambers and Waiwood, 1996; Kjesbu, 1989; Ouellet et al., 2001; Trippel, 1998) and goby Pomatoschistus marmoratus (Mazzoldi et al., 2002). The reverse pattern has been noted for autumn spawning species, where the eggs increase in size during the spawning season (Chambers, 1997). The general synthesis of these patterns, including species that spawn all year-round, is the smaller eggs are produced late spring through summer when temperatures are relatively warm, and larger eggs are produced in late autumn through winter when waters are colder (Chambers, 1997). There are exceptions to this general trend, for example, silverside (Menidia menidia) unfertilised egg diameter was not different between eggs spawned early or late in the season; however, lower incubation temp caused significantly greater length at hatching (Bengston et al., 1987). Other seasonal changes include a within-season change in offspring sexratio, which appears to be maternally determined, for example, male bias early in breeding season for frog (Sakisaka et al., 2000), and female bias early in breeding season for fish, M. menidia (Conover, 1984). A seasonal decline in the size of larval morphological traits, including standard length, myotome height, eye diameter, jaw length, yolk area and finfold area occurred from early to mid to late season, and survival was reduced late in the season at low food levels (haddock M. aeglefinus, Rideout et al., 2005b). 2.2.3. Temperature Temperature fluctuations in aquatic environments are generally less than those in terrestrial systems because the large heat capacity of water acts as a thermal buffer; however, temperature still varies on both temporal (e.g., daily, seasonal) and spatial scales in aquatic systems. Temperature determines the rate of metabolism and growth in ectotherms such as fish, and can modify the trajectory of development in early life history stages. It is one of the most commonly studied environmental parameters affecting maternally mediated traits in aquatic ectotherms, and can affect offspring traits though a number of mechanisms. Temperature can directly influence female metabolism during oogenesis, vitellogenesis or pregnancy, and once offspring are liberated from the females, the temperature they experience in the maternally selected environment can further influence phenotypic traits (e.g., rotifers Synchaeta pectinata, Stelzer, 2002). Temperature experienced by the offspring interacts with maternal effects and influences a range of offspring traits in ectotherms, including growth (A. melanopus, Green and McCormick, 2005a), gender (M. menidia, Conover, 1984), performance, such as swimming ability (A. melanopus, Green and Fisher, 2004), survival

18

Bridget S. Green

(A. melanopus Green and McCormick, 2005a), time to hatch (Oncorhynchus tshawytscha, Heath et al., 1993) and size at hatching (Pleuronectes ferrugineus, Benoit and Pepin, 1999). The complexity of the ‘maternal effects’–‘environmental temperature’ relationship is demonstrated in a range of taxa, the eggs of many of which are generally easier to raise and manipulate in large numbers than for fish. For most of the experiments described below it would be difficult to replicate the scale of experimentation on fish. Embryonic survival, age and size at hatching of the offspring of frogs (Rana temporaria) collected from a range of latitudes and raised in a half-sibling design with varying temperatures were strongly affected by an interaction of maternal effects and temperature, whereby frog embryos from different populations differed in developmental time, not linearly related to temperature (Laugen et al., 2003a). In a very different ectotherm taxa, the rotifer, temperature of the maternal environment directly and considerably affected offspring size through differential maternal allocation, an effect which snowballed until adult size was reached (Stelzer, 2002). Rotifers are an ideal model for partitioning out maternal and environmental effects as they can be bred to reproduce only parthenogenically, thereby removing the effects of cross breeding (Stelzer, 2002). Temperature may interact with a large range of female traits to influence offspring, eliciting sometimes subtle responses, for example, female temperature environment interacted with the number of mates and influenced egg viability in dung flies (Tregenza et al., 2003). In squid, temperature was not an important influence on number of eggs, survival or lipid content in eggs, whereas female ration had highly significant effects on these measures of offspring quality (Steer et al., 2004). In fishes, the effect of temperature on maternally mediated offspring traits varies considerably between species and with latitude, and there are large differences in seasonal temperature range with latitude. Tropical and temperate examples are provided separately here, but as phylogenetic differences have not been addressed, an overall difference in the response of animals from these ecosystems is not implied. An apparent time-lag between an environmental temperature and the expression of its influence on offspring through maternal effects depends on the duration of oogenesis and vitellogenesis, which can occur over many months in fishes depending on their reproductive strategy. In fishes with determinate fecundity, where egg production is set before the spawning season (predominantly a trait of temperate latitude fish), environmental conditions prior to the spawning season influence female fecundity and egg size. Warm temperature experienced by herring (Clupea sp.) 60–90 days before spawning led to a trade-off between egg size and number, resulting in the production of more numerous smaller eggs (Tanasichuk and Ware, 1987), and reduced temperature arrested vitellogenesis in virgin Atlantic cod G. morhua (Yoneda and Wright, 2005).

Maternal Effects in Fish Populations

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The expression of the maternal effect can depend on the prevailing temperature, influencing a fecund female or acting directly on the released offspring. Maternal effects interacted with temperature to affect variance in embryo development time in the yellowtail flounder P. ferrugineus (Benoit and Pepin, 1999). Sex ratio of Atlantic silverside, M. menidia, was influenced by a female-temperature interaction when exposed to differences temperatures regimes as embryos and larvae (Conover and Kynard, 1981). Survival of chum salmon (Oncorhynchus keta) eggs to hatching was highest at a mid-range egg incubation temperature, and there was an interaction of female size with incubation temperature resulting in lower survival at extremes of temperature for eggs from large females compared with eggs from smaller females (Beacham and Murray, 1985). A number of studies assess maternal or female effects and temperature effects separately, but do not explicitly analyse (or at least present the results of) a female  environment interaction (e.g., Bengston et al., 1987; Heath et al., 1993; H
ie et al., 1999a). Conversely, in aquaculture studies, females are more generally pooled to examine environmental effects such as temperature (e.g., Baynes and Howell, 1996; Yang and Chen, 2005), despite the facilities existing for close examination of these interactions. The site-attached habits of many tropical species (both pelagic and benthic spawning) make them ideal models to assess the interaction of environment and female and its effects on offspring traits. Despite this, few studies have assessed maternal and temperature effects in tropical fish. When examined over the range of temperature experienced under natural conditions, temperature had no apparent effect on the nest-tending behaviour of adult the red and black anemonefish, A. melanopus (Green and McCormick, 2005b). In a diallel cross experiment on the same species, temperature interacted with male and female parent and influenced growth rate and mortality of larvae, but not size at metamorphosis, and temperature interacted with female identity to influence swimming ability of pre-settlement fish (Green and McCormick, 2005a). 2.2.3.1. Environmental clines in growth Latitudinal or altitudinal clines in growth and reproductive factors occur in ectotherms, and are generally thought to be the response of ectotherms to temperature or seasonality varying along a physical and geographical gradient, for example, lizards (Forsman and Shine, 1995), fish (Schultz et al., 1996) and frogs (Laugen et al., 2003b). While such a gradient of effects on offspring traits are sometimes relegated to genetic drift between geographically isolated populations (e.g., fishes; Yamahira and Conover, 2002), maternal effects are also a source of this variation (e.g., frogs; Laugen et al., 2002). Maternally mediated differences in egg size contribute to population divergence along with genetic divergence; however, maternal effects seem not to override the genetic differences apparent in some populations over a large scale (Laugen et al., 2002). Combined latitudinal and maternal effects have been described in insects

20

Bridget S. Green

(Mousseau and Dingle, 1991), lizards (Sinervo and Adolph, 1994), fish (Brown et al., 1998) and frogs (Laurila et al., 2002). A meta-analysis of egg size variation in coho salmon (Oncorhynchus kisutch) attributed the observed variation in egg size to the variability both within (female) and between population (latitudinal) effects (Fleming and Gross, 1990). 2.2.3.2. Environmentally determined sex determination In sexually labile species, the microenvironment in which a female deposits her eggs or larvae can determine the sex of offspring, providing a unique avenue for the expression of a maternal effect or influence. Temperature-dependent sex determination (TSD) operates over seasonal gradients as well as small scale physical gradients, and is linked to the thermal regime the eggs or larvae experience. In some reptiles, including crocodilians (Lang and Andrews, 1994), turtles (Ewert et al., 1994) and lizards (Warner and Shine, 2005), gender is commonly determined by the thermal regime the embryos experience during a thermosensitive period of embryonic development, and temperature is explicitly determined by the depth the females bury their eggs. (Recently, this finding has been challenged and advanced in lizards, where maternal nutrition also determined gender; Warner et al., 2007.) In gonochoristic fishes, temperature for development of the larvae and juvenile can also be critical to the gender determination of the offspring, and this has been linked back to the timing of spawning, particularly in temperate climates where there are marked seasonal fluctuations (in order of 20  C) in water temperature, for example, southern flounder Paralichthys lethostigma (Luckenbach et al., 2003) and Atlantic silverside M. menidia (Conover and Kynard, 1981). Fishes are facultatively flexible about where and when they lay their eggs and this can engender a maternal component to sex determination and consequent sex ratio differences within a population. Additionally, there is significant ‘between female’ variation in offspring sex ratio, even when the females are experimentally spawned at the same time, for example, M. menidia (Conover and Heins, 1987a; Conover and Kynard, 1981; Lagomarsino and Conover, 1993). A series of laboratory experiments demonstrated a maternal (Conover and Heins, 1987b; Conover and Kynard, 1981) and paternal (Conover and Heins, 1987b) component interacting with a simulated seasonal environmental shift resulting in temperature-dependant sex determination in M. menidia. Most approaches to measuring TSD in fishes demonstrate a female effect indirectly by experimentally manipulating temperature of a clutch to simulate seasonal shifts. Sex determination is generally set late in larval development, for example, M. menidia (Conover and Kynard, 1981), Odonthesthes bonariensis and Patagonia hatcheri (Stru¨ssmann et al., 1997) or within a restricted window related to size, for example, marbled sole, Limanda yokohamae (Goto et al., 2000), though some species are sensitive to TSD throughout larval development, for example, sea bass D. labrax (Koumoundouros et al., 2002). TSD was not

21

Maternal Effects in Fish Populations

found in northern populations of two cyprinodontid fishes, F. heteroclitus and Cyprinodon variegates either in the field or in the laboratory (Conover and Demond, 1991). The influence of maternal effects through TSD may have fitness implications. Labile sex determination is an advantage when individual fitness in a particular environment is gender dependent (Conover, 1984; Conover and Heins, 1987a) and can occur across a season to favor growth of one sex over the other if reproductive success depends on size, for example, Atlantic silverside M. menidia (Conover, 1984), tidewater silverside M. peninsulae (Yamahira and Conover, 2003), sea bass Dicentrarchus labrax (Koumoundouros et al., 2002), and two atherinids O. bonariensis and P. hatcheri (Stru¨ssmann et al., 1997). There are two reported reaction norms for TSD within a population. Firstly, there is an inverse relationship between temperature during larval development and proportion of offspring that differentiate as females (Fig. 1.1; M. menidia, Conover and Kynard, 1981; Odontesthes bonariensi and P. hatcheri, Stru¨ssmann et al., 1997). That is, as temperature experienced during larval development increases, the proportion of female offspring in a clutch decreases, resulting in a male bias at warmer temperatures. The second reported response is that high and low temperatures induce a male biased sex ratio and mid-range temperatures induce a 1:1 sex ratio (Fig. 1.1; southern flounder P. lethostigma, Luckenbach et al., 2003; hirame P. olivaceus, Yamamoto, 1999). The apparent differences in the shape of the response curve of gender expression to temperature may arise if the range 100 80 60 40 20 0 14

16

18

20

22

24

26

28

Temperature ⬚C

Figure 1.1 Temperature determined sex determination in early life history stages of six fish species. ‘% females’ represents the proportion of each clutch that expresses the female gender. —Pejerrey, Odontesthes bonariensis (atherinid) (Str€ ussmann et al., 1997), D—P. hatcheri (atherinid) (Str€ ussmann et al., 1997), □—southern flounder, Paralichthys lethostigma (Luckenbach et al., 2003), x—European sea bass, Dicentrus labrax (Koumoundouros et al., 2002), x—barfin flounder, Verasper moseri (Goto et al., 1999), ▲—hirame, Paralichthys olivaceus (Yamamoto, 1999).

22

Bridget S. Green

of temperatures each species is tested at represents only a portion of the possible range of temperatures larvae might experience in the wild during the thermosensitive stage. For example, marbled sole L. yokohamae (Goto et al., 2000), barfin flounder Verasper moseri (Goto et al., 1999) and sockeye salmon Oncorhynchus nerka (Azuma et al., 2004) were only tested over two temperatures, and so it is inconclusive if the relationship between temperature and sex ration is linear or whether the observed linear relationship is part of a bell-shaped curve. Most importantly, in the context of maternal effects, these experiments suggest that seasonal timing of spawning and the accompanying temperature shifts could introduce a maternal or female effect on offspring quality due to the influence temperature has on offspring sex ratio. Maternal effects throughout a spawning season can alter sex ratios in frogs (Sakisaka et al., 2000) and fishes (Conover and Kynard, 1981). This is thought to be adaptive to either maximise investment or maximising time to development of males by producing them early in the season. This is particularly for species where males can reproduce in their first year, but the females take two years. By producing males early in the season there is an increased chance that some offspring will reproduce within 12 months which increases the parents’ reproductive fitness. 2.2.4. Salinity Salinity levels of aquatic systems vary from 0 to 36 parts per thousand (ppt) and some systems fluctuate seasonally due to rainfall or aseasonally due to oceanic upwellings, downwellings or seeps. Oceanic ecosystems have a relatively stable salinity around 35 ppt (except the Red and Baltic Seas), and most freshwater streams by definition have salinities of zero; landlocked lakes may have high salinities and inland seas, such as the Baltic Sea, may have distinct haloclines. Salinity in transitional environments at the fringe of land and sea, such as estuaries, littoral zones and inland seas can fluctuate widely with season and particularly with rainfall in watershed areas (see discussion in Wootton, 1990). An interaction of maternal effects and salinity on offspring quality will most likely occur in estuarine and inshore species where the largest salinity fluctuations are experienced. Changes in salinity in transitional environments can create some level of physiological stress in the resident fishes as the physiological cost of responding to changes in salinity may be at the expense of processes such as growth or reproduction, and reproduction in euryhaline species may be inhibited by freshwater influx (Billard et al., 1981). An interaction of maternal effect and salinity is also of interest in the aquaculture industry, where an option of rearing anadromous species in freshwater water without affecting growth or reproduction may reduce maintenance requirements and costs. The few studies examining the interaction of salinity and maternal effects have demonstrated that salinity changes affect a range of both female reproductive and offspring traits. Mangrove rivulus (Rivulus marmoratus)

Maternal Effects in Fish Populations

23

reared at lowered salinity matured later and at larger sizes than fish at ‘normal’ or high salinities, and also produced fewer, larger eggs which had higher hatching success and decreased time to hatching (Lin and Dunson, 1995). Salinity exposure of females enhanced the salinity tolerance of their offspring in the guppy (P. reticulata), increasing survival under high salinity exposure (Shikano and Fujio, 1998a,b). Indirect interactions between maternal effects and salinity occurred in Baltic cod (G. morhua) where neutral buoyancy is critical for egg survival. Oxygen poor water predominates beneath a halocline of this inland sea, and to compensate, larger females produced larger eggs with neutral buoyancy at a lower salinity, which float above the halocline and therefore above the oxygen poor water, facilitating survival in the unusual conditions of the Baltic Sea (Vallin and Nissling, 2000). Under high salinity, males can show decreased parental care of eggs, including reduced fanning and egg-cleaning in the Florida Flagfish Jordanella floridae (St Mary et al., 2001). 2.2.5. Prey abundance and quality Prey availability influences the resources available to a female for oogenesis and reproduction, for example, Atlantic cod G. morhua (Dossantos et al., 1993). When quality or abundance of food is limited to the adults it may result in a trade-off in size, quality or number of eggs produced by the females (Gagliano and McCormick, 2007), or may result in more variability in offspring quality within a clutch, for example, lizards (Warner et al., 2007), or reproductive investment may be reduced, for example, lizards (Du, 2006) and fish Acanthochromis polycanthus (Donelson et al., 2008). Seasonal cycles or pulses of high quality food can increase the energy available to a female, which in turn increases female condition, enabling her to allocate more resources to reproduction and ultimately the number or quality of offspring, for example, fish P. amboinensis (Kerrigan, 1997; McCormick, 2003). In polychaete worms (Capitella sp.), an increase in adult food quality enabled the adults to grow twice as fast, produce more, smaller eggs, which were larger in volume and energy content than broods produced by siblings on a lesser diet (Qian and Chia, 1991). In some terrestrial vertebrates, if food is a marginal resource, the female may skip a reproductive season in favour of growth, and an increase in size may increase fecundity the following year, for example, Galapagos finches (Hau et al., 2004) and water skinks (Schwarzkopf, 1993). Such flexible allocation is not universal though and some animals will reproduce regardless of the resource availability, for example, common frogs R. temporaria (Lardner and Loman, 2003). It is more difficult to track seasonal or annual effects of food availability in fishes as they are highly mobile and difficult to recapture or observe during spawning. The effects of prey availability on reproductive investment is most effectively studied in wild populations where the dynamics of costs and

24

Bridget S. Green

cost avoidance can be measured (Schwarzkopf, 1993) and individual prey consumption, growth and reproduction can be measured. The discrete habitat use by many terrestrial vertebrates and insects lends them to such an examination; in contrast, many fishes are highly mobile and often difficult to track over any length of time. Tropical fishes are good models to investigate the effects of food availability on maternal effects and reproductive quality because many species are site attached and lay benthic eggs, and so female and offspring quality can be tracked over time, relative to abundances and quality of natural prey items. For example, lipid rich coral propagules released in a mass spawning event (occurring once per lunar month over 2 or 3 summer months) increased female condition, and subsequent eggs spawned had larger yolk sacs and oil globules (McCormick, 2003). In two similar experiments, wild nesting female Pomacentrus amboinenesis supplemented with a pulse of high quality food during the reproductive season produced eggs with larger yolk-sacs than field controls that were not supplementary fed (Gagliano and McCormick, 2007; Kerrigan, 1997). Increased yolk-sac size, however, did not result in larger larvae at hatching in either study, an unexpected result which is symptomatic of the complexity of the influence of field variables on maternal and offspring traits (Gagliano and McCormick, 2007; Kerrigan, 1997). The direct effects of prey abundance and nutritional quality on fish reproduction are more difficult to measure in wild populations of temperate and/or pelagic fish because many fish are mobile and few temperate fishes guard demersal eggs. Also, typically fishes must be destructively sampled to determine spawning status. Indirect measures are generally used to estimates the influence of prey abundance on offspring quality. Interannual fecundity estimates may be correlated to the quality and quantity of prey items coinciding with oogenesis, for example, ArctoNorwegian cod G. morhua (Kjesbu et al., 1998); or the amount of fat storage, which is seen as an indicator of nutritional status, for example, Baltic herring C. harengus (Rajasilta, 1992). Instances of skipped spawning in female teleosts have been demonstrated microscopically in a variety of species including G. morhua, P. americanus, Reinhardtius hippoglossus, Hoplostethus atlanticus, M. aeglefinus, Pleuronectes platessa, Acanthopagrus australis, Solea solea, S. maximus, D. labrax and Microstomus pacificus (Rideout et al., 2005a). A short modelling exercise in that review demonstrated that there could be a benefit to total lifetime reproductive output in skipping a spawning season as chance of mortality is reduced (Rideout et al., 2005a). Skipped spawning in fishes is believed to be a response to poor nutrition, although this is typically based on fishes kept in captivity (Ali and Wootton, 1999; Burton, 1994; Burton and Idler, 1984; Hislop et al., 1978; Ma et al., 1998; Rijnsdorp, 1990), as there is little definitive field evidence of reduced food availability causing spawning omission. Generally, direct evidence of a link between prey abundance and reproduction is

Maternal Effects in Fish Populations

25

difficult to demonstrate in mobile pelagic spawning fish, but can be inferred through correlative studies. As noted in other sections of this review, the natural environment is complex and trade-offs in egg attributes and maternal food abundance interact with other environmental variables such as offspring prey density, oxygen availability and competition, making it difficult to isolate maternal effects as the sole source of offspring variation. Winemiller and Rose (1993) modelled larval fish survival under different initial size and number scenarios including prey density. In a virtual variable environment it paid to be big, but when prey was abundant, more small fishes survived, thereby increasing parental fitness. In laboratory experiments simulating some level of environmental complexity, reproductive quality of R. marmoratus, a self-fertilising hermaphrodite inhabiting estuaries, was influenced by an interaction of maternal food availability and salinity. Under high feeding levels, females produced larger eggs than individuals under low feeding levels, and when high food was combined with high salinity the size advantage increased (Lin and Dunson, 1995). One of the pathways through which food availability affects egg size is within a clutch due to proximity to the blood vessels within the ovary. Under low prey abundance (food is limiting), eggs positioned closest to the blood vessels within the ovary gain a size advantage over those further from the blood vessels (Kamler, 1992). Efforts to enhance reproductive output in the aquaculture industry provide numerous examples of the influence of maternal food quality on fecundity, reproductive output, and egg and larval quality, and while these are generally not analysed as a true maternal effect (in the narrow sense), they can be considered a female effect or female influence. As the aquaculture industry is aimed at maximising production whilst minimising cost, a wide range of broodstock food types, quality and abundances have been tested for their effects on egg and offspring quality. Fecundity in continuous spawners with short vitellogenic periods is influenced by essential dietary nutrients (Izquierdo et al., 2001). Broodstock dietary lipid enhancement does not always affect traditional fecundity and offspring quality measures such as egg number, egg weight, fertilisation rate, hatching, survival to and weight at first feeding; however, increased dietary lipid resulted in a reduced amount of fatty acids in the eggs and larvae, for example, Atlantic salmon S. salar (Rennie et al., 2005) and Atlantic halibut Hippoglossus hippoglossus (Mazorra et al., 2003). Quality of polar lipids (e.g., walleye Stizostedion vitreum, Czesny and Dabrowski, 1998) and protein (e.g., sea bass D. labrax, Cerda et al., 1994a,b, 1995) in the maternal diet can affect factors such as egg buoyancy and egg and larval survival. Dietary supplements of astaxanthin and paprika powder increased egg production, egg quality and larval survival in yellowtail (Seriola quinqueradiata), and astaxanthin increased fecundity in striped jack, Pseudocaranx dentex (Watanabe and Vassallo-Agius, 2003). These are only a few of numerous examples of broodstock nutrition

26

Bridget S. Green

trials and their impacts on offspring. Izquierdo et al. (2001) have compiled a more comprehensive review of specific effects of broodstock nutrition on reproductive quality. 2.2.6. Contaminants Anthropogenic pollutants (xenobiotics) derived from industry, farming, urban gardening practices and sewage disposal are often transferred into the surrounding aquatic ecosystems. Xenobiotics can directly affect fish health and reproduction through endocrine disruption and damage to neural processes, and can be transferred from female to her offspring via vitellogen in eggs. Oviparous fishes mobilise fat stores (vitellogen) from hepatic lipids to produce eggs, and these lipophilic fat stores are a major area of bioaccumulation of organic contaminants. The maternal transfer of xenobiotics to embryos is a major concern particular to oviparous organisms because they do not have the mechanism for protecting the developing foetus from exposure to contaminants that viviparous organisms have (Vannier and Raynaud, 1975). Furthermore, developing embryos are generally more sensitive to contaminants than adults and can be adversely affected by relatively small quantities (Wiener and Spry, 1996 referred to in Hammerschmidt et al., 1999) as the signals for organisation, cellular differentiation, organogenesis and growth are endocrinal, and minute quantities of contaminants can influence or interrupt the flow of these signals. Although the major route of exposure to such contaminants for a developing embryo is the maternal deposition into the oocyte (Westerlund et al., 2000), nest-site selection can play a role in benthic eggs as there is opportunity for exposure to xenobiotics from the sediment and water. Contaminants can enter the female via contact with sediment, water or food. Pesticides such as PCB and DDT can inhibit reproduction (Billard et al., 1981) and can accumulate and affect offspring viability (summarised in Billard et al., 1981). Contaminant effects on development include sublethal effects such as reduced hatchability, deformities, increased time to hatch; and lethal effects such as embryo and larval mortality (Table 1.2). Laboratory maternal exposure to a range of PCB (polychlorinated biphenyls) congeners resulted in transfer to the oocyte and embryo mortality in zebrafish (D. rerio) (Westerlund et al., 2000). Reduction in fecundity and quality of eggs and larvae has been associated with many endocrine disruptors such as PCBs, TBT and DDT (Table 1.2), and there are many demonstrations of a direct relationship between the body burden of xenobiotics of wild-caught females and her eggs with detrimental effects on the embryos, for example, sockeye salmon O. nerka (Debruyn et al., 2004), starry flounder Platichthys stellatus (Spies and Rice, 1988), English sole Parophrys vetulus (Collier et al., 1992), mummichog F. heteroclitus (Black et al., 1998) and from laboratory studies that experimentally contaminate females, for example, Japanese medaka Oryzias latipes (Nakayama et al., 2005; Nirmala et al., 1999) and

Table 1.2

Summary of the effects of contaminants on offspring, via a maternal effect or simulated maternal effect

Exposure and source

Reproductive or offspring trait examined for an effect

Negative effect found Reference

f, w, an f, l, an

Survival of offspring Blue sac syndrome

No Yes

Johnston et al. (2005) Heiden et al. (2005)

Common name

Species name

Contaminant

Walleye Zebrafish

Sander vitreus Danio rerio

Japanese medaka

Oryzias latipes

s, l, an

Bradycardia

Yes

Colman et al. (2005)

Japanese medaka

O. latipes

Organochlorines TCDD (endocrine disruptor) AZA-1 (phycotoxin, ie from toxic algae) AZA-1

s, l, an

Yes

Colman et al. (2005)

Japanese medaka

O. latipes

AZA-1

s, l, an

Yes

Colman et al. (2005)

Japanese medaka Japanese medaka

O. latipes O. latipes

AZA-1 AZA-1

s, l, an s, l, an

Yes Yes

Colman et al. (2005) Colman et al. (2005)

Japanese medaka

O. latipes

AZA-1

s, l, an

Yes

Colman et al. (2005)

Japanese medaka Japanese medaka Japanese medaka

O. latipes O. latipes TBT

TBT TBT f, l, an

f, l, an f, l, an Swim-up failure

Reduced hatching success Retarded development Reduced viability Reduced somatic growth Delayed onset of blood circulation and pigmentation Fertilisation success Hatching success Yes

Yes TBT Yes

Nakayama et al. (2005) Nakayama et al. (2005) Nakayama et al. (2005) (continued)

28 Table 1.2

(continued)

Common name

Species name

Contaminant

Exposure and source

Japanese medaka

O. latipes

TBT

f, l, an

Japanese medaka

O. latipes

PCB

f, l, an

Sockeye salmon

Oncorhynchus nerka

PCB, PCD, PCDF (hydrophobic organic contaminants)

f, w, an

Starry flounder

Platichthys stellatus

PCB

f, w, mr

English sole

Parphrys vetulus

PCB

f, w, mr

Japanese medaka American plaice

O. latipes Hippoglossoides platessoides O. latipes O. latipes

DDT Organics

f, l, an m

TBTPCB TBTPCB

f, l, an f, l, an

Japanese medaka Japanese medaka

Reproductive or offspring trait examined for an effect

Negative effect found Reference

Yes

Nakayama et al. (2005)

Yes

Nakayama et al. (2005)

Yes

Debruyn et al. (2004)

Yes

Spies and Rice (1988)

No

Collier et al. (1992)

Larval productio

No Yes

Metcalfe et al. (2000) Nagler and Cyr (1997)

Spawning frequency Number of eggs

Yes Yes

Nirmala et al. (1999) Nirmala et al. (1999)

Abnormal eye development (small or no eyes) Increased time to hatch Increased concentration in eggs (to level associated with 30% egg mortality) Embryological success Reproductive success

Japanese medaka Japanese medaka

O. latipes O. latipes

TBTPCB TBT

f, l, an f, l, an

Winter flounder

Pseudopleuronectes americanus

PCB

f, w, est

Rock sole

Pleuronectes bilineatus Pleuronectes bilineatus

AH (aromatic hydrocarbons PCB

Rock sole

Yes Yes

Nirmala et al. (1999) Nirmala et al. (1999)

Yes

Black et al. (1988)

f, w, mr

Fertilisation success Reduced embryo survival Smaller larvae (length and weight) Egg weight

Yes

Johnson et al. (1998)

f, w, mr

Egg weight

Yes

Johnson et al. (1998)

f, female; s, simulated (i.e., directly to embryo); m, male; l, laboratory; w, wild contamination; fw, freshwater; mr, marine; est, estuarine; an, anadromous; , negative effect.

29

30

Bridget S. Green

fathead minnow (Hall and Oris, 1991; see Table 1.2 for more details). Bleach draft mill effluent increased age to maturity, reduced fecundity and egg size in the white sucker Catostomus commersoni (Munkittrick et al., 1991). The concentration of organic contaminants in the female ovaries can be magnified in fishes that undergo a spawning migration, for example, Pacific salmon, sockeye salmon (O. nerka) as they deplete lipids to fuel their migration, resulting in a concentration of contaminant in ovarian tissue which can then be passed onto the eggs (Debruyn et al., 2004). The cross-generational anthropogenic contaminant effects on fishes and their offspring are not isolated to highly industrialised regions. Maternal transfer of toxic levels of mercury to eggs (yellow perch, Perca flavescens) has been identified in remote lakes where the mercury was anthropogenic, derived from atmospheric deposition (Hammerschmidt et al., 1999). Xenobiotics can influence offspring quality through the male parent also. Reproductive performance of male American plaice (Hippoglossoides platessoides) was compromised by exposure to contaminated sediments resulting in reduced egg fertilisation success (Nagler and Cyr, 1997). More comprehensive summaries of the levels and types of contaminants and a more extensive summary of the range of their effects on offspring have been collated and reviewed by other authors (Kime, 1995; Rolland, 2000; Van deer Meeren and Næss, 1993). 2.2.6.1. Adaptation to anthropogenic change A potential source of variation in population traits is the influence of anthropogenic changes to the environment that can act to promote adaptive changes, nominally through maternal effects, or non-additive genetic influences. Such effects can be seen through local adaptation to acidity in the egg capsules and hatching size of amphibians, for example, Rana arvalis (Pierce and Harvey, 1987; Ra¨sa¨nen et al., 2003), inducible defence mechanism in Daphnia against toxic cyanobacteria which it can pass to its offspring (Gustafsson et al., 2005) and adaptation in fishes, including tomcod, Microgadus tomcod (Yuan et al., 2006) and mummichogs, F. heteroclitus (Nacci et al., 1999) to contamination by dioxin-like compounds. One consequence of this adaptation is that while the fishes do not show an adverse reaction, they are still likely to be bioaccumulating the contaminant, which can then be transferred along the food chain to higher consumers (Kime, 1995).

2.2.7. Other environmental effects and maternal effects 2.2.7.1. Stress: Competition, predator and culture conditions Stressful ecological or aquaculture conditions, caused by factors such as predator threat, conspecific competition or sub-optimal husbandry, can have adverse affects on the condition of females and her offspring. In general, stress in vertebrates increases production of glucocorticosteriods which can have a suppressive effect on reproductive endocrinology (see review in Schreck et al., 2001).

Maternal Effects in Fish Populations

31

Consequently, a stressful environment for a female can result in reduced quality of offspring (fish, McCormick, 1998 and birds, Saino et al., 2005). Cortisol is the most commonly measured stress response in female teleosts that affects offspring quality. In a common territorial tropical fish P. amboinensis, density of females interacting with breeding mothers elicited an increase in maternal cortisol levels and decreased the size of larvae produced (McCormick, 2006). A previous manipulation of the same species, which increased the visual competitor signal but not the interaction by housing a conspecific female in a clear container close to the nesting female, resulted in larvae that were larger (approximately 3% longer with 2% greater head depth) than larvae from females that spawned in isolation (Kerrigan, 1997). Acute stress, and accompanying increase in cortisol levels in the months leading up to ovulation lead to a reduction in egg weight and volume, but not the number of eggs produced by female rainbow trout (Oncorhynchus mykiss), lower sperm counts in males and reduced survival of offspring (Campbell et al., 1992). When the effects of stress were examined only over the final stages of maturation in the rainbow trout, stress applied early in vitellogenesis resulted in smaller eggs and larvae (Contreras-Sanchez et al., 1998). Experimentally elevated maternal corticosteroid in European starlings resulted in a female-biased sex ratio in the offspring, as well as lighter, slower growing males at hatching, which the authors suggest is an adaptive response to an uncertain environment (Love et al., 2005). It is likely more commonalities in the effects of stress on offspring will unfold as more species and pathways are examined. 2.2.7.2. Oxygen Oxygen can be limiting in aquatic systems, and particularly in enclosed or semi-enclosed waterways where eutrophication occurs, stagnant, slow-moving still waters, or close to the benthos where some fishes deposit their eggs. The egg stage is the most likely stage where a maternally mediated effect of environmental oxygen might be manifest, as most other stages of a fishes life are mobile, allowing fish to modify their behaviour to avoid low oxygen (Breitburg, 1994). Oxygen supply to the eggs can be a critical determinant of developmental success (Chaffee and Strathmann, 1984; Ferna´ndez et al., 2003) and some species of fish choose nest sites with reference to the oxygen environment ( Jones and Reynolds, 1999; Lukas and Orth, 1995; Takegaki, 2001), or tend their nest to compensate for sub-optimal oxygen conditions (Green and McCormick, 2005b; Takegaki and Nakazono, 1999). Maternal choice of spawning or nesting site relative to oxygen content can impinge on the quality of offspring, and conversely, environment quality may restrict the value of female reproductive investment. Larger eggs are typically viewed as a better reproductive investment, however larger eggs require more oxygen, and as egg volume increases, the relative surface area decreases, resulting in an increased need for oxygen concurrent to a reduced relative surface for oxygen diffusion.

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Bridget S. Green

As oxygen is limiting in many benthic habitats, particularly those used for spawning by salmonids, being a large female is only useful if you can access the best spawning sites relative to oxygen content, otherwise, producing large eggs will reduce fitness as large eggs have less chance of surviving when oxygen is limiting (Hendry and Day, 2003; Hendry et al., 2001). If oxygen is limiting, then the expectation from models is that larger eggs are a disadvantage (Einum et al., 2002; Hendry et al., 2001). However, contrary to this prediction, while brown trout (Salmo trutta) egg mortality was higher for all eggs under reduced oxygen conditions, smaller eggs suffered higher levels of mortality than larger eggs under the same low oxygen conditions. The authors suggested that reduced survival in smaller eggs may be due to a reduced ability to cope with stress of low oxygen (Einum et al., 2002). Asynchronous development due to reduced oxygen availability is common in aquatic taxa that produce egg masses, particularly three-dimensional egg masses, for example, crabs (Ferna´ndez et al., 2003), gastropods (Chaffee and Strathmann, 1984; Lardies and Ferna´ndez, 2002) and squid (Steer et al., 2003), and is dependent to some degree on how parents construct the egg mass and nest. Other pathways for a maternal effect to interact with oxygen availability include nest site choice with reference to oxygen availability, for example, gobies ( Jones and Reynolds, 1999) and smallmouth bass Micropterus dolomieu (Lukas and Orth, 1995; Takegaki, 2001), and nest-tending to compensate for low oxygen (Green and McCormick, 2005b; Takegaki and Nakazono, 1999). Nest tending directly increases the amount of oxygen available to the eggs, and parents increase their tending activity when ambient oxygen is low, for example, anemonefish A. melanopus (Green and McCormick, 2005b). Further examples and implications of parental nest-tending on offspring environment will be discussed in the section on nest-tending. 2.2.8. Adaptive transgenerational plasticity The relative importance of a maternal effect to offspring quality and viability may depend on the environment the offspring encounter (Reznick, 1991; Reznick et al., 1996). One line of theory suggests that maternally derived phenotypic differences in offspring traits reflect adaptations by the female to varying environmental conditions that would be met by the offspring (Heath and Blouw, 1998; Hinckley, 1990; Plaistow et al., 2004). This should increase the chance the offspring will survive, therefore maximising the female’s lifetime reproductive fitness. Such adaptive maternal effects have been referred to as ‘cross-generational norms of reaction’ and may apportion a role in evolution to maternal effects (Riska, 1991). Life history theory predicts a shift towards fewer larger propagules where conditions for juvenile growth are poor, for example, low resource abundance, high competition and high predation ( Johnston and Leggett, 2002); that is, if a female takes low food as a cue for harsh conditions then it is optimal for them to lay few, better provisioned eggs that grow faster and are more likely

Maternal Effects in Fish Populations

33

to survive (Plaistow et al., 2004), and the reverse is expected under a contrasting set of environmental conditions (also known as ‘negative covariance’; Crump, 1981). There is limited evidence across all taxa supporting this theory. Plasticity could well be just a ‘spandrel’, that is, something functional or beautiful that was ‘undesigned’, which only exists as a sideeffect of a true adaptation (Gould and Lewontin, 1979); or an unavoidable consequence of physiological constraints (see Heath and Blouw, 1998; Stelzer, 2002). There are three main criteria for adaptive maternal effects to occur: (1) ecologically important variation exists among offspring environments, (2) cues in the maternal environment give reliable information about the offspring environment and (3) that mothers can alter the phenotype of their offspring in a way that is adaptive for the anticipated environment (Spitzer, 2004). Given these criteria and the difficulty in tracing environment through the life-cycle of a vertebrate, there are few examples of adaptive maternal effects in vertebrates. Female scop owls (Otus scops) can bias the sex of their offspring at egg production to invest differentially in their survival and growth to favour one sex over the other (Blanco et al., 2002), and acid tolerance on frog embryos (R. arvalis and Rana sylvatica) occurs when a female has encountered high acid levels (Pierce and Harvey, 1987; Ra¨sa¨nen et al., 2003). Maternal effects are sometimes not apparent until offspring are in a variable environment, for example, salamanders maternal  environmental effects (Semlitsch and Gibbons, 1990). A caveat for transgenerational adaptive plasticity to occur is that the parental environment is predictive of the future environment (Mousseau and Fox, 1998) and consequently its expression is dependent on the mode of reproduction. Mammals and birds have long incubation and post-birth offspring care, and it is in life-histories such as these that the current environment may be predictive of the future environment and therefore be an opportunity to capitalise on transgenerational plasticity. Maternal effects are strongest in early life stages of mammals, stages which are thought to be a more important contribution to evolutionary change. Transgenerational adaptive plasticity is more commonly reported in insects where the host– herbivore interactions are more specialised, and the offspring will spend its’ entire life cycle with a parentally chosen seed or fruit (e.g., Fox et al., 1997). When the insect–host relationships are general, transgenerational adaptive plasticity is harder to detect (e.g., Spitzer, 2004). Many fish have dispersive offspring, and prepare for and produce eggs a long way, both temporally and spatially, from where the offspring will grow. Consequently, it would be difficult for parents to predict a future environment as it is uncertain in which environment the propagules will be. The hypothesised adaptive plasticity is difficult to investigate and find support for in fishes (Bernardo, 1996). A transgenerational fitness effect would most likely be detected in species that can change their pattern of allocation to their offspring in response to

34

Bridget S. Green

environmental change. Viviparous fishes such as guppies are a good model as they can recruit fat stores for a litter immediately prior to producing that litter, and they produce well-developed larvae that do not disperse far. This is in contrast to many other fishes, for example, winter flounder (P. americanus) where fecundity is determined in the spring preceding a winter spawning event (Burton, 1994), and larvae are dispersive. Guppy females responded to their food environment as predicted in life history theory by adjusting their investment in their offspring, when food availability was low they produced fewer larger, fatter offspring, and waited longer between broods to do this (Reznick and Yang, 1993).

