Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-20T17:32:11.213Z Has data issue: false hasContentIssue false

Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem?

Published online by Cambridge University Press:  13 July 2007

David Ainley*
Affiliation:
H.T. Harvey & Associates, 3150 Almaden Expressway, San Jose, CA 95118, USA
Grant Ballard
Affiliation:
PRBO Conservation Science, Bolinas CA 94924USA; and Ecology, Evolution, and Behaviour, School of Biological Sciences, University of Auckland, New Zealand
Steve Ackley
Affiliation:
Civil & Environmental Engineering, Clarkson University, Potsdam, NY 13699, USA
Louise K. Blight
Affiliation:
Aquatic Ecosystems Research Laboratory, University of British Columbia, 2202 Main Mall, Vancouver, BC V6T 1Z4, Canada
Joseph T. Eastman
Affiliation:
Biomedical Sciences, Ohio University, Athens, OH 45701, USA
Steven D. Emslie
Affiliation:
Biology and Marine Biology, University of North Carolina, Wilmington, NC 28403, USA
Amélie Lescroël
Affiliation:
H.T. Harvey & Associates, 3150 Almaden Expressway, San Jose, CA 95118, USA
Silvia Olmastroni
Affiliation:
Dipartimento Scienze Ambientali, Università di Siena, Via Mattioli 4 53100 Siena, Italy
Susan E. Townsend
Affiliation:
709 56th Street, Oakland, CA 94609, USA
Cynthia T. Tynan
Affiliation:
PO Box 438, West Falmouth, MA 02574, USA
Peter Wilson
Affiliation:
17 Modena Crescent, Auckland, New Zealand
Eric Woehler
Affiliation:
School of Zoology, University of Tasmania, Sandy Bay, TAS 7000, Australia

Abstract

Investigations in recent years of the ecological structure and processes of the Southern Ocean have almost exclusively taken a bottom-up, forcing-by-physical-processes approach relating various species' population trends to climate change. Just 20 years ago, however, researchers focused on a broader set of hypotheses, in part formed around a paradigm positing interspecific interactions as central to structuring the ecosystem (forcing by biotic processes, top-down), and particularly on a “krill surplus” caused by the removal from the system of more than a million baleen whales. Since then, this latter idea has disappeared from favour with little debate. Moreover, it recently has been shown that concurrent with whaling there was a massive depletion of finfish in the Southern Ocean, a finding also ignored in deference to climate-related explanations of ecosystem change. We present two examples from the literature, one involving gelatinous organisms and the other involving penguins, in which climate has been used to explain species' population trends but which could better be explained by including species interactions in the modelling. We conclude by questioning the almost complete shift in paradigms that has occurred and discuss whether it is leading Southern Ocean marine ecological science in an instructive direction.

Type
Opinion
Copyright
Copyright © Antarctic Science Ltd 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

“New opinions are always suspected, and usually opposed, without any other reason but because they are not already common.” John Locke (1690), “An Enquiry Concerning Human Understanding”

