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:
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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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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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Bridget S. Green
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