2.3. Maternal attributes 2.3.1. Female identity Female identity generally is described as a maternal factor when no other measured female trait describes the variance in offspring traits. Female identity may encompass all the morphological, physiological and behavioural traits of a female discussed in the following sections. This ‘other’ grouping for the unexplained sources of offspring variance well represents the complexity of studying maternal effects in fishes and our limited understanding of all the factors influencing reproduction. Female identity has been documented as a factor influencing offspring variability and quality in a range of fish species, covering freshwater, estuarine and marine guilds. In a number of instances, when variance is ascribed to maternal identity, ecologically valuable differences in offspring traits between females (‘between female effect’) were identified, but the approaches were not fine-scale enough to determine whether there was a maternal effect in the narrow sense, or the more general ‘female effect’ (which can include genetic effects). There were between-female differences in the sex ratio of offspring in the silverside M. menidia, which interacted with environmental temperature of the larvae (Conover and Kynard, 1981); and female identity (but not female size or weight) interacted with male identity and temperature to effect larval growth, mortality, and swimming ability in the red and black anemonefish, Ampiprion melanopus (Green and McCormick, 2005a). The interaction of female and male identity explained between 7.6% and 32.8% of variation in Baltic cod (G. morhua) offspring traits, embryo survival, larval standard length, yolk-sac area, yolk utilisation and resistance to starvation (Trippel et al., 2005). Female identity explained a large proportion (82.5%) of variation in egg diameter and 22% in hatching length, and also interacted with temperature of offspring in the yellowtail flounder, P. ferrugineus (Benoit and Pepin, 1999). Maternal identity is most likely to arise as the sole significant female source of variance in offspring traits from studies with a small number of females (e.g., Green and McCormick, 2005a). The likelihood that a

Maternal Effects in Fish Populations

35

maternal effect could be attributed to gross morphological differences is reduced when sampled females represent only a narrow size range (Benoit and Pepin, 1999). Maternal identity in striped bass (Morone saxatilis) and capelin (Mallotus villosus) described variation in a range of traits (egg dry weight, oil volume, standard length and dry weight of hatchlings) that could not be explained by maternal weight (Brown et al., 1998; Chambers et al., 1989). Female identity described 35% of the variance in Atlantic cod (G. morhua) egg size, whereas no link could be found between length or mass of the female and her egg size (Chambers and Waiwood, 1996); and was significantly related to larval length, yolk volume, dry weight and DNA content in yellow perch P. flavescens (Heyer et al., 2001), embryo survival in rainbow trout O. mykiss (Nagler et al., 2000), hatch rate, and larval weight in Artic charr Salvelinus alpinus (De March, 1991). Maternal identity influenced length and weight of juveniles at 12 weeks, 6 months and 15 months in the Atlantic salmon S. salar, accounting for 9–28% of the variability, although family was not replicated in this design (Bailey and Loudenslager, 1986). Heart rate changes during ontogeny are more similar between siblings than non-siblings in snakes, frogs and birds throughout embryological development, suggesting a maternal influence, though the maternal trait responsible was not specified (Burggren, 1999). Female identity is a serviceable measure that some unidentified attributes of the source female have influenced quality or quantity in offspring in the absence of any other correlated trait, and may increase the chance of identifying the presence of a maternal influence or effect. 2.3.2. Female age For decades, maternal age has been identified as a source of variation in recruitment (Nikolskii, 1962) and offspring quality (Gall, 1974) within fish stocks. Adult longevity and age-based measures can influence population dynamics in fishes. Specifically, recruitment variation has been linked to female longevity (Longhurst, 2002), and the inclusion of age variation in models greatly improved the predictive power of the S/R relationship (Marteinsdottir and Thorarinsson, 1998). In broad-scale analyses, reproductive effort has been demonstrated to increase with age (Charlesworth and Leon, 1976; Roff, 1991), although whether this was a heritable trait or a maternal effect was not determined. The influence of maternal age on offspring quality is primarily of interest in fisheries because of its importance to year-class strength predictions that are traditionally employed to manage fish stocks and estimate maximum sustainable yield. Age is generally used for population analyses, tracking cohorts through time, estimating number in the next cohort after emigration natural mortality and fishing mortality. Age-length relationships for a population, such as the von Bertalanffy growth function, are applied to estimate the size and biomass of a cohort.

36

Bridget S. Green

The utility of age to estimate population-level trends does not automatically translate to a relationship between individual female age and indices of recruitment. In fact, the extension of this link from population to individual is a common ecological fallacy. Maternal age has recently received high profile attention and was hypothesised, but not directly demonstrated, to be an important element of variation in recruitment in fisheries (Berkeley et al., 2004a,b; Birkeland and Dayton, 2005; Bobko and Berkeley, 2004; Palumbi, 2004). Rather these studies refer to a positive relationship between female age and offspring condition. A positive correlation between a single female trait and an offspring trait in 17 individuals in a laboratory does not confer a similar trend in the field where a range of pressures are acting. Similarly, it does not infer effects of overfishing as implied in each of these manuscripts. The extrapolation of laboratory results from a number of small individuals to entire populations, and from one trait to recruitment are frequent misrepresentations of the expression and importance of maternal effects in fishes. Only few studies to our knowledge, have demonstrated a link between female age and recruitment, by assessing population trends (Wright and Gibb, 2005). I have two further concerns with the use of age as a maternal effect. Firstly, that age is confounded with numerous co-varying traits and is often interchanged with these co-varying traits and described as the source of a maternal effect or influence; and secondly that age is not a phenotypic variable. The following section will discuss the use of age as a maternal effect in the context of these misuses. 2.3.2.1. Traits that co-vary with age Many physiological, morphological and behavioural traits in fishes change with the progression time, and therefore, the fish’s age. Indeterminate growth which is common in fish, means that unlike most other vertebrates, fish continue to grow after maturity, and so age continues to increase or co-vary with size (Table 1.3). Correlation does not definitively indicate a causal relationship. Age is better described as an indicator or covariate of other phenotypic traits that are important in determining the quality and abundance of offspring. Age is typically tied to traits of a fish such as size, weight, spawning experience—for example, haddock, M. aeglefinus and witch flounder Glyptocephalus cynoglossus (Wigley, 1999)—seasonal timing of spawning and length of spawning season—for example, cod G. morhua (Chambers and Waiwood, 1996; Kjesbu, 1994)—or dominance, and subsequent ability to access the best territories or mates. Any of these phenotypic traits could drive phenotypic variation in offspring. A good test of the importance of age to maternal effects would be to examine its effects in taxa with determinant growth, as this would at least allow age to be examined without the co-varying effects of size differences. In some studies where female age was touted to affect offspring quality, co-varying female traits such as length were not accounted for, for example,

Table 1.3 Summary of some published examples examining the effect of maternal age on offspring traits and the covariance of maternal size with age

Length effect

Magnitude of size Age effect (r) effect

Species

Offspring trait

Rainbow trout, Salmo irideus Rainbow trout, Salmo irideus White sea salmon, Salmo salar Atlantic salmon, S. salar Rainbow trout, Salmo gairdneri Goby, Rhinogobius sp Goby, Rhinogobius sp Goby, Rhinogobius sp Black rock fish, Sebastes melanops

Fingerling growth Egg size

Yes

0.48

Yes

Egg size

Yes

0.56

Yes

Egg size

Yes

0.46

nm

Egg size and growth Egg size

nm Yes

0.63

Yes

Egg number

Yes

0.90

Yes

Clutch area

Yes

0.89

Larval growth (mm)

Yes

0.71

nm

Magnitude of age Do age effect (r) and size or p value co-vary?

Yes

Yes

Yes

Relationship between age and length Reference

Yes

m

Gall (1974)

0.48

Yes

s
Galkina (1970)

0.50

Yes

a<s

Galkina (1970)

nm

m

Galkina (1970)

Yes

m

Pitman (1979)

Yes

m

Yes

m

Yes

m

Yes

s
Tamada and Iwata (2005) Tamada and Iwata (2005) Tamada and Iwata (2005) Berkeley et al. (2004a)

<0.05

<0.05

0.84

(continued)

Table 1.3 (continued) Magnitude Do age of age effect (r) and size or p value co-vary?

Species

Offspring trait

Length effect

Magnitude of size Age effect (r) effect

Haddock, Melanogrammus aeglefinus Walleye, Stizostedion vitreum white sucker, Catostomus commersoni Walleye Pollock, Theragra chalcogramma Atlantic cod, Gadus morhua

Egg diameter

Yes

0.47

Yes

Egg dry mass

Yes

0.63

Yes

Egg dry mass

Yes

0.61

Yes

Egg size

No

Fecundity

Yes

0.99

Yes

0.71

Yes

Weight

Yes

Yes

Yes

Yes

m

Atlantic cod, G. morhua

Relationship between age and length Reference

Yes

m

Hislop (1988)

0.71

Yes

s
Johnston (1997)

0.56

Yes

s¼a

Johnston (1997)

no

nm

Hinckley (1990) a<s

Yoneda and Wright (2004) Kjesbu et al. (1996)

nm, not measured; yes, confirms a maternal influence or effect found through that female trait maternal length effect; s < a is where the size effect was less than the age effect; a < s is where the age effect were less than the size effect; s ¼ a the size and age effects were similar; m ¼ size mentioned but not quantified (m).

Maternal Effects in Fish Populations

39

rainbow trout Salmo gairdneri (Pitman, 1979) and so the relative importance of the morphological versus life-history traits in determining offspring quality was not determined (Table 1.3). Furthermore, numerous studies acknowledge the covariance between size and age, but do not assess this relationship any further when attributing variance due to maternal effects, and often just select one variable in favour of the others in describing maternal traits to offspring quality, for example, goby Rhinogobius sp. (Tamada and Iwata, 2005). Relative fecundity (eggs g1) of youngest, recruit-spawning haddock was just over half of that of older, repeat spawners fish, and this would have a strong effect on estimation of egg production from female SSB (Hislop, 1988), and therefore provides good reason to incorporate maternal affects quantitative data into fisheries assessments. Younger fish (in repeat spawning species) also produce the most variability within clutches of eggs, and as fish size increases with age of female, the variability in size decreases (Kamler, 1992). Adaptive sex allocation in the brushtail possum was related to spawning experience, a covariate of female age, as females breeding for the first time were likely to produce sons, and subsequently breeding attempts were female biased (Isaac et al., 2005). Age is often interchanged with spawning experience and timing of spawning within a season. There is evidence within a number of species suggesting that repeat-spawners not only produced more eggs, but also produced better quality eggs than firsttime spawners (recruit spawners) (Hislop, 1988). But few studies examine the influences of these co-varying traits separately. Within a population, repeat spawners are typically older fish, simply by virtue of it taking longer to reach the second reproductive season than the first reproductive season. Size as a phenotypic trait is more likely to provide a generalised relationship to recruitment potential (Marshall et al., 1998). Given the size-selective nature of some fisheries and subsequent truncation of age and size classes, I agree that it is critical to provide managers with information about the predicted and realised effects of the removal of larger, older fish from a spawning population. However, of more than 140 papers I examined for evidence of maternal effects in fishes, 11 studies (17 stocks or species) (Berkeley et al., 2004a; Galkina, 1970; Gall, 1974; Hislop, 1988; Johnston, 1997; Johnston and Leggett, 2002; Kjesbu et al., 1996; Pitman, 1979; Tamada and Iwata, 2005; Wright and Gibb, 2005; Yoneda and Wright, 2004) measured the effects of maternal age on offspring quality and only three identified age as key (Berkeley et al., 2004a; Johnston, 1997; Wright and Gibb, 2005). Similarly, in most instances where the influence of maternal age was examined, age was not the sole predictor, rather age and size co-varied, but the individual effects were not separated (Table 1.1; Tamada and Iwata, 2005). In Atlantic salmon (S. salar) when age was held constant, a large proportion of variance in offspring (74–81%) was attributable to size ( Jonsson et al., 1996). When the relative effects of maternal age and length

40

Bridget S. Green

are examined separately, maternal length is typically a better predictor of offspring condition than maternal age, and adding maternal age to a model containing population, maternal length and their interaction explained only a further 0.3% variation in egg size ( Johnston and Leggett, 2002). Age-specific patterns in offspring quality may be related to the history of fishing within a population and therefore plasticity in age and size of maturity; the inherent covariance between size and age in species with indeterminate growth (Miller et al., 1988); or covariance of age and weight, spawning experience, seasonal timing of spawning (Castro and Cowen, 1991; Forrester, 1990; Paris and Cowen, 2004). In fact, numerous studies that examine age and size of females and their influence on offspring, do not examine age and size of individual females so that the relative contribution of each can be identified, rather they measure length and use a length-age relationship to infer the effects of age (e.g., Vallin and Nissling, 2000). 2.3.2.2. Is age a phenotypic variable? Despite the resurgence of interest in female broodstock age to characterise variation in fish populations, it is questionable whether female age can accurately be considered a maternal effect as it is not a true phenotypic variable, or a function of the female environment. A phenotype is generally defined as ‘the physical expression of the interaction of the organism genotype and the organism’s environment’. Age is not part of the environment nor the genotype, rather it is a measure of the progression of time, or ontogeny. The role of age in determining maternal effects in fishes is similar to maternal identity: it may be serviceable as a grouping to demonstrate that a maternal effect exists, particularly when low samples sizes do not allow morphological indicators to be identified, but is likely not the sole cause of it. Many genes have agedependant patterns of gene expression and subsequently many age-specific responses are genetic rather than phenotypic (Atchley et al., 1997). Furthermore, fish rarely survive to senesce, and so the effects of ageing through senescence are an unlikely contributor to variation in offspring traits. Effects in offspring quality attributable to age are likely due to female effects, which can encompass heritable traits. Age as a maternal trait may be important in aquaculture studies where optimising quality of offspring is fundamental. If selection of brood fish results in larger or faster-growing offspring then hatchery efficiency increases, however if this is tied to the age of the female then it becomes a trade-off in increasing the time for maintaining brood-stock and the benefits in the offspring (Gall, 1974). Alternatively, if female age covaries with size (and size is a more likely predictor of offspring quality), then it may be more efficient to select broodstock based on size, selecting for the individuals with higher growth, that reach a larger size earlier, regardless of the age of the female, thus reducing the time taken to achieve good quality broodstock.

Maternal Effects in Fish Populations

41

2.3.2.3. Early maturity Timing of maturity is a maternal trait which may influence offspring quality as the female allocates resources to reproduction over growth. When fish mature at a smaller size or younger age than the population norm it is considered to be early maturation. Life history theory predicts that females will mature earlier when there is high adult mortality, and for most fisheries, heavy fishing harvest is a source of high adult mortality. High predation or fishing pressure has been demonstrated to shift the age or size at maturation in heavily exploited stocks, and where natural predation is high, in model species such as guppies P. reticulata (Reznick and Ghalambor, 2005) and silverside M. menidia (Conover et al., 2005). In guppies, this coincided with production of lighter weight and higher numbers of offspring per clutch. Combining these metrics into a measure of reproductive allotment indicates that guppies under high predation devoted 40–50% more resources to each clutch (Reznick and Ghalambor, 2005). While the authors argued that this represented genetic differences, it may also be a result of maternal phenotypic variability. The proportion of mature-at-age fish is an important parameter in the estimation of population growth and potential fishery yield (e.g., Morgan, 1999). Like many fisheries stock estimates, the proportion mature-at-age is a derived estimate from length frequency within a population (Morgan and Hoenig, 1997), and a given age group straddles many length classes (Morgan, 1999). Age at maturity is generally closely related to length at maturity, but length is typically a more determinate factor of egg number. Age and size at maturation are not independent traits (Stearns and Koella, 1986). In a broadranging review of timing of maturity in flatfishes, maturity was typically constrained by size, although in some species there was little plasticity for age at maturity and therefore little variation in age at maturity (Roff, 1991). Population changes in age at maturity or sex-change, in the case of sequential hermaphrodites, are common signs of a heavily exploited population. Age and size at maturation generally decrease with the removal of older, larger fish from the population (Trippel, 1995), for example, chub mackerel Scomber japonicus (Watanabe and Yatsu, 2006); however, this trend is not universal and sometimes size or age at maturation increases with increased fishing pressure (e.g., pacific halibut Hippoglossus stenolepis; Schmitt and Skud, 1978 cited in Trippel, 1995) or predation (Belk, 1998; Cichon, 1997). Reduced age at maturity results in smaller-bodied fish contributing to the spawning stock—and coupled with the decreased number of older, larger fish, these early maturing fish in a heavily fished population will eventually contribute disproportionately to the spawning stock. Atlantic cod populations on George’s Banks were reduced to first-time spawners (Trippel, 1995). The reduction of size and age at maturity is generally considered to be a phenotypic response to fishing pressure (Olsen et al., 2004), although there is some evidence that this might also have a genetic component (Walsh et al., 2006) involving a shift in gene frequency causing evolutionary change, for example, M. menidia (Conover and Munch, 2002;

42

Bridget S. Green

Walsh et al., 2006) and European grayling Thymallus thymallus (Haugen and V
llestad, 2001; see discussion in Stockwell et al., 2003). On a positive note, when high mortality was halted and population increased through restoration of a river system, age but not size at maturity increased for both male and female Cui-ui Chasmistes cujus (Scoppettone and Rissler, 2007). In heavily exploited fisheries, fishing is the greatest agent of mortality and therefore the most likely source of phenotypic plasticity. In populations where there has been a shift in size at maturity which influenced recruitment, when fishing was reduced or a proportion of the stock protected then a recovery is likely. Distinguishing between evolutionary and plastic components of harvest-induced changed in size or age at maturation is central to the current debate on the pathway to early maturation (Ernande et al., 2004). The two pathways have been defined as: (1) Compensation—a phenotypic response based on density dependence and lowered competition, therefore providing more access to resources, resulting in faster growth and consequently earlier maturation (Trippel, 1995). The plastic component to a change in stage at maturation is a potential pathway for a maternal effect. (2) Genetic selection size-selectivity for early maturity—heavy fishing could result in a shift in gene frequencies over time, as larger/older fish do not survive to pass their genes on (Trippel, 1995). The genetic component to a change in a size or length at maturity could impart a maternal influence on offspring. There may be an adaptive significance in initiating breeding at different ages, including: (1) reproductive optimisation, (2) trade-offs of somatic growth-at-age for reproductive quality and (3) increased natural mortality as a penalty for early maturity (Murawski et al., 2001). The risk of death before reproduction is large therefore to increase reproductive value it pays to reproduce early, reducing the chance of mortality before reproduction (Rothschild, 1986). 2.3.3. Female size Size is one of the most obvious traits of an organism (LaBarbera, 1989), and one of the easiest to measure. As a consequence, maternal size is perhaps the most commonly measured and reported correlate of offspring quality or quantity. A positive relationship between female size and offspring size or number of eggs exists in a range of taxa, including vertebrates, for example, turtles (Congdon and Gibbons, 1987); fishes (Fleming and Gross, 1990; Jonsson et al., 1996); lizards (Sinervo and Doughty, 1996); invertebrates, such as the subsocial burrower bug Adomerus triguttulus (Kudo and Nakahira, 2004), cladocera Daphnia magna (Boersma et al., 2000), bryozoa Bugula neritina (Marshall and Keough, 2004a); and plants (Sakai and Harada, 2001; Venable, 1992). In some species, larger female size is always an advantage as in the least it offers a fecundity advantage to the female (e.g., tussock moth, Orgyia spp., Tammaru et al., 2002). An understanding of the mechanisms driving this relationship is often what is lacking in

Maternal Effects in Fish Populations

43

understanding how size confers a maternal effect. Marshall and Keough (2004b) describe three likely reasons that larger females may produce larger offspring, two amongst them may be related to a maternal effect (or at least a maternal influence): (1) larval size is fixed and changes with maternal size due to changes in anatomical, physiological or nutritional constraints, (2) larger offspring may be a fixed genetic trait related to higher quality larger mothers (very few studies in fishes are powerful enough to determine this) and (3) offspring size may be plastic, and respond to maternal investment aimed at maximising their own fitness. A range of metrics are employed to describe female size as a predictor of offspring quality, including female length, weight and Fulton’s K (body weight/body length3) (see also Section 2.2.4). These variables are typically related, though not equally predictive of fecundity or other measures of reproductive quality (Koops et al., 2004). While weight and Fulton’s K may be more indicative of the amount of energy available for reproduction, these measures will vary throughout the year with food availability and reproductive effort, and so timing of sampling can influence their quantity. Length is an accumulation of growth and thus represents a broader snapshot of condition of the fish, but this measure too has exceptions to its utility. Length-based regressions can overestimate the relationship between female condition and fecundity (Koops et al., 2004). Non-reproductive guppies (P. reticulata) will store energy in fat tissues rather than redirect it to somatic growth (Reznick, 1983), which results in size providing an underestimate of energy available for reproduction. Given isometric scaling laws (volume ¼ length3), a female’s capacity to store eggs increases as a cube of her body length, longer females theoretically can produce significantly more eggs than smaller females. A link between female size and offspring traits in fishes is reported in numerous and diverse ways (Table 1.4). Egg diameter and dry weight increased significantly with length of female haddock M. aeglefinus (Hislop, 1988). Larger females produced longer offspring (chum salmon O. keta, Beacham and Murray, 1985), but not larger eggs (Atlantic silverside M. menidia, Bengston et al., 1987). Female length and body weight resulted in larger egg and yolk volume and larger SL at hatching in the black porgy Acanthopagrus schlegeli (Huang et al., 1999) and conversely, smaller females resulted in smaller eggs in Atlantic salmon S. salar (Berg et al., 2001). Relative fecundity (eggs g1) of smallest cod (300 eggs g1) was just over half of that of larger fish (500 eggs g1) in Northeast artic cod G. morhua (Marshall et al., 1998). There was no relationship found between female length, weight or Fulton’s K and offspring quality measures in A. melanopus, although there were significant effects of female identity (Green and McCormick, 2005a). Coho salmon (O. kisutch) individual egg mass increased significantly with female length in 20 of 30 population brood years, and total clutch biomass and number increased with female length in

Table 1.4

Evidence of maternal effects and maternal influences in fishes

Species

Female trait

Offspring response

Source

Method

Zebrafish, D. rerio Haddock, M. aeglefinus Atlantic cod, G. morhua G. morhua

17b Estradiol

Embryo mortality

l

fm

Batch number

Egg diameter

wp

expt, spc

Between fish

l

10 f

12.4

l

10 f

55.3

M. aeglefinus

Body weight

M. aeglefinus

Body weight

Total egg dry weight total egg dry weight Mean batch fecundity Initial egg diameter

M. aeglefinus

Body weight

Yellow perch, Perca flavescens M. aeglefinus

Mercury concentration Condition factor

M. aeglefinus

Condition factor

M. aeglefinus

Condition factor

M. aeglefinus

Condition factor

Pink salmon, Oncorhynchus gorbuscha

Dam (sire) early versus late spawners

Between year

Result rij

Sig

0.87

0.68

***

wpc

0.63

**

wpc

0.57

**

Composite egg diameter Mercury in eggs

wp

Fecundity

wpc

0.54

**

Mean batch fecundity Initial egg diameter

wpc

0.32

ns

wpc

0.64

***

wpc

0.56

**

Composite egg diameter Fecundity of 16 mo old spawners

wpc

60 m  120 f, h-s

%Fvc

***

wpc

corr

MEvc

*

0.96

ns

Reference

Westerlund et al. (2000) Rideout et al. (2005b) Kjesbu et al. (1996) Kjesbu et al. (1996) Trippel and Neil (2004) Trippel and Neil (2004) Trippel and Neil (2004) Hammerschmidt et al. (1999) Trippel and Neil (2004) Trippel and Neil (2004) Trippel and Neil (2004) Trippel and Neil (2004) Smoker et al. (2000)

O. gorbuscha

Atlantic salmon S. salar Brown trout, S. trutta Rainbow trout, O. mykiss Goby Rhinogobius sp Sea bass Dicentrarchus labrax Ambon damsel, Pomacentrus amboinensis P. amboinensis

P. amboinensis P. amboinensis

dam (sire) early versus late spawners Female length

Egg size of 16 mo old spawners Egg diameter

wpc

60 m120 f, h-s

***

wp

66, expt

***

Egg size

Growth to juvenile

l

8  8, expt

ns

Egg size

Progeny growth after 1 year Starvation tolerance Fertilisation rate, 48 h survival, hatching rate, larval length Larval morphology (sl, yolk-sac size, head hieght, eye diameter) Larval morphology (sl, yolk-sac size, head hieght, eye diameter) Size of larvae

l

10  10, d

ns

wpc

72 f  60 m, expt 7 f  6 m, d, expt

*

Cortisol in eggs

Egg size Female  male

Cortisol level, manipulated externally to mimic natural variation Testosterone

Level of cortisol in egg when laid Level of cortisol in egg when laid

wpc

**

Smoker et al. (2000) 95

Berg et al. (2001) Einum and Fleming (1999) Herbinger et al. (1995) Tamada and Iwata (2005) Saillant et al. (2001)

wpc

six clutches

***

McCormick (1999)

wpc

five clutches

***

McCormick (1999)

w

10 f, corr

0.692

***

w

10 f, corr

0.538

**

McCormick (1998) McCormick (1998)

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

Method

Result rij

Sig

Whitefish, Corengus sp

Mate choice

Black rockfish, Sebastes melanops S. melanops

Maternal age

Mortality— resistance to bacterial infection Oil globule

wpc

16 f

0.91

*

Berkeley et al. (2004a)

Maternal age

Growth in length

wpc

16 f

0.84

*

S. melanops

Maternal age

Growth in mass

wpc

16 f

0.83

*

S. melanops

Maternal age

wpc

16 f

0.9

*

S. melanops

Maternal age

wpc

16 f

0.54

*

S. melanops

Maternal age

wpc

16 f

0.46

*

Goby Rhinogobius sp

Maternal age

Time to 50% starvation Initial larval length Larval condition at parturition Egg size

Berkeley et al. (2004a) Berkeley et al. (2004a) Berkeley et al. (2004a) Berkeley et al. (2004a)

wpc

72 f, 60 m, expt

Walleye pollock T. chalcogramma T. chalcogramma Nase, Chondrostoma nasa Guppy, Poecilia reticulata

Maternal age

Egg diameter

wp

r

0.245

ns

Maternal age Maternal age

Egg dry weight Egg dry weight

wp wp

r 20 f, 34 m, pm

0.297 0.721

ns ***

Hinckley (1990) Keckeis et al. (2000)

Maternal food (increased ration)

Number of offspring

l

10 f, multiple males

ng

Reznick et al. (1996)

10  10 cross

MEvc

%Fvc

Reference

Wedekind et al. (2001)

***

Berkeley et al. (2004a) Tamada and Iwata (2005) Hinckley (1990)

Guppy, P. reticulata Poecilid, Priapichthys festae Poecilid, Heterandria formosa Atlantic tomcod, Microgadus tomcod M. tomcod

Maternal food (low ration) Maternal food (increased ration) Maternal food (increased ration) Maternal identity

Fat reserves

l

Number of offspring

l

Number of offspring

Reznick et al. (1996) Reznick et al. (1996)

10 f, multiple males 13 f, multiple males

ng

l

15 f, multiple males

*

Egg diameter

wpc

14 f  14 m, 9f5m

**

91

Maternal identity

Length at hatch

wpc

14 f  14 m, 9f5m

**

33

M. tomcod

Maternal identity

Starvation resistance

wpc

14 f  14 m, 9f5m

**

30

Red and black anemonefish, Amphiprion melanopus A. melanopus

Maternal identity

Growth rate to metamorphosis

wpc

4 f  4 m, d

ns

5

Maternal identity

Mortality to metamorphosis

wpc

4 f  4 m, d

**

12

Rainbow trout, S. gairdneri S. gairdneri

Maternal identity

Weight at first feeding Length at first feeding Length at 12 weeks

l

**

1.32

**

0.96

Refstie (1980)

wpc,l

1 m, 3 f h-s (? crosses) 1 m, 3 f h-s (? crosses) 12 m, 29 f

Green and McCormick (2005a) Refstie (1980)

0.06

Bailey and Loudenslager (1986) Bailey and Loudenslager (1986)

Maternal identity

l

*

Reznick et al. (1996)

Atlantic salmon, S. salar

Maternal identity

S. salar

Maternal identity

Weight at 12 weeks

wpc,l

12 m, 29 f

0.02

S. salar

Maternal identity

Length at 6 months

wpc,l

12 m, 29 f

0.02

Green and Chambers (2007) Green and Chambers (2007) Green and Chambers (2007) Green and McCormick (2005a)

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

Method

Result rij

Sig

MEvc

%Fvc

Reference

Bailey and Loudenslager (1986) Bailey and Loudenslager (1986) Bailey and Loudenslager (1986) Bailey and Loudenslager (1986) Heath et al. (1993)

S. salar

Maternal identity

Weight at 6 months

wpc,l

12 m, 29 f

0.18

S. salar

Maternal identity

Length at 15 months

wpc,l

12 m, 29 f

0.01

S. salar

Maternal identity

Weight at 15 months

wpc,l

12 m, 29 f

0.04

Chinook salmon, O. tshawytscha O. tshawytscha

Maternal identity

Wet weight

4 f, 8 m

***

Maternal identity

4 f, 8 m

***

O. tshawytscha

Maternal identity

4 f, 8 m

**

O. tshawytscha

Maternal identity

4f, 8m

***

Heath et al. (1993)

O. tshawytscha

Maternal identity

4 f, 8 m

ns

O. tshawytscha

Maternal identity

4 f, 8 m

**

Rainbow trout, O. mykiss O.mykiss

Maternal identity

RG (%/d), relative growth Cortisol (control fish, not stressed) Glucose (control fish, not stressed) Cortisol (stressed fish) Glucose (stressed fish) Egg and larval survival Egg and larval survival Development time

l

4  4 cross

*

l

33

*

Heath et al. (1993) Heath et al. (1993) Nagler et al. (2000) Nagler et al. (2000)

l

4 f  6 m, d

ns

Maternal identity Maternal identity

Heath et al. (1993) Heath et al. (1993)

Lake trout, Salvelinus namaycush S. namaycush

Pakkasmaa and Jones (2002) Maternal identity

Size at hatching,

l

4 f  6 m, d

*

Sea bass D. labrax

Maternal identity

wp

7 f  6 m, d, expt

***

Yellowtail flounder, Pleuronectes ferrugineus P. ferrugineus

Maternal identity

Egg viability, 48 h survival, hatching rate, larvae length, egg size Egg diameter,

wp

4 f  pm

***

82.5

Benoit and Pepin (1999)

Maternal identity

Hatch length

wp

4 f  pm

**

22.0

Atlantic cod, G. morhua

Maternal identity

Egg size

wpc

10 f  10 m, expt

***

Lake Michigan yellow perch P. flavescens P. flavescens

Maternal identity

wp

10 f, pm, expt

***

wp

10 f, pm, expt

**

Herring, Clupea harengus C. harengus

Maternal identity

wpc

2  2, d, expt

***

Maternal identity

Larval TL, larval dry weight, DNA Larval yolk volume, Larval size at hatching Larval dry weight

Benoit and Pepin (1999) Chambers and Waiwood (1996) Heyer et al. (2001)

wpc

2  2, d

***

C. harengus

Maternal identity

DNA, RNA

wpc

2  2, d

***

Masu salmon, Oncorhynchus masou Atlantic salmon, S. salar

Maternal identity

Otolith size

wpc

expt, 4  4, d

***

Maternal identity

Weight

wpc

Maternal identity

Pakkasmaa and Jones (2002) Saillant et al. (2001)

35

0.39

Heyer et al. (2001) H
ie et al. (1999b) H
ie et al. (1999b) H
ie et al. (1999b) Yamamoto and Reinhardt (2003) Refstie and Steine (1978)

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

S. salar

Maternal identity

Length

wpc

S. salar

Maternal identity

Weight

wpc

S. salar

Maternal identity

Length

wpc

S. salar

Maternal identity

Weight

wpc

S. salar

Maternal identity

Length

wpc

Arctic charr, Salvelinus alpinus

Maternal identity

l

Salmo trutta (f)  Salvelinus fontinali (m) S. trutta (f)  S. fontinali (m) S. trutta (f)  S. fontinali (m) S. trutta (f)  S. fontinali (m)

Maternal identity

Hatch success, mean weight at 30 and 75 days Survival to eyed stage, control

Method

Result rij

1 m–3 f h-s (308 families) 1 m–3 f hs (308 fam) 1 m–3 f hs (308 fam) 1 m–3 f hs (308 fam) 1 m–3 f hs (308 fam) 1 m–3 f hs (308 fam) 4  4 d, inc

l

5 m  5 f  3, d

Sig

0.42 0.59 0.63 *

0.96

*

l

5 m  5 f  3, d

***

Maternal identity

Survival to hatching, hybrid Survival to 90 d, hybrid

l

5 m  5 f  3, d

***

l

5 m  5 f  3, d

***

wp

4 f  pm

ns

Development time

Reference

Refstie and Steine (1978) Refstie and Steine (1978) Refstie and Steine (1978) Refstie and Steine (1978) Refstie and Steine (1978) De March (1991)

0.39

Survival to eyed stage, hybrid

Maternal identity

%Fvc

0.39

Maternal identity

Maternal identity

MEvc

0.75

Blanc and Poisson (1983) Blanc and Poisson (1983) Blanc and Poisson (1983) Blanc and Poisson (1983) Benoit and Pepin (1999)

Yellowtail flounder, P. ferrugineus Herring C. harengus C. harengus

Maternal identity

Lapillus diameter

wp

Maternal identity

Sagitta diameter

wp

C. harengus

Maternal identity

Standard length

wp

C. harengus

Maternal identity

Larval dry mass

wp

C. harengus

Maternal identity

Egg diameter

wp

Atlantic haddock, M. aeglefinus M. aeglefinus

Maternal length (fl)

Fecundity

Maternal length (fl)

M. aeglefinus

Maternal length (fl)

M. aeglefinus

Maternal length (fl)

Coho salmon, O. kisutch Walleye pollock T. chalcogramma M. aeglefinus M. aeglefinus M. aeglefinus M. aeglefinus Northeast Artic cod G. morhua Walleye pollock T. chalcogramma

wpc

3m3f3 e, d 3m3f3 e, d 3m3f3 e, d 3m3f3 e, d 3m3f3 e, d 22  22, expt

*

0.699

***

Mean batch fecundity Initial egg diameter

wpc

22  22

0.73

***

wpc

22  22

0.5

*

wpc

22  22

0.47

*

Maternal length

Composite egg diameter Egg size or number

wp

pub

***

Maternal length

Egg diameter

wp

r

0.728– 0.976 0.21

ns

Maternal length Maternal length Maternal length Maternal length Maternal length

Egg diameter Egg dry weight Egg diameter Egg dry weight Eggs g1

wp wp wp wp wp

F only F only F only F only corr

0.47 0.45 0.28 0.21 0.47

*** *** ** * **

Hislop (1988) Hislop (1988) Hislop (1988) Hislop (1988) Marshall et al. (1998)

Maternal length

Egg dry weight

wp

R

0.29

ns

Hinckley (1990)

* * * *

H
ie et al. (1999a) H
ie et al. (1999a) H
ie et al. (1999a) H
ie et al. (1999a) H
ie et al. (1999a) Trippel and Neil (2004) Trippel and Neil (2004) Trippel and Neil (2004) Trippel and Neil (2004) Fleming and Gross (1990) Hinckley (1990)

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

Method

Result rij

Sig

Black rockfish, Sebastes melanops S. melanops

Maternal length

Growth in length

wpc

16 f

0.71

*

Berkeley et al. (2004a)

Maternal length

Growth in mass

wpc

16 f

0.66

*

S. melanops

Maternal length

wpc

16 f

0.62

*

Haddock, M. aeglefinus M. aeglefinus brook charr, Salvelinus fontinalis S. fontinalis S. fontinalis Atlantic cod, G. morhua G. morhua

Maternal length

Time to 50% starvation Egg diameter

wp

unfert

0.47

***

Berkeley et al. (2004a) Berkeley et al. (2004a) Hislop (1988)

Maternal length Maternal length (fork length)

Dry weight Embryo fork length

wp wpc,l

unfert 12 m, 23 f, h-s

0.45 0.77

*** ***

Maternal length (fl) Maternal length (fl) Maternal length and weight Maternal length and weight Maternal length and weight Maternal length and weight Maternal length and weight Maternal length and weight Maternal liver weight