References

Ackley, S., Wadhams, P., Comiso, J.C. & Worby, A.P. 2003. Decadal decrease of Antarctic sea ice extent inferred from whaling records revisited on the basis of historical and modern sea ice records. Polar Research, 22, 1925.CrossRefGoogle Scholar
Ainley, D.G. 2002a. The Adélie penguin: bellwether of climate change. New York: Columbia University Press, 310 pp.CrossRefGoogle Scholar
Ainley, D.G. 2002b. The Ross Sea, Antarctica: where all ecosystem processes still remain for study. CCAMLR Document WG-EMM 02/60. Hobart, Australia.Google Scholar
Ainley, D.G., Clarke, E.D., Arrigo, K., Fraser, W.R., Kato, A., Barton, K.J. & Wilson, P.R. 2005. Decadal-scale changes in the climate and biota of the Pacific sector of the Southern Ocean, 1950s to the 1990s. Antarctic Science, 17, 171182.CrossRefGoogle Scholar
Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature, 432, 100103.CrossRefGoogle ScholarPubMed
Ballance, L., Pitman, R.L., Hewitt, R.P., Siniff, D.B., Trivelpiece, W.Z., Clapham, P.J. & Brownell, R.L. Jr 2006. The removal of large whales from the Southern Ocean: evidence for long-term ecosystem effects? In Estes, J.A., Demaster, D.P., Doak, D.F., Williams, T.E. &Brownell, R.L. Jreds. Whales, whaling and ocean ecosystems. Berkeley, CA: University of California Press, 215230.Google Scholar
Barbraud, C. & Weimerskirch, H. 2001. Emperor penguins and climate change. Nature, 411, 183186.Google Scholar
Barbraud, C. & Weimerskirch, H. 2006. Antarctic birds breed later in response to climate change. Proceedings of the National Academy of Science, 103, 62486251.Google Scholar
Barrera-Oro, E. 2003. Analysis of dietary overlap in Antarctic fish (Notothenioidei) from the South Shetland Islands: no evidence of food competition. Polar Biology, 26, 631637.Google Scholar
Barrera-Oro, E.R., Casaux, R.J. & Marschoff, E.R. 2005. Dietary composition of juvenile Dissostichus eleginoides (Pisces, Nototheniidae) around Shag Rocks and South Georgia, Antarctica. Polar Biology, 28, 637641.Google Scholar
Beddington, J.R. & May, R.M. 1982. The harvesting of interacting species in a natural ecosystem. Scientific American, November 1982, 6269.Google Scholar
Bengtson, J.L. & Laws, P.M. 1985. Trends in crabeater seal age at maturity: an insight into Antarctic marine interactions. In Siegfried, W.R., Condy, P.R. & Laws, R.M., eds. Antarctic nutrient cycles and food webs. Berlin: Springer, 669675.CrossRefGoogle Scholar
Best, P.B. 1993. Increase rates in severely depleted stocks of baleen whales. ICES Journal of Marine Science, 50, 169186.CrossRefGoogle Scholar
Branch, T.A. & Williams, T.M. 2006. Legacy of industrial whaling: could killer whales be responsible for declines of sea lions, elephant seals, and minke whales in the Southern Hemisphere? In Estes, J.A., Demaster, D.P., Doak, D.F., Williams, T.E. & Brownell, R.L. Jreds. Whales, whaling and ocean ecosystems. Berkeley, CA: University of California Press, 262278.Google Scholar
Branch, T.A., Matsuoka, K. & Miyashita, T. 2004. Evidence for increases in Antarctic blue whales based on Bayesian modelling. Marine Mammal Science, 20, 726–654.CrossRefGoogle Scholar
Brierley, A.S., Axelsen, B.E., Buecher, E., Sparks, C.A.J., Boyer, H. & Gibbons, M.J. 2001. Acoustic observations of jellyfish in the Namibian Benguela. Marine Ecology Progress Series, 210, 5566.CrossRefGoogle Scholar
Brodeur, R.D., Sugisaki, H. & Hunt, G.L. Jr 2002. Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Marine Ecology Progress Series, 233, 89103.CrossRefGoogle Scholar
Brown, M.R. & Brownell, R.L. 2001. Review of catches of great whales taken in the proposed South Pacific sanctuary region. International Whaling Commission SC, 110.Google Scholar