Yolk sac volume Alevin fork length Number of batches

wpc,l wpc,l l

12 m, 23 f, h-s 12 m, 23 f, h-s 10 f, 10 m

0.78 0.31 0.88

*** ns ***

Spawning period

l

10 f, 10 m

0.84

***

Fecundity

l

10 f, 10 m

0.95

***

Weighted mean egg diameter Weighted mean egg dry weight Total egg dry weight Egg diameter

l

10 f, 10 m

0.51

*

l

10 f, 10 m

0.61

**

l

10 f, 10 m

0.96

***

wp

r

0.17

ns

Perry et al. (2004) Perry et al. (2004) Kjesbu et al. (1996) Kjesbu et al. (1996) Kjesbu et al. (1996) Kjesbu et al. (1996) Kjesbu et al. (1996) Kjesbu et al. (1996) Hinckley (1990)

Egg dry weight

wp

r

0.07

ns

Hinckley (1990)

wp

15 m, 15 f

G. morhua G. morhua G. morhua G. morhua Walleye pollock T. chalcogramma T. chalcogramma

Maternal liver weight Maternal size

**

MEvc

1.81

1.82 0.05

%Fvc

Reference

Hislop (1988) Perry et al. (2004)

Chum salmon, Oncorhynchus keta Atlantic cod, G. morhua Walleye pollock T. chalcogramma T. chalcogramma Sea bass D. labrax D. labrax

Maternal temp

Yolk reserves, body tissue, size at emergence Egg diameter

wpc

Maternal weight

Egg diameter

wp

Maternal weight Maternal weight

Egg dry weight Spawn volume

wp wp

Maternal weight

wp

D. labrax

Maternal weight

Time from induction to stripping Egg viability

D. labrax

Maternal weight

pH of ovarian fluid

wp

D. labrax

Maternal weight

Fertilisation rate

wp

D. labrax

Maternal weight

Egg area

wp

D. labrax

Maternal weight

wp

D. labrax

Maternal weight

Egg survival to 48 h Hatch rate

D. labrax

Maternal weight

Atlantic haddock, M. aeglefinus Brook charr, S. fontinalis S. fontinalis

Maternal weight

Maternal weight Maternal weight

wp

wp

Total length of larvae Fecundity

wp

Embryo fork length Yolk sac volume

wpc,l

wpc

wpc,l

17 f  17 m, 21 f  21 m r

*** 0.08

ns

r expt, 7 f, 6 m, d expt, 7 f, 6 m, d

0.12 0.58

ns *

0.39

*

expt, 7 f, 6 m, d expt, 7 f, 6 m, d expt, 7 f, 6 m, d expt, 7 f, 6 m, d expt, 7 f, 6 m, d expt, 7 f, 6 m, d expt, 7 f, 6 m, d 22  22

0.32

*

0.37

*

0.09

*

0.64

*

0.67

*

0.75

*

0.39

*

0.76

***

0.82

***

0.86

***

12 m  23 f, hs 12 m, 23 f, h-s

Beacham and Murray (1985) Ouellet et al. (2001) Hinckley (1990)

Hinckley (1990) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Saillant et al. (2001) Trippel and Neil (2004) 0.61  0.05

Perry et al. (2004) Perry et al. (2004)

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

Sig

MEvc

%Fvc

Reference

Perry et al. (2004)

12 m  23 f, hs 12 m  23 f, hs 12 m  23 f, hs 12 m  23 f, hs 1365 f, corr

0.406

***

0.773

***

0.739

***

1.630

Perry et al. (2004)

0.271

ns

0.072

Perry et al. (2004)

0.30

***

wp

20 f and 34 m, pm

0.62

*

Egg wet weight

wp

0.64

*

Larval size, yolk-sac size

wp

20 f and 34 m, pm 20 f, 20 m

Growth rate to metamorphosis

wpc

4 f  4 m, d

**

Paternal effect

Larval weight

wpc

*

Paternal effect

Larval length

wpc

Paternal effect

Weight at first feeding

l

1 m, 3 f h-s, 308 families 1 m, 3 f hs (308 fam) 1 m–3 f h-s

Maternal weight

Alevin fork length

wpc,l

S. fontinalis

Maternal weight

wpc,l

S. fontinalis

Maternal weight

Embryo fork length Yolk sac volume

S. fontinalis

Maternal weight

Alevin fork length

wpc,l

Atlantic salmon, S. salar Nase, Chondrostoma nasa C. nasa

Maternal weight

Egg weight

wp, l

Maternal weight

Egg energy content

Maternal weight

P. amboinensis

Female food availability (increased ration) Paternal effect

Rainbow trout, S. gairdneri

Result rij

0.57  0.06 0.18  0.04 1.640

S. fontinalis

Red and black anemonefish, Amphiprio melanopus Atlantic salmon, S. salar S. salar

Method

wpc,l

Perry et al. (2004)

Jonsson et al. (1996) Keckeis et al. (2000) Keckeis et al. (2000) Kerrigan (1997)

***

* ns

52

0.18– 0.02 0.07– 0.02 0.19

Green and McCormick (2005a) Refstie and Steine (1978) Refstie and Steine (1978) Refstie (1980)

S. gairdneri

Paternal effect

Chinook salmon, Oncorynchus tshawytscha O. tshawytscha

Paternal effect

O. tshawytscha

Paternal effect

O. tshawytscha

Paternal effect

O. tshawytscha

Paternal effect

O. tshawytscha

Paternal effect

Brown trout, S. trutta fario Four species freshwater salmonids Sea bass D. labrax Herring, C. harengus Brook charr, S. fontinalis S. fontinalis

Paternal heritability Paternal identity

l

1 m–3 f hs

ns

l

4 f, 8 m

**

Heath et al. (1993)

Rg (%/d), relative growth Cortisol (control fish, not stressed) Glucose (control fish, not stressed) Cortisol (stressed fish) Glucose (stressed fish) Final wet weight, % weight gain Swelling size of egg

l

4 f, 8 m

***

l

4 f, 8 m

***

Heath et al. (1993) Heath et al. (1993)

l

4 f, 8 m

***

Heath et al. (1993)

l

4 f, 8 m

***

l

4 f, 8 m

*

l

Paternal identity

Hatching rate

wp

Paternal identity

Dna, rna, rna:dna

wpc

20 m  10 f,d, expt 5  5, d, 8  8, linear regression expt, 7 f  6 m, d 2  2, d, expt

Heath et al. (1993) Heath et al. (1993) Vandeputte et al. (2002) Pakkasmaa et al. (2001)

Paternal length (fork length) Paternal length (fl)

Embryo fork length Yolk sac volume

wpc,l

Paternal effect

Length at first feeding Wet weight

Wp, l

wpc,l

12 m  23 f, hs 12 m  23 f, hs

0.06

0.28 Variable, ns, *** ***

Refstie (1980)

0.002

ns

0.093

Saillant et al. (2001) H
ie et al. (1999b) Perry et al. (2004)

0.466

ns

0.012

Perry et al. (2004)

***

(continued)

Table 1.4

(continued)

Species

Female trait

Offspring response

Source

Method

Result rij

Sig

MEvc

S. fontinalis

Paternal length (fl)

Alevin fork length

wpc,l

0.291

**

0.296

Beaweed pipefish Syngnathus schlegeli Atlantic cod, G. morhua

Paternal size

Number and size of offspring

wpc

12m  23 f, hs 50 m, corr

0.71

**

Watanabe and Watanabe (2002)

Paternal size

wpc

8 f, 16 m, 51 batches

*

Rakitin et al. (2001)

S. fontinalis

Paternal weight

wpc,l

12 m, 23 f, h-s

0.005

ns

0.136

Perry et al. (2004)

S. fontinalis S. fontinalis

Paternal weight Paternal weight

No. of larvae sired when competing for female Embryo fork length Yolk sac volume Alevin fork length

wpc,l wpc,l

0.468 0.286

ns **

0.085 0.254

Perry et al. (2004) Perry et al. (2004)

Zebrafish D. rerio Rainbow trout, S. gairdneri S. gairdneri

Pcb concentration

Embryo survival

l

12 m, 23 f, h-s 12 m  23 f, hs fm

Maternal identity

Fingerling weight

l

Maternal identity

Smolt weight

S. gairdneri

Maternal identity

Adult weight

S. gairdneri

Maternal identity

S. gairdneri

Maternal identity

Abdominal fat score Sexual maturity

Atlantic cod, G. morhua

Pre-spawning condition

Weighted mean egg dimeater

G. morhua

Pre-spawning condition

Egg dry mass

wp

21 f, 31 m, d, pm 21 f, 31 m, d, pm 21 f, 31 m, d, pm 21 f, 31 m, d, pm 21 f, 31 m, d, pm 17 f  17 m (17 families), 21 f  21 m 17 f  17 m (17

%Fvc

Reference

Perry et al. (2004)

* ***

2.3

Westerlund et al. (2000) Gjerde (1988)

***

1.1

Gjerde (1988)

***

3

Gjerde (1988)

***

1.1

Gjerde (1988)

***

4.4

Gjerde (1988)

0.890

**

Ouellet et al. (2001)

0.930

***

Ouellet et al. (2001)

G. morhua

Pre-spawning condition

Egg energy content

Pink salmon, Oncorhynchus gorbuscha O. gorbuscha

Sire early versus late spawners Sire early versus late spawners Size (SL)

Fecundity of 16 mo old spawners Egg size of 16 mo old spawners Egg size

wp

Size (SL)

Egg number

wp

Social competition Spawning experience Spawning experience

Larger offspring Egg and larval size

wp wpc

RNA:DNA

wpc

Goby Rhinogobius sp Goby Rhinogobius sp P. amboinensis Atlantic cod, G. morhua Atlantic cod, G. morhua

wpcc

wpcc

families), 21 f  21 m 17 f  17 m (17 families), 21 f  21 m 60 m, 120 f, hs 60 m, 120 f, hs expt, 72 f, 60 m expt, 72 f, 60 m 20 f, 20 m 30 m  30 f, no cross 30 m  30 f, no cross

0.870

**

Ouellet et al. (2001)

**

Smoker et al. (2000)

ns

Smoker et al. (2000) Tamada and Iwata (2005) Tamada and Iwata (2005) Kerrigan (1997) Clemmesen et al. (2003) Clemmesen et al. (2003)

*** *** *** * ns

*Relationship positive and significant at <0.05. **Relationship positive and significant at <0.01. ***Relationship positive and significant at p<0.001, ng ¼ none given. Expt. experimental cross analysed with ANOVA; corr [r], correlation with no crosses; f, females; m, males; 8 m  8 f ¼ 8 fam’s; d, diallel cross; for example, 8 m  8 f ¼ 64 fam; pm, pooled milt; h-s, half-sib; inc, incomplete design; supp, supplemental; cf, cross fostering; spc, single pair crosses; rij, correlation of female and offspring (i ¼ female attribute, j ¼ offspring); MEvc, variance due to maternal effects, narrow sense heritability; %Fvc, all variance due to female as a proportion of total variaance measured; l, laboratory raised; w, wild observation; wp, wild population; wpc, wild population held in captivity; pub, previously published data; rij, correlation of female and offspring; i, female attribute; j, offspring; fm, female manipulate.

58

Bridget S. Green

19 of 21 populations (Fleming and Gross, 1990), suggesting that this is not a standard relationship but is contingent on other unmeasured factors: possibly genetic differences due to reproductive isolation driven by natal homing behaviour, common in salmonids. Female body size was responsible for 37% of variation in the size of eggs among individuals within populations, and in 67% of populations egg size among individuals across brood lines was significantly and positively correlated with female body length (Fleming and Gross, 1990) (Table 1.4). Typically female-offspring size relationships are not univariate, rather there is often co-variation with one or more other traits or environmental conditions. For example, Einum et al. (2002) demonstrated that withinclutch oxygen consumption decreases with increasing egg size and this effect is more pronounced for offspring from large than for small females. Any advantage of maternal size, whether larger mothers results in larger offspring or more numerous smaller offspring, may be dependent on habitat, as the optimal propagule size for a given habitat quality is achieved (optimality models, Hendry et al., 2001). Optimal egg size theory predicts that larger mothers can improve the survival of their offspring by optimising (and generally maximising) the size of the offspring. Morphofunctional restrictions in small-bodied turtles (Chrysemys picta and Deirochelys reticularia) constrain the relationship between female size and propagule. The pelvic girdle structure, essential for locomotion, support and limb retraction, limits the size of the pelvic aperture, which in turn constrains the size of the eggs that can be produced (Congdon and Gibbons, 1987). In a bryozoan (B. neritina), larger mothers tended to be more fecund therefore each offspring required more resources to deal with more sibling competition (Marshall and Keough, 2004b). 2.3.4. Female condition In fish biology, condition is broadly used to describe general aspects of fish health, and has many definitions: the quantity of energy reserves available to an organism (Ferron and Leggett, 1994); or, to quote Le Cren (1951), ‘the variation from the expected weight for length of individual fish or relevant group of individuals as indications of fatness, general ‘‘well-being’’, gonad development etc’ (p. 202), and refers to differences in weight at a given length (Cone, 1990). In this sense, fish condition is largely derived from food-dependent variation in stored lipid energy (Marshall et al., 1999). As variability in food abundance is inextricably linked to female growth rate and size as well as condition, some aspects of the influence of female condition on offspring quality have been covered in the broad sense in the ‘prey abundance’ and ‘female size’ sections of this review (Sections 2.2.5 and 2.3.3). This section will focus on female condition as a measure of stored energy, and how this may be manifested as a maternal effect.

Maternal Effects in Fish Populations

59

2.3.4.1. Utility of the range of condition measures A suite of morphometric, biochemical and physiology measures are used as direct estimates of maternal condition or as proxies and indirect measures of maternal condition which might influence the quality or quantity of progeny (Table 1.5). Fulton’s K condition factor [100  (Weight/Length3)] is one of the most commonly used (and abused) estimates in fisheries science (see Table 1.4 in Lambert et al., 2003) as it is easy to attain. As a derived index, Fulton’s K has a number of assumptions governing its application which are frequently overlooked. It assumes isometry (maintaining the same body proportions through growth), and that slopes of the length/weight relationship are uniformly equal to 3. Violation of these assumption leads to over- or under estimates of condition in a population (Cone, 1989). For example, if K is above 3 then it appears that K increases with fish length, and if it is below 3 then K decreases with fish length (Cone, 1989). If the mean lengths of the populations under comparison are not the same, then differences may be assumed using Fulton’s K when these differences do not exist. In one reported case where the assumptions were tested and validated, Fulton’s K was a good predictor of productivity in cod G. morhua (Ratz and Lloret, 2003). However, few studies make mention of checking the assumptions of Fulton’s K before applying it. If the assumptions are not met, Fultons’ K may not inform much about the condition (in terms of energy storage) of the fish. Condition factor was not predictive of measured fat content in clupeids (Strange and Pelton, 1987) or Atlantic salmon (Sutton et al., 2000). Lambert et al. (2003) provides a good review of a variety of maternal condition measures and their relationship to egg production, in the field and laboratory, at the individual and group level. The remainder of this section on maternal condition will focus specifically on maternal energy reserves and how this influences offspring quality. Using direct measures of female energy reserves is more likely to result in effective biological reference points for predicting recruitment (Marshall et al., 2000).

(a) Direct measures of maternal energy reserves: For female condition to directly influence offspring quality, the mechanism must include maternal energy reserves operating through the ovary (Bunnell et al., 2005) and may include lipid content of the liver, ovary or whole body. (b) Indirect and derived measures of maternal energy reserves: Proxies or indirect measures are generally used in favor of direct measures because they are cheaper and faster to attain, non-fatal or available in archived samples. For example, liver weight was a good predictor of liver lipid content (Marshall et al., 2000). Other examples of derived measures of maternal condition include length–weight regression (Cone, 1989), HSI (hepatic somatic index), body water content, visceral–somatic index, gut index, protein–energy ratio, GSI (gonado-somatic index), morphometric measures, ovary egg density, nucleic acids and enzymes,

Table 1.5

A range of female condition measures commonly used in the study of maternal effects and maternal influences

Maternal trait (condition measure)

Pathway

Measure of condition

Fulton’s K Liver lipid Whole body lipid Length Length weight regression HSI (hepatic somatic index) Body water content Visceral-somatic index Gut index Protein-energy ratio GSI (gonado-somatic index) Ovary egg density Nucleic acids Enzyme activity Fat content Visceral fat Fecundity Relative fecundity Vitellogenic oocytes Liver weight

m, p b, p b, p m m m b, p m m, p b, p m m, p b b b, p b, p p p p m, p

ind, r dir, r dir, a ind, r ind, r ind, r ind, r ind, r ind, r ind, r dir,r ind, r ind, r ind, r ind, r ind, r ind, r ind, r ind, r ind, r

m, morphological; b, biochemical; p, physiological; ind, indirect; dir, direct; r, relative measure; a, absolute measure.

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though these latter two are better indicators of growth than energy reserves per se. The utility of each derived index as a measure of reserves is species- or stock-specific and there is no indirect measure that acts as a reliable proxy across all species and stocks of fishes. The influence of female condition on offspring quality is generally addressed at one of two levels, averaged over populations, and correlated to traits of the offspring such as recruitment, or tracked with individuals. Population analyses of Atlantic cod (G. morhua) female condition and offspring traits demonstrated that mean female condition was predictive of abundance of offspring (Ratz and Lloret, 2003); and total liver energy was directly proportional to total eggs produced in G. morhua over 26 years of data collection in the Barents Sea (Marshall et al., 1999). To examine a relationship between maternal condition and offspring traits at the individual level typically requires laboratory experiments tracking individual females through reproduction and measuring offspring quality, abundance or survival. Taxa such as birds lend themselves to robust manipulation of female condition to partition out the effects of female condition on offspring quality through cross-fostering which allows the separation of maternal state occurring through egg production, incubation and chick-rearing (Gorman and Nager, 2004). These authors were able to document an effect of female condition on the fecundity of the next generation. Assessment of female condition using indices such as liver energy content has increased the accuracy of estimated egg production in heavily exploited stocks of cod (G. morhua) when compared with estimates derived from SSB, leading to improvement in stock recruitment predictions (Marshall et al., 1999), including total egg production and recruitment of age 3 fish to the population (Marshall et al., 2000). (c) Timing of measurement: For condition measures to provide an accurate assessment of maternal effects on offspring condition, maternal reserves need to be measured at a time when they can affect the nutritional quality of the offspring (i.e., gametogenesis, oogenesis or vitellogenesis; see Box 1.1 for definitions). Fluctuations in maternal condition parameters are often ignored due to the frequency of sampling effort required to obtain them (Lambert et al., 2003). Measuring the condition of spawning condition fish that underwent vitellogenesis months prior will assess the female’s recent feeding history, but not what was available for the offspring. The liver is an area of short-term storage (Wheater et al., 1979) and lipids are the most immediately available nutrient (Love, 1980); therefore, a single measure of intermediate levels of hepatic lipids could reflect intensive feeding of a poor-condition animal or starvation of a well-conditioned animal (sensu Dutil et al., 1998). Moreover, the timing of nutritional condition within the maturational cycle is critical for successful reproduction. For example, winter

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flounder (P. americanus) is a winter spawning species that provisions it eggs in spring, three to six months prior to spawning. P. americanus will forego spawning if nutrition is poor in spring as they do not have enough reserves for provisioning gametogenesis (Burton, 1994). Visceral fat has been linked to an endocrine switch in the gametogenic cycle in walleye S. vitreum (Henderson et al., 1996; Lambert et al., 2003). Sampling fish throughout the year, or understanding the reproductive cycle and the timing of provisioning for eggs, offers a better opportunity to link female condition to reproductive events and can better inform the link between female condition and offspring quality and the causes of foregoing reproduction. (d) Detection: In ecosystems with few trophic relationships it may be easier to detect a relationship between trophic and reproductive variables, for example, food limited ecosystems such as the Barents Sea or Icelandic shelf (Lambert et al., 2003). Certainly it appears that the most predictive condition measures for reproductive productivity vary with each stock within the ocean they are measured. Lambert et al. (2003) summarised the variation in predictive power of condition measures for cod G. morhua across five different ocean or sea basins. In summary, in Icelandic cod the hepatosomatic index was a better predictor of fecundity than Fulton’s K (Marteinsdottir and Begg, 2002), for Baltic cod fecundity was unrelated to female condition (Kraus et al., 2002) and in northeast Artic cod hepatosomatic index was predictive of fecundity and recruitment (Marshall et al., 1998). 2.3.5. Social status High social status is generally assumed to confer benefits attained by increased access to resources such as food, habitat and high quality mates, which theoretically should result in increased reproductive output (Martin-Smith and Armstrong, 2002). One of the indirect effects of social status is that competitive dominants not only have better access to food resources, but can also use them more efficiently (steelhead trout S. gairdneri, Abbott and Dill, 1989) and therefore have higher lipid reserves for reproduction. This pathway from social environment to offspring quality is an opportunity for the expression of maternal effects. While the benefit of social status on reproduction is a common phenomenon amongst mammals (e.g., baboons, Wasser et al., 2004), and social insects (Alexander and Sherman, 1977), there is very little evidence of such benefits occurring in adult female fishes. However, dominance-related benefits occur in juvenile salmon (Huntingford and Garcia de Leaniz, 1997; Metcalfe, 1986; Metcalfe and Thorpe, 1992) and dominant adult males can monopolise spawning opportunities, for example, white-spotted charr Salvelinus leucomaenis (Maekawa et al., 2001), and Atlantic salmon, S. salar (Fleming, 1998; Garant et al., 2003). Social dominance and its subsequent benefits are most likely to

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occur when the resources are predictable; a caveat that rarely occurs in natural aquatic ecosystems but might occur frequently in aquaculture and artificial breeding facilities. Adjunct to benefits conferred through better access to resources are disadvantages due to social stress. In primates, increased social stress due to low position in a hierarchy increases ill health and decreases reproductive success and access to quality mates (Sapolsky, 2005). Interactions with conspecific females raised stress hormones and resulted in smaller offspring a territorial damselfish, P. amboinensis (McCormick, 2006), and although dominance status was not measured in these studies, tropical territorial species offer an interesting opportunity to examine these effects in wild populations. Another territorial damselfish group, the anemonefish (Premnas and Amphiprion sp.), live in groups in sea-anemones which offer protection from predators. For many species social groups are made up of a single reproductive pair and numerous subordinate non-breeders. Within these groups are size-dominated social hierarchies which restrict growth in subordinate fish, thereby reducing their life-time reproductive potential. The subordinate fish do not become reproductively active until one of the dominant pair dies. The female is the highest ranking fish, and if she dies her partner changes sex and becomes the dominant female and the topranking non-breeder becomes the reproductive male (Bell, 1976; Buston, 2003; Fricke, 1983). The queue to being a reproductive female can be a long one, and on the way, growth occurs in the steps allowed by social hierarchy changes. Given the complex social structures occurring in fishes and the frequency of social status causing maternal effects in other taxa, the effects of social dominance on the reproductive success of fishes are certainly an area that warrants further investigation, as it is a direct pathway for the expression of maternal effects in fishes. 2.3.6. Maternal behaviour Maternal reproductive behaviour is a pathway for maternal effects to influence offspring quality as behavioural decisions of the mother, such as nest site or mate choice selection can influence the quality and amount of resources available to developing young (Dufty et al., 2002). Females are responsible for provisioning the eggs (pre-oviposition), spawning site choice (oviposition), and in the case of nesting species, the environment in which the eggs develop and parental nest care or brooding the eggs (post-oviposition). The extent that female behaviour can influence offspring quality depends on reproductive mode, embryo parity, attributes of egg placement and the length of time for each stage of development. Maternal behavioural choices can be initiated at various stages throughout the production cycle, including: before gametes are produced, during gamete production, at the time of fertilisation (oviposition), during gamete maturation (i.e., early embryonic development of the offspring) and post-hatching.

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Here is another field which warrants its own comprehensive review, so I will attempt to synthesise only the key points of interest here. 2.3.6.1. Pre-spawning and oviposition behaviour There are three likely pathways for a maternal effect to be manifest in the pre-spawning behaviour of females. These include mate choice, nest-site selection and nest-site construction. In some reproductive modes there will be no distinction between these three categories as choosing a mate may involve spawning in his selected territory and pre-constructed nest-site, and part of mate choice can be based on quality of territory or nest-site. However, in many reproductive modes, female behaviours during one or more of these processes can influence the quality of her offspring. Paternal investment may include building the nest, defending the nest against predators, and fanning to oxygenate the eggs. Males in some species will demonstrate conspicuous secondary sexual characteristics such as courtship behaviours, breeding coloration to attract a female to their nest (Perrin, 1995). The influences of sexual selection and male social dominance, size or quality on reproductive success are core to the study of reproduction in terrestrial ecology (Kirkpatrick, 1985). Female preference for a mate is based on some aspect of male behaviour or morphology which indicates male quality, according to indicator models of sexual selection (Zahavi, 1975). While male quality is often a male genetic trait, the female choice for a mate is a potential pathway for a maternal effect. Individual female mallard (duck) laid larger eggs after copulating with preferred males, and smaller eggs after copulating with less preferred males, resulting in offspring with better body condition when paired with preferred males. Preferred male was a measure of female choice and male quality. In an elegant extension to this study the authors then controlled for the differences in maternal investment, which led them to conclude that the differences in offspring size were neither related to female or male genotype, but were a maternal effect in response to male quality (Cunningham and Russell, 2000). Similarly, dung beetle females breeding with the dominant phenotype (horned males) produce heavier brood masses (Hunt and Simmons, 2000). In aquatic systems, many fishes provision there eggs well before copulation and therefore do not demonstrate variation in egg size due to the paternal phenotype, however in some fishes this phenomenon does exist. (a) Mate choice: Mate choice is predicted to enhance survival chances of the offspring (Wedekind et al., 2001) and there are two ways a female can enhance her offspring quality through mate choice. Firstly, females can select for a higher quality partner (genotype or phenotype) who will provide better genes, quality gametes and parenting ability or a better nest-site, which can all affect offspring quality (Doty and Welch, 2001); secondly, females can change their own investment in their offspring according to the quality of the male they are partnered with.

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Female choice of male secondary sexual characteristics can influence offspring fitness (Mousseau and Fox, 1998). Traditionally, these secondary sexual characteristics represent gene quality, though selected traits might also represent good recent feeding history for example, colour (carotenoids), gloss and weight. Sire attractiveness in whitefish (Coregonus sp.) increased the expression of a maternal effect as males with stronger ornamentation sired offspring with highest resistance to bacterial infection, resulting in lower mortality (Wedekind et al., 2001). Parasite load and nest location were important signals for female mate choice and mating success in the threespine stickleback, G. aculeatus (Blais et al., 2004). Female gobies (Rhinogobius brunneus) used current speed of the location where courtship behaviour was displayed as a signal for high quality males to mates with. Males displaying under higher velocity water flow had highest offspring survival (Takahashi and Kohda, 2004). It was indirectly demonstrated that females choose males and nest-sites according to proximity to cleaner stations in a tropical fish (longfin damselfish Stegastes diencaeus, Cheney and Coˆte´, 2003), but no direct influence on offspring quality was detected. Female guppies that mated with multiple mates produced larger and more offspring, had shorter gestation periods and better schooling and escape abilities than females mated with only one mate (Evans and Magurran, 2000; Ojanguren et al., 2005). As female guppies invest in the yolk before fertilisation (lecithotrophy), possible mechanisms for larger sizes are selective abortion and reallocation of resources, or delayed fertilisation assisted by sperm storage (Ojanguren et al., 2005). When mate choice (and the chance of differential female investment in response to male quality) was removed, and male quality alone was tested, sire quality increased offspring predator avoidance in guppies (Evans et al., 2004a). The attractiveness of mate qualities changed with age and sexual experience of the female in guppies (Kodric-Brown and Nicoletto, 2001). Female banggai cardinalfish (Pterapogon kauderni) altered their investment in egg size according to the size of the male they were mated with, and this occurred very quickly (Kolm, 2001; Kolm and Olsson, 2003). In a species where males brood the offspring (pipefish Syngnathus typhle), broods from preferred matings had better predator escape ability and survival, but not necessarily faster growth. Female choice resulted in faster-growing offspring but male choice did not (Sandvik et al., 2000). In highly exploited fish stocks, mate competition, mate choice, and other components of mating systems can affect population growth rate deleteriously (Rowe and Hutchings, 2003). Dominant and larger males achieve more ‘ventral mounts’ from females and have higher fertilisation success (Atlantic cod, G. morhua, Hutchings et al., 1999) and unfortunately heavy fishing pressure is exemplified by selective removal of larger more aggressive males, a phenomenon that may be contributing to this species slow recovery in spite of fishing moratoriums (Rowe and Hutchings, 2003).

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When assessing the reproductive potential of a stock, male participation is assumed equal across males, however if female mate choice plays a role and larger dominant males are able to dominate fertilisation then the inclusion of ‘lesser’ males in a stock assessment may produce misleading or inaccurate results (Trippel, 2003). In aquaculture, the field of mate choice is generally overlooked as fish are typically stripped of their gametes for in vitro fertilisation: this acts to reduce undesirable variability and heterogeneity but also removes the possibility of females altering their investment (number of quality of eggs released) depending on the male she spawns with. Female courtship displays and other secondary sexual characteristics such as ornaments are further traits that may introduce a parental effect into offspring quality through male choice of mate. If strong maternal traits are common then males should select for larger fitter, more fecund females (Pelabon et al., 2003), but this is often not the case. Also if males offer some brood protection and there is a bias in the operational sex ratio, then the females must compete over mates (Sandvik et al., 2000). (b) Nest-site selection and construction: Nest-site selection can be important in providing nutrients, oxygen, protection from predators, and ideal development temperature amongst other environmental variables, and is ultimately critical for survival of offspring to hatching (in optimum condition). Choice of ‘hot nests’ in heliothermic (basking lizards) was important in providing ideal incubation conditions for lizard eggs (Shine, 2004). Numerous studies examine female preference for nest site relative to environmental variables, but only a sub-sample of these measure the direct consequences to offspring quality of nest-site selection, that is, the maternal effect. Nest site selection can be an indirect genetic effect (Hunt and Simmons, 2000) or a non-genetic effect on offspring quality. A general covariate of nest-choice is male quality, as larger males tend to obtain better territories. Female gobies (Padagobius martensi) had a distinct preference for a larger nest-site, and larger males held larger nest sites, but when the investigators tested for a female preference for larger males they could not identify one (Bisazza, 1989). In a number of species, females prefer to spawn in nests that already have eggs, as an indicator of offspring survival likelihood, for example, river bullhead (Cottus gobio), fathead minnow (Pimephales promelas), fantail darter (Etheostoma flabellare), tessellated darter (E. olmstedi), damselfish (Chrysiptera cyanea), garibaldi (Hypsypos rubicundus), Mediterranean blenny (Aidablennius sphinx) and three-spined stickleback (G. aculeatus) ( Jamieson, 1995). High water flow can disrupt spawning and reduce survivorship of young (smallmouth bass, M. dolomieu, Lukas and Orth, 1995). Female common gobies (Pomatoschistus microps) prefer to spawn in nests with the smallest entrance, which reduces detection by predators, but because the size of the entrance hole influences water flow and therefore oxygen through the nest, when oxygen is low this preference

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disappears ( Jones and Reynolds, 1999). Females prefer larger nests to smaller nests (freshwater goby Padogobius martensi, Bisazza, 1989 and mottled sculpin Cottus bairdi, Downhower, 1980), and sheltered nest-sites compared to exposed sites (three-spine stickle-back G. aculeatus, Sargent, 1982) Each of these choices for nest-site can alter exposure to environmental variables which influence egg development and survival, resulting in both direct and indirect maternal influences on offspring quality. Modelled simulations of larval transport pathways in pelagic spawning fishes indicate that the choice of spawning site is a critical factor in survival to suitable recruitment grounds (Paris et al., 2005). Predation risk is amongst other environmental factors in the consideration of mate choice and nest–site selection ( Johnson and Basolo, 2003). Terrestrial animals, such as birds, will assess predation risk at each nest site, choosing safety from predators over microclimate and proximity to food (Forstmeier and Weiss, 2004). It should be noted that in birds, nest predation is the main cause of reproductive failure. While it is likely that high mortality of fish eggs and larvae (estimated at 99.9%, Ferron and Leggett, 1994) is due to predators, there are few clear demonstrations of fishes assessing predation risk in the choice of nest site (but see above mentioned goby example, Jones and Reynolds, 1999). The choice of nest-site or host can induce plasticity in offspring traits through a maternal effect. In the seed beetle (Stator limbatus), egg size varies significantly with selection of host plant. Females produce large number of small eggs on the host plant that favours survival, and small numbers of large eggs on the host plant with low survival (resulting from high mortality penetrating the seed coat). Seed beetles were flexible in adapting egg size to host (Fox et al., 1997). 2.3.6.2. Spawning behaviour

(a) Mating success. Maternal mating behaviour can have a large influence on the quality and number of offspring. Females actively influence the type and amount of resources available to their developing young by where they lay their eggs and with whom they mate (Dufty et al., 2002). Relative male size can influence mating success (cod, G. morhua). Males that were more that 25% of the length of the female had low seasonal reproductive success (Rakitin et al., 2001). Group spawning resulted in higher fertilisation success than single male spawning in the bluehead wrasse (Thalassoma bifasciatum, Robertson, 1996). (b) Placement of eggs. In addition to selecting a good nest-site, the actual placement of eggs within a nest-site can also influence phenotypically plastic traits. Individual variation in habitat preferences can play a role in metapopulation dynamics, local adaptation and sympatric speciation (Davis and Stamps, 2004). For sexually labile species such as turtles, depth of laying determines offspring gender (Valenzuela, 2001). Location

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can be linked with quality as buoyancy can become very important in some environments (Vallin and Nissling, 2000). Proximal embryos in a squid egg strand developed more slowly and suffered higher mortality than their distal siblings in the southern calamari, Sepioteuthis australis (Steer et al., 2002). Competition for nesting sites can be so intense in salmonids that females reuse nest-sites with eggs already in them. Redd superimposition in brook trout (S. fontinalis) resulted in the loss of 28–38% of broods, though larger females had deeper nests which increased survival of their broods in two ways by reducing the chance the nest-site would be re-used, and placing their eggs in the stream of ground-water flow (Blanchfield and Ridgway, 2005). (c) Oviposition and spawning. The process of spawning can introduce variation to offspring through order of laying, choice of nest-site, predation, microclimate and advection. Larval size at hatching is a result of the initial egg size (and therefore a summation of the female and her environment) and the environmental conditions experienced during egg development (Fleming and Gross, 1990; Green et al., 2006), which usually occurs in a location determined by the female. Maternal effects have been considered (though rarely) in the comparative physiology literature. Eggs from the centre of a clutch in a benthic spawning species (A. melanopus) were larger than eggs on the periphery of the clutch, though this difference was not related to the laying order (Green et al., 2006). Order of laying can influence variation within a clutch. For example, in newts (Hynobious nigrescens and H. lichenatus) the female lays the largest eggs first and egg size is reduced as reproductive resources are depleted (Takahashi and Iwasawa, 1988). Female pied flycatchers (Ficedula hypoleuca) partition resources and lay the largest eggs last (Potti, 1993). 2.3.6.3. Post-spawning behaviours After gametes are released, factors such as parental care, microclimate, predation can influence quality and survival. Maternal effects may be introduced via any of these factors.

(a) Parental care. Parental care is ‘any investment by a parent, other than egg yolk, that increases the survival of the offspring until they are independent of all parental resources’ (Sargent et al., 1987, p. 33). Twenty-one percentage of families of bony fish show parental care of eggs (CluttonBrock, 1991). In species with bi-parental care, both parents can alter the offspring phenotype, as the level of care is dependant upon the provisioning competence of both parents (Hunt and Simmons, 2000). Many organisms can use behaviour to buffer environmental effects such as temperature (wood frog R. sylvatica, Freidenburg and Skelly, 2004) and oxygen (anemonefish A. melanopus, Green and McCormick, 2005b). In this sense, parental behaviour potentially reduces variation in offspring

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traits that may otherwise result from a variable environment, leading to maternal or parental effects on the offspring. Male gobies reduce their own feeding rate when tending a nest, losing condition to optimise their nest environment (Skolbekken and Utne-Palm, 2001). Crespi and Lessig (2004) used a cross-fostering experiment in salamanders to demonstrate that post-oviposition events, namely nest care, had a greater influence on factors such as body size than pre-oviposition events. Cross-fostering experiments are frequently used in studies of bird populations to bisect the effects of the parental allocation to the egg and post-oviposition care of the egg and hatchling. This facilitates partitioning the variance due to parent and environment. Survival of nestlings was related to foster-parent care while egg mass was related to the originally maternally determined egg size in the alpine swift (Bize et al., 2002). In lizards, choice of nest-site was critical to the thermal regime experienced by the nest, moreso than female basking behaviour or the evolution of viviparity (Shine, 2004). In striped mice paternal nest care increased growth rate of offspring in extreme environments but had no effects in a benign environment, suggesting the non-genetic parental effects can be tightly linked to environmental conditions (Schradin and Pillay, 2005). While many studies look at the costs and trade-offs to parents showing ‘good’ parental care or qualities of good genes, very few studies then examine how this translates to offspring quality or survival, and fewer even still examine a maternal component to this. (b) Specialised brooding. Specialised brooding systems in fishes such as mouth and pouch brooding afford further pathways for the expression of parental effects. Potential sources of maternal and paternal effects are the physical attributes of the brooder, including the brooding parts such as the mouth and pouch. In fishes, males are more frequently involved in brooding than females. Male pouch brooding, which occurs only in pipefishes and seahorses (Sygnathids), is also known as paternal viviparity. Larger male seaweed pipefish, Syngnathus schlegeli, attracted females which produced larger eggs, and had higher volume pouches and lower density eggs, which resulted in larger, heavier offspring emerging from larger males (Watanabe and Watanabe, 2002). Large parents produced offspring that were larger and had higher survival than offspring from younger and smaller parents, and for males large body size was positively correlated to offspring number in the yellow seahorse Hippocampus kuda (Dzyuba et al., 2006). Both of these studies suggest that low density in a larger pouch may offer physiological support during gestation or there are physiological restrictions such as oxygen supply or specific salinity in the pouch (Monteiro et al., 2005) such that low offspring density in the pouch favours growth (Dzyuba et al., 2006; Watanabe and Watanabe, 2002). Mouth brooding is also predominantly

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a male task, and occurs in Apogonids and Cichlids. Females of the mouth-brooding bangaii cardinal fish (P. kauderni) produced heavier eggs and heavier clutches for a larger male, according to the differential allocation hypothesis (Kolm, 2002) and larger males brood heavier egg clutches, independent of female size (Kolm, 2001). pH of the buccal cavity can influence offspring success, as slightly acidic conditions were necessary for egg fertilisation in Saratherodon aurea (Noakes, 1979). Not surprisingly, filial cannibalism often occurs in mouth-brooders, that is, the male eats the young that are incubating in his mouth. It seems that it is a phenotypically plastic trait in Apogon doederleini (Takeyama et al., 2007) and the occurrence changes with male age, condition and mate availability (Kondoh and Okuda, 2002; Okuda, 1999; Takeyama et al., 2002, 2007). Filial cannibalism is an extreme pathway for a parental effect. (c) Feeding. In marine mammals there is a connection between marine environment and reproductive performance, through resource acquisition and allocation to offspring. Female fur seals must balance optimal foraging and prey acquisition with frequent visits to the rookery to feed their pup. Females with greater diving times and better foraging sites raised pups with the highest growth rate (Beauplet et al., 2004). While in general fishes do not feed their young, there are a number of mechanisms where post-oogenesis nutrition is provided, offering another portal for a maternal or parental effect. Two such mechanisms are matrotrophy and glancing. Matrotrophy is a subdivision of viviparity, and is the nourishment of viviparous embryos by resources provided between fertilisation and parturition, and occurs in a number of species including fishes from the family Scorpaenidae (subfamily Sebastes, the rockfishes) and the coelacanth (Boehlert and Yoklavich, 1984). Glancing occurs after hatching when the larvae or juveniles remain in close association with the parents and are seen to touch the parents’ skin with their mouths, and in some cases receive nutrition from this, appearing to feed off mucous coating parents skin (Kavanagh, 1998; Noakes, 1979). Glancing or parent-contact occurs in only a handful of fish species (approximately 28 species, mostly cichlids). Most observations are descriptive, however Kavanagh (1998) demonstrated ingestion of the mucous by the offspring in A. polycanthus (Pomacentridae), though this author suggested it did not occur in large enough quantities to be a substantial part of offspring nutrition. In two species of catfish the young feed off a milky proteinaceous fluid secreted by the skin of the parents (Noakes, 1979). I am not aware of any direct studies on either of these feeding modes as a pathway for a maternal effect, but mention them here as it is a likely sources of phenotypic variability that is dependent on female (and male) condition.

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2.3.7. Paternal effect Paternal effects on offspring traits in fishes and other organisms are infrequently examined in studies of the non-genetic parental effects on offspring traits. This is due in part to the historic belief that males contribute no more than DNA to their offspring, resulting in little opportunity for non-genetic effects. Recent studies on human sperm have demonstrated that in addition to DNA, sperm carries RNA and other proteins which contribute still unknown things to offspring, and so in humans, sperm is more important to offspring quality than previously thought (Ainsworth, 2005). Amongst the pathways for the expression of paternal effects are female choice and subsequent female investment in propagules, sperm quality and delivery, paternal brooding, male site selection and nest construction. Paternal effects can also incorporate influences from the previous generation, known as grandfather effects, although these are determined by the maternal genome which in turn was determined by the grandpaternal genome (Reznick, 1981). If egg size was purely a trait of the mother, then there should be no difference in egg size between sires (Roff, 1997), yet there are examples from a range of taxa where females produce different egg sizes or number depending on mate quality, for example, jungle fowl, Gallus gallus (Parker, 2003); pea fowl, Pavo cristatus (Loyau et al., 2007); zebrafish, D. rerio (Spence and Smith, 2006). Artificial insemination uncouples mate choice from copulation, and allows mate quality to be assessed separately from perceived mate quality. Mate quality may impose a paternal effect or a genetic effect, while perceived mate quality can elicit a change in female investment in response to mate quality. For example, when female jungle fowl were caged with vascetomised male jungle fowl and artificially inseminated, the number of eggs produced increased with the size of the comb of the co-habitant (perceived mate) not the sperm donor (actual mate) (Parker, 2003). When female guppies (P. reticulata) were artificially inseminated, escape response in offspring increased with quality of male coloration, which was likely a paternal genetic effect, but may be non-genetic (Evans et al., 2004b). In fishes there are numerous examples were paternity affected offspring traits, whether through a paternal effect (strictly non-genetic) or the broader paternal influence, which may incorporate unmeasured genetic influences. Chinook salmon (O. tshawytscha) had a reduction in initial magnitude of maternal effect in fry after emergence and increase in sire effects after this time (Heath et al., 1999), suggesting the relative importance of maternal and paternal change with ontogeny, possibly as genetic influences (paternal) were expressed, and the effects of non-genetic influences were reduced. The magnitude of a paternal effect in winter flounder offspring (P. americanus) changed with ontogeny, expressed as an increase in larval length from hatch through to day 8, and an increase in eye diameter, head depth and

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body area when expressed as maternal  paternal interaction (Butts and Litvak, 2007). This study also demonstrated that the paternal effect was greater than the maternal effect for fertilisation success and less for all other traits measured (morphological and timing such as time to hatch, hatch success and yolk utilisation efficiency). Paternal viviparity, or male brooding, is a notable pathway for a paternal effect in fishes. Sygnathids, which include pipefishes and seahorses, are a particular case where the non-genetic male effect would influence offspring quality as male sygnathids brood their young in a pouch. The pouch environment the male provides can directly influence the development of the offspring. For further details see ‘male brooding’ in Section 2.3.6. Further occurrences of paternal effects have been described in nonbrooding species. The expression of a paternal effect can depend on traits of the female. Rideout et al. (2004) suggested that the expression of a paternal effect depended on differences in egg size between females. If egg sizes are similar, it would be easier to observe paternal effects, but if egg sizes are very different, these effects may be obscured. Paternal effects influenced size at hatching in herring larvae C. harengus (Evans and Geffen, 1998; Panagiotaki and Geffen, 1992). Sperm motility affected the size of larvae at hatching in Atlantic herring (C. harengus), but there was no difference in sperm quality and fertilisation rate between first time and repeat spawners (Evans and Geffen, 1998). The majority of variance in growth until metamorphosis (52%) was ascribed to paternal effects in an anemonefish, A. melanopus (Green and McCormick, 2005a), which has extensive male nest care until hatching (Green and McCormick, 2005b). While it is likely that variation in offspring quality due to female traits will be higher than that due to paternal traits as the females provisions the eggs with nutrients, hormones, antibodies, etc., and generally chooses spawning location, this does not exclude the male contribution as a significant source of offspring variation. Sperm competition in Atlantic cod (G. morhua) resulted in difference fertilisation success rather than difference quality of offspring in direct tests of pair fertilisation competition (Rakitin et al., 1999, 2001). In group spawning fish such as Atlantic cod, larger and more dominants males can achieve higher fertilisation success (Hutchings et al., 1999). When Atlantic salmon (S. salar) were hand-stripped, a fertilisation strategy that removes female choice of sire and the concomitant influences of such a choice, there was no evidence of offspring size relative to male phenotype (Einum, 2003). Timing of sperm release during a spawning event is another pathway for a paternal effect in fishes. In two sessile marine invertebrates, the sea urchins, Heliocidaris erythrogramma and Holopneustes purpurescens, males which spawned first successfully fertilised the largest and most fertile eggs, and consequently sire the largest offspring (Marshall et al., 2004).

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2.4. Summary of evidence of maternal effects Maternal effects and maternal influences (see Box 1.1 for definitions) occur in many fish species via a range of maternal and offspring traits, as described above in this review. Examples from mammals, insects, birds and marine invertebrates provide a broader framework for examining maternal effects in fishes, and offer some directions for future research. These systems have been used to compare the patterns that have been identified and the questions that have been asked, and from here, to elucidate the questions that have not yet been examined in the study of maternal effects in fishes. The complex breeding designs required to partition a true maternal effect from genetic influences has limited the number of true maternal effects found in fishes (Table 1.4). However, a wide range of cases of maternal influences affecting offspring traits have been described here. The purpose of the next section is to further summarise the offspring traits affected.

3. Offspring Traits Affected One of the challenges in the examination of maternal effects in fishes is the choice of offspring traits to measure, as trait choice is central to assessing the expression of maternal effects. The range of offspring traits can be broadly divided into genetic, morphological, physiological, behavioural, and ontogenetic (Table 1.6). Ontogenetic traits arise from the preceding four categories, but are quantified in time units. For example, size is a morphological trait, but change in size over time (growth) is an ontogenetic trait. Morphological traits are the most commonly measured in fishes probably as these are the easiest and cheapest to attain. Some commonly measured morphological traits are egg size, larval size, otolith size or growth increment, yolk size. Physiological traits include lipids, hormones, colour, RNA/DNA, metabolic rate (often measured by oxygen consumption) and disease resistance. Behavioural traits include performance, such as swimming ability, predator escape or sprint speed (Table 1.6). The disadvantage of all these traits is that they change over time and most published measurements are point samples taken from a developmental trajectory, and there is a risk that differences may be obscured or exaggerated by comparing different stages of development (Fig. 1.2). Ontogenetic traits take the developmental trajectory into account, measuring development in salutatory steps (Balon, 1985) and include developmental time, time to metamorphosis, survivorship, diapause length, growth. Many studies of maternal effects in fishes aim to examine the effects of maternal effects on recruitment. Within a population, this is assessed by correlating a maternal trait to recruitment, both measured from large

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Table 1.6

Traits that have been measured in the early life-stages of marine fishes

Trait

Trait groupa

Item measured (units of measure) b

State or rate

Initial size of fertilised egg Survival of embryo to developmental event or sub-stage Age of embryo at developmental event or sub-stage Developmental rate of embryo to event or sub-stage Size of embryo at developmental event or sub-stage Growth rate of embryo

L, M L

Diameter (mm), weight (mg) Live or dead

S S

D

Time between two sequential embryonic stages (h or d) Rate between two sequential embryonic stages (d1) Length3 (mm), weightb(mg)

S

Survival to hatching Age of larva at hatching Developmental rate to hatching

L L L

Size of larva at hatching Shape of larva at hatching Energy reserves of larva at hatching

L, M M P P

Condition of larva at hatching

M, P B, P B, P B, L, P L

D, L L, M L, P

Length change (mm/d), weight change (mg/d) Live or dead (count) Time from fertilisation of egg to hatching (d) Time from fertilisation of egg to hatching (d1) Length3 (mm), weightb(mg) Lengths between landmarks (mm) Yolk axes (mm), conversion to volume Oil globule axes (mm), conversion to volume Weight per unit length (mg/mm) RNA/DNA (mg/mg) Total or constituent storage lipids (mg/mg) Time to starvation (d) Live or dead (count)

R S R S S R S S S S S S S S S

Survival of larva to developmental event or sub-stage Age of larva at developmental event or sub-stage Developmental rate of larva to event or sub-stage Size of larva at developmental event or sub-stage Size-at-age of larva Growth rate of larva Condition-at-age of larva

Consumption rate of larva Swimming rate of larva Attack avoidance by larva Survival to larval-juvenile transition (metamorphosis) Age at larval-juvenile transition (metamorphosis) Developmental rate to larval-juvenile transition (metamorphosis) Size at larval–juvenile transition (metamorphosis) Survival of juvenile to developmental event or sub-stage

D D, L L, M L, M L, P M, P B, P B, P B B B L D

time between two sequential larval stages (h or d) Rate between two sequential larval stages (d1) Lengthc(mm), weightb(mg)

S

Lengthc(mm), weightb(mg) Lengthc(mm/d), weightb(mg/d) Weight per unit length (mg/mm) RNA/DNA (mg/mg) Total or constituent storage lipids (mg/mg) Numbers consumed per unit time (num/ min) Distance per unit time (mm/sec) Number attacks per success (num/num) Live or dead (count)

S R S S S R

R S

R R S

D, L

Time from hatching of egg to metamorphosis (d) Rate to metamorphosis (d1)

S R

L, M

Lengthc(mm), weightb(mg)

S

L

Live or dead (count)

S

75

(continued)

Table 1.6

a

(continued)

Trait

Trait groupa

Item measured (units of measure)

State or rate

Age of juvenile at developmental event or sub-stage Developmental rate of juvenile to event or sub-stage Size of juvenile at developmental event or sub-stage Size-at-age of juvenile Growth rate of juvenile Condition-at-age of juvenile

D

Time between two sequential juvenile stages (h or d) Rate between two sequential juvenile stages (d1) Lengthc(mm), weightb(mg)

S

Lengthc(mm), weightb(mg) Lengthc(mm/d), weightb(mg/d) Weight per unit length (mg/mm) RNA/DNA (mg/mg) Total or constituent storage lipids (mg/mg) Numbers consumed per unit time (num/ min) Distance per unit time (mm/sec) Number attacks per success (num/num)

S R S S S R

D, L L, M

Consumption rate of juvenile

L, M L, P M, P B, P B, P B

Swimming rate of juvenile Attack avoidance by juvenile

B B

R S

R R

L, life history; M, morphological; D, developmental; B, behavioural; P, physiological; C, biochemical. Weights measured as either wet or dry weight. c Lengths measured as either standard or total length. Each trait belongs to one or more trait groups. Many traits can be measured in multiple ways. Traits are most commonly measured as static features but rates of change can be derived from these. b

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Maternal Effects in Fish Populations

Size

A

Juvenile e va ar

Eg

g

E

La gg

w

B

Size

e rva

L

x y

Egg

Larvae

Egg

Larvae

Juvenile

Size

C

z

Juvenile Time

Figure 1.2 Hypothetical growth from eggs to juvenile to illustrate a number of the challenges in using offspring size at a single point in time to identify maternal effects. For each graph the solid line is growth 1, the dashed line is growth 2 and the dotted line is growth 3. (A) Two growth trajectories with the same shape but different starting point in time, if compared at line w then growth may be considered quite different, even though they were the same size as eggs, they hatched at the same size and metamorphosed at the same size. (B) Three different growth trajectories starting from the same point. Fish following growth pattern 2 and 3 at line y are the same size, and are at comparable development stages. Growth 1 fish are just hatching, and so are at a different ontogenetic stage even though similar sized, but they reached that size faster. Similarly with sizes along line x: While fish from growth patterns 1 and 2 are similar size they are at different developmental stages. (C) Three growth trajectories with different initial sizes, growth 1 and 3 follow the same trajectory but fish following growth 1 were larger eggs, and that size advantage is maintained through to the juvenile stage. Fish following growth 2 were larger eggs that growth 3, but egg and larval growth were slower. If measured and compared to growth 3 at point z then the larval size is the same and a maternal effect through egg size might be overlooked, so the best point of comparison might be at an ontogenetic stage, for example, as an egg, at hatching or at metamorphosis or a transition to juveniles.

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numbers of individuals. Often such a correlation is reduced to cause and effect. To assess maternal effects of an individual fish on its own offspring, there are three transition stages to assess within the generalised life-cycle of fish. There are assumptions relating to the survival from each step to the next (Table 1.7), and through this pathway, a maternal attribute (size in Table 1.7) is purported to influence recruitment. One of the current unifying theories in maternal effects suggests that larger females produce larger eggs which result in large larvae which have more chance at survival. Each step of this theory has numerous assumptions, few of which have withstood rigorous testing. For any maternal effect to influence recruitment, it requires that mortality in the early stages of fishes is selective, acting on maternally derived offspring traits, and selecting for or against some level of quality. ‘Lower’ quality juvenile were selectively removed from population of damselfish, P. amboinensis (Hoey and McCormick, 2004) and North Sea haddock, M. aeglefinus (Wright and Gibb, 2005) and high quality fish selectively survived. While there is some evidence to support the assumptions at each life stage, to our knowledge, only one study has demonstrated a correlative link between older females and higher recruitment (Wright and Gibb, 2005), thus suggesting that a maternal effect was maintained through the three transition stages within the generalised life-cycle of a fish. In organisms where it is possible to follow a generation from female through the life stages, there are demonstrated connections between female, Table 1.7 Do larger females produce better or more recruits? Life stage transition

Assumption

Female to egg Larger females produce larger eggs Egg to larvae Larger eggs produce (hatching) larger/better larvae

Larvae to Larger larvae result juvenile or in better recruit recruitment Female to Larger/older females recruitment produces better recruitment

References

Hislop (1988); 43 spp, 121 pop’s Hendry et al. (2001); 21 spp, 89 pop’s Heath and Blouw (1998) Chambers et al. (1989); Ouellet et al. (2001); 16 spp, 23 pop’s Heath and Blouw (1998); 13 spp, 18 pop’s Gall (1974); Reznick (1991) Bergenius et al. (2002); Hoey and McCormick (2004); Meekan and Fortier (1996) Wright and Gibb (2005)

Generalised life stage transitions in fish and the assumptions that apply to each stage if larger females are better. References include citations that support the assumption at each life history transition.

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embryonic and larval or juvenile quality, for example, Seed beetles Callosobruchus maculatus (Fox et al., 2004), and bryozoans, Watersipora subtorquata (Marshall and Keough, 2004a, called ‘carry-over effects’). Within fishes, stages in the life-cycle have been demonstrated to have carry-over effects to the next stage, but not through the whole life cycle (Table 1.4). Larger haddock females, M. aeglefinus produced heavier eggs (Hislop, 1988). Larger egg produced larger, faster growing Chinook salmon (O. tshawytscha) fingerlings until 75 days after hatching (Gall, 1974). Faster larval growth resulted in higher recruitment in Acanthurus chirurgus (Bergenius et al., 2002). Although maternal effects in fishes are said to be negligible beyond the early juvenile stages (Heath and Blouw, 1998), any occurrence of maternal effects in the early stages could determine which individuals survive and are best resourced to reproduce in the next generation.

3.1. Response variable selection Trait choice and number, and the timing of trait measurement can determine whether a maternal effect is detected. In Chinook salmon (O. tshawytscha), a period was observed whereby the progeny generally exhibited a phenotype opposite to that of their mother. Offspring from eggs laid by large mothers were smaller than offspring hatching from eggs laid by small mothers, but this pattern was not consistent throughout whole developmental period (Heath et al., 1999). Interpretation of the relationship between female size and egg size in this study would clearly be affected by the time the eggs were measured. In whitefish (Coregonus lavaretus), early versus late mortality were not related to each other, but were related to parental quality (Wedekind et al., 2001). In many cases, a maternal effect in trait diminishes with time, as the main maternal influence was on egg size, as packaged by the female (Atchley, 1984; Atchley and Zhu, 1997; Heath et al., 1999). In a full factorial cross of Chinook salmon, a paternal effect can became more apparent after the major egg size influence diminished (Heath et al., 1999). Indicators or measures of quality, condition or fitness in offspring may be misleading, particularly in early developmental stages. For example, total length in tadpoles was misleading as it did not indicate survival, however snout-vent length did (Kaplan, 1991). In fishes, egg size is the most commonly reported trait affected by maternal effects, possibly as this is the simplest thing to measure, however, it is not always the trait that is the best predictor of offspring success. There was limited impact of egg characteristics on their viability and hatching success in Atlantic cod, G. morhua (Ouellet et al., 2001). Larval size is another frequently used indicator of maternal effects, but size is a stage that fishes pass through in early ontogeny and so condition of the fish per se may not have altered, just the trajectory of development (Fig. 1.2). Size

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also has a strong genetic component, and so unless offspring traits are measured in an f 2 reciprocal cross or in a cross-fostered offspring, then the genetic component is not always filtered out. Nevertheless, larval size in fish may reflect a maternal effect (e.g., Kerrigan, 1997). Parental environment can directly influence offspring physiological capabilities. For example, fucoid algal embryos tolerance to heat stress depended on whether parents had been exposed to heat stress (Li and Brawley, 2004). In some terrestrial vertebrates, maternal effects are frequently seen in the differential deposition of various egg constituents including androgens and antioxidants (Royle et al., 2003). A small number of studies have examined physiological pathways for maternal effects in fishes. Stress hormones were transferred from mother to egg in the ambon damselfish (P. amboinensis) (McCormick, 1999, 2006), but stress in females did not influence hatching success in cod (G. morhua) (Morgan et al., 1999). Maternal size and age directly affected the egg size and energy content in the nase, a freshwater cyprinid (Keckeis et al., 2000). Maternal antibody transmission was critical to chick immunity in birds (Muller et al., 2004; Saino et al., 2002b). The maternally aliquoted yolk and cytoplasm can be a key source of hormones, nutrients and antibodies that are directly transmitted from mother to the offspring in fishes (McCormick, 1998, 1999, 2006; Pilz et al., 2003). An offspring trait that may be overlooked in fish eggs is hatching asynchrony within and between clutches. Hatching asynchrony occurs when embryos within a clutch hatch out of synchrony, or at different times, and is hypothesised to occur to spread the risk of starvation, predation or mortality. Risk-spreading through hatching asynchrony occurs in birds (Laaksonen, 2004) and squid (Steer et al., 2002), but is rarely considered in fishes, although many fish species produce multiple broods within a few days. Hatching asynchrony did occur both within and between clutches in tomcod M. tomcod from two contrasting yet geographically close environments. Clutches from a less stable environment took longer to hatch and had greater hatching asynchrony (Green and Chambers, 2007). Hatching asynchrony may be an adaptive parental strategy to provide phenotypic variation and reduce sibling competition, or to produce diverse offspring with variable life history strategies as a riskspreading strategy in spatially and temporally variable environments. This is also known as the ‘offspring quality assurance hypothesis’ (Amundsen and Slagsvold, 1996). At both the population and individual level, asynchrony may be important in unpredictable environments. In birds, higher levels of asynchrony in hatching results in higher levels of variation in offspring dispersal distance from natal sites which reduces direct sibling competition. Further, maternal effects on chick characteristics were greater through hatching asynchrony than through egg allocation, due to sibling competition (Laaksonen, 2004).

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3.2. Trade-off between offspring size and number Optimal offspring size theory suggests that when reproductive resources are limited, a female will trade-off size and number of her propagules by increasing one at the cost of reducing the other (Smith and Fretwell, 1974). This will maximise her fitness by ensuring the maximum numbers of her offspring survive. Female Chinook salmon (O. tshawytscha) that laid larger eggs, laid substantially fewer eggs, and egg size correlated to yolk-sac larvae survival (Heath et al., 1999). Females in some taxa can adapt clutch size and numbers according to environmental conditions, in a predictable way. While this has been demonstrated in the planktonic crustacean Daphnia (McKee and Ebert, 1996), and anolis lizards (Sinervo and Licht, 1991) amongst other taxa, it is much more difficult to assess evidence for this trade-off in fishes, as it is difficult to track females or offspring in the wild. Inherent in the theory in this trade-off is that larger offspring have a better chance of survival. In fishes, bigger is not always better, in Artic charr (S. alpinus) smaller offspring developed faster (Valdimarsson et al., 2002), although larger eggs in Atlantic salmon gave rise to larger faster growing offspring (Einum, 2003). In addition to species-specific bestowal strategies, and production of dispersive or non-dispersive offspring, fishes demonstrate a range of strategies in provisioning their offspring. Firstly, when females are well fed they have increased investment in eggs, including better provisioning or bigger eggs (e.g., P. amboinensis, Gagliano and McCormick, 2007; Kerrigan, 1997); or conversely, when females are well-fed they produce more numerous, smaller eggs, preparing lots of offspring for a plentiful environment (e.g., poecilids, Reznick et al., 1996). This second strategy is believed to increase their fitness by producing lots of offspring which they do not need to provision as well as they will be born into a plentiful environment ( Jonsson et al., 1996). It is still early in the study of maternal effects in fishes, and so general patterns relating to female investment and environmental variation are yet to emerge. There is a parent-offspring conflict in optimality of egg size versus number. For the individual offspring an increase in size is better, while for the parent the trade-off between egg size and number should be optimised to maximise their lifetime fitness. Intergenerational discounting describes the trade-off in egg size and number that occurs between generations (Livnat et al., 2005).

3.3. Time course of effects (traits and ontogeny) Given the discrete life stages within many fish species, there is potential for maternal effects to be manifest differently according to the ontogenetic stage. The influence of maternal traits on offspring generally decline with

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development of the offspring, as the influence of the offspring’s own genetic architecture takes over (Atchley and Zhu, 1997; Heath and Blouw, 1998; Perry et al., 2004), so stage of development examined is critical to the interpretation of the results (see further discussion in Section 3.1). Attributes that provided an advantage during the egg stage may not be entirely beneficial in the larval stage (Hendry et al., 2001). While there are few (if any) physical examples of this, optimality models predicted differential advantages throughout different life stages in salmon. In reality, to my knowledge, no study of fishes to date has tracked a maternal effect through all of the early life stages. The majority of studies examine the influence maternal effects had on the egg stage (Table 1.4) as this is the simplest stage to examine and is assumed to affect performance, but this assumption is often confounded by genetics and mode of measurement (e.g., birds, Krist, 2004). At the time of hatching, the male genotype has had time to assert itself and there may be a detectable male effect (Roff, 1997) which was not detectable in egg size. In Chinook salmon (O. tshawytscha) a period was observed whereby the progeny generally exhibited a phenotype opposite that of their mother (i.e., offspring from eggs laid by large mothers are smaller than offspring hatching from eggs laid by small mothers), but this was not consistent throughout the whole developmental period (Heath et al., 1999). Offspring size is often used as an indicator of maternal effects, but in early ontogeny, size is a stage that fishes pass through. A single measure of size may not reveal much about the condition or quality of the fish per se (Fig. 1.2). Life history stages vary in sensitivity to maternal effects. Early stages are more likely to show variation due to maternal effects than late stages (e.g., diapause in insects, Mousseau and Dingle, 1991). In viviparous species the nature of the traits varies throughout development. Eggs have different dimensions to larvae, although size, length, width and weight are commonly used to summarise condition. Morphometric measures throughout ontogeny are measuring different aspects of the offspring. Egg length is a measure of the female allocation and the environment. It may be restricted by the size of the female’s pelvic girdle or cloaca, or diffusion through a surface area to supply a given volume for respiration. The length of hatched larvae has a different set of constraints, including maternal allocation, environment, Reynold’s number for locomotion through water, camouflage from predators and size advantage over prey to afford nutrition. The measurement of any trait is a measurement of the sum total of a range of inputs, and previous traits values, as well as maternal effects.

3.4. Difficulties in studying maternal effects and environment The study of the interaction of maternal effects and maternal environment is considerably more sophisticated in non-fish environments, than in aquatic environments, principally due to the ease in which large-scale experiments

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can be carried out on organisms such as insects, which might only require a single seed to complete their entire life-cycle. As such, the specific genetic and non-genetic architecture has been determined in a number of insects (e.g., seed beetle, Fox et al., 2004) and variance specifically due to quality of the female’s environment has been examined (e.g., yellow dung flies, Tregenza et al., 2003). This sophistication is far more difficult to achieve in the marine environment, where a dispersive larval stage is common, and offspring number in the millions. Much of the evidence to date of the interaction of maternal effects and environment in fishes comes from gobies and salmonids, which both lay benthic eggs, facilitating the study of the interaction between female choice of nest site, environmental conditions at the nest site and egg number quality and survival. 3.4.1. Detection of maternal effects There are a number of reasons a maternal effect might not be detected including: (a) Choice of observed or measured traits. Response in the measured traits (whether maternal or offspring) may be suppressed by covariance with an unmeasured trait. For example, the apparent effects of maternal age on her offspring might well be confounded by the increase in size that goes with that as most fishes have indeterminate size (Hislop, 1988). Fish age and size often co-vary and are frequently used interchangeably (though often incorrectly and without precise definition of the relationship). Another common source of error in measuring maternal effects is directly comparing traits such as size and weight of eggs sampled from difference stages of the reproductive cycle. (b) Error in measurement. The error (or imprecision) in measuring, including accuracy of the tools used for measurement, may be greater than the variance due to maternal effort. (c) Experimental design and analysis. Sample size, amount of replication or level of examination may be insufficient to detect an effect, that is, individual, batch, or population. (d) Single versus multi-factor responses. The simplest experimental approach to the study of maternal effects is to measure a single trait of female and one of offspring, and report this relationship with a measure of significance or variation. In reality the interactions between female and offspring are generally more complex, involving multiple factors and multiple traits, which can act to mask or enhance the expression of maternal effects through an interactive effect. For example, in Daphnia—generally chosen for its simplicity as a lab model—temperature, food and maternal phenotype interacted in an unpredictable and very complex way to affect offspring traits. Newborn weight increased with mother weight, and under low food conditions newborns were heaviest. Temperature effects

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on newborn weight were only significant as an interaction term with food and clutch number, and produced counter-intuitive patterns. In low-food conditions newborns were lightest at the lowest temperature, heaviest at intermediate temperatures and intermediate at the highest temperatures. The opposite pattern occurred under high-food conditions (McKee and Ebert, 1996). This example clearly illustrates the complexity of measuring a maternal effect and environmental variation even in this simple organism. (e) Laboratory versus field studies. Laboratory and field studies can provide different results in the examination of variation in offspring traits as they are under different environmental constraints, and they provide different opportunities for sampling and access to the study specimens. The integration of laboratory and field experiments into the examination and assessment of variance in offspring traits can increase the scope of assessable traits (see discussion in Lambert and Thorsen, 2003). While laboratory experiments in captive fish cannot replicate wild conditions, they can control a range of variables, while others are manipulated, allowing the researcher to partition out responses to specific changes. Similarly, while many variables cannot be controlled for in wild conditions, a well-planned experiment can assess responses in offspring traits to their natural conditions and numerically partition the effects of individual variables. The main challenge remains to cautiously interpret results from laboratory experiments, without extrapolating their outcomes to the wild where many more complex pressures operate.

4. Summary Maternal effects are an important component of the nature versus nurture debate (i.e., genetic constituents c.f. environmental influences) (Burggren, 1999), however, the relative importance of maternal effects to fish population dynamics needs further investigation. A large number of fish studies reporting on maternal effects have not separated the environmental and genetic components as sources of variation, so strictly speaking they have only examined maternal influences. To separate maternal effects from maternal influences requires the application of more sophisticated techniques than the most commonly used correlation between a single female trait and one or more offspring traits. Techniques such as egg manipulation, cross-fostering, full-factorial breeding experiments or mapping the genome will partition the genetic influences from the environmental influences, allowing for the identification of a maternal effect in the narrow sense, which has rarely been identified in fishes. However, the identification of maternal influences without partitioning out the genetic component has

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great value in fisheries science if it enables predictions of future year-class strength or other quality attributes based on traits of the current female stock. The diversity in the number of fish species, and the range of reproductive habits and environments inhabited make it difficult to find consistent patterns between a female trait and offspring traits that could be used as general theories in the study of maternal effects. Studies on fishes are underrepresented in the literature of sexual selection and parental care due in the main to the difficulty in making observations and tagging individuals, and the limited background demographic and biological detail available on many species (Amundsen, 2003). These same limitations apply to most aspects of the study of maternal effects. To date, the common theories in the study of maternal effects, such as bigger females produce bigger or better offspring, are not observed universally in fishes. There are enough exceptions to this particular generalisation to suggest that it is not a unifying theory of maternal effects. Given the numerous potential sources of maternal effects, from female traits and environmental conditions, and the variety of possible expressions of a maternal effect in an offspring, it is not possible to measure these effects in every species of fish under exploitation. Therefore I recommend future efforts focus on detecting common trends in maternal effects on offspring traits, examining female traits or environmental conditions that may act synergistically, and using traits that co-vary, such as size and age, to better predict a whole fishery response to maternal effects. To achieve the latter, it would be necessary to review size versus age and their inherent covariance and provide the relative weighting of each across a number of species. When female trait and environmental variables have been considered in a multivariate framework there has frequently been a synergistic effect identified. The advancement of the study of maternal effects in fish populations would be aided by moving away from single variable assessments and correlations, and focussing more attention on the interactions on variables as they operate in a complex environment. In the introduction I mused that for maternal effects to be usefully incorporated into S/R relationships there must be a strong and consistent or at least predictable relationship between offspring quality and attributes of the parent within a species, and this relationship would be more effective if it existed between species or higher level taxonomic or life history grouping. The field of study is so new to marine fishes that few reliably predictable relationships have emerged. Future efforts might explore the trends in maternal effects across groupings of species based on patterns of growth, mode of reproduction and longevity rather than individual species in order to identify patterns of maternal effects in fish populations.

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ACKNOWLEDGEMENTS BSG was supported by a National Academies NRC fellowship at the NOAA National Marine Fisheries Service Howard Marine Laboratory, Highlands, New Jersey. Many thanks to R.C. Chambers who was instrumental in the conception and planning of this manuscript, and contributed significantly to Table 1.6. I also thank R.C. Chambers, David Sims and an anomynous reviewer for editorial comments.

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Sexual Segregation in Marine Fish, Reptiles, Birds and Mammals: Behaviour Patterns, Mechanisms and Conservation Implications Victoria J. Wearmouth* and David W. Sims*,† Contents 1. Introduction 2. Types of Sexual Segregation 2.1. Habitat versus social segregation 2.2. Detecting types of sexual segregation 2.3. Measurement problems for marine species 3. Sexual Segregation in Marine Vertebrates 3.1. Sexual segregation in marine mammals 3.2. Sexual segregation in marine birds 3.3. Sexual segregation in marine reptiles 3.4. Sexual segregation in marine fish 4. Mechanisms Underlying Sexual Segregation: Hypotheses 4.1. Predation-risk hypothesis (reproductive strategy hypothesis) 4.2. Forage selection hypothesis (sexual dimorphism—body-size hypothesis) incorporating the scramble competition and incisor breadth hypotheses 4.3. Activity budget hypothesis (body-size dimorphism hypothesis) 4.4. Thermal niche–fecundity hypothesis 4.5. Social factors hypothesis (social preference and social avoidance hypotheses) 5. Sexual Segregation in Catshark: A Case Study 6. Conservation Implications of Sexual Segregation 7. A Synthesis and Future Directions for Research Acknowledgements References * {

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Advances in Marine Biology, Volume 54 ISSN 0065-2881, DOI: 10.1016/S0065-2881(08)00002-3

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Abstract Sexual segregation occurs when members of a species separate such that the sexes live apart, either singly or in single-sex groups. It can be broadly categorised into two types: habitat segregation and social segregation. Sexual segregation is a behavioural phenomenon that is widespread in the animal kingdom yet the underlying causes remain poorly understood. Sexual segregation has been widely studied among terrestrial mammals such as ungulates, but it has been less well documented in the marine environment. This chapter clarifies terms and concepts which have emerged from the investigation of sexual segregation in terrestrial ecology and examines how a similar methodological approach may be complicated by differences of marine species. Here we discuss the behavioural patterns of sexual segregation among marine fish, reptile, bird and mammal species. Five hypotheses have been forwarded to account for sexual segregation, largely emerging from investigation of sexual segregation in terrestrial ungulates: the predation risk, forage selection, activity budget, thermal niche–fecundity and social factors hypotheses. These mechanisms are reviewed following careful assessment of their applicability to marine vertebrate species and case studies of marine vertebrates which support each mechanism recounted. Rigorous testing of all hypotheses is lacking from both the terrestrial and marine vertebrate literature and those analyses which have been attempted are often confounded by factors such as sexual body-size dimorphism. In this context, we indicate the value of studying model species which are monomorphic with respect to body size and discuss possible underlying causes for sexual segregation in this species. We also discuss why it is important to understand sexual segregation, for example, by illustrating how differential exploitation of the sexes by humans can lead to population decline.

1. Introduction There is a burgeoning literature documenting sex differences in animal behaviour. These differences range from divergent foraging strategies (e.g., feeding rates) to gross differences in the geographical distribution of the sexes. Investigating sex differences in habitat use is of particular relevance, because understanding the mechanisms governing how and why the sexes differentially distribute themselves in nature is important in attempts to predict population processes and dynamics. It also has resonance in the successful management and conservation of animal populations since spatial dynamics of the sexes influences overlap with area-focused human activities such as hunting and fishing.

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Sexual segregation can be defined as the separation of members of a species such that the sexes live apart, either singly or in single-sex groups. Sexual segregation is widespread in the animal kingdom. This is particularly so for the class Mammalia; it is almost ubiquitous among ungulate populations (for reviews, see Bowyer, 2004; Main et al., 1996; Ruckstuhl and Neuhaus, 2002) and it also occurs in cetaceans (Brown et al., 1995; Martin and da Silva, 2004), carnivores (Beck et al., 2003c; Wielgus and Bunnell, 2000), bats (Altringham and Senior, 2005), elephants (Stokke and du Toit, 2002), marsupial mammals (Broome, 2001) and primates (Pellegrini, 2004). However, sexual segregation is a behavioural strategy which is not confined to mammals. It is seen in reptiles (Shine et al., 2000; Wikelski and Trillmich, 1994), fish (Croft et al., 2004; Robichaud and Rose, 2003; Sims et al., 2001) and birds (Gonzalez-Solis, 2004; Gonzalez-Solis et al., 2000; Lewis et al., 2002). Yet, despite the widespread nature of sexual segregation, the underlying causes remain poorly understood. Investigative studies to date have tended to focus on sexual segregation in terrestrial vertebrates and on ungulates in particular. These species typically exhibit pronounced sexual dimorphism with respect to adult body size. Sex differences in body size are likely to confer significant sex differences in attributes such as predation risk, nutritional requirements and activity budgets, all of which are likely to influence spatial and temporal habitat use of the sexes. This is important to consider because it may be equally likely that individuals from each sex would segregate, regardless of their sex, simply due to differences in their body size. Therefore, sexually size-dimorphic species may not be the most appropriate behavioural models for examining differences due to sex per se since body-size differences represent a principal confounding effect. Within the marine realm, no systematic investigations have been conducted into the underlying causes of sexual segregation in any vertebrate to date, but there have been several descriptive studies and potential causes have been proposed. Hence, there is a need to bring together the literature on marine vertebrates generally with respect to patterns of sexual segregation, and relate these findings to observations made for terrestrial, aquatic and aerial species. This chapter, therefore, reviews the evidence for and assesses the implications of sexual segregation in marine vertebrates (fish, reptiles, birds, mammals). The aims of this chapter are to clarify terms and concepts, to appraise current hypotheses that have emerged from the study of a diverse range of species and to assess their applicability to marine species in particular. A principal motivation here is to identify the similarities and differences in sexual segregation behaviour and its causes between terrestrial and marine vertebrates; are general features apparent or does a watery world confer key differences not present elsewhere?