Bushula, T., Pakhomov, E.A., Kaehler, S., Davis, S. & Kalin, R.M. 2005. Diet and daily ration of two nototheniid fish on the shelf of the sub-Antarctic Prince Edward Islands. Polar Biology, 28, 585593.CrossRefGoogle Scholar
Casaux, R.J., Mazzotta, A.S. & Barrera-Oro, E.R. 1990. Seasonal aspects of the biology and diet of nearshore nototheniid fish at Potter Cove, South Shetland Islands, Antarctica. Polar Biology, 11, 6372.CrossRefGoogle Scholar
Carpenter, S.R. & Kitchell, J.F. 1988. Consumer control of lake productivity. BioScience, 38, 764769.CrossRefGoogle Scholar
Clapham, P.J. & Baker, C.S. 2001. How many whales were killed in the Southern Hemisphere in the 20th century? Report of the International Whaling Commission, 53, 3 pp.Google Scholar
Condy, P.R., Van Aarde, R.J. & Bester, M.N. 1978. The seasonal occurrence and behaviour of killer whales (Orcinus orca) at Marion Island. Journal of Zoology, 184, 449464.CrossRefGoogle Scholar
Croxall, J.P. 1992. Southern Ocean environmental changes: effects on seabird, seal, and whale populations. Philosophical Transactions of the Royal Society, B338, 319328.Google Scholar
Croxall, J.P., Trathan, P.N. & Murphy, E.J. 2002. Environmental change and Antarctic seabird populations. Science, 297, 15101514.Google Scholar
Curran, M.A.J., Van Ommen, T.D., Morgan, V.I., Phillips, K.L. & Palmer, A.S. 2003. Ice core evidence for sea ice decline since the 1950s. Science, 302, 12031206.Google Scholar
De La Mare, W.K. 1997. Abrupt mid-twentieth century decline in Antarctic sea ice extent from whaling records. Nature, 389, 5760.Google Scholar
Dunlap, R.T. 2006. Why does history matter in ecology. Ecology, 87, 1339.Google Scholar
El-Sayed, S. 1994. Southern Ocean ecology: the BIOMASS perspective. Cambridge: Cambridge University Press, 399 pp.Google Scholar
Emslie, S.E. & McDaniel, J.D. 2002. Adélie penguin diet and climate change during the middle to late Holocene in northern Marguerite Bay, Antarctic Peninsula. Polar Biology, 25, 222229.CrossRefGoogle Scholar
Forcada, J., Trathan, P.N., Reid, K., Murphy, E.J. & Croxall, J.P. 2006. Contrasting population changes in sympatric penguin species in association with climate warming. Global Change Biology, 12, 411423.Google Scholar
Frank, K.T., Petrie, B., Choi, J.S. & Leggett, W.C. 2005. Trophic cascades in a formerly cod-dominated ecosystem. Science, 308, 16211623.CrossRefGoogle Scholar
Fraser, W.R. & Patterson, D.L. 1997. Human disturbance and long-term changes in Adélie penguin populations: a natural experiment at Palmer Station, Antarctica. In Bataglia, B., Valencia, J. & Walton, D.W.H., eds. Antarctic communities: species, structure and survival. Cambridge: Cambridge University Press, 445452.Google Scholar
Fraser, W.R. & Hofmann, E.E. 2003. A predator's perspective on causal links between climate change, physical forcing and ecosystem response. Marine Ecology Progress Series, 265, 115.Google Scholar
Fraser, W.R., Trivelpiece, W.Z., Ainley, D.G. & Trivelpiece, S.G. 1992. Increases in Antarctic penguin populations: reduced competition with whales or a loss of sea ice due to environmental warming? Polar Biology, 11, 525531.CrossRefGoogle Scholar
Guinet, C. 1992. Comportement de chasse des Orques (Orcinus orca) autour des Iles Crozet. Canadian Journal of Zoology, 70, 16561667.CrossRefGoogle Scholar
Guinet, C. & Bouvier, J. 1995. Development of intentional stranding hunting techniques in killer whale (Orcinus orca) calves at Crozet Archipelago. Canadian Journal of Zoology, 73, 2733.CrossRefGoogle Scholar
Heymans, J.J., Shannon, L.J. & Jarre, A. 2004. Changes in the northern Benguela ecosystem over three decades: 1970s, 1980s, and 1990s. Ecological