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2. Types of Sexual Segregation 2.1. Habitat versus social segregation Sexual segregation can be broadly categorised into two types: habitat segregation and social segregation. Habitat segregation occurs where the sexes differ in their use of the physical environment, whilst social segregation is the tendency for a species to form single-sex groups. However, socially segregating species may also exhibit sex-specific habitat use (social and habitat segregation). In addition, habitat- and socially segregating species may or may not separate spatially (Fig. 2.1). For example, in the marine flatfish known as dab, Limanda limanda, both sexes are captured by trawl on the same grounds (i.e., no spatial segregation), but social segregation is evident in the foraging behaviour of the sexes: The proportion of females with full stomachs is higher in the morning than in the afternoon, whereas the reverse appears the case for males (Temming and Hammer, 1994). In contrast, habitat segregation in male and female northern elephant seals, Mirounga angustirostris, leads to spatial separation of the sexes: Males forage on the continental margin and generally feed on benthic prey, whereas females range more widely over deep water and feed on vertically migrating pelagic prey (Le Boeuf et al., 2000). Sexual segregation is a behavioural pattern that is likely to be influenced by both social and ecological factors, such as the temporal pattern of mating opportunities, population density and the availability of resources. Within terrestrial mammals such as ungulates, sexual segregation is generally seen only outside the breeding season (when the sexes aggregate to mate) and therefore should be more pronounced in species with a discrete breeding season. However, this general observation does not appear to be the case for species in the marine environment. For example, sexual segregation is only seen in breeding populations of green turtles (G. Hays, personal communication). High population densities generally facilitate group fission, as the availability of suitable group mates should be sufficient for new group formation. However, in socially sexually segregating species which cooccur within the same habitat, high population densities may make sexual segregation difficult to identify as inter-group distances will be reduced. The effect of resource abundance on animal distributions will depend on whether the sexes exploit similar or diverging habitats, and, equally, whether habitats are homo- or heterogeneous. The underlying causes of social segregation are likely to differ from those of habitat segregation. Habitat segregation results from sex differences in a species’ responses to variability in factors such as resource availability, predation and environmental conditions, whereas social segregation results from inter-sexual asynchrony or aversion, or intra-sexual affinity. It is therefore

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A

B

No segregation

Social segregation

C

D

Habitat segregation

Social and habitat segregation

E

F

Social and spatial segregation

Habitat and spatial segregation

G

Social, habitat and spatial segregation

Figure 2.1 The distribution of 12 social groups (dashed circles) across habitats (grey and white) under different sexual segregation scenarios. The diagrams depict: (A) No segregation: the sexes associate at random and are equally distributed between habitats; (B) Social segregation: unisexual groups are equally distributed between habitats; (C) Habitat segregation: the majority of groups are mixed sex but most males utilise the grey habitat (n ¼ 8), whereas females prefer the white habitat; (D) Social and habitat segregation: unisexual male groups utilise the grey habitat, unisexual female groups utilise the white habitat; (E) Social and spatial segregation: unisexual groups are equally distributed between habitats but occupy different areas; (F) Habitat and spatial segregation: the sexes associate at random but males prefer the grey habitat which is spatially separated from the white habitat preferred by females; (G) Social, habitat and spatial segregation: unisexual male groups utilise the grey habitat which is spatially separated from the habitat utilised by female groups (the white habitat).

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useful to try and identify the type of segregation which occurs as it may help determine the underlying causes of the behaviours. The two types of sexual segregation are, however, not mutually exclusive. If a species exhibits sexspecific preferences over spatially separated habitats, the sexes may well live in different social groups (Conradt, 2005). Similarly, social segregation may also result in habitat segregation (Bon et al., 2001; Conradt, 1999). Thus, identifying the proximate cause of sexual segregation is not straightforward.

2.2. Detecting types of sexual segregation In an attempt to overcome the apparent dilemma of what causes sexual segregation, Conradt (1998b) developed the segregation coefficient. Unlike measures of ecological overlap (e.g., the percentage of animals in unisex versus mixed-sex groups), the segregation coefficient is not stochastically dependent on animal density, group sizes and sex ratio (Conradt, 2005). By estimating the product of the proportion of males which segregate and the proportion of females which segregate, the segregation coefficient (SC) measures the degree of segregation in an animal population (see Box 2.1). If males and females are found in completely separate groups (complete segregation), SC takes a value of 1. If there is no segregation (males and females meet randomly in groups), SC will be 0. Values of SC between 0 and 1 reflect partial segregation (where only a proportion of animals in the population segregate). The segregation coefficient can be used to quantify the degree of social, habitat or spatial segregation exhibited by a population, thus enabling identification of the type(s) of segregation exhibited. For example, if the sexes use spatially separated habitats, but socialise randomly within habitats (i.e., social segregation is a by-product of habitat segregation) then SCsocial ¼ SChabitat. On the other hand, if animal classes segregate socially within habitats, additionally to segregation between habitats, then SCsocial > SChabitat (Conradt, 2005). In addition, the segregation coefficient can be used to quantitatively compare the degree of segregation within and between species and populations. The segregation coefficient has been successful in some cases for identifying degrees of sexual segregation in relation to various factors in social animals within particular taxa (i.e., ungulates). However, this measure can only be used effectively for group-living animals. This appears to overlook the need to identify sexual segregation in solitary animals. The issue is further complicated because it has been stated that ‘in the case of solitary animals, the concept of inter-sexual social segregation does not apply’ (Conradt, 1998b), ‘since a single animal is not social’ (Neuhaus and Ruckstuhl, 2004a). The implication is that solitary animals are not likely to exhibit social segregation, even if they occur in the same habitat. Nevertheless, where solitary animals actively avoid members of the opposite sex, as has been suggested in the river

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Box 2.1 The segregation coefficient (after Conradt, 1998b)

Conradt’s segregation coefficient (SC) determines the degree of sexual segregation in animal populations using the following formula:

vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi u k u X þY 1 X xi yi  SC ¼ t1  XY x þ yi  1 i¼1 i

ð1Þ

where for SCsocial: xi is the number of males in the ith group; yi is the number of females in the ith group; k is the number of groups with at least two animals (i.e., solitary animals are excluded); X is the total number of males in all k groups; Y is the total number of females in all k groups. SChabitat: xi is the number of males in the ith habitat type; yi is the number of females in the ith habitat type; k is the number of habitat types which are used by at least two animals; X is the total number of males in all k habitat types; Y is the total number of females in all k habitat types (the measure is sensitive to the classification of habitat types). SCspatial: xi is the number of males in the ith grid square; yi is the number of females in the ith grid square; k is the number of grid squares which are used by at least two animals; X is the total number of males in all k grid squares; Y is the total number of females in all k grid squares (the measure is sensitive to grid square size, i.e., spatial scale). It is important that sample sizes are large. The resulting segregation coefficient or degree of segregation ranges from 0 (no segregation) to 1 (all males and females segregate). dolphin or boto (Inia geoffrensis: Martin and da Silva, 2004), they appear to exhibit social segregation. Therefore, Conradt’s indices of sexual segregation do not apply to numerous species that are principally solitary in their behaviour.

2.3. Measurement problems for marine species Determining the underlying causes of sexual segregation in the marine environment presents a particular challenge. This is mainly due to the fact that studying marine vertebrates in their natural surroundings is complicated by the fact that they live in a relatively inaccessible and concealing environment (Sundstrom et al., 2001). Additionally, unlike most terrestrial ungulates, marine vertebrates live in a strongly three-dimensional environment and, whilst it may be relatively simple to observe the behaviour of shallow

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reef-dwelling species which may also be held in captivity, other species may move or migrate both horizontally and vertically on a regular basis and sometimes across large spatial scales. In such circumstances, it is extremely difficult to determine which individuals constitute a population. In addition, there is often a lack of information on the sex of the individual, which may be attributable to a general difficulty in identifying the sex of individuals based on external morphology (Catry et al., 2005; Gilardi, 1992). Therefore, in an environment where it is difficult to determine which individuals constitute a group/population and where it is virtually impossible to distinguish the sex of all individuals, Conradt’s indices are largely inappropriate. Understanding the underlying causes of sexual segregation in marine vertebrates is further complicated by their foraging behaviour. Whereas terrestrial ungulates are herbivorous and foraging can be observed directly and food type and quantity can be determined (or at least estimated with some accuracy), many marine vertebrates are predatory and forage on mobile prey. This makes identification of foraging behaviour and forage type very difficult since to fully understand individual foraging behaviours one must first have some knowledge of the behaviour, abundance and availability of the prey species. Much of our current knowledge of marine vertebrate diet comes from the analysis of scats or the stomach contents of dead animals. However, dietary analyses using scats may underestimate foraging niche breadth as only hard parts (e.g., fish otoliths and bones, squid beaks) are identifiable (Pierce and Boyle, 1991). In addition, these techniques only provide an indication of forage selection over a narrow time period (governed by digestion rates: Sims et al., 1996), and as moribund animals are unlikely to exhibit normal foraging behaviour, stomach content analyses may also be unrepresentative. Information on diet is needed over temporal scales relevant to life-history characteristics. With the application of new techniques, such as mammal-blubber fatty acid profiles which reflect prey consumed over a period of weeks or months (Beck et al., 2005), this information gap is being closed in some taxa. Pinnipeds, marine birds and marine reptiles, with few exceptions, breed on land. Consequently, much of our understanding of the behaviour of representatives from these three groups stems from observations made at or near breeding colonies. The development of remote telemetry systems for tracking movements of individuals and the environment they move through is now extending our understanding of pinniped, bird and reptile behaviour into the non-breeding seasons (Hays et al., 2004; RopertCoudert and Wilson, 2005). These remote monitoring techniques also provide insights into the habits of cetaceans and fish, which are wholly marine. In the case of fish, acoustic telemetry has been widely used to investigate habitat choice in marine species. Attaching an acoustic pinger to an individual fish enables its movements to be tracked in real-time.

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Initially, acoustic signals were tracked manually using a directional hydrophone (e.g., Carey and Scharold, 1990; Sims et al., 2001), a labour-intensive and expensive technique that has yielded only short-term tracks when used continuously (from days to up to 2 weeks). More recently, remote monitoring of acoustically tracked fish has been facilitated by the development of radio-acoustic positioning systems (a triangle of three moored hydrophones which radio-link to a base station on land where the location of the fish is calculated and displayed in real-time) (for a review, see Klimley et al., 2001). In addition, using acoustic pingers with sensors, where depth or ambient temperature is encoded within the acoustic pulse sequence, has enabled reconstruction of an animal’s three-dimensional trajectory and provided information on the abiotic conditions at an animal’s location. Acoustic telemetry techniques are spatially constrained by the distance sound energy travels in seawater and this distance can be dramatically reduced if the environment is acoustically noisy (e.g., strongly tidal areas) and/or bathymetry is not uniform in the local area. More recently, satellitelinked archival transmitters incorporating a data-logging (termed ‘archival’) tag with a satellite transmitter for relaying stored summary data have been used widely to track large marine fish such as sharks (Sims et al., 2003) and tuna (Block et al., 2001). Similarly, satellite transmitters have been attached directly to the dorsal fin of sharks to enable direct tracking of movements. Here, transmissions to over-passing satellites are made when fish surface and the transmitter becomes dry, which is necessary since ultra-high frequency radiowaves will not penetrate seawater (Weng et al., 2005). Archival tags record data from onboard sensors that allow, for example, post hoc track reconstruction and detailed diving behaviour analysis (Shepard et al., 2006). These tags can collect data such as light level, direction heading and sea temperature which can be used determine an animal’s geographical location using light-level geolocation (see Sims et al., 2006b) or dead reckoning (see Wilson et al., 2008), record environmental conditions at the animal location (such as temperature, salinity and light) and monitor energy acquisition that is, feeding (using stomach/oesophageal temperature or inter-mandibular angle sensors) and expenditure (motion sensors and heartbeat frequency). Indeed, archival tags have been developed to record almost every aspect of an individuals daily life, including gut evacuation rates via a cloacal opening/closing sensor (for a review, see Wilson, 2004). Furthermore, early acoustic pingers, satellite transmitters and archival tags were cumbersome, but increases in memory have been coupled with decreases in component sizes and power consumption, and therefore also unit size. Thus, the periods over which animals can be monitored have increased from hours to months whilst the sampling frequency has decreased from minutes or seconds to fractions of a second (Wilson, 2004). Despite this, the sophistication of electronic tags available for tracking or estimating geographic location and other activities, deployment times have so far been

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too short for tags capable of recording variables of use in assessing the potential causes of sexual segregation, for example, prey type (Wilson et al., 2002). This then represents a key deficiency in studies attempted so far: A detailed picture of movements and behaviour is singularly lacking for the majority of marine species. Moreover, despite the utilisation of state-ofthe-art technology, one vital piece of information is frequently lacking from many investigative studies: the sex of the animal. This may be due to the difficulty in distinguishing (by non-invasive means) the sexes in many species (Magurran and Garcia, 2000). Nonetheless, whilst detailed behavioural information is not always available, sexual segregation has been documented in many species of marine vertebrate to date. Here we review the evidence for and patterns of sexual segregation in marine mammals, birds, reptiles and fish.

3. Sexual Segregation in Marine Vertebrates 3.1. Sexual segregation in marine mammals Like their terrestrial counterparts, sexual segregation is widespread in mammals that inhabit marine environments. There are five groups of marine mammals: sireneans (manatees and dugongs); cetaceans (whales, dolphins and porpoises); and, within the Order Carnivora, there are the pinnipeds (seals, sea lions and walruses), polar bear (Family Ursidae) and the European and South American sea otters (Family Mustelidae). This section of this chapter will examine sexual segregation in cetaceans and pinnipeds, the best studied and most speciose marine mammal groups. 3.1.1. Sexual segregation in Cetacea The order Cetacea comprises 90 species and all except 5 (the freshwater dolphins) are marine. Many cetacean species socially segregate into same age or sex groups. In 1968, Gaskin described the composition of schools of sperm whale, Physeter macrocephalus, the cetacean species that shows the greatest body-size dimorphism between the sexes (females 9.5–11 m, males 13–18 m: Whitehead and Weilgart, 2000). Six major social categories were identified for P. macrocephalus: solitary males, male pairs, schools of bachelor males, mixed-sex schools (immatures), harems (predominantly female with 1–4 large males) and nursery groups (females and their dependent offspring) (Gaskin, 1968). Subsequent studies have enhanced our understanding of the composition of these social groupings. Female sperm whales appear to maintain long-term social bonds, associating in matrilineally related units (Lyrholm et al., 1999; Whitehead et al., 1991). In contrast, males disperse from natal family units into bachelor schools (Whitehead and Weilgart, 2000). With increasing age and size, male sociality decreases

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(Lyrholm et al., 1999) and male pairs are thought to represent the final stage in the break-up of bachelor male schools into solitary animals (Gaskin, 1968). However, strong and persistent social bonds among females of a species do not form the basis for all cetacean social groupings. Female and immature northern bottlenose whales (Hyperoodon ampullatus) form only a loose network of associations and show no preferential associations or long-term bonds, whereas mature and subadult males form stronger associations with individuals in their own age and sex class, with associations between some males lasting for several years (Gowans et al., 2001, 2008). In contrast, some species do not appear to segregate socially: Both male and female resident killer whales (Orcinus orca) remain in their natal group for life (Connor, 2002; Fig. 2.2). Spatial segregation of the sexes is common in cetacean societies. Indeed, whilst male and female killer whales do not segregate socially, there is evidence to suggest that, within these natal groups, the sexes may segregate by water depth with larger males diving deeper or avoiding shallow water (Michaud, 2005). Similarly, male sperm whales are generally found in deep water, whereas females are found only rarely in waters more than 1000 m deep (Whitehead and Weilgart, 2000). Humpback whales exhibit both social and spatial sexual segregation: Maternal humpback whales (Megaptera novaeangliae) segregate from all other humpback whale groups, preferentially occupying shallower, nearshore waters (Clapham, 2000; Smultea, 1994). Similar patterns are also seen in the river dolphin or boto (Inia geoffrensis) with females and their calves moving away from rivers and into floodplain habitat as seasonal water levels increase, whereas males remain in rivers (Martin and da Silva, 2004). As well as sex differences in ‘local’ distribution, large-scale (e.g., latitudinal) spatial separation of the sexes is also seen.

Figure 2.2 Resident killer whales (Orcinus orca) do not segregate socially: Both males and females remain in their natal groups for life. Photo courtesy of J. Eveson (Ardnamurchan Charters), with permission.

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Female and juvenile groups of sperm whale are mainly found at low latitudes, remaining close to tropical breeding grounds throughout the year (Gaskin, 1973; Lyrholm et al., 1999; Whitehead and Weilgart, 2000). Adolescent males disperse from these low-latitude natal family units, initially into bachelor schools, but show decreased sociality as they mature and move to higher latitudes (Whitehead and Weilgart, 2000). In addition, as breeding males (25 years old) must migrate from high-latitude feeding grounds to tropical breeding grounds, sex differences are evident in the annual home ranges of mature individuals (Whitehead and Weilgart, 2000). Sex differences in home range size are also seen in bottlenose dolphins (Tursiops truncatus). In the Gulf of Mexico, females were found to utilise small core areas which they shared with other females, whilst males frequently ranged to either end of and even beyond the 40-km long study area (Wells et al., 1987, 1996, cited in Connor et al., 2000). Sex differences are also seen in cetacean migration patterns. The humpback whale breeds in low-latitudes in winter, then migrates to high-latitude polar or sub-polar waters to feed in summer. Commercial whaling catches of humpback whales near winter-breeding colonies were highly skewed towards males (Brown et al., 1995), yet sex ratio at birth is 1:1 (Clapham, 2000). From this, Brown et al. (1995) inferred that around 50% of Antarctic females remain in feeding areas throughout winter. There is even evidence of sexual segregation within migrating individuals, with males appearing on breeding grounds earlier and having longer residence times than females (Stevick et al., 2003). Finally, sex differences in foraging patterns have been documented. Stable isotope analysis has revealed that the trophic position of male beluga whales in the Estuary and Gulf of St. Lawrence, Canada, is higher than that of females: Males were more 15N- and 13C-enriched than females (Lesage et al., 2001). Similarly, stomach content analysis revealed sex differences in the diet of common dolphins (Delphinus delphis) captured in Natal, South Africa. During the annual migration or ‘run’ of sardine (young South African pilchards, Sardinops ocellatus), male dolphins tended to concentrate on this single prey species, whereas the diet of females was more diverse: Mature females were the only individuals which fed on flying fish, and consumed larger, heavier prey with a greater reliance on squid (Young and Cockcroft, 1994). However, differences were also seen between females. Lactating females consumed more squid than pregnant females and a greater proportion of larger, faster-swimming fish (mackerel, Scomber japonicus; and elf, Pomatomus saltatrix) (Young and Cockcroft, 1994). Similarly, dietary differences occur between pregnant or non-lactating and lactating female harbour porpoise (Phocoena phocoena) and spotted dolphin (Stenella attenuata), with lactating females ingesting more fish in both cases (Bernard and Hohn, 1989; Recchia and Read, 1989). Lactating harbour porpoises also had a significantly higher total caloric intake than non-lactating females or mature males (Recchia and Read, 1989). In addition, there was evidence of

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differences in stomach fullness between pregnant and lactating spotted dolphins (Bernard and Hohn, 1989). These latter studies suggest that factors such as an individual’s reproductive status may have more influence on dietary niche specialisation than sex. 3.1.2. Sexual segregation in pinnipeds Pinnipeds are marine mammals of the order Carnivora, comprising the families Odobenidae (walruses), Otariidae (eared seals) and Phocidae (true seals). Spatial separation of the sexes has been inferred from sightings of South American sea lions (Otaria flavescens) from fishing vessels which suggest that males move further offshore than females (Alonso et al., 2000). The occurrence of sex differences in habitat use in this species has been supported by satellite-tracking studies revealing that females remain on the continental shelf, whereas males venture to the shelf break (Campagna et al., 2001). Deployments of data-logging time-depth recorders and/or satellite tracking has revealed similar patterns in grey seals (Halichoerus grypus: Breed et al., 2006) and New Zealand fur seals (Arctocephalus forsteri: Page et al., 2005). In both cases, females remained on the continental shelf, whereas males foraged along or beyond the shelf break. These sex differences in habitat use may be related to the breeding system: Offspring provisioning may constrain female habitat use. Indeed, foraging trip length in lactating New Zealand fur seals appears to be dictated by the fasting ability of the pups, as central place foraging females exhibit shorter foraging trip durations than unconstrained males (5 d and 9 d, respectively) (Page et al., 2005). Similarly, adult female Galapagos sea lions (Zalophus wollebaeki) with offspring had smaller home range sizes than nonbreeding females (Wolf and Trillmich, 2007). By remaining on the continental shelf, female South American sea lions remained close to rookeries (Campagna et al., 2001) whilst female Antarctic fur seals (A. gazella) remain close to their South Georgia breeding colony during the post-breeding period when males head south towards the South Orkney Islands (Boyd et al., 1998). Such sex differences in foraging trip locations may result in sex differences in dietary niche. For example, pre-breeding male South American sea lions travelled about twice as far east and into deeper waters than lactating females. Stomach contents analyses were consistent with these results, suggesting that females are coastal, benthic feeders whereas males are pelagic (Campagna et al., 2001). However, dietary niche separation may not be solely attributable to geographic separation of foraging locations as, in some species, the sexes forage in separate regions of the water column. Male Antarctic fur seals dive deeper than lactating females and exploit prey at the bottom of the surface mixed layer of the ocean, whereas females forage within this zone (Boyd et al., 1998). Similarly, male New Zealand fur seals dive deeper and for longer than lactating females (Page et al., 2005).

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Not all cases of dietary niche specialisation, however, are related to offspring provisioning: Sex differences occur among non-breeding individuals and in breeding individuals outside the breeding season. These differences appear to start early in life: Sex differences are seen in body composition of suckling Australian fur seal (Arctocephalus pusillus doriferus) pups, with females having larger body lipid stores than males (Arnould and Hindell, 2002). Furthermore, juvenile female southern elephant seals spend more time at sea than juvenile males (Field et al., 2005) and post-weaning Antarctic fur seal males forage significantly further away from land and from their natal colony (Warren et al., 2006). Among mature individuals of a species, the grey seal, Halichoerus grypus, has been particularly well studied outside of the breeding season. Austin et al. (2004) found that males were more likely to display directed, longdistance travel, only returning to the Sable Island breeding colony just prior to the breeding season, whereas females were more likely to be resident, remaining close to Sable Island and making short return trips to and from a single place. H. grypus also exhibits sex differences in foraging behaviour. Whilst males dive deeper during foraging bouts, females spend more time diving and less time hauled-out between trips, undertaking longer bouts with a greater proportion of each bout spent at depth and with more dives per bout (Beck et al., 2003b,c). However, it is likely that these sex differences in dive bout characteristics vary seasonally. Stomach temperature telemetry has revealed that, just prior to the breeding season, the number of feeding events per day was greater in males than females (by 2.2 times), as was the time associated with feeding per day (56.6 vs 43.9 min, respectively) whilst the length of time between meals was significantly less in males than females (541.4 vs 1092.6 min, respectively) (Austin et al., 2006). These results support observations of significant sex differences in the seasonal patterns of total body energy in adult grey seals. Whilst females exhibit greater energy content (after accounting for body mass) throughout the year, with them regaining body energy quickly following the breeding season, males, in contrast, only gained energy just prior to the breeding season (Beck et al., 2003a). Dietary analysis also suggests significant dietary segregation between male and female grey seals, with mature males eating larger and older prey than females and younger seals (<4 year) of both sexes (Hauksson and Bogason, 1997). Stable isotope analysis indicates that males feed more heavily on benthic prey, whereas adult females appear to feed more on pelagic prey (Tucker et al., 2007). Similar analysis has revealed sex differentiation in diet in hooded, Cystophora cristata, and harp seals, Phoca groenlandica, where males are more 15N enriched than females and the difference between the sexes increases with age (Lesage et al., 2001). Pronounced sex differences in foraging location and pattern are a characteristic of northern elephant seal distributions. Whereas males show directed movement to focal foraging areas along the continental margin,

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travelling up to 21,000 km in 250 days at sea; females range across a wider area of the northeast Pacific Ocean but cover only about 18,000 km over 300 days (Le Boeuf et al., 2000; Stewart and Delong, 1995). On reaching the continental margin, males exhibit flat-bottomed dives and feed on benthic prey (Le Boeuf et al., 2000). In contrast, females did not proceed directly to a particular site, but searched for prey whilst in transit and apparently pursued prey when they encountered it, as inferred from jagged bottom dives which tracked the sound scattering layer presumably comprising patchy, vertically migrating, pelagic prey in the water column (Le Boeuf et al., 2000). California sea lions also exhibit geographical segregation during the non-breeding season. Only adult and subadult males are encountered on southern Vancouver Island as females do not venture north of central California (Morejohn, 1968; Orr and Poulter, 1965, cited in Bigg, 1973). Similarly, female harbour seal (Phoca vitulina) foraging trip duration and range are significantly shorter than that of males (Thompson et al., 1998). Sex differences are also seen in the terrestrial habitat use of pinnipeds. The sexes are often segregated during the breeding season, for example, some common seal, Phoca vitulina, haul-out groups are male dominated whereas others comprise mostly females with pups (Thompson, 1989). Similarly, ringed seals (Pusa hispida) in their fast-ice breeding habitat segregate by age and by sex. Adult females occupy the inner, most stable ice areas, subadults predominate in the outer parts of the fast-ice, where the ice conditions are more unstable, and adult males are scattered across these two areas (Krafft et al., 2007). By contrast, it is male Galapagos sea lions that are found further inshore. In this species, habitat use is influenced by the costs of locomotion and thermoregulation, thus, flat, shady habitats directly adjacent to the sea are preferred over inland habitats which offer only shade. Mature females are generally found in the optimal habitat. Only a small number of large territorial males manage to establish semiaquatic territories, a pattern of sexual segregation which, whilst more pronounced during the reproductive period, still occurs during the non-reproductive period (Wolf et al., 2005). As one might expect, sex differences are also seen in terrestrial habitat use during the pupping season, when female common seals are seen to haul out more frequently than males (Thompson et al., 1997). However, perhaps less expected was that sex differences in the distribution of common seals were evident during the annual moult. This event occurs shortly after weaning and, whereas males haul out every day at the beginning of moult (to increase skin temperature and therefore to speed up the moult), females spend more time at sea (Thompson et al., 1989). To summarise, sexual segregation is widespread in mammals that inhabit marine environments. In many cetacean societies, social groups are often based around bonds between females, with males breaking off from maternal groups at adolescence to form male coalitions or to remain solitary. However, male-biased social groupings also occur and in some species, the

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males remain in the natal group for life. In marine mammals in general, spatial sexual segregation is commonplace. At the local scale, sex differences are seen in attributes such as depth use and distance from the shore. However, spatial segregation also occurs on latitudinal scales, leading to gross differences in the home ranges of the sexes and possibly even sexspecific migrations. These spatial separations of the sexes appear to be largely attributable to offspring provisioning, with females remaining either close to pupping areas or to environments where offspring survival is enhanced (i.e., away from predators or strong currents). Sex differences are also seen in foraging behaviour. As previously mentioned, the sexes may forage in different areas and at different depths, but sex differences are also seen in dive duration and prey species consumed. Reproductive status may be the proximate or ultimate cause of these differences due to the constraints of offspring provisioning on foraging range and the disparity in the time needed for each sex to prepare to the following mating season. However, as sex differences are also seen in the behaviour of immatures, reproductive status cannot explain sexual segregation in all species.

3.2. Sexual segregation in marine birds Despite a general wealth of information on the habits of terrestrial birds, relatively little is known about the behaviour of marine birds. The scarcity of information on sex differences in the behaviour of marine birds may also be partly attributable to a general difficulty in identifying the sex of individuals based on external morphology (Catry et al., 2005; Gilardi, 1992). Indeed, most information which exists on sexual segregation in seabirds concerns the wandering albatross (Diomedea exulans) and the northern giant petrel (Macronectes halli), two species with particularly marked sexual size dimorphism (Gonzalez-Solis, 2004; Xavier and Croxall, 2005). This section of this chapter starts by discussing sexual segregation in wandering albatross and the northern giant petrel, and then compares and contrasts the behavioural patterns observed in these two species with those patterns documented in several other species of seabird. The wandering albatross exhibits sex differences in the spatial distribution of foraging locations. By satellite-tracking foraging birds commuting to and from breeding colonies, it has been demonstrated that females, the smaller sex, frequently commute to the shelf edge and feed in oceanic waters, whereas males spend more time on the shelf or shelf slope (Weimerskirch et al., 1997; Xavier et al., 2004). Female wandering albatross make longer foraging trips, travel greater distances and forage further from the colony (Xavier and Croxall, 2005). Thus, it seems the foraging effort of females far exceeds that of males (Salamolard and Weimerskirch, 1993). Nonetheless, males apparently forage more efficiently than females (Weimerskirch et al., 1997). As both sexes feed on the same prey types (squid and other

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cephalopods) (Xavier and Croxall, 2005), these results suggest that resource quality differs between the foraging locations of the sexes: It is possible that the habitats exploited by males are more profitable than those used by females. Nevertheless, a more significant relationship between trip duration and mass gain for females suggests that, whilst the female foraging areas may provide lower energy yield, they were perhaps more predictable and less patchy than male foraging areas (Weimerskirch, 1995). Male and female northern giant petrels also exploit spatially separated foraging grounds and, like wandering albatross, differential habitat exploitation leads to fundamental differences in distance covered, spatial pattern and predictability of resources exploited, imposing different foraging strategies on each sex (Gonzalez-Solis and Croxall, 2005). However, differential habitat exploitation in northern giant petrel has resulted in sex differences in diet. Whilst scavenging on coastal penguin and seal carcasses is the preferred foraging strategy of both sexes, they also consume burrowing petrels, fish and cephalopods (Gonzalez-Solis et al., 2000; Hunter and Brooke, 1992). Satellite tracking and direct observation of breeding birds has revealed that males primarily forage coastally, scavenging carrion on beaches, but females have a more pelagic distribution and consume larger proportions of fish and cephalopods (Gonzalez-Solis, 2004; Gonzalez-Solis and Croxall, 2005; Gonzalez-Solis et al., 2000, 2002; Hunter and Brooke, 1992). As with wandering albatross, whilst female foraging effort (flight speed, distance covered, duration of foraging trips) is greater, foraging efficiency (proportionate daily mass gain whilst foraging) is significantly greater for males (Gonzalez-Solis et al., 2000). Like the northern giant petrel, male southern giant petrels, Macronectes giganteus, also forage closer to the coast than females (Gonzalez-Solis and Croxall, 2005). However, separation in diet is less marked than in the northern giant petrel (Hunter and Brooke, 1992), its sister species which is more sexually size dimorphic. Spatial separation of the sexes also occurs in Buller’s albatrosses (Diomedea b. bulleri) and in Magellanic (Spheniscus magellanicus) and Ade´lie penguins (Pygoscelis adeliae). Satellite tracking revealed that, whilst distances covered during foraging trips are similar between male and female Buller’s albatrosses, females foraged further from breeding colonies and in different sectors to males (Stahl and Sagar, 2000). Stable isotope analysis of Magellanic penguin males revealed that they consume fish and squid, foraging further inshore and taking significantly more anchovies than other prey species (Forero et al., 2002). Female Ade´lie penguins also ranged greater distances than males, undertaking longer foraging trips and, like northern giant petrels and magellanic penguins, exhibited sex differences in diet: Females consumed larger quantities of krill, whereas males fed more extensively on fish (Clarke et al., 1998). However, Volkman et al. (1980) attributed this heterogeneity in diet to a highly synchronous breeding cycle

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(the male takes the first 2-week incubation shift) and short-term differences in food availability rather than differential habitat exploitation. Despite the aforementioned studies, it is not always male seabirds that stay closer to the breeding colony. Male brown boobies (Sula leucogaster) undertake significantly longer foraging trips than females, a behavioural pattern which may be explained by reversed sexual size dimorphism in this species (the females are larger than the males) (Lewis et al., 2005). However, South Georgian shags, Phalacrocorax georgianus, exhibit malebiased size dimorphism and yet males spend more time flying, diving and on the sea than females, which spend more time at the nest (Wanless et al., 1995). Indeed, contrasting strategies are even seen in closely related species. Black-browed (Thalassarche melanophrys) and grey-headed (T. chrysostoma) albatross exhibit male-biased size dimorphism and in both species the sexes exploit largely mutually exclusive core foraging ranges. However, in blackbrowed albatross, the female travels further from breeding colonies than males, but in grey-headed albatross males travel further than females (Phillips et al., 2004). The pattern of sexual segregation may also vary geographically. For example, whilst Lewis et al. (2005) found male brown boobies foraged further off-shore than females in the Central Pacific Ocean, Gilardi (1992) found the opposite pattern in the eastern Pacific Ocean. Another form of spatial sexual separation seen in seabirds is segregation of foraging location by water depth, a pattern which is seen in king cormorants (Phalacrocorax albiventer), blue-eyed Crozet shags (Phalacrocorax melanogenis) and blue-footed boobies (Sula nebouxii). In both king cormorants and blue-eyed Crozet shags, where the body size of males exceeds that of females, the male dives deeper than females (Cook et al., 2007; Kato et al., 2000). Similarly, in the blue-footed booby, which exhibits reversed sexual size dimorphism, it is the larger female that dives significantly deeper than the male (Zavalaga et al., 2007). However, sexual size dimorphism cannot be the only explanation for sex-specific diving behaviour in seabirds as the monomorphic northern gannet, Morus bassanus, also exhibits sex differences in diving behaviour whilst foraging. Female gannets are more selective and undertake longer, deeper dives and spend more time on the surface (Lewis et al., 2002). Sex differences in dive depth do not always translate into sex differences in diet or provisioning as compensation in terms of increased dive frequency (female king cormorant: Kato et al., 2000) or increased time allocated to diving (female blue-eyed Crozet shags: Cook et al., 2007) may occur. However, there is evidence to suggest that the deeper diving, larger sex, whilst consuming the same prey species, consumes larger individuals (Cook et al., 2007; Zavalaga et al., 2007). Spatial sexual segregation may be temporal in some species. Blue-eyed shags (Phalacrocorax atriceps), South Georgian shags (P. georgianus), Crozet shags and king cormorants, all exhibit diurnal temporal separation of foraging with females foraging in the morning and males foraging in the

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afternoon (Bernstein and Maxson, 1984; Cook et al., 2007; Kato et al., 2000; Wanless et al., 1995). At the larger temporal scale, male wandering albatross, Diomedea exulans, arrives at the South Georgia breeding colony 2 weeks earlier than females (Tickell, 1986, cited in Xavier and Croxall, 2005). As exemplified by the above-mentioned studies, much of what is known about seabird sexual segregation is generally restricted to observations made during the breeding season. This is because seabirds must return to a breeding colony to nest. However, with advances in miniaturisation of data-logging and satellite transmitter technology, our knowledge of seabird life history is expanding beyond terrestrial/maritime observations made during breeding to the foraging ecology of non-breeding birds. In addition, the availability of small, long-life batteries in devices has enabled studies to extend well into the overwintering period. Evidence suggests that wandering albatross also segregate sexually between breeding attempts. Weimerskirch and Wilson (2000) demonstrated spatial separation of the sexes during the non-breeding period, with individuals restricting movements to preferred sectors to which they probably return year after year. Females tracked from the Crozet Islands in the southern Indian Ocean used tropical and subtropical waters south of Madagascar, whereas males occupied sub-Antarctic and Antarctic waters just north of the pack ice. In contrast, the activity and pelagic movements of northern giant petrels were more similar between the sexes outside breeding seasons, although there was evidence to suggest that the greater use of coastal habitats by males persists throughout the year (Xavier and Croxall, 2005). Sexual segregation of overwintering birds is also characteristic of wading species. For example, oystercatchers, Haemalopus ostralegus, exhibit sexual segregation in foraging niche as males chiefly prey upon near surface, mudflat species such as cockles and mussels whereas females consume more deep-living prey (Durell et al., 1993; Swennen et al., 1983). In contrast, overwintering western sandpiper, Calidris mauri, exhibits spatial segregation at a much coarser spatial scale: females tend to winter south of males (Mathot et al., 2007). In summary, spatial segregation of the sexes is widespread in marine birds. In breeding populations, the smaller sex will generally forage further offshore. Spatial separation of the foraging niche of the sexes may lead to sex differences in diet, whether in prey species or prey size. Sex differences in foraging efficiency may also result, although apparently at the cost of resource predictability. Sexual segregation of foraging niche appears largely attributable to sexual size dimorphism, with the smaller sex species foraging further offshore. Similarly, as is the case with marine mammals, the larger sex is generally able to forage at greater depths. However, there are exceptions. Sex differences are seen in the diving behaviour of monomorphic species and in some species the larger sex will undertake longer foraging

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excursions, opposite patterns are seen in closely related species and geographical variation also occurs. Therefore, sexual size dimorphism is unlikely to be the only explanation for segregation in marine birds.

3.3. Sexual segregation in marine reptiles The diversity of present-day marine reptiles is low, being limited to only three groups: sea snakes, marine turtles and the marine iguana. Yet, representatives of all three groups segregate sexually. All reptiles are air breathers and thus must periodically return to the water’s surface. Whilst this aids the study of these animals, it does not limit marine reptile distribution to coastal waters: Marine turtles migrate across oceans (Hays et al., 2004) and exhibit shifts in behaviour at the ocean-basin scale (Hays et al., 2006). Many marine reptiles must return to land to breed, offering an opportunity for the attachment of tracking devices. However, the need to return to land is not absolute. Whilst some species rely on the marine environment only for food (e.g., marine iguanas), the wholly marine Hydrophiinae (a subgroup of the sea snakes) spend their entire lives in the sea where they give birth to live young. Within marine reptile breeding populations, sex differences in habitat use appear widespread. For example, the turtle-headed sea snake, Emydocephalus annulatus, exhibits male–female differences in habitat occupancy. This species consumes the eggs of damselfish and blennies which nest in coral rubble substrates and the habitat use of juvenile and adult females, E. annulatus, which spend most of their time foraging, closely matches the distribution of the nests of these fish (Shine et al., 2003). However, breeding males do not feed and shift their behaviour towards mate searching: They actively court any adult female they encounter, swim more rapidly and are found across a broader range of habitat types (Shine et al., 2003). Turtles, probably the best studied of the marine reptiles, also exhibit sex differences in behaviour during the breeding season. Green turtles (Chelonia mydas) on mating grounds at Ascension Island in the mid-Atlantic Ocean display sex differences in activity patterns. With the aid of satellite-tracking technology, Hays et al. (2001) have demonstrated that the dive duration of male green turtles (typically <15 min) is much shorter than that of females during the internesting period, reflecting greater levels of activity. A similar pattern has been observed in loggerhead turtles (Caretta caretta) in the Mediterranean (Schofield et al., 2006). Spatial sexual segregation of green turtles on breeding grounds off Australia has also been documented. Booth and Peters (1972) made underwater observations of a section of lagoon occupied only by resting females. Unmated males patrolled the area but did not attempt to mate with females within the lagoon. As soon as a female left the lagoon, she was immediately courted by the circling males. Mating pairs entered the lagoon, often followed by an escort of up to five males, but, whilst the mating pair were open to ‘attack’ by a member of the escort, these

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unattached males ignored other unmated females within the sheltered area. Similarly, the identification of an area of male predominance within the green turtle breeding areas of Oman has been suggested to represent a designated mating ground (Ross, 1984). At the end of the breeding season, both male and female green turtles migrate away from nesting grounds to distant foraging grounds. There is a sex difference in the timing of this migration: Male green turtles leave the nesting grounds much earlier than females (Godley et al., 2002), but there is currently no evidence of sexual segregation at any other time in the life cycle of marine turtles (G. Hays personal communication). In contrast, sexual segregation outside the breeding season has been documented in both marine snakes and the marine iguana. The Galapagos marine iguana, Amblyrhynchus cristatus, which feeds exclusively on marine algae, exhibits sex differences in foraging location. Whilst most individuals obtained their algal diet from foraging in intertidal areas which were only accessible for a short time each day at low tide, large males were able to feed independently of the tidal cycle by diving to forage in subtidal areas (Wikelski and Trillmich, 1994). High grazer density in intertidal areas and a gradient of increasing availability of food with distance down the shore enabled male subtidal foragers to consume more macrophytic algae per unit effort than intertidal foragers, thereby increasing intake rates (Buttemer and Dawson, 1993; Wikelski and Trillmich, 1994). Intertidal foragers compensated for lower intake rates by foraging at every opportunity (every day, whereas subtidal foragers fed every second day) and by increasing bite rate (Wikelski and Trillmich, 1994; Fig. 2.3). Sex differences are also present in the diving behaviour of the yellowlipped sea krait, Laticauda columbrina. This species exhibits substantial sex

Figure 2.3 Only large male Galapagos marine iguanas, Amblyrhynchus cristatus, dive to forage subtidally. Photo courtesy of M. Evans, with permission.

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differences in body size, with males being about one-third the bulk of females (Pernetta, 1977). Female-biased size dimorphism is common in snakes due to the necessity for females to carry numerous large eggs and which, at least in part, may enable females of several species to forage deeper (Shine and Wall, 2005). However, as this species also exhibits dietary niche specialisation of the sexes (males consume smaller, reef-flat species such as morays, whilst females consume larger species such as conger eels associated with the waters adjacent to the reef: Pernetta, 1977; Shetty and Shine, 2002), Pernetta (1977) suggested that female-biased dimorphism based on reproductive strategy has been reinforced by enhanced survival of larger and larger females that can exploit previously unused food resources. However, it is likely that significant sexual dimorphism in head morphology plays a significant role (Shine and Wall, 2005). Female yellow-lipped sea kraits have longer, wider heads than males of same length, and have disproportionately larger jaws, characteristics which increase the upper size limit of prey that can be consumed (Shetty and Shine, 2002). Sex differences were also observed in stomach fullness: Females generally consumed only one prey item per foraging trip (compared to multiple items in males), and contained prey more frequently than males (Pernetta, 1977; Shetty and Shine, 2002). Taken together these studies show that sexual segregation is seen in all three groups of present-day marine reptile. Sex differences in behaviour are particularly apparent within breeding populations. Whilst males are actively searching for mates, females appear to range less, matching their distribution to that of their prey or aggregating with other females. However, sexual segregation of foraging niche is also seen outside the breeding season. Once again, this appears to be largely attributable to sexual size dimorphism, with the larger sex diving deeper to consume larger prey.

3.4. Sexual segregation in marine fish With over 15,000 known species, marine fish are the most diverse group of marine vertebrates. Fish are considered wholly aquatic since completion of their lifecycle does not rely on the terrestrial environment and, unlike all species discussed thus far, they are not air breathers. As a result, our understanding of the behavioural ecology of this group of marine vertebrates, relative to their abundance and diversity, is particularly limited. Relatively more is known about the behavioural ecology of freshwater fishes. Indeed, the Trinidadian guppy, Poecilia reticulata, is one of the only aquatic vertebrates for which hypotheses about sexual segregation have been investigated (see: Croft et al., 2004, 2006). This part of this chapter examines sexual segregation in both marine teleosts (bony fishes) and marine elasmobranchs (sharks and rays). Relatively more is known about sexual segregation in elasmobranchs, perhaps due to the ability to determine elasmobranch gender based on external morphology alone; male

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elasmobranchs possess external paired intromittent organs called claspers, which are used by the male to transfer sperm into the female cloaca. 3.4.1. Sexual segregation in teleost fish One of the best documented sex differences in behaviour among marine teleost fish is sex-specific foraging behaviour. For example, male dolphinfish, Coryphaena hippurus, consume proportionately more active, fast swimming species such as flyingfish and squid than do females (Oxenford and Hunte, 1999). Similarly, female clingfish, Diademichthys lineatus, eat shrimp eggs and bivalves more frequently than adult males (Magurran and Garcia, 2000) whilst female dab, Limanda limanda feed on significantly more ophiurids (brittlestars) than males (Temming and Hammer, 1994). However, sex differences in the foraging behaviour are not limited to dietary preferences in this latter species. Females dab had significantly more food in their stomachs than males of the same size, and there were differences in the diurnal feeding rhythm between males and females, with females feeding in the morning and males in the afternoon (Temming and Hammer, 1994). Sex differences have also been documented in the time allocated to feeding behaviour. For example, male sandperch, Parapercis polyophthalma, spent much less time foraging and more on territorial and social activities than females. Male and female sandperch foraged in the same habitats and consumed similar prey items, but female bite rates were 3 times greater, resulting in a mean weight of food per stomach that was 2.4 times greater than that in males (Sano, 1993). Similarly, the bite rate of the female sharknose cleaning goby, Elacatinus evelynae, also exceeds that of males as a result of spending 5 times longer cleaning (Whiteman and Coˆte´, 2002). However, feeding rate does not appear to be fixed and, in the case of the sharknose cleaning goby, can be influenced by the presence of the opposite sex: female cleaning rate was significantly lower when males were present, whereas males cleaned for longer and took more bites when females were present (Whiteman and Coˆte´, 2002). Sex differences are also apparent in the spatial distribution of some teleost species. For example, in American eel, Anguilla rostrata, the sexes differ in habitat choice and geographic distribution. Male eels are primarily found in south-eastern U.S. estuaries, where they are close to the spawning areas of the Sargasso Sea, whereas females are more widely distributed both within rivers and along the eastern American coastline (Magurran and Garcia, 2000). In Atlantic salmon, Salmo salar, males undertake their seaward migration earlier than females ( Jonsson et al., 1990). Sex differences in occupancy of spawning grounds occur in Atlantic cod, Gadus morhua. Males remain on spawning grounds whilst females move in and out of these male-dominated spawning aggregations when ready to release an egg batch (Robichaud and Rose, 2003).

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Clearly, for the majority of marine teleost species virtually nothing is known about sexual segregation, that is, whether it is present in the first place and if it is, what are the patterns and why may they occur? As mentioned previously, this has much to do with the difficulties of sexing teleosts where no external clues as to sex are present. Despite this, it appears that males and females within a teleost species do differ in many regards, not least in their foraging behaviour, so it may be expected that sexual segregation by habitat, for example, may indeed by quite common in this taxa. 3.4.2. Sexual segregation in elasmobranch fish There are about 900 extant species of elasmobranch, among which sexual segregation is considered to be a general characteristic (Springer, 1967). In a recent review of sexual segregation among sharks, Sims (2005) noted evidence for sexual segregation in 38 out of the 400 or so extant shark species. Whilst it would appear that a behaviour exhibited by 10% of all available shark species does not constitute a general behaviour across all elasmobranchs, this small proportion reflects how little we currently know about the general biology of the majority of species. Elasmobranchs are difficult to observe due to the relative inaccessibility of the marine environment. However, of the species which have been studied in sufficient detail, sexual segregation is a general characteristic. Despite its widespread nature, sex differences in shark and ray behaviour have not been investigated until relatively recently. The first evidence for sexual segregation in elasmobranch populations came from fisheries observations which recorded unequal sex ratios in trawl catches. An ‘excess’ of female thornback ray, Raja clavata, was reported in catches whilst males were thought to outnumber females in the starry ray, Amblyraja radiata (Day, 1884). On investigating Scottish landings of Rajiformes, Fulton (1890, 1903) also noted a bias towards females in thornback ray (65.7% female), and, additionally in the sandy ray, Leucoraja circularis (61.7%), and partially in the common skate, Dipturus batis (51.3%). However, unlike the observations of Day (1884), female starry ray were more frequent than males (54.7%) (Fulton, 1890, 1903). Indeed, the only elasmobranch species investigated for which Fulton did not report a femalebiased sex ratio was the shagreen ray (L. fullonica); the sex ratio was equal based on eight individuals examined (Fulton, 1903). Unequal sex ratios were also reported in landings of Canadian Rajiformes. Females dominated landings of little skate (Leucoraja erinacea) by 55%, winter skate (L. ocellata) by 61%, thorny skate (A. radiata) by 60% and barndoor skate (Dipturus laevis) by 65% (Craigie, 1927). Unequal sex ratios have also been reported for the dogfishes. Ford (1921) noted male dominance in landings of smoothhound, Mustelus vulgaris, in the western English Channel inshore fisheries off Plymouth, United Kingdom,

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whilst autumn landings of spurdog, Squalus acanthias, were female dominated (up to 92%). Similarly, females dominated Canadian spurdog landings (68% female) (Craigie, 1927). Deviation from a 1:1 sex ratio was also observed in the Pacific dogfish, Squalus suckleyi, with the direction of the bias varying between locations and possibly also between seasons (Craigie, 1927). Despite widespread reporting of biased sex ratios in elasmobranch landings and the different direction of this bias apparent between geographical locations, Ford (1921) and Steven (1933) were the only researchers to investigate whether these inequalities reflected a bias in the operational sex ratio or differential behaviour of the sexes. Segregation by age is thought to be a universal feature of shark populations (Springer, 1967) and it is thought that size-assorted schools of active shark species may be maintained by the different swimming speeds that can be sustained by different-sized individuals (Wardle et al., 1996). By examining the catches of individual vessels, Ford (1921) and Steven (1933) were able to identify that, where catches were composed of immature individuals, the sexes occurred in approximately equal proportions, indicating no deviation from a 1:1 sex ratio at birth. However, biased sex ratios did occur in catches of mature specimens. Steven (1933) recorded a pattern in the landings of thornback ray within the fishing season ( January–March), as determined from availability of good size fish on the fishing grounds. Females predominated in inshore areas throughout the majority of the season, but declined towards the end of March when male numbers began to increase, which was suggested to indicate male migration into inshore areas (Steven, 1933). Ford’s (1921) Plymouth investigations also revealed sex-specific seasonal migrations into inshore areas. Several thousand specimens of lesser spotted dogfish (Scyliorhinus canicula) were examined at Plymouth and showed that males dominated catches during winter (65% of numbers caught), whereas females marginally predominated in summer (58%). Ford (1921) and Steven (1933) were in broad agreement that sexual segregation of adult fish, and the consequential sampling of unisexual aggregations, provided the most satisfactory explanation for sex-biased landings. Therefore, it appeared there was sexual segregation present in the species studied as a consequence of sex differences in behaviour. These changes over time were interpreted as being the result of same sex individuals clustering more often in preferred habitat rather than in other available habitats. This form of segregation has been termed ‘geographical’ sexual segregation (Backus et al., 1956). Over the next 40 years, numerous studies similarly documented unequal sex ratios in fishery and fishery-independent catches of sharks. Geographical segregation was shown to be present in oceanic whitetip sharks (Carcharhinus longimanus) in the Gulf of Mexico (Backus et al., 1956) and in school

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sharks (Galeorhinus galeus) off southern Australia (Olsen, 1954). As illustrated by Ford and Steven (Ford, 1921; Steven, 1933) in thornbacks and lesser spotted dogfish, geographical segregation in elasmobranchs is often temporal in nature: for example, male cownose rays, Rhinoptera bonasus, dominate in Chesapeake Bay from June to early July and gravid females from late July through to mid-September (Smith and Merriner, 1987). Temporal geographic segregation is often characterised by seasonal movements of mature females into shallow water. Indeed, landings of G. galeus off California showed that not only did catch composition vary by area with respect to the ratio of sexes present, but also with depth, with females occurring in shallower water than males (Ripley, 1946). This probably accounts for the fact that gravid females of some shark species undertake long-distance migrations to sheltered nursery grounds to give birth away from adult sharks (Feldheim et al., 2002). In these locations, females do not feed and do not stay in the area. Indeed, a further explanation for age segregation in sharks may be to reduce the risk of cannibalism and depredation of juveniles and sub-adults by mature individuals (Ebert, 2002; Morrissey and Gruber, 1993; Snelson et al., 1984). The migration of gravid females to designated inshore pupping grounds has been documented in oceanic white-tip shark (Backus et al., 1956), leopard sharks (Triakis semifasciata: Ebert and Ebert, 2005), Caribbean sharpnose sharks (Rhizoprionodon porosus: Mattos et al., 2001) and spurdog (Squalus acanthias: Hickling, 1930). Spurdog have attracted particular attention. This pelagic-demersal species forms large schools, which are targeted by commercial fishers (Compagno, 1984). Ford (1921) collected data on the number of spurdog landed at Plymouth, England, and found that 92% of those captured in November were mature females. Over the following year, records showed that the sex ratio of landings varied widely, with four categories of schools evident: large females that were mostly gravid, exclusively mature males, immature females and immature males and females in equal number. Ford (1921) concluded that inequality in sex composition of the schools was largely due to the tendency of individual, S. acanthias, to school with others of similar size and sex. This type of sexual segregation was termed ‘behavioural’ (Backus et al., 1956). However, sexual segregation is by no means restricted to mature individuals. Klimley (1987) noted that female scalloped hammerhead sharks, Sphyrna lewini, moved away from inshore nursery areas at a younger age than males. This early offshore migration was followed by an apparent increased consumption of pelagic prey and greater predatory success, as inferred from larger stomach content masses in females than in males of the same size. Similarly, dietary differences between the sexes are not only seen in juveniles: Sex differences in the diet blue sharks, Prionace glauca, have been interpreted to result from sex-specific preferences in foraging locations (McCord and Campana, 2003).

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Temperature may also influence the habitat selection of the sexes. Grey reef sharks, Carcharhinus amblyrhynchos, form female-only aggregations in the shallow lagoons of Johnston Atoll in the Central Pacific Ocean. The water temperatures in the lagoons were 1–2  C warmer than in the open ocean and segregation was maximal at the warmest time of the day (Economakis and Lobel, 1998). Sexual segregation in white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia, may also be related to temperature. Males were more prevalent during winter, spring and summer, with a peak in sightings during September when water temperatures were lowest (males observed within the temperature range 14.3–17.8  C), whereas females predominated during autumn when water temperatures were highest (females present within the temperature range 15.7–18.1  C) (Robbins, 2007). The selection of shallower habitats by female nurse, Ginglymostoma cirratum; tiger, Galeocerdo cuvier and blue sharks (Carrier et al., 1994; Heithaus et al., 2006; Litvinov, 2006) may also be related to sex-specific temperature preferences. By the end of the 1960s, there was a burgeoning literature of observations of sexual segregation in sharks (Bullis, 1967; Springer, 1967). Further studies in the 1970s and 1980s expanded the number of species for which sexual segregation was observed or suspected (e.g., Carcharias taurus: Gilmore et al., 1983, Sphyrna lewini: Klimley, 1985, Carcharhinus amblyrhynchos: McKibben and Nelson, 1986, Sphyrna tiburo: Myrberg and Gruber, 1974, Prionace glauca: Pratt, 1979; Stevens, 1976). Despite this, by 1987, the causes of sexual segregation had not been formally investigated in any species, although differences in swimming capabilities, dietary preferences, absence of aggression between similar-sized sharks, or migration of gravid females to nursery grounds were all forwarded as possible explanations (Klimley, 1987; Springer, 1967). In summary for fish, within marine teleost fish, sexual segregation has been observed in foraging behaviour as well as the spatial distribution of breeding populations. However, these observations are limited to only a few species, primarily due to an inability to identify the sex of the majority of teleost fish based on external morphology. In contrast, sexual segregation is considered a general characteristic of elasmobranch populations. Several hypotheses have been forwarded to account for sexual segregation in this group of marine vertebrates. ‘Geographical sexual segregation’ is thought to result from sex differences in habitat preferences, for example, when females migrate to designated inshore nursery areas for oviposition/parturition. ‘Behavioural sexual segregation’ also occurs. Unisexual schools are thought to form in schooling species as a result of differences in the swimming capabilities of the sexes, although an absence of aggression between individuals of a similar size may also be important. Yet, despite the generality of sexual segregation among elasmobranches, the underlying causes of sexual segregation remain to be rigorously tested in any species.

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4. Mechanisms Underlying Sexual Segregation: Hypotheses Whilst sexual segregation is a widespread phenomenon among animals, the underlying causes remain poorly understood. Much attention has been devoted to understanding sexual segregation in group-living ungulates, particularly among species within Ruminata. These investigations have inspired several explanatory hypotheses, summarised below, with assumptions and predictions summarised in Table 2.1. Sexually segregating ungulates typically exhibit sexual dimorphism with respect to body size (i.e., there is a significant difference between the sizes of mature males and females), with male-biased size dimorphism being the prevalent form. Therefore, the ecological implications of sexual size dimorphism feature heavily in hypotheses attempting to account for sexual segregation. As such, this may complicate the interpretation of predictions from hypotheses when investigating species which exhibit female-biased sexual size dimorphism, or are monomorphic with respect to body size. In addition, as these conceptual models have been developed from research which primarily focuses on endothermic vertebrates, the assumptions and prediction of the hypotheses necessarily relate to specific features of these organisms. Interpreting sexual segregation in ectotherms within the same framework proves difficult, particularly as not all of the sexual segregation hypotheses are mutually exclusive. As a result, the assumptions and predictions of some of the hypotheses have been re-framed where necessary to apply more closely to specific features of ectotherm life history and ecology. It is our view that incorporation of ectotherms within the existing (mammal-focused) theoretical framework will help by translating and broadening the application of the existing hypotheses.

4.1. Predation-risk hypothesis (reproductive strategy hypothesis) The predation-risk hypothesis focuses on sex differences in the way individuals strive to maximise their lifetime reproductive success. It is assumed that females and/or their offspring are more at risk to predation than males. These sex differences in predation risk occur due to sexual dimorphism in body size, or because gestation and/or parental care (supervision of small, slow-moving, predator naı¨ve offspring) impede predator evasion. Therefore, female habitat choice is primarily driven by a necessity to reduce predation risk, maximising offspring security, even at the cost of sub-optimal foraging conditions. On the other hand, male habitat choice is driven by resource availability. Males strive to maximise future mating opportunities and thus must be able to compete successfully for mates. Therefore, males

Table 2.1

Summary of assumptions and key predictions of the hypothesis forwarded to account for sexual segregation

Hypothesis

Assumptions

Predictions

Case studies

Predation-risk hypothesis

Female reproductive success is determined by offspring survival Male reproductive success is influenced by size and/ or condition Offspring (and the smaller sex) are more vulnerable to predation The larger sex has greater absolute metabolic requirements, but more efficient digestion

Females select habitats that enhance offspring survival

Leopard sharks (Ebert and Ebert, 2005) Spotted dolphins (Bernard and Hohn, 1989) Elephant seals (Le Boeuf et al., 2000)

Forage selection hypothesis

Reproductive females must satisfy the nutritional demands of gestation and lactation Sex-specific morphological adaptations influence foraging efficiency

Males exploit areas where resources are abundant Provisioning parents and offspring occupy ‘safer’ habitats The larger sex exploits areas where resources are abundant, the smaller sex exploits areas with highquality resources Reproductive females segregate from both males and non-reproducing females More efficient foragers competitively exclude other individuals from preferred resources

Grey seals (Austin et al., 2006) Common dolphins (Young and Cockcroft, 1994) Northern giant petrels (Gonzalez-Solis, 2004)

(continued)

Table 2.1

(continued)

Hypothesis

Assumptions

Predictions

Case studies

Activity budget hypothesis

Large differences in activity budgets, resulting from sexual dimorphism in body size and/or reproductive investment make synchrony of behaviour costly in group-living species and leads to divergent habitat requirements in solitary species Ambient temperature influences fecundity and sex differences exist in the temperatures at which fecundity is maximised; for example, optimal temperatures for sperm and egg production differ Social affinity (intra-sexual cooperation or information transfer), social aversion (avoidance of aggression) or a combination of both determine social groupings

In group-living species, animals with similar activity budgets will form groups in solitary species, size- or reproductive mode-specific habitat use is exhibited

South Georgian shags (Wanless et al., 1995) Marine iguanas (Wikelski and Trillmich, 1994) Wandering albatross (Phillips et al., 2004)

The sexes select different thermal habitats in an effort to maximise reproductive success

Cod (Robichaud and Rose, 2003) Grey reef shark (Economakis and Lobel, 1998)

Groups comprise individuals of varying ages (experience) or group size decreases with age. In many cases, group members are related. The ‘aggressor’ is aggressive and dominant to the ‘avoider’

Sperm whales (Lyrholm et al., 1999) Nurse sharks (Carrier et al., 1994) Bottlenose dolphins (Connor et al., 1992)

Thermal niche– fecundity hypothesis

Social factors hypothesis

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exploit areas with abundant, high-quality forage and engage in behavioural patterns to maximise body condition in preparation for mating, even when these behaviours increase risks of predation. The predation-risk hypothesis is also applicable to situations where males experience higher predation rates as a result of female-biased sexual dimorphism. For example, male harbour porpoise (Phocaena phocaena) are found in more protected waters than the larger females which inhabit riskier habitats where they are subject to attack from white sharks and killer whales, but where they can satisfy their huge nutritional needs resulting from simultaneous pregnancy and lactation (Michaud, 2005). As the predation-risk hypothesis focuses on reproductive strategy, we have extended the definition of the hypothesis to include situations where female habitat selection is influenced by the habitat requirements of its offspring. For example, it has been hypothesised that habitat selection in female sperm whales may be constrained by the thermal requirements of the calf, resulting in a restriction to low latitudes (Gaskin, 1973; Lyrholm et al., 1999; Whitehead and Weilgart, 2000). The adoption of a more risk-averse strategy by females may explain sex differences in the diet of dolphinfish (Coryphaena hippurus). A greater proportion of active, fast swimming prey species in male diets suggests intersexual differences in schooling behaviour, with males spending more time away from flotsam (Oxenford and Hunte, 1999). Sex differences in diet may also result from females, altering their behaviour to reduce predation risk to their offspring. For example, lactating spotted dolphins remain close to their calf at the surface rather than exploiting squid at depth (Bernard and Hohn, 1989). Predation risk is also thought to influence the distribution of beluga whales, Delphinapterus leucas. Summer aggregations of female belugas in coastal waters are thought to result from the approach of killer whales which leads to crowding close to shore (Michaud, 2005). Similarly, the selection of shallow, nearshore waters by maternal humpback whales (Megaptera novaeangliae) in the tropics and bottlenose dolphins of Australia has been suggested to minimise the possibility of predation by sharks and/or killer whales (Clapham, 2000; Mann et al., 2000; Smultea, 1994). In contrast, it is predicted that foraging in inshore areas renders male elephant seals (Mirounga angustirostris) more at risk to predation by sharks and killer whales than females foraging on more patchy, pelagic prey in open water. Nevertheless, it is suggested that greater mass gain in males, indicating that they forage in more productive habitats, presumably makes this risk worthwhile (Le Boeuf et al., 2000). Rather than segregating spatially to reduce predation, some species may group socially to benefit from a dilution effect. Dusky dolphins, for example, form nursery groups during surface-active feeding bouts (Michaud, 2005). The predation-risk hypothesis also provides the most parsimonious explanation for sex differences in the spatial distribution of pinnipeds during

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the breeding season, where female distribution is constrained by the necessity to provision dependent young. However, the predation-risk hypothesis may also be applicable to species which do not exhibit parental care. In several species of shark, for example, gravid females migrate to designated pupping areas, which are often sheltered, inshore areas where predation rates are low, where they give birth to live young. This behavioural pattern is seen in oceanic white-tips (Carcharhinus longimanus: Backus et al., 1956) leopard shark (Trikas semifasciata: Ebert and Ebert, 2005) and lemon shark (Negaprion brevirostris: Feldheim et al., 2002). Similarly, it is likely that seasonal changes in haul-out site used in common seals (Phoca vitulina) result from the females need for safe pupping and lactation sites (Thompson, 1989). Where both parents undertake parental care of the offspring, it may be the male whose habitat use is more influenced by offspring provisioning than that of the female. This appears to be the case for brown boobies (Sula leucogaster) and Ade´lie penguins (Pygoscelis adeliae). Male brown boobies remain close to the colony to maintain territory and prevent or acquire extra-pair copulations (Gilardi, 1992). Similarly, male Ade´lie penguins are more aggressive than females and thus are more efficient at protecting the nest from skua and human predators (Clarke et al., 1998). One consequence of this role reversal is segregation of foraging location. Male dominate in close-at-hand foraging sites whilst females go further afield, presumably to reduce intraspecific competition (Catry et al., 2005; Clarke et al., 1998).

4.2. Forage selection hypothesis (sexual dimorphism— body-size hypothesis) incorporating the scramble competition and incisor breadth hypotheses The forage selection hypothesis focuses on sex differences in nutritional requirements. It is assumed that sex-related differences in body size confer significant differences in nutritional requirements. As gut capacity is a constant proportion of body mass, large-bodied animals are able to retain food longer and digest more efficiently (Gross, 1998). Therefore, whilst large-bodied animals have greater overall metabolic requirements they can meet their metabolic requirements by consuming a lower quality diet than small-bodied animals. It is proposed that the larger-bodied sex selects habitats where intake rates are high, if necessary at the expense of dietary quality, whereas small-bodied individuals must compensate for their digestive inferiority and so are constrained to sites where they can obtain a highquality diet. However, there is some controversy surrounding a prediction of this hypothesis, and it is that males actively seek out habitats with abundant, low-quality forage. The scramble competition and incisor breadth hypotheses provide a possible mechanism for this observation. It is argued that, where competition for forage is high, males are competitively excluded by smaller females.

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The bite size of ungulate grazers, at least, is a function of the width of the incisor teeth and forage height, and, as larger-bodied males have narrower incisor breadth in relation to body size, under heavy grazing pressure where forage height is low, they are less efficient competitors for forage than smaller-bodied females (Illius and Gordon, 1987). Thus, suitability of a patch may differ between the sexes and, as resource value decreases with increasing competition, the ideal free distribution predicts that individuals should distribute themselves such that all individuals receive equal fitness gains (Goss-Custard and Sutherland, 1997; Parker, 1978). In addition, males demonstrate greater mobility and an absence of parental responsibilities and thus are more inclined to avoid competition (Main, 1998). Similarly, as energetic requirements are also affected by reproductive condition, competition from lactating females may force the exclusion of other females and males from high-quality habitats as the lactating females strive to satisfy their additional metabolic requirements. Whilst we have incorporated the sexual dimorphism—body-size hypothesis within the forage selection hypothesis, the existence of sexual dimorphism in body size alone is not sufficient to justify the selection of this hypothesis to explain sexual segregation. Indeed, sexual dimorphism in body size also featured heavily in the assumptions of the predation-risk hypothesis. Similarly, there is considerable overlap between the forage selection hypothesis and the activity budget hypothesis (see Section 4.3). For example, sex differences in dietary niche may be explained by differential habitat selection based on attributes such as diving ability and flight efficiency, which are influenced by body size, rather than by size-specific nutritional requirements. Where this is the case, we have suggested that the activity budget hypothesis may provide a more parsimonious explanation for sexual segregation than forage selection. There exists much evidence of sex-specific forage selection in marine vertebrates. However, in relatively few instances, can these differences be explained by sexual dimorphism alone, in concordance with the forage selection hypothesis. This is due to one prediction of the forage selection hypothesis which appears rare in marine vertebrate populations, and this is the competitive exclusion of the larger sex from high-quality habitats by greater foraging efficiency in the smaller sex. It has been argued above that the incisor breadth hypothesis provides a mechanism for this form of competition to operate. However, this argument may not be relevant in the marine environment. For example, sex differences in the diet of magellanic penguins (Spheniscus magellanicus) and blue-eyed Crozet shags (Phalacrocorax melanogenis) have been attributed to larger male size and consequential larger bills, enabling the capture of a higher proportion of fish, and larger fish, than females resulting in more efficient foraging (Cook et al., 2007; Forero et al., 2002). Indeed, competitive exclusion of the smaller sex by the larger sex may be more commonplace among marine vertebrates. However, one apparent

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exception is the grey seal (Halichoerus grypus), where it has been suggested that males may consume prey of lower energetic value and so must feed more (Austin et al., 2006). In contrast, the prediction that female diet should differ based on reproductive status is well supported in the marine vertebrate literature. The diet of lactating females differs from that of other females in both common (Delphinus delphis) and spotted dolphins (Stenella attenuata), where it has been suggested that the diet of lactating females reflects their divergent nutritional requirements, for example, consuming food such as flyingfish which are high in protein, calcium and phosphorous; and squid which have a high water content (Bernard and Hohn, 1989; Young and Cockcroft, 1994). Sex-specific nutritional requirements, for example, the need to restore calcium levels, have also been forwarded to explain sexual segregation in female wandering albatross (Diomedea exulans: Phillips et al., 2004; Xavier and Croxall, 2005) and the sexually monomorphic northern gannet (Morus bassanus: Lewis et al., 2002). Similarly, differences in the seasonal pattern of reproductive investment of the sexes may also lead to sexual segregation. Grey seals (H. grypus) mate shortly after parturition. Females must therefore recover condition earlier in the year than males to support the developing embryo and thus spend more time diving and exhibit greater selectivity (Austin et al., 2006; Beck et al., 2003a,b, Breed et al., 2006). The need for females to recover condition quickly may also influence the moulting behaviour of the sexes, further contributing to the spatial separation of the sexes. Male common seals (Phoca vitulina) haul out every day during moult (where high skin temperature increases the speed of moult), whereas females spend more time at sea after lactation, enabling them to feed intensively at the cost of slower moult (Thompson et al., 1989). Sex-specific morphological adaptations which lead to sex differences in foraging efficiency and thus sex differences in foraging location may be predicted under the forage selection hypothesis. Northern giant petrels (Macronectes halli), oystercatchers (Haematopus ostralegus) and western sandpipers (Calidris mauri) for example, all exhibit sex differences in bill morphology which contributes to divergent dietary niches of the sexes. Male northern giant petrels have disproportionately larger bills than females (Gonzalez-Solis and Croxall, 2005), which may result in increased foraging efficiency of males over females and thus competitive exclusion of females from mutually preferred resources (Gonzalez-Solis, 2004). In oystercatchers, females generally have pointed bill tips whereas male bills are blunt, resulting in dietary specialisation of the sexes and, as a consequence, sexual segregation of foraging locations; females forage for worms and clams on mudflats, whilst males feed at mussel beds (Durell et al., 1993; Swennen et al., 1983). Oystercatchers foraging in mudflats have difficulty in maintaining adequate intake rates at low tide resulting is lower body condition and survival;

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therefore, tend to forage longer and supplement their diet by foraging in fields (Durell et al., 1993). Longer-billed western sandpipers are able to extract prey that are buried more deeply in the sediment and, by investigating the vertical distribution of invertebrates, Mathot et al. (2007) demonstrated that latitudinal sexual segregation of this species (longer-billed females winter south of males) reflected the abundance of surface prey, which declined in abundance with decreasing latitude. Similarly, sexual dimorphism in head morphology of the yellow-lipped sea krait (Laticauda columbrina) may contribute to dietary niche specialisation of the sexes. Female sea kraits have longer, wider heads than males of the same length, enabling them to consume larger eels than males relative to their head size and body length, whilst the smaller heads of males may enable them to reach further into crevices to obtain small eels (Pernetta, 1977; Shetty and Shine, 2002). It has also been suggested that the larger snout seen in female clingfish (Diademichthys lineatus) contributes to the sex differences in diet seen in this species (Magurran and Garcia, 2000). Likewise, female dab have heavier stomachs and intestines (empty weight) than males which may increase both passage rates and assimilation efficiency in this, the faster growing sex (Temming and Hammer, 1994).

4.3. Activity budget hypothesis (body-size dimorphism hypothesis) The activity budget hypothesis, developed simultaneously by Conradt (1998a) and Ruckstuhl (1998) for ungulate species, focuses on sex differences in activity budgets. It is proposed that species which exhibit sexual dimorphism in body size also exhibit sex differences in energetic requirements, digestive efficiencies and possibly also movement rates, resulting in high fission rates in mixed-sex groups and thus the formation of single-sex groups. These sex-related differences in activity budgets make synchrony of behaviour costly, resulting in high fission rates in mixed-sex groups and thus the formation of single-sex groups. To test this hypothesis, Conradt (1998a) developed an index of activity synchronisation (see Box 2.2) and was able to demonstrate that red deer (Cervus elaphus) in mixed-sex groups were significantly less synchronised in their activity than deer in single-sex groups. However, the factors which render the segregation coefficient largely inappropriate for quantifying the degree of sexual segregation in marine vertebrates (namely the difficulty in determining which individuals constitute a group/population and the sex of all individuals within a group) are also applicable to the synchronisation coefficient. The activity budget hypotheses can be extended to species in which the reproductive investment of the sexes is not equal; for example, in most mammals this is the case due to the increased energetic demands of lactation. Alternatively, in solitary animals, sex differences in activity budgets may

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The synchronisation coefficient (after Conradt, 1998a)

Conradt’s synchronisation coefficient (SynC) determines the degree of synchronisation in single-sex groups (or single-sex parts of mixed-sex groups) of an animal population using the following formula: 20:00 X

SynC ¼ 1 

h ¼ 08:00

! kh Nh ðNh  1Þ X ah;i rh;i N Ah Rh i ¼ 1 nh;i  1

ð2:2Þ

where h is hour of the day, N is total number of animals observed, Nh is total number of animals observed in hth hour of the day, Ah is total number of active animals observed in the hth hour of the day, Rh is total number of resting animals observed in the hth hour of the day, nh,i is number of animals observed in the hth hour of the day in ith group, ah, i is number of active animals observed in hth hour of the day in ith group, and kh is number of groups observed in hth hour of the day. The resulting synchronisation coefficient or index of synchronisation ranges from 0 (no synchronisation in activity within groups) to 1 (complete synchrony of activity within groups). The degree of synchronisation between males and females in mixed-sex groups can be measured using the following formula:

SynCðmalefemaleÞ ¼1

2X 0:00 h ¼ 08:00

kh Nh Nh2 X xa;h;i yr;h;i þ xr;h;i ya;h;i N Ah R h i ¼ 1 2xh;i yh;i

! ð2:3Þ

where xa,h,i is number of active males observed in hth hour of the day in ith group, xr,h,i is number of resting males observed in hth hour of the day in ith group, xh,i is number of males observed in hth hour of the day in ith group (xh,i ¼ xa,h,i þ xr,h,i), ya,h,i is number of active females observed in hth hour of the day in ith group, yr,h,i is number of resting females observed in hth hour of the day in ith group, yh,i is number of males observed in hth hour of the day in ith group (yh,i ¼ ya,h,i þ yr,h,i).

result in sex-specific habitat use. As sex-related differences in activity budgets will increase with divergence in the body size of the sexes, so should the tendency to form sex-segregated groups. This is because, whilst

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the larger sex will have higher absolute energy requirements, an allometric relationship between metabolic rate and body size results in the smaller sex having a higher metabolic rate and higher energy requirement per unit of body mass. Therefore, monomorphic species are not expected to form single-sex groups unless reproducing females need to compensate for the higher energy demands of reproduction. The activity budget hypothesis may explain size-related scaling of foraging trip duration and range in common seals (Phoca vitulina). Thompson et al. (1998) have suggested that high levels of intraspecific competition for prey in inshore areas, results in larger males travelling as far from the central resting place as possible within energy and time limits. However, as female foraging duration and range were short for their body size, the increased costs of reproduction in females (and possibly also an increased cost of transport in pregnant females) likely also influences the activity budgets of the sexes in this species. Sex-specific swimming capabilities have also been forwarded to explain sexual segregation in transport of sharks (Smith and Merriner, 1987; Springer, 1967). Body-size dimorphism is also known to influence diving ability in marine vertebrates. In air breathers, smaller individuals have a smaller functional oxygen store (Wanless et al., 1995) and thus sexual size dimorphism constrains diving capability physiologically. For example, in the bluefooted booby (Sula nebouxii), females are larger so a positive relationship between body size and dive depth means females dive significantly deeper and longer than males, suggesting that separation of vertical feeding niche based upon sex is mediated by sexual size dimorphism in this species (Zavalaga et al., 2007). Sexual body-size dimorphism and the consequential effects on diving capability have also been forwarded as an explanation for sexual segregation in killer whales (Orcinus orca: Michaud, 2005), New Zealand fur seals (Arctocephalus fosteri: Page et al., 2005) and South Georgian shags (Phalacrocorax georgianus: Wanless et al., 1995). However, the smaller sex may compensate for shallower dive depths by undertaking longer foraging excursions and/or increasing dive rate. Indeed, this has been observed in brown (Sula leucogaster) and red-footed boobies (S. sula) where the increase in dive rate of the smaller males is scaled to the degree of sexual dimorphism (Lewis et al., 2005). Sex differences in the temporal pattern of diving behaviour may also be related to body size. It has been suggested, for example, that male blue-eyed Crozet shags (Phalacrocorax melanogenis) and female northern gannets (Morus bassanus) forage at depth in the afternoon when the penetration of sunlight is maximal (Cook et al., 2007; Lewis et al., 2002). Thus, sexual body-size dimorphism and the consequential differences in activity budgets can lead to sex differences in foraging behaviour as well as foraging location (Fig. 2.4). In ectothermic marine reptiles, diving capabilities are likely to be constrained by temperature rather than by an individual’s functional oxygen

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Figure 2.4 In blue-footed boobies, Sula nebouxii, females (right) are larger than males (left) and consequently undertake significantly deeper foraging dives and remain underwater for longer. Photo courtesy of M. Evans, with permission.

store. In marine iguanas for example, due to mass-related changes in cooling and heating rates, only large males are able to forage subtidally, where food availability and consequential intake rates are increased (Wikelski and Trillmich, 1994). By painting some individuals white and thereby manipulating rewarming rates, Wikelski and Trillmich (1994) were able to demonstrate that large males adopted a strategy of ‘forage while warm and warm up when getting inefficient at grazing’. In marine birds, body-size dimorphism influences flight efficiency. Indeed, the mediation of flight performance through dimorphism in body mass has been highlighted as an important determinant of at-sea distribution of wandering albatross since larger males need winds to fly (Phillips et al., 2004). This may, therefore, lead to niche divergence. Increased flight efficiency in the smaller sex, combined with high levels of intraspecific competition and dominance of the larger sex close to breeding sites, has also been highlighted as a possible mechanism underlying sex differences in foraging location and an increased foraging range in the smaller sex in both giant petrels (Gonzalez-Solis and Croxall, 2005) and boobies (Lewis et al., 2005). Female flight efficiency relative to that of males is further increased in northern giant petrels through trait exaggeration. Isometric analysis has revealed that not only do males have longer bills than expected, but females have longer wings than expected (Gonzalez-Solis, 2004). The energetic constraints of offspring provisioning may influence activity pattern of humpback whales (Megaptera novaeangliae) and explain latitudinal segregation in this species. It may be advantageous for pregnant or lactating females not to migrate to tropical breeding grounds due to energetic costs of reproduction (Brown et al., 1995). In addition, the necessity for maternal females to select habitats based on the activity budgets of their

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offspring has been suggested to explain sexual segregation of female humpback whales with a calf into shallow, nearshore waters to avoid turbulent offshore or deep-sea conditions (Clapham, 2000; Smultea, 1994).

4.4. Thermal niche–fecundity hypothesis The thermal niche–fecundity hypothesis, like the predation-risk hypothesis, focuses on intra-specific differences in the way the sexes strive to maximise their lifetime reproductive success. This hypothesis, however, assumes fecundity is temperature dependent and that sex differences occur in the temperature at which fecundity is maximised. Therefore, it is predicted that the sexes occupy different thermal habitats in an effort to maximise reproductive output. The thermal niche–fecundity hypothesis emerged with the onset of the study of sexual segregation in ectotherms (Sims, 2005). For ectotherms, body temperature is largely determined by ambient temperature and, as body temperature influences many aspects of thermal biology including activity, metabolism, and growth, habitat selection plays a key role in thermoregulation. Behavioural thermoregulation enables ectotherms to select appropriate body temperatures for specific activities (Shine and Wall, 2005), hence differences in thermal optima have the potential to generate sex differences in habitat use. Body temperature is known to influence rates of egg development in many invertebrates and fish, for example, a 1  C drop in temperature during vitellogenesis can delay spawning of Atlantic cod, Gadus morhua, by up to 10 days (Kjesbu, 1994). Similarly, body temperature may also influence rates of sperm production in males, and low temperatures are known to inhibit sperm formation in male sticklebacks (Wootton, 1976). Therefore, thermal habitat selection may play a key role in determining individual fecundity, and each individual should, theoretically, select habitats at their appropriate optimal temperature in an attempt to maximise reproductive success. The thermal niche–fecundity hypothesis may explain sexual segregation in Atlantic cod, which have been shown to exhibit sex differences in residency times on spawning grounds (Robichaud and Rose, 2003). Robichaud and Rose (2003) showed that male cod remained resident, whereas females moved in and out of these male-dominated spawning aggregations. They proposed females moved into warmer waters to ‘incubate’ developing eggs before subsequently returning to aggregation sites for spawning. The thermal-niche hypothesis has also been proposed to explain sexual segregation in grey reef (Carcharhinus amblyrhynchos) and white sharks (Carcharodon carcharias). Female grey reef sharks have been observed to aggregate in the shallow lagoons of Johnston Atoll in the Central Pacific Ocean where water temperatures are 1–2  C warmer than in the open ocean.

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As sampled sharks contained embryos in the early stages of development, Economakis and Lobel (1998) hypothesised that pregnant female sharks were aggregating in shallow warm waters to raise their body temperature thereby increasing rate of embryonic development. A similar aggregation of female white sharks at the Neptune Islands, South Australia during the warmest months of the year has been suggested to represent female preference for warm water habitats where developmental growth rates of their young are increased (Robbins, 2007).

4.5. Social factors hypothesis (social preference and social avoidance hypotheses) Under the social factors hypothesis, social mechanisms drive sexual segregation. This hypothesis is generally interpreted in terms of social preferences. The formation of same-sex groups may enable reproductively naı¨ve individuals to locate suitable breeding sites and potential breeding partners. Similarly, social affinities between males may reflect the need for males to develop fighting skills, establish dominance relationships and evaluate potential rivals (Main et al., 1996). An alternative hypothesis is that of social avoidance, inter-sexual aggression, such as aggressiveness of females during parturition, or the avoidance of sparring males may drive sexual segregation. Inter-sexual social avoidance may also arise where there is a conflict of interests between individuals of the two sexes (Parker, 2006). Social conflict usually develops from asymmetry between the reproductive strategies of the sexes: typically, female lifetime fecundity is a function of age and condition, whereas that of males is determined by the number of offspring they sire (Magurran and Garcia, 2000). As a consequence, optimum rates of mating frequency also differ between the sexes and male harassment of females may result (Parker, 2006). The social factors hypothesis has received increasing support in recent years as investigations have begun on sexual segregation in species other than ungulates. Indeed, the social affinity hypothesis has received little support within the terrestrial ungulate literature (Main et al., 1996), but on several occasions has been forwarded to explain sexual segregation in marine mammals. Michaud (2005) suggested that, in cetacean societies, the benefits of being a member of a stable group, such as communal care of calves and cultural transmission of learned information, outweigh the costs associated with group living. Cooperative care of offspring has been suggested to be a primary function of female units in sperm whales (Lyrholm et al., 1999; Whitehead and Weilgart, 2000; Whitehead et al., 1991). Similarly, it has also been suggested that female sperm whales may benefit from coordinated foraging formations and combined memory for distribution of temporally variable food sources (Whitehead and Weilgart, 2000; Whitehead et al., 1991). As sperm whales form matrilineally related female

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units, it is thought that kin selection may have played a role in their evolution (Lyrholm et al., 1999). In this context, the social affinity hypothesis could also explain the grouping behaviour of females with differing reproductive development. In some species, a combination of social affinity and social aversion may explain sexual segregation. It is suggested that cooperative behaviour of males (social affinity) and male avoidance (social aversion) could account for sexual segregation in bottlenose dolphins. A high proportion of strandings of bottlenose dolphin calves show signs of attack from conspecifics (Dunn et al., 2002; Patterson et al., 1998). Males of this species appear to cooperate in pairs and triplets to sequester and control the movements of females (Connor et al., 1992). These male ‘alliances’ preferentially coerce females in mating condition (Connor et al., 1992; Scott et al., 2005), which, together with direct observation of an aggressive interaction between an adult bottlenose dolphin and a dead bottlenose calf (Patterson et al., 1998) has been taken to suggest infanticide occurs in this species. This is supported by the fact that the inter-birth period is long in this species but that females become sexually receptive following death of dependent offspring (Dunn et al., 2002). Social affinity and aversion may also explain sex differences in the behaviour of green turtles (Chelonia mydas). It is thought that males maintain relatively high activity levels in an attempt to locate and mate with as many females as possible to maximise reproductive output (Hays et al., 2001). However, energetic limitations constrain both how long a male will stay at the breeding grounds and how much he will be able to partake in reproductive activities before compromising chances of survivorship. This may account for observed sex differences in the timing of migration (Godley et al., 2002). In contrast, females aggregate in an area away from males. The utilisation of a female-only reserve, together with the documentation of behaviours which appear to avoid copulation and the storage of sperm (females can lay all their eggs after just one mating), are thought to represent female social avoidance of mating males (Booth and Peters, 1972). Analogous behaviours are also seen in loggerhead turtles (Caretta caretta). Males are always ‘on the prowl’ whilst females often just seek to be solitary to let their eggs develop prior to laying (Schofield et al., 2006). Male mate searching behaviour also explains male–female differences in habitat occupancy in the turtle-headed sea snake, Emydocephalus annulatus. Whilst the distribution of adult females closely matches that of their reef prey, males do not feed during breeding, but swim more rapidly, are found across a broader range of habitat types, including sandy substrates where black females may stand out more, and actively court any adult female they encounter (Shine et al., 2003). Similarly, female sandperch, Parapercis polyophthalma, allocate most of their time to foraging and resting, whereas males spend more time engaging in social activities and actively patrol the borders of their territories (Sano, 1993).

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The social avoidance of males by females presumably to avoid unsolicited mating attempts and potential injuries arising from such unwanted activity may explain sexual segregation in female humpback whales (Megaptera novaeangliae), Galapagos (Zalophus wollebaeki) and South American sea lions (Otaria flavescens) and nurse sharks (Ginglymostoma cirratum). It has been suggested that maternal female humpback whales may use shallower water to reduce interactions with conspecifics. The temporal pattern of segregation by maternal humpbacks coincides with periods of increased courting and aggression by adult males, activities that cows may wish to avoid to reduce harassment and injury to calves (Clapham, 2000; Smultea, 1994). Cow–calf use of shallow habitat may discourage courting males, which may select deep water to avoid collisions with the sea floor or coral (Smultea, 1994). Similarly, female Galapagos and southern sea lions with pups aggregate within the territories of dominant males to avoid harassment from other males, which has been shown to influence pup survival and growth (Connor, 2002; Wolf et al., 2005). Female nurse sharks, like green turtles, inhabit female-only areas, exhibit behaviours which appear to avoid copulation and are capable of storing sperm. Therefore, it is thought that sexual segregation in this species represents female social avoidance of mating males: They may wish to control the frequency of mating attempts or alternatively, to control access by particular males (Carrier et al., 1994; Fig. 2.5).

5. Sexual Segregation in Catshark: A Case Study In this chapter, we have (1) described the principal findings of previous research which finds evidence of sexual segregation in marine mammals, birds, reptiles and fish, (2) reviewed the hypotheses which have been proposed to explain sexual segregation and (3) have attempted to use this existing framework to account for the cases of sexual segregation we have described. This latter task has proved particularly difficult. An author will often suggest a possible mechanism which may underlie the sex-specific behaviours they describe, but, more often than not, this explanation will feature predictions of several of the hypotheses proposed to account for sexual segregation in animals. Confounding factors such as sex differences in body size and offspring provisioning may cloud the distinction between the predictions of the hypotheses and may lead one to focus on proximate rather than ultimate causes of segregation. For example, species which are sexually dimorphic with respect to body size may exploit sex-specific foraging locations and prey types, but as a result of sex differences in flight efficiency (activity budget hypothesis) rather than forage selection (forage selection hypothesis). In addition, there is often a lack of information on various aspects of the behaviour of the species in question, making critical

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Figure 2.5 Female Gala´pagos sea lions, Zalophus wollebaeki, aggregate within the territories of dominant males, avoiding harassment from other males and thus enhancing survival of their pups (shown above). Photo courtesy of M. Evans, with permission.

evaluation of the hypotheses impossible. What is needed is the systematic behavioural study of individual marine vertebrate species such that numerous proposed hypotheses for the determinants of sexual segregation can be formally examined to discount particular potential explanations. Here we present a case study of recent research on a common marine vertebrate which exhibits sexual segregation, the small spotted catshark, Scyliorhinus canicula. This species is monomorphic with respect to body size and does not exhibit any parental care. A lack of sexual dimorphism, high relative abundance and a largely coastal distribution, coupled with a small adult size enabling laboratory experiments, combine to identify S. canicula as a good model species with which to investigate the underlying causes of sex differences in behaviour and sexual segregation. However, whilst there exists an abundance of information on the physiology, feeding ecology and reproductive cycle of this species (Rodriguez-Cabello et al., 1998), comparatively little was known about its natural, free-ranging behaviour until relatively recently. Greer Walker et al. (1980) were the first to track this catshark species acoustically, but only short-term tracks (<1 day) of male movements

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were achieved. Moreover, these short trackings only demonstrated that, post-tagging, dogfish simply swam in the direction of the prevailing current. This study clearly is not able to elucidate natural patterns in behaviour. Small spotted catshark movements were investigated by Rodriguez-Cabello et al. (1998) using mark-recapture, concluding that this species did not travel long distances. Sims et al. (2001) were the first to investigate the behaviour of individual male and female small spotted catsharks in any detail. Through the application of acoustic telemetry, they showed male and female S. canicula exhibited alternative behavioural strategies. In the study location in southwest Ireland (Lough Hyne, a tidal sea lough), males were observed to be crepuscularly and nocturnally active, moving from deep (12–24 m) to shallower (<4 m) water to feed at dusk and during the night. In contrast, females refuged in shallow water (0.5–1.5 m) rock crevices and caves during daytime and were nocturnally active in deeper water only once every 2 or 3 days. The home ranges of the sexes also appeared spatially separated (Sims et al., 2001). More recently, Sims et al. (2006a) demonstrated the existence of diel vertical migration (DVM) in this bottom-living species. Through the use of short- and long-term acoustic and archival telemetry, they were able to show that male catshark undertook nocturnal along-bottom movements up submarine slopes from deeper, colder areas occupied during the day into warmer, shallow, prey-rich habitats at night. The results suggested that, whilst males forage in warm water, they prefer to rest and digest in cooler water. Energetic modelling of this ‘hunt warm–rest cool’ strategy indicated male daily energy costs were reduced by just over 4%, implying that male S. canicula uses DVM as an energy conservation strategy that increases bioenergetic efficiency (Sims et al., 2006a; Fig. 2.6).

Figure 2.6 During daylight hours, female small spotted catshark (S. canicula) refuge rock crevices in shallow water habitats, whereas males exhibit saltatory behaviour in comparatively deeper water.

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Overall, sexual segregation is a general feature of shark populations yet remains to be investigated in the majority of species. In a review of sex differences in habitat selection and reproductive strategies of sharks, Sims (2005) used S. canicula as a model species with which to investigate the sexual segregation hypotheses. The forage selection hypothesis was discounted for this species as it did not exhibit sex differences in dietary niche. The predation-risk hypothesis was not likely since small spotted catshark are subject to low levels of seasonal predation in the sea lough study site and yet females refuge throughout the year. The activity budget hypothesis was not investigated explicitly, however, both the thermal niche–fecundity and social factors hypotheses were highlighted as possible mechanisms for segregation in this species. As ectotherms, thermal habitat selection plays a key role in determining catshark energy budgets. Females generally select warmer waters than males. In a tidal sea lough, daytime refuging in shallow water exposes female catshark to temperatures exceeding 18  C during August and September, whereas temperature exposure of males, which remain at depth during the day and only enter the shallows as they cool at night, peaks at 15.7  C (Sims, 2003). Although increased rates of embryonic development in females have been suggested to be associated with the selection of warmer habitats, direct evidence is lacking. Indeed, there may possibly be an inhibitory effect. Male small spotted catshark, in contrast, actively select cooler water temperatures even at the expense of short-term feeding opportunities (Sims et al., 2006a). However, the selection by males of cooler water on the whole may be related to optimum temperatures for sperm production (Kime and Hews, 1982). Elasmobranch courtship and mating involves a prolonged series of complex behaviours. Single females may be pursued by multiple males, with injuries arising from both aggressive courtship and mating. During copulation itself in S. canicula, extreme contortion is involved as the male coils his body tightly around the pelvic region of the female (Dodd, 1983). Hence, courtship and mating can be prolonged, not only because of multiple males all vying for the female but because copulation itself requires the maintenance of body contact and postural control. However, female S. canicula (along with many other elasmobranch species) are known to store sperm, which suggests that copulation need not precede every ovulation in this species. To maintain scope for fecundity and growth, female catshark may therefore seek to limit energetically demanding (and injurous) mating activity. Unisexual refuging behaviour in this species may function to reduce levels of male sexual harassment to individual females and facilitate female choice. Nevertheless, despite the fact that several hypotheses for sexual segregation have been partially examined in this species, dedicated studies are needed to test these hypotheses fully (Sims, 2005).

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The only other marine vertebrates in which a similar analysis has been attempted are the grey seal (Breed et al., 2006), the wandering albatross (Xavier and Croxall, 2005) and the giant petrels (Gonzalez-Solis and Croxall, 2005; see previous sections). However, critical analysis of the underlying causes of sexual segregation in all these species is confounded by the fact that they all exhibit sexual body-size dimorphism. Behavioural experiments are particularly informative when testing competing hypotheses explaining sexual segregation (Catry et al., 2005). However, controlled laboratory manipulations are not feasible in large, wide-ranging marine vertebrates such as seals and albatross. Thus, there is much need for hypothesis-led research which uses an integrative approach of field-based tracking and complementary laboratory studies to evaluate the potential of the sexual segregation hypotheses in a monomorphic species.

6. Conservation Implications of Sexual Segregation Sex differences in behaviour are widespread among marine vertebrates. Where these differences between the sexes are sufficiently diverse, spatial or temporal segregation may result. Understanding sex-based differences in the spatio-temporal dynamics of animal populations is of fundamental importance for their successful management. This is particularly so for k-selected species, such as marine mammals and large marine birds, reptiles and fish, which typically exhibit slow growth, late maturation and low fecundity. One potential implication of sexual segregation is differential exploitation of the sexes of target animals by humans. Commercial whaling catches of humpback whales near winter-breeding colonies were highly skewed towards males (Brown et al., 1995), yet sex ratio at birth is 1:1 (Clapham, 2000). This sex bias is now known to result from sex differences in migration patterns: around 50% of Antarctic females remain in high-latitude feeding areas throughout winter, whilst the majority of the population migrates to breeding areas in low-latitudes in winter (Brown et al., 1995). The observed sex bias may be exacerbated by evidence of sexual segregation within migrating individuals. Males appear on breeding grounds earlier and have longer residence times than females (Stevick et al., 2003). However, male-biased exploitation is likely to have less impact on humpback whale populations than female-biased exploitation. This is primarily due to the fact that male mating success is variable: Some males will father many offspring, whilst others may not father any. In contrast, the majority of females will either be pregnant or provisioning offspring for much, if not all of their

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reproductive years. As a result, a decrease in the size of the female population will result in a decrease in the fecundity of the population. The broad-scale effects of differential exploitation of the sexes by fisheries on sexually segregated shark and ray populations remains, however, so poorly studied that any implications have yet to be clearly identified. But there is anecdotal evidence that suggests human exploitation of sexually segregated sharks may lead to dramatic population declines. The existence of sexual segregation in the demersal-pelagic shark, spurdog (Squalus acanthias), with mature females aggregating to form large unisexual schools, probably resulted in sex-biased exploitation. Schools of mature females were found to dominate landings in southwest England during the early part of the 20th century. This was probably a major factor responsible for the collapse of the spurdog fishery in the English Channel when between 1928 and 1931, landings declined from 2710.3 tons to 802.4 tons (Steven, 1933). Similarly, basking shark (Cetorhinus maximus) catches from harpoon fisheries off West Ireland and northwest Scotland were principally large females, and which was thought to have contributed to an apparent population collapse (Anderson, 1990; McNally, 1976). Although sexual segregation is beginning to be mapped spatially at the large scale for high value sharks, for example, shortfin mako shark, Isurus oxyrinchus (Mucientes et al., in press), there is no requirement by fishing vessels to document the sexes of sharks and rays captured. Therefore, the role of fisheries in exacerbating declines in elasmobranch populations due to spatial targeting of particular areas, where one sex may predominate over another, is at present masked by a lack of data. Female-biased mortality may also result from indirect harvesting. Wandering albatross are frequently killed when they attempt to scavenge baited hooks deployed by long-line fishing vessels (Nel et al., 2002). In 1991, it was estimated that the number of albatross killed annually on Japanese longlines in the southern oceans could exceed 44,000 (Brothers, 1991). The wandering albatross breeding population at Bird Island, South Georgia, declined at a rate of 1% per annum over the 30-year period between 1961 and 1991 (Croxall et al., 1990). However, annual declines of up to 6% have been reported for other populations (Weimerskirch and Jouventin, 1987). High rates of incidental capture by longliners recorded by Brothers (1991) substantiate claims that these declines are due to fishing activity. In addition, sex differences in foraging zones (females forage further offshore where pelagic tuna longliners operate) are evident. Consequently, sex-specific susceptibility rates result in females having a lower rate of survival than males (Croxall et al., 1990). Similarly, giant petrels also experience female-biased mortality as a result of interactions with fisheries. Light measurements recorded for geolocation purposes have revealed that this species associates with nocturnal fisheries which use lights to ‘jig’ for squid.

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Because of sex differences in foraging locations, only females are associated with these fisheries during breeding (Gonzalez-Solis and Croxall, 2005). Interactions between wandering albatross and marine fisheries also influence chick survival. The at-sea distribution of adult males overlaps with that of the Patagonian toothfish (Dissostichus eleginoides) fishery. The probability of incidental capture in this demersal fishery is low, but males scavenge fishery debris (such as discarded fish heads) which they then bring back and feed to their chicks (Nel et al., 2002). Longline hooks are often consumed with the cut-off heads, and thus are also fed to the chicks, which may result in chick fatality. Like whales and sharks, albatross are extreme k-selected species. Fisheries observations reveal that most birds seen following longliners are current breeders (Croxall et al., 1999) and, as albatross are highly monogamous, sexbiased mortality will decrease the fecundity of the population, not only through individual mortality but also by decreasing the number of potential breeding pairs. For this reason, even male-biased mortality may adversely affect population fecundity. Indirect interactions with fisheries may also influence survival, with species and/or sexes which forage on commercially exploited species suffering most. For example, the survival of Hawaiian monk seal, Monachus schauinslandi, populations is endangered as a result of a population decline attributed to starvation of juveniles, which largely feed on commercially exploited fish species (Goodman-Lowe, 1998). Similarly, a decline in seal populations would likely have an adverse affect on northern giant petrel, Macronectes halli, populations. Time of egg hatching corresponds with that of pupping in the local seal populations, with each bird species matching a different seal species (Hunter and Brooke, 1992), indicating a high level of reliance on this food source. If seal populations decline, large, heavy males may not be able to feed offshore, resulting in male-biased mortality. Sex-specific diets may in addition lead to differential exposure to environmental pollutants. Carrion-scavenging male giant petrels forage on the South Georgian coast, which is relatively pristine. In contrast, females forage on the Patagonian shelf, which is polluted by river transport discharges, offshore oil operations and high shipping activity. As a result, females have higher levels of metal contamination in their blood than males (Gonzalez-Solis and Croxall, 2005). Similarly, as females feed at higher trophic levels (Antarctic food webs are comprised of fewer trophic levels than those north of the Antarctic polar front, i.e., in Patagonian waters), their feathers have a higher mercury content than those of males (Becker et al., 2002, cited in Gonzalez-Solis et al., 2002). Another implication of sexual segregation concerns the use of designated cetacean calving and elasmobranch pupping sites, which are frequently situated in shallow, nearshore areas. Whilst the protection of humpback whale calving areas has been recommended under management plans, little

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information on the qualities that define such sites has been gathered (Smultea, 1994). However, the management of these areas may be further complicated if different reproductive stages and events occur under different jurisdictions and the sexes are not equally distributed throughout the species’ range. For example, southwest Atlantic sand tiger sharks mate within Argentinian waters and yet are found in Brazilian waters whilst pregnant (Lucifora et al., 2002). Management strategies involving more than one country are difficult to coordinate and implement, especially if the interests of the countries concerned differ. In addition, little attention has focused on the effects of human use of the coastal zone and its implications on population viability, despite the likely importance of these sites for juveniles (Smultea, 1994). Finally, climate change also has the potential to impact sexually segregating marine vertebrate populations. Not only will increased sea temperatures have the potential to influence animal distributions (e.g., through range expansion: McMahon and Hays, 2006), but the sex ratio of entire populations may be influenced. Sexual differentiation of a number of turtle species is affected by the incubation temperatures of the eggs, and a few tenths of a degree can alter the sex ratio of the hatchlings (Mrosovsky, 1995; Mrosovsky and Yntema, 1980). Current climate warming scenarios predict a continuation in the current warming trend and, as higher temperatures bias the sex ratio in favour of females, there exists potential for increasingly feminised marine turtle populations. Whilst there has been suggestion that turtle populations may be able to adapt to climate warming by adjusting pivotal temperature (the temperature at which the sex determination switches from male to female), or by altering nesting spatially (e.g., by nesting under shade) or temporally (i.e., earlier) (Hawkes et al., 2007), there is currently little evidence to support such adaptation. Indeed, feminisation represents a real threat to marine turtle populations: Males currently constitute less than 10% of the Florida loggerhead population (Hawkes et al., 2007). Warmer incubation temperatures may also affect organismal traits that are likely to be related to lifetime reproductive success, and the nature of this effect could differ between the sexes (Shine, 1999). Colder incubation temperatures produce shorter, fatter but more active and faster moving hatchlings (Shine and Harlow, 1993). In addition, should temperatures increase to lethally high levels, hatchling production itself could be adversely affected. With a temperature increase in as little as 3  C, many loggerhead turtle nests in southern Florida would begin to experience incubation temperatures above lethal limits (Hawkes et al., 2007; Fig. 2.7). But what affect will these factors have on sexual segregation in marine turtles? The distance males need to move to locate females is a function of male density (Hays et al., 2001). Therefore, an increasing proportion of females will mean males will find it easier to find mates, male harassment

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Figure 2.7 Florida’s Loggerhead turtle (Caretta caretta) population is becoming increasingly feminised as a result of climate change. Incubation temperatures influence hatchling sex determination with warmer temperatures favouring females.

of females for mating opportunities will decrease, and therefore sexual segregation will also decrease. Similarly, as males will not have to search as hard or compete for mates, they will be able to remain on breeding grounds for longer, which may also reduce temporal segregation of the sexes. However, if the proportion of females increases to 100%, the population will become extinct.

7. A Synthesis and Future Directions for Research This chapter has examined sexual segregation in marine vertebrates (mammals, birds, reptiles and fish) and found the incidence of this phenomenon widespread within all groups. Marine vertebrates exhibit sex differences in habitat selection over varying spatial (local to latitudinal) and temporal

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(diurnal to annual) scales and in two dimensions (horizontal and vertical). Sex-specific dietary specialisation, in terms of forage size, quantity, quality was widespread, as was sex differences in activity rates and mating strategies. In some instances, adaptive evolution has led to exaggerated traits, increasing the divergence between the habits of the sexes, whereas in other species segregation appears more plastic and will only occur under certain conditions. In addition, sexual segregation appears to be based not only on differences between the sexes and also on the reproductive status of individuals. Current hypotheses forwarded to account for sexual segregation were also reviewed: the predation risk, forage selection, activity budget, thermal niche–fecundity and social factors hypotheses. Whilst these hypotheses have arisen primarily from the literature concerned with terrestrial ungulate behaviour, with relatively little adaptation to account for specific life-history differences, it has been possible to apply these hypotheses to marine vertebrate case studies across a broad range of both endothermic and ectothermic species. With the exception of the thermal niche–fecundity hypothesis, evidence was found supporting each hypothesis within most marine vertebrate groups. A common theme throughout the sexual segregation literature is the search for a unifying hypothesis. In a review of studies of sexual segregation in ungulates, Main et al. (1996) found most evidence supported the predation-risk hypothesis. A similar review by Ruckstuhl and Neuhaus (2002) concluded that sex differences in activity budgets were the most likely driving force behind sexual segregation. The findings of Ruckstuhl and Neuhaus (2002) were subsequently refuted by Bowyer (2004) who, in a review of sexual segregation in ruminants, stated that, as the activity budget hypothesis cannot explain spatial separation and differential habitat or forage use, the forage selection and predation-risk hypotheses were the only hypotheses necessary to explain sexual segregation in ruminants. Clearly, this raises the question of how likely is it that the underlying causes for sexual segregation are similar across species? Is there a unifying principle? In several species, more than one hypothesis has been developed to account for sexual segregation within a species. For example, sex-specific foraging locations in wandering albatross (Diomedea exulans) are influenced by activity budgets since smaller birds are more efficient flyers, but possibly also by sex differences in nutrient requirements such as a need for females to replenish calcium levels after egg-laying (Phillips et al., 2004; Xavier and Croxall, 2005). Smultea (1994) also suggested multiple causes for sexual segregation in humpback whales (Megaptera novaeangliae): Maternal females may select nearshore waters to avoid predators, or more turbulent offshore conditions, or, alternately, to avoid sexual harassment from males. Furthermore, humpback whales appear to segregate for different reasons at different spatial scales. It has been proposed that an energy conservation strategy may explain why reproducing females do not migrate to breeding

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grounds with conspecifics, consistent with the activity budget hypothesis, whereas, as detailed above, predation risk or social aversion may explain sexual segregation by depth (Smultea, 1994). Thus, given that several hypotheses have been developed to account for sexual segregation both between and within a species, it seems more likely that several important factors may contribute. The social factors hypothesis has received little support to date and thus has been largely overlooked by recent studies (e.g., Ruckstuhl and Neuhaus, 2002). Sexual segregation hypotheses are generally assumed to explain either social or habitat segregation and indices have been developed to quantify the degree of social and habitat segregation in animal populations (Conradt, 1998b). These indices have been suggested to provide a useful first step to identify likely hypotheses (Conradt, 2005). However, classifications rely on the assumption that solitary animals are not social and therefore cannot segregate for social reasons (Conradt, 1998b; Neuhaus and Ruckstuhl, 2004a). This chapter suggests that solitary animals may exhibit habitat segregation for social reasons. Therefore, wide appraisal of the literature indicates that these indices should not be used to exclude hypotheses when investigating sexual segregation in animals which do not live in groups. The causes of sexual segregation appear complex and in some species seem equivocal. Yet, despite this, several researchers on ungulates assert that, whilst several ecological variables may be influential, there exists a common underlying cause for sexual segregation across species (Main, 1998). Ruckstuhl and Neuhaus contend that the activity budget hypothesis is that proximate cause that sex differences in activity budgets are most likely driving sexual segregation and that sex differences in predation risk and forage selection are additive factors (Neuhaus and Ruckstuhl, 2004b; Ruckstuhl and Neuhaus, 2002). However, the activity budget hypothesis has received some criticism. Mooring and Rominger (2004) suggest that ‘perhaps the most serious problem with the activity budget hypothesis is that activity budgets are inherently flexible and are not fundamental attributes of animals (such as body size, predation risk and reproductive strategies)’. Indeed, this would appear to be the case, with individuals adjusting their activity budgets to coordinate with the activity patterns of conspecifics. For example, sub-adult male bighorn sheep, Ovis canadensis, have been shown to switch between nursery and male bachelor groups and to alter their activity budget accordingly (Ruckstuhl, 1998, 1999). Thus, it would appear that activity synchrony is not a passive process, and, as such, is likely to incur a cost to the synchronising individual (Conradt, 1998a). Whether a unifying theory is feasible, probable or detectable, depends to a large extent on all competing hypotheses being tested. As a first step, any confounding factors should be eliminated, or at least minimised where possible to avoid bias. The degree of sexual size dimorphism a species exhibits is known to influence sex differences in behaviour and will

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therefore also impact sexual segregation. For example, in a meta-analysis of data extracted from the literature on 40 species of large herbivores, Mysterud (2000) noted that the frequency of ecological segregation was higher among more dimorphic species as a result of diverging nutritional needs. Similarly, sex differences in the trip duration and diving behaviour of sexually size-dimorphic brown booby, Sula leucogaster (females 38% bigger) and red-footed booby, S. sula (females 15% bigger) were scaled to the degree of size-dimorphism between the sexes (Lewis et al., 2005). Significant differences in 15N enrichment were not found in species with lower levels of sexual dimorphism; therefore, body-size dimorphism may lead to sex differences in trophic position—males have a higher position and are bigger (Lesage et al., 2001). However, sexual segregation does occur in monomorphic species (for a review of sexual segregation in monomorphic ungulates see: Ruckstuhl and Neuhaus, 2002). For example, the monomorphic northern gannet, Morus bassanus, exhibits sex differences in foraging behaviour; females are more selective, exhibit longer, deeper dives and spend more time on the surface (Lewis et al., 2002). Therefore, as body-size differences may affect factors such as predation risk, nutritional requirements and activity budgets, the search for a ubiquitous underlying cause for sexual segregation may be best employed by studying species that are not sexually dimorphic. If the differences in body-size effects are removed, it seems logical to assume that the effects of other variables on sexual segregation can be evaluated more objectively. To this end, future research in this area should have a greater focus on the systematic study of sexually size monomorphic species. A handful of marine vertebrate researchers have, in retrospect, attempted to explain sexual segregation in their study species within the sexual segregation framework. However, the hypotheses proposed have not been rigorously tested. Such investigations are difficult to conduct due to the large size of study animals and the general inability for performing ‘natural-experimental’ manipulations at the appropriate scales. However, within marine vertebrates, the catsharks (of which there are about 100 species) may provide a useful model group with which to investigate the underlying causes of sexual segregation. Importantly, many are monomorphic with respect to body size, they do not exhibit parental care, and they are relatively abundant with a small adult size amenable to manipulations in laboratory aquaria. The latter characteristic emphasises what it perhaps most sorely needed to make progress in this field—the systematic test of hypotheses with the aid of behavioural manipulations. Without doubt, future research should employ a multi-faceted approach, incorporating field observation and manipulative experiments under controlled conditions to attempt to elucidate proximate and ultimate explanations of sexual segregation in species. Understanding the underlying causes of sexual segregation is important for conservation reasons due to the need to understand space used by individuals to help with their conservation, but also because of the potential

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for differential human exploitation of the sexes, for example, through spatially focused fisheries. To effectively manage animal populations, careful and thorough evaluation of distribution, habitat requirements and potential threats to populations are needed (Catry et al., 2005). This information, especially where the sexes are concerned, is frequently lacking. Widespread sex-specific habitat and/or forage selection in marine vertebrates advocates separate treatment of the sexes in population models and management plans. However, in the case of marine fisheries for large pelagic fish such as sharks, there is currently no requirement for vessels to record the sexes of captured individuals. Given the widespread decline in many marine vertebrates worldwide, there is a clear and prescient need to understand in greater detail the spatial and temporal dynamics of sexes within populations. The careful study of the behavioural strategies underpinning observed distributions including sexual segregation are a means to approach effectively particular conservation problems. Nevertheless, marine vertebrates range widely within the marine environment and often span national jurisdictions, where different regulations may apply, and which makes effective population management extremely difficult. The studies reviewed in this chapter are the first step towards a greater understanding of spatial population dynamics, a field which we think when mature has the potential to contribute significantly not only to behavioural ecology and evolution, but to management strategies and conservations priorities also.

ACKNOWLEDGEMENTS The authors thank G. Hays for information on marine turtles, and J. Partridge, I. Cuthill, G. Jones and R. Wilson for helpful comments on earlier versions of this chapter. VJW was funded by the Fisheries Society of the British Isles Ph.D. studentship and DWS was supported by a Natural Environment Research Council (NERC)-funded Marine Biological Association Research Fellowship and by the NERC Oceans 2025 Strategic Research Programme (Theme 6: Science for Sustainable Marine Resources).

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C H A P T E R

T H R E E

Sieving a Living: A Review of the Biology, Ecology and Conservation Status of the Plankton-Feeding Basking Shark Cetorhinus Maximus David W. Sims*,† Contents 172 174 174 175 179 179 179 182 183 183 183 184 186 189 203 203 207 208 209 209 209 209 209 210

1. Introduction 2. Description of the Species 2.1. Taxonomy 2.2. Morphology and structure 3. Distribution and Habitat 3.1. Total area 3.2. Habitat associations 3.3. Differential distribution 3.4. Climate-driven changes 4. Bionomics and Life History 4.1. Reproduction 4.2. Growth and maturity 4.3. Food and feeding 4.4. Behaviour 5. Population 5.1. Structure 5.2. Abundance and density 5.3. Recruitment 5.4. Mortality 6. Exploitation 6.1. Fishing gear and boats 6.2. Fishing areas and seasons 6.3. Fishing results 6.4. Decline in numbers

* {

Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth PL1 2PB, United Kingdom Marine Biology and Ecology Research Centre, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth PL4 8AA, United Kingdom

Advances in Marine Biology, Volume 54 ISSN 0065-2881, DOI: 10.1016/S0065-2881(08)00003-5

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2008 Elsevier Ltd. All rights reserved.

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7. Management and Protection 7.1. Management 7.2. Protection 8. Future Directions Acknowledgements References

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Abstract The basking shark Cetorhinus maximus is the world’s second largest fish reaching lengths up to 12 m and weighing up to 4 tonnes. It inhabits warm-temperate to boreal waters circumglobally and has been the subject of fisheries exploitation for at least 200 years. There is current concern over its population levels as a consequence of directed harpoon and net fisheries that in the north-east Atlantic Ocean alone took over 100,000 mature individuals between 1946 and 1997. As a consequence, it is not known whether populations are recovering or are at a fraction of their historical, pre-fishing biomass. They are currently Redlisted as vulnerable globally, and endangered in the north-east Atlantic. The basking shark is one of only three shark species that filter seawater for planktonic prey and this strategy dominates key aspects of its life history. Until recently, very little was known about the biology, ecology and behaviour of this elusive species. The advent of satellite-linked electronic tags for tracking has resulted in considerable progress in furthering our understanding of basking shark behaviour, foraging, activity patterns, horizontal and vertical movements, migrations and broader scale distributions. Genetic studies are also beginning to reveal important insights into aspects of their global population structure, behaviour and evolutionary history. This chapter reviews the taxonomy, distribution and habitat, bionomics and life history, behaviour, population structure, exploitation, management and conservation status of the basking shark. In doing so, it reveals that whilst important behavioural and ecological information has been gained, there are still considerable gaps in knowledge. In particular, these relate to the need to resolve population sizes, spatial dynamics such as population sub-structuring and sexual segregation, the critical habitats occupied by pregnant females, and the distribution and scale of fishery by-catch rates. Although challenging, it is arguable that without achieving these goals the conservation status of the basking shark will be difficult to assess accurately.

1. Introduction Populations of many large marine vertebrates are threatened by high levels of fisheries exploitation (both targeted and as by-catch) (Baum et al., 2003). This applies particularly to sharks, skates and rays (elasmobranch fishes) that have life-history traits that make them especially vulnerable to

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levels of harvest mortality that are above that of natural mortality (Brander, 1981). In particular, many elasmobranchs have a late age at maturity and low fecundity leading to low rates of reproduction (Pratt and Casey, 1990). This results in little scope for the compensatory mechanisms that enable many teleost fish species like cod or mackerel to withstand unnaturally high levels of mortality. As a consequence, elasmobranch fisheries not only exhibit rapid declines in catch rates as exploitation increases, but there is a greater potential for the fishery to collapse (Casey and Myers, 1998). The majority of over 400 species of shark are macropredators and scavengers, while only three species obtain food by filtering seawater. These however, are among the largest living sharks, and among marine vertebrates only whales are larger. The basking shark (Cetorhinus maximus) is the second largest known fish species attaining lengths up to 12 m and a weight of
4 tonnes (Fig. 3.1). This species is greater in size than the rare megamouth (Megachasma pelagios), but smaller than the whale shark (Rhincodon typus) of tropical regions. Organised fisheries for basking shark have existed in the north-east Atlantic region since at least 200 years ago (Fairfax, 1998; McNally, 1976). Indeed, the earliest directed fisheries for pelagic shark were probably for this species (Pawson and Vince, 1999). Despite the commercial interest, surprisingly little is known generally about key aspects of basking shark biology and ecology, including their realised global distributions, population sizes and subdivisions, their reproductive biology, growth and longevity. Recent advances in electronic tag technology have enabled considerable progress within the last few years to be made in identifying movements, behaviour and habitat preferences. In this respect, a new insight has been

Figure 3.1 The basking shark Cetorhinus maximus is the world’s second largest fish. Photo courtesy of J. Stafford-Deitsch, with permission.

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their seasonal movements and activity patterns, particularly those during winter. Furthermore, recent genetic studies have elucidated at least large scale divisions among populations. There have been numerous focused reviews of the literature available for basking shark since Kunzlik’s (1988) treatment, principally as part of proposals seeking to list the species on international conservation treaties (e.g., Convention on International Trade in Endangered Species (CITES), Convention for Conservation of Migratory Species). However, these are not broadly available and none have appraised the most recent scientific literature in appropriate detail across all aspects of basking shark ecology, behaviour and biology. Significant new scientific information has been added, particularly in the last 10 years that warrants this present overview. Therefore, the purpose of this review, 20 years after that of Kunzlik’s (1988), is to present a full description and interpretation of the scientific results obtained to date, with inclusion of anecdotal information from grey literature sources where appropriate, and to identify any significant gaps in our knowledge, especially where it impacts this species’ conservation status.

2. Description of the Species 2.1. Taxonomy The basking shark was first scientifically described and named Squalus maximus (literally ‘largest shark’) by Gunnerus in 1765. As Squalus was a catch-all genus for cartilaginous fish generally, Blainville in 1816 erected a new subgenus of Squalus named Cetorhinus (literally ‘whale shark’). There were many objective synonyms of Squalus (Cetorhinus) maximus between 1765 and 1960, including Halsydrus pontoppidani, Squalus pelegrinus, Squalus peregrinus, Squalus rhinoceros and Cetorhinus maximus forma infanuncula (Compagno, 1984). For example, the latter name was erected by Van Deinse and Adriani (1953) to describe a putative subspecies of basking shark which they found to lack filtering gill rakers. This latter proposition was successfully refuted by Parker and Boeseman (1954) from observations and their subsequent interpretation that basking sharks shed gill rakers on an apparently seasonal cycle (see Section 4.4.2). Despite attempts to erect subspecies, especially for individuals found between different ocean basins, it is generally considered that there is only a single species of basking shark. Springer and Gilbert (1976) rejected the concept of at least four species subdivided on the grounds of differences in body proportions between individuals in the North Atlantic/Mediterranean, South Atlantic and waters around Australia. As such differences occur naturally during growth, it was considered that separation into species merely reflected these differences and was therefore insufficient evidence for division (Kunzlik, 1988; Springer and Gilbert, 1976).

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The basking shark, Cetorhinus maximus, is the only species placed within the family Cetorhinidae, which is considered a sister group to Lamnidae (Compagno, 1990; Martin and Naylor, 1997). These families constitute two of the seven placed within the order Lamniformes (mackerel sharks) (Compagno, 1984). Lamniformes is one of eight orders of shark within class Chondrichthyes (subclass Elasmobranchii). The interrelationships of shark taxa including those species within Lamniformes are not without controversy. Maisey (1985) argued that the megamouth shark, Megachasma pelagios, should be included within Cetorhinidae on account of its similarities with C. maximus jaw suspension and dental array, rather than forming a new monotypic family (Megachasmidae) as proposed by Taylor et al. (1983). However, as noted in Dulvy and Reynolds (1997), the cladistic phylogeny of the monophyletic Lamniformes (Compagno, 1990) is consistent with the molecular phylogenies of Martin et al. (1992) and Naylor et al. (1997). Furthermore, recent molecular analysis of cytochrome b gene sequences implies independent origins of filter-feeding within Lamniformes, and hence argues against C. maximus and M. pelagios forming sister taxa within Cetorhinidae (Martin and Naylor, 1997) (Fig. 3.2).

2.2. Morphology and structure The basking shark is a large-bodied fish with a fusiform body shape. Detailed general descriptions of external morphology and internal anatomy are given in Matthews and Parker (1950) and which are summarised in the Species Mitsukurina owstoni (1) Carcharias taurus (2) Odontaspis ferox (2) Odontaspis horonhai (2) Pseudocarcharias kamoharai (3) Megachasma pelagios (4) Alopias vulpinus (5) Alopias superciliosus (5) Alopias pelagicus (5) Cetorhinus maximus (6) Lamna nasus (7) Lamna ditropis (7) Carcharodon carcharias (7) Isurus paucus (7) Isurus oxyrinchus (7)

Figure 3.2 Interrelationships of species within Lamniformes derived from molecular data (redrawn from Martin and Naylor, 1997) and which is consistent with the phylogeny derived from cladistic analysis (Compagno, 1990). The same number beside species names denotes placement within the same family: (1) Mitsukurinidae, (2) Odontaspididae, (3) Pseudocarchariidae, (4) Megachasmidae, (5) Alopiidae, (6) Cetorhinidae and (7) Lamnidae.

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review by Kunzlik (1988). Nothing needs to be added to these treatments here other than to provide the reader with a brief overview of the species field marks that are of particular interest, and to describe the differences in fin dimensions between juvenile and adult individuals. Particular information on fins is warranted because these are harvested commercially (Clarke et al., 2006). The colour of the body surface varies in descriptions, from black to dark grey through slate grey to brown (Kunzlik, 1988; Matthews and Parker, 1950). When observed in sunlight in its natural habitat, basking sharks appear grey–brown with lighter dappled or irregular longitudinal patterns along its lateral surface. When dead and out of water, basking sharks appear slate or dark grey–black. The variations in body colour reported may, therefore, reflect changes due to death and/or removal from water (Kunzlik, 1988). The large body size is a feature that helps distinguish this shark from all others (Compagno, 1984; Matthews and Parker, 1950). Basking sharks have been credited with maximum total lengths between 12.2 and 15.2 m (Compagno, 1984), whilst theoretical maxima have been given as 12.76 and 13.72 m (Kunzlik, 1988; Parker and Stott, 1965). Compagno (1984) states that even if these are correct, most specimens do not exceed 9.8 m total length. However, the longest reliable measurement of a shark caught in static fishing gear in Newfoundland was found to be a 12.2-m long male (Lien and Fawcett, 1986). Consequently, the basking shark is the second largest shark species (elasmobranch, and fish-like vertebrate) in the world after the whale shark (Rhincodon typus). The body mass of basking sharks in relation to total length is not well known on account of the difficulties associated with weighing large specimens. Maximum body masses of 5–6 tonnes have been ascribed to adult sharks in popular accounts. However, two Californian specimens measuring 8.5 and 9.1 m total length weighed 2991 and 3909 kg, respectively (Bigelow and Schroeder, 1948). The body mass of an 8.3-m total length female shark taken off Florida, USA, was found to be 1980 kg (Springer and Gilbert, 1976), and a 6.0 m individual from Scotland, UK, weighed
2000 kg (Stott, 1980). An adult female and an adult male basking shark of 6 and 7 m total length taken off Plymouth, UK, weighed 1678 and 1924 kg, respectively (Bone and Roberts, 1969). Kruska (1988) measured the mass of a 3.75 m long specimen to be 385 kg. Basking sharks have correspondingly large fins and a caudal peduncle with strong lateral keels. The first dorsal fin measured in an adult female of 8.3 m total body length (LT) was 1.1 m in height (Springer and Gilbert, 1976). The pectoral fins were similar in length (
1.3 m) to the first dorsal fin height, whereas the leading edge of the caudal fin was 1.7 m in length. In contrast, the length of the pectoral fins of a 2.6-m LT immature female, C. maximus, was nearly twice that of the dorsal fin height (0.22 m), whereas the

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leading edge of the caudal fin was nearly 0.7 m long (Izawa and Shibata, 1993). Presumably these differences in fin proportions relate to ontogenic changes in gross morphology. In addition to the pointed snout and huge sub-terminal mouth, there are minute hooked teeth (
5 mm in height) arranged in 3–7 functional rows on the upper and lower jaws, respectively (Matthews and Parker, 1950). The teeth are modified placoid dermal denticles. Small denticles of the normal type point posteriorly over the entire skin surface which is also covered with a dark-coloured mucus to the level of the summits of the denticles (Matthews and Parker, 1950). During behavioural studies, this foul-smelling mucus was deposited on ropes (used to deploy plankton nets) as basking sharks brushed past them during normal swimming (D. W. Sims, unpublished observations). Taking skin swabs of this mucus may be an effective, non-invasive method for obtaining basking shark DNA for molecular studies, although this method has yet to be achieved successfully on a frequent enough basis to support such work. Basking sharks are also typified by their enormous gill slits that virtually encircle the head (Fig. 3.1). The five gill slits on each side of the pharyngeal area are openings between the gill arches upon which there are two distinct structures: the gill lamellae that enable respiration by the exchange of oxygen with seawater, and anteriorly, the gill rakers which are comb-like structures arranged in a single row along the distal portion of each gill arch (Fig. 3.3). When the mouth is open, two rows of gill rakers on separate gill arches extend across each gill slit gap and are involved in filtration of zooplankton prey from the continuous flow of seawater produced by

Figure 3.3 The gill arches of the basking shark nearly encircle the head and support structures known as gill rakers (the black, comb-like processes) that have a key role in filtering zooplankton from seawater.

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forward swimming (so-called ram-filter feeding). The rakers are erected when the mouth opens by contraction of the muscle on the aboral half of the foot of the raker, and are held in position against the water flow by elastic fibres in the connective tissue strip (Matthews and Parker, 1950). When the slits are closed, the rakers lie flat against the surface of the arches. In an adult specimen, the gill rakers are about 0.1 m long in the centre of the gill arch and the inter-raker distance is about 0.8 mm (Matthews and Parker, 1950). Early anatomical investigations of summer and winter-caught specimens suggested that gill rakers are shed in late autumn or early winter, re-grow through the winter and erupt through the gill-arch epidermis in late winter/early spring, in time for spring feeding coinciding with the seasonal increase in zooplankton abundance (Matthews, 1962; Parker and Boeseman, 1954). However, recent re-appraisal of these data indicate gillraker shedding is by no means ubiquitous; basking sharks with gill rakers present and food in their stomachs are known during winter and their tracked behaviour indicates active foraging during this time (Sims, 1999; see Section 4.3). The liver of the basking shark is large and makes up between 15 and 25% of its body weight (Kunzlik, 1988). The hydrocarbons of zooplankton pass through the basking shark alimentary canal without fractionation or structural modification, and are resorbed in the spiral valve and deposited in the liver (Blumer, 1967). Even though squalene is present only in traces in zooplankton, it is abundant in the liver of basking sharks, which contains between 11.8 and 38.0% squalene (Blumer, 1967; Kunzlik, 1988). The liver functions as both an energy store and as a hydrostatic organ for increasing static lift (Baldridge, 1972; Bone and Roberts, 1969). The skeleton of the basking shark is cartilaginous with varying degrees of calcification throughout, but like that of other sharks, these structures are not ossified (Kunzlik, 1988). The paired sexual organs (claspers) of male sharks are located ventrally at the base of the paired pelvic fins and these become progressively calcified with maturity. Sharks have been aged by counting growth zones visualised in structures such as dorsal spines and vertebral centra (for review see Cailliet, 1990). These growth zones are comprised of opaque bands that have cells with high concentrations of calcium and phosphorus and translucent bands that are less mineralised (Yudin and Cailliet, 1990). Species such as the blue shark appear to deposit alternate dark and light concentric rings annually (Stevens, 1975), but quantifying age at length has been verified in less than 10 species (Cailliet, 1990). The number of rings present in the vertebral centra of basking sharks varies along an individual’s body length and so ageing this species has proved problematic (Parker and Stott, 1965). Recent progress has been made, however, in ageing filter-feeding whale sharks using X-radiography of vertebral centra (Wintner, 2000).

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3. Distribution and Habitat 3.1. Total area The basking shark is a coastal-pelagic shark known to inhabit the boreal to warm-temperate waters of the continental and insular shelves circumglobally. It has been recorded in the western Atlantic from Newfoundland to Florida and from southern Brazil to Argentina (Compagno, 1984; Toma´s and Gomes, 1989; Wood, 1957). Exceptionally, at least two individuals are known from as far south as the Dominican Republic in the Caribbean. One of these was washed ashore moribund in water of about 24  C, suggesting warmer temperature waters are probably usually avoided by this species. An individual tracked with a satellite-linked archival tag was found to enter Caribbean waters but did so by remaining in deeper, cooler waters. In the eastern Atlantic, C. maximus is present from Iceland, Norway and as far north as the Russian White Sea (southern Barents Sea) extending south to the Mediterranean, and in the Southern Hemisphere from the western Cape province and South Africa (Compagno, 1984; Konstantinov and Nizovtsev, 1980). They are also present in the Pacific Ocean; from Japan, the Koreas, China, Australia (south of 25 N) and New Zealand in the west, and from the Gulf of Alaska to Baja California, Peru and Chile in the east (Compagno, 1984). The basking shark has been recorded primarily from coastal areas; however, this may not represent its entire habitat range as distribution throughout the epipelagic zone of ocean basins is possible. However, sightings data away from coastal areas are generally lacking, which could indicate either ‘hidden’ abundance at depth in oceanic regions, or a general lack of basking sharks away from productive coastal zones (Southall et al., 2005). At least 10 basking sharks satellite tracked in the north-east Atlantic over periods between 1.7 and 7 months were found to remain associated with the European continental shelf (Sims et al., 2003b, 2006); however, a large 8-m long shark was tracked moving west from U.K. waters to Newfoundland (Gore et al., 2008). Since relatively few basking shark movements have been tracked (and only in the Atlantic Ocean), and sightings data in oceanic regions are very limited, our knowledge of the total area distribution of this species may at present be considerably underestimated.

3.2. Habitat associations Basking sharks have a strong tendency to aggregate in coastal areas of continental shelves dominated by transitional waters between stratified and mixed water columns (Sims et al., 2006). These transition zones are known as tidal fronts and are often sites of enhanced zooplankton abundance (Sims and Quayle, 1998). Wherever fronts are well defined,

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for example, in the north-east Atlantic off south-west England (e.g., Ushant front, Celtic Sea, shelf edge/Goban Spur), in the Irish Sea off the Isle of Man, and off north-western Scotland (e.g., Hebridean Sea, Outer Hebrides), annual sightings of basking sharks are well documented (Fig. 3.4). Basking sharks also occur along continental shelf-edge habitats where fronts are often present (Sims et al., 2003), but these physical structures are produced by different oceanographic processes, principally by internal waves (Le Fe`vre, 1986; Fig. 3.5A). A recent study in European waters collated location data for basking shark from public sightings, effort-corrected vessel surveys and satellite-tag geolocation data to identify more closely the spatial distribution of basking sharks among continental shelf and shelf-edge habitats (Southall et al., 2005). Public sightings and vessel surveys only located basking sharks at the sea surface, whereas archival tag geolocations provided positions independent of surface behaviour. The broad distribution patterns revealed by these different methods were similar, but there were considerable differences in density distributions. Across the European shelf, surface sightings data showed high densities, or ‘hotspots’, in the Hebridean Sea, Clyde Sea, Irish Sea and close inshore off southwest England. Satellite-tag geolocations, in contrast, identified two areas where individuals spent considerable time

Outer Hebrides

Clyde Sea

Hebridean Sea Ireland

Goban Spur

North Sea Irish UK Sea Celtic Sea front

Celtic Sea English Channel Hurd Deep Brittany Ushant

Shelf Edge

France

Bay of Biscay

Figure 3.4 Map of the European shelf area with location names referred to in the text. This is the region where the most ecological research on basking sharks has been undertaken.

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A

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100

80 Ireland

60 UK 40

20 France

Figure 3.5 (A) The location of the main tidal fronts (black lines) and the shelf-edge break front (dashed lines) in the European shelf area overlaid on a contour map of calanoid copepod biomass derived from Continuous Plankton Recorder data. Scale bar is biomass in mg m3. (B) Satellite-tag geolocations of tracked basking sharks between 2001 and 2002. Note the hotspots of copepod abundance in areas where basking sharks were located, for example, western English Channel, Celtic Sea, west of Ireland and north-west Scotland. Redrawn from Sims et al. (2006).

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outside the distributions indicated by surveys and public sightings: the Celtic Sea and the western approaches to the English Channel (Southall et al., 2005; Figs. 3.4 and 3.5B). The latter regions are dominated by tidal fronts, but here sharks tend to forage just below the surface where they are out of sight of observers for much of the time (Fig 3.5A). In this sense, they represent a ‘hidden’ abundance of basking sharks that would not have been detected without satellite-tracking technology. In terms of thermal habitat, basking sharks appear to have a relatively wide range of tolerance but may show preferences for a particular range of water temperatures. A shark tracked off the US east coast from Massachusetts to North Carolina occupied temperatures between 5.8 and 21.0  C, but also showed an apparent preference, with 72% of the temperature recordings occurring between 15.0 and 17.5  C (Skomal et al., 2004). Water temperatures recorded by archival tags attached to basking sharks occupying European shelf and shelf-edge habitats during summer, autumn and winter indicate a temperature range of between 8 and 16  C that was conserved among different individuals (Sims et al., 2003b).

3.3. Differential distribution Although population segregation by body size and sex within a species is a general characteristic of shark species worldwide (Klimley, 1987; Sims, 2005; Wearmouth and Sims 2008), there is no clear evidence to indicate differential distribution in the basking shark. Juvenile (2–3 m total length, LT) and putative sub-adult (3–5 m LT) sharks have been frequently observed in the same areas and summer-feeding aggregations as adults (Berrow and Heardman, 1994; Sims et al., 1997). However, there was some indication that juveniles and sharks <3 m LT appeared to feed later in the summer at the surface compared to larger individuals (Sims et al., 1997), which may reflect habitat segregation by size. However, this may have been driven by biotic factors, such as zooplankton abundance, rather than age-segregated distribution or migration per se. In the years (1999–2005) since the observations of Sims et al. (1997) were made off Plymouth in the Western English Channel, a shift towards smaller-sized sharks in this area as the summer progresses has been less obvious (D. W. Sims, unpublished observations). Similarly, whether sexual segregation of the population occurs has not been shown unambiguously. Males and females have been observed in the same areas during summer (Matthews and Parker, 1950; Maxwell, 1952; O’Connor, 1953; Sims et al., 2000a; Watkins, 1958), although more females than males have been caught in directed fisheries (Kunzlik, 1988) suggesting females may segregate from males, at least when they occur at the surface. Pregnant females are virtually unknown from these same locations so differential habitat utilisation by mature males and females at certain times in the reproductive cycle may well occur.

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3.4. Climate-driven changes Climate has important effects on migratory species through effects on physical and biotic environments including predator–prey interactions (Robinson et al., 2008). Whilst at smaller spatial scales, basking shark distribution and occurrence appears strongly linked to zooplankton abundance (see Section 4.4), the factors influencing broader scale patterns in their abundance and distribution remain largely unknown. A recent study of long-term sightings collected off south-west Britain between 1988 and 2001 indicate that the number of basking sharks observed was highly correlated with abiotic factors, in particular sea surface temperature (SST) and the lagged effect of SST in the previous month (Cotton et al., 2005). This correlation between annual surface sightings and SST over large spatiotemporal scales suggests annual changes in the number of basking sharks recorded at the surface are probably closely related to the availability of climate-driven thermal habitat (Cotton et al., 2005), which may also influence zooplankton abundance and distribution. Although the general effects of climate variations on basking shark movements, longer-term distributions and population abundance have not been studied rigorously, this preliminary study does support the hypothesis that behavioural responses at small scales due to foraging movements are linked by broad-scale responses to temperature variation.

4. Bionomics and Life History 4.1. Reproduction Matthews (1950) gives a detailed account of reproduction in the basking shark based upon macro and microscopic anatomical investigations of dissected specimens from Scotland, UK. To summarise the main points of interest briefly, Matthews (1950) suggested the basking shark to be ovoviviparous, that is, live young are produced from eggs that hatch within the body. This mode of reproduction is common among large-bodied elasmobranchs, including the whale shark ( Joung et al., 1996). In female basking sharks, only the right ovary is functional, and may contain at least six million ova each about 0.5 mm in diameter (Matthews, 1950), presumably to provision oophagous foetuses for the entire gestation period. Smaller numbers of more heavily yolked ova are more commonly found in sharks (Kunzlik, 1988). Fertilisation in the basking shark, as in all other sharks is internal: The intromittent organs (claspers) are inserted via the female’s cloaca into the vagina and transfer large quantities of sperm packets or spermatophores. In male basking sharks, spermatophores are up to about 3 cm in diameter, each with a core of sperm and a firm translucent cortex.

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The spermatophores float in a clear seminal fluid and Matthews (1950) estimated that about 18 L of them are transferred to the female during mating. The period of gestation is not known with any certainty, but estimates as high as 3.5 years have been proposed (Parker and Stott, 1965), although a period of just over 1 year has been estimated from the same length–frequency data (Holden, 1974). There is only one published record of a pregnant female being captured despite organised fisheries for basking sharks in the north-east Atlantic dating back at least 200 years. According to this single account, a female basking shark was caught in August 1936 off the mid-western coast of Norway and towed into Teigboden (Sund, 1943). Whilst being towed the shark gave birth to six pups, each about 1.5–2.0 m LT, five of which began swimming open-mouthed at the surface, presumably feeding. The sixth pup was stillborn. Therefore, if this number of pups is representative of normal parturition rates, it seems the basking shark exhibits low fecundity even when compared to other relatively large-bodied ovoviviparous sharks (Compagno, 1984; Sims, 2005). As is the case for embryo development and parturition, growth and age at maturity in this species are very poorly understood (see next section).

4.2. Growth and maturity Male basking sharks are thought to become sexually mature between 5 and 7 m, at ages between 12 and 16 years, whereas females mature at 8.1–9.8 m and possibly 16–20 years (Compagno, 1984). Maximum length is not known precisely, although 10–12 m appears to be a maximum, with individuals between 9.8 and 12.2 m having been reported (Lien and Fawcett 1986; Parker and Stott 1965). Matthews (1950) and Matthews and Parker (1950) observed mature males at lengths between 6.8 and 8.1 m. Rapid increase in male clasper length occurred between 6.0 and 7.5 m body length with little change thereafter (Francis and Duffy, 2002). Female length at maturity is uncertain, but females between 7.7 and 8.2 m long were considered mature by Matthews (1950) and Matthews and Parker (1950). Mean age at first maturity in females is thought to be reached at about 18 years. The growth rate of basking sharks is not known exactly, but has been estimated to be 0.4 m per year (Pauly, 1978, 2002). Attempts to estimate age of basking shark have used two methods: (1) length–frequency analysis has been used to derive length-at-age growth curves (Matthews, 1950; Parker and Boeseman 1954; Parker and Stott 1965) and (2) vertebral centra analysis has been used to relate observed numbers of ‘age rings’ to measured body length (Parker and Stott, 1965). For the length–frequency analysis, which attempts to relate successive modes in the length–frequency distribution with successive age groups, measurements of 93 fishery-caught individuals from the north-east Atlantic were used. These data resulted in suggestions

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that a size of not <2 m length was typical of the first summer, a mean size of 3.09 m was attained in the following summer and that the mean size in the next winter was 3.52 m (Parker and Stott, 1965). This growth increment of 0.43 m was assumed to represent half a years growth. Parker and Stott (1965) derived a growth curve for C. maximus from these empirical data using the assumptions that growth was asymptotic and best described by a von Bertalanffy growth function, that the length at parturition was 1.5 m LT, and that the maximum length asymptote was 11.0 m LT. The growth curve produced indicated that a 5-m long shark will be about 4 years old, whereas a 9-m long individual will be at least 12.5 years old. More recent studies by Pauly (1978, 2002), however, cast some doubt on these estimates. Pauly (1978) argued that since basking sharks may lose their gill rakers and do not feed during colder months, or at the least feeding was reduced, the total annual growth, not half-year growth, was about 0.43 m. The von Bertalanffy relationship based on this assumption obviously describes slower growth, with a 3.75-m long shark being at least 5 years old (Pauly, 1978). On the basis of this derived relationship, Pauly (1978) estimated longevity at about 40–50 years. New data showing basking sharks remain active in winter consistent with foraging (Sims et al., 2003b) suggest this assumption about a food-limited growth increment requires some re-assessment. Unfortunately, there are very few re-sightings of individual basking sharks to validate growth increases. An opportunistic re-sighting of a female shark by Sims et al. (2000b) showed that this 5.0-m long shark had apparently increased in LT by between
1.4 and 2.4 m in just over 3 years, or 0.46– 0.80 m year1. Clearly, this empirical growth-increment range, reflecting measurement imprecision, is unable to provide unequivocal support for either the Parker and Stott (1965) estimate (0.86 m year1) or the Pauly (1978, 2002) assertion (0.43 m year1) since the empirical range lies between these two estimates. Thus, there is a need for accurate and sustained photo-identification studies to verify growth increments of individual basking sharks at different maturation phases. Validation of age-at-length using growth rings in vertebral centra of basking sharks has proved difficult as a means of estimating growth rate. The number of rings apparently decreases caudally suggesting an uneven laying down of rings during growth, as a function of body length and with respect to time (Parker and Stott, 1965). Without a consistent number of vertebral rings along the body length, it is not possible with any certainty to be able to determine age-at-length reliably. Furthermore, there appear to be seven rings present at birth (Parker and Stott, 1965). This led Parker and Stott (1965) to suggest that basking sharks lay down two growth rings per year, a rate which was consistent with their von Bertalanffy growth curve (see above). Parker and Stott (1965) showed that vertebral centra of basking sharks between 3.5 and 5.5 m LT contained 9–16 rings, whereas those from 7.5 to 9.0 m LT possessed between 26 and 32 rings. The latter authors

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suggested for basking sharks that two opaque bands were deposited per year perhaps as a function of increased somatic growth during the two main periods of plankton productivity in temperate waters. Although this idea of two growth rings per year and seven at birth has been repudiated recently by Pauly (2002), the suggestions of Parker and Stott (1965) are not entirely without foundation. The Pacific angel shark (Squatina californica) has 6 or 7 bands present in the vertebral centra at birth and up to 42 in the largest adults (Natanson and Cailliet, 1990). It was demonstrated that these bands were not deposited annually as they are in some species (e.g., Prionace glauca; Cailliet, 1990; Stevens, 1975), but deposition was related to somatic growth. Nonetheless, Pauly (1978) demonstrates that von Bertalanffy growth curves derived separately from the 0.43 m growth increment, and from growth-ring data at a deposition rate of one band per year are approximately equal. This is further supported by re-analysis using modern methods (Pauly, 2002). Except for these re-analyses and re-interpretation of existing data as described above, there has been no new contemporary work to progress age determination in basking sharks to identify growth rates.

4.3. Food and feeding The basking shark feeds upon zooplankton prey it captures by forward swimming with an open mouth so that a passive water flow passes across the gill-raker apparatus. Unlike the megamouth and whale sharks that may rely upon suction or gulp feeding to capture swarms of zooplankton (Clark and Nelson, 1997; Diamond, 1985), the basking shark is an obligate ram filter feeder. But exactly how the particulate prey is filtered remains unresolved. It has been assumed that the erect gill rakers filter particulate matter of a suitable size from the passive water flow directly, that is, like a mechanical filter (Kunzlik, 1988; Matthews and Parker, 1950; for review see Gerking, 1991). Apparently, when the mouth closes the rakers collapse on the gill arches and deposit zooplankton onto mucus that is produced in vast quantities by cells at their base (Matthews and Parker, 1950). However, the gill rakers are very thin, stiff bristles so it is not easy to see how these function to retain plankton on their surfaces, because zooplankton are similarly of small diameter and unlikely to adhere to them as the rakers contain no mucus-producing cells. It seems reasonable to assume that the small gap between the rakers (the inter-raker distance), which is about 0.8 mm in adults, could prevent particulate prey from passing through. However, basking sharks only swallow plankton every 30–60 s (Hallacher, 1977; D.W. Sims, unpublished observations) so it remains unclear how plankton is retained and trapped in position without loss for this length of time before swallowing, especially given the relatively fast swim speeds this species uses (
1 m s1) (Sims, 2000a). A recent study of filter-feeding in small-bodied teleost fish suggests instead that rakers function as a crossflow

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filter (Sanderson et al., 2001). Particles are not retained on rakers but are concentrated in the oral cavity towards the oesophagus as water exits between the rakers. Apparently the crossflow prevents particles from clogging the gaps between the rakers (Sanderson et al., 2001). Further study of the fluid dynamics in basking shark models may elucidate a similar system. Recent experimental work on the fluid dynamics of whale shark filter feeding appears to support crossflow filtration as the likely mechanism for extracting zooplankton (P. Motta, personal communication). Even though the actual mechanics of filter-feeding in basking sharks remains unknown, the prey captured by them has been recorded for several specimens. Post mortem studies on basking shark stomachs show that off Scotland calanoid copepods were generally the predominant prey group (Matthews and Parker, 1950; Watkins, 1958). Matthews and Parker (1950) found Calanus and other copepods, in addition to fish eggs, cirripede and decapod larvae. Records of the copepods Oithona, Calanus and Pseudocalanus have also been made from basking shark stomachs (Matthews and Parker, 1950). The main zooplankton species identified from shark-feeding paths in the English Channel off Plymouth were Calanus helgolandicus, Pseudocalanus elongatus, Temora longicornis, Centropages typicus and Acartia clausi (Sims and Merrett, 1997; Fig. 3.6). The density of total zooplankton counted from samples taken in shark-feeding areas was about 2320 m3 (Sims, 1999).

Figure 3.6 Basking sharks filter feed on dense assemblages of large zooplankton, principally comprising the calanoid copepod Calanus (shown centre), but also, for example, other copepods, crab zoea and fish larvae (all pictured). This photograph is of a partial sample taken from the feeding path of a basking shark.

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The density of calanoid copepods ranged from 1050 to 1480 m3 with C. helgolandicus of 2 mm mean length making up about 70% of this total by number (Sims and Merrett, 1997). Mysid larvae, decapod larvae, chaetognaths, larvaceans, polychaetes, cladocerans, fish larvae and post-larvae, and fish eggs were also recorded (Sims and Merrett, 1997). Calanoid copepods almost entirely dominated the stomach contents of a 3.3-m long female shark examined dead after being found tangled in nets in the English Channel (D.W. Sims, unpublished observations). However, in other regions basking sharks can utilise larger zooplankton prey. The stomach contents of an 8.1-m long basking shark off the east coast of Japan was found to contain only specimens of the pelagic shrimp Sergestes similis, which had been preyed upon by the shark at a depth below 100 m at night (Mutoh and Omori, 1978). The shrimps in the shark’s stomach ranged in body length from 40 to 54 mm. The length–frequency distribution for shrimps taken by the shark were similar to that sampled using trawl nets (Mutoh and Omori, 1978). The cardiac stomach contents of a large basking shark have been found to weigh over 0.5 tonnes, of which only 30% was organic matter (Matthews and Parker, 1950). The rates of gastro-intestinal evacuation in basking sharks are unknown; however, filtration rates have been estimated using measurements of swimming speed and mouth gape area. Using a swimming speed of 1.03 m s1 for a 7 m shark with a mouth gape area of 0.4 m2, a maximum filtration rate of 1484 m3 h1 was estimated (Parker and Boeseman, 1954). This estimate has perpetuated in the literature and popular accounts since, however, it fails to take into account the inefficiencies associated with filter-feeding, namely buccal flow velocity cannot be assumed to equal forward swimming velocity, and swallowing (prey handling) time was not considered. A more recent study in the Western English Channel measured the swimming speeds of 4.0–6.5-m long basking sharks accurately and found that they filter feed at speeds some 24% slower than when cruise swimming with the mouth closed (Sims, 2000a). Basking sharks were observed filter feeding at a mean speed of 0.85 m s1 ( 0.05 S.E.) and larger 9-m long sharks apparently do not swim appreciably faster (Harden-Jones, 1973). Therefore, using these recent measurements, a more accurate seawater filtration rate for a 7 m basking shark (mouth gape area ca. 0.4 m2) swimming at a speed of 0.85 m s1 was calculated to be 881 m3 h1, allowing for an observed swallowing (prey handling) time of 6 s min1 (Hallacher, 1977) and assuming the actual buccal flow velocity to be 80% of the forward swimming velocity (Sanderson et al., 1994). This suggests basking sharks filter seawater for food at a rate some 41% lower than previously thought. Using these estimates, it is possible to approximate what quantity of zooplankton a 5–7 m long basking shark might consume in a day. Multiplying the water filtration rate of 881 m3 h1 by the median zooplankton

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biomass value sampled from shark feeding paths (median 1.45 g m3, n = 60 samples; Sims and Merrett, 1997) indicate that if basking sharks feed constantly in food patches they may consume about 30.7 kg d1.

4.4. Behaviour 4.4.1. Foraging In U.K. waters where most research on basking shark foraging behaviour has been conducted, they are most frequently seen along the north, west and south-west coasts of Britain feeding at the waters’ surface during summer months (Berrow and Heardman, 1994; Sims et al., 1997). In the north-west and north-east Atlantic, surface foraging occurs from around April to October usually with a peak in sightings from May until August (Berrow and Heardman, 1994; Kenney et al., 1985; Southall et al., 2005). The seasonal increase in the surface sightings of basking sharks in British waters during May and early June coincides with increased zooplankton abundance at this time (Sims, 1999; Sims et al., 1997; Southall et al., 2005). Similarly, observations of surface-feeding basking sharks in Clayoquot Sound, British Columbia, were coincident with the season of highest plankton productivity in the region (Darling and Keogh, 1994). In contrast, basking sharks in the north-east Pacific off the central and southern California coast have been observed at the surface from October to May, with peaks in October and March (Squire, 1990). Surfacing behaviour in this particular region, therefore, occurred both well before and after the June peak in phytoplankton abundance (Squire, 1990). Further studies are required to establish the timing of surface behaviours with respect to seasonal trends in zooplankton abundance as relationships appear to differ between geographic regions. Some progress has been made recently, but data from broader spatial scales over many years need to be analysed in detail with appropriate statistical methods (Cotton et al., 2005). However, the general pattern appears to be that foraging is focused in productive continental shelf and shelf-edge habitats broadly coinciding with seasonal increases in zooplankton abundance (see Section 4.4.4). Basking sharks observed at the surface in summer feed almost continuously, and frequently occur in large aggregations. In the Western English Channel, groups numbering between 3 and 12 individuals have been closely tracked (Sims and Quayle, 1998; Sims et al., 1997). For example, over a period of a few days, 25 different individuals were observed within a relatively small area (200  200 m) consistent with the limits of a highdensity zooplankton patch (Sims, 1999). Aggregations of apparently up to 200–400 individuals have been reported from U.K. regions such as southwest England and north-west Scotland (Doyle et al., 2005). There does not appear to be any social organisation within these feeding groups, except perhaps courtship behaviour (see Section 4.4.3). Basking sharks are

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primarily solitary, but their propensity to exhibit prolonged feeding behaviour in specific areas probably results in the formation of feeding aggregations. These have been shown to occur most often near oceanographic or topographic features (Sims and Quayle, 1998). A tagged basking shark tracked by Argos satellites was shown to remain close to a thermal boundary, or front, between two water masses of different temperature in the Clyde Sea, Scotland (Priede, 1984). There have been similar sightings of basking sharks feeding close to frontal features in the western Atlantic (e.g., Choy and Adams, 1995). 4.4.2. Front-located foraging A thermal front is a region characterised by a larger-than-average horizontal gradient in water temperature, which forms a boundary among warm, stratified and cold, mixed waters (Le Fe`vre, 1986; Fig. 3.7). Fronts can be formed by changes in tidal current speed as a function of depth, by underwater topographical features that deflect currents to the surface, or by internal waves near shelf edges (Le Fe`vre, 1986; Wolanski and Hamner, 1988). Fronts have biological significance because they are often associated with enhanced primary and secondary production (plankton). This may be due to the favourable conditions presented by nutrients diffusing from cold, mixed water into warmer water that can confer higher rates of growth, or by aggregation of particulate plankton at these boundaries due to complex upwelling and downwelling currents (Le Fe`vre, 1986). Fronts are of significance to marine vertebrates generally (Wolanski and Hamner, 1988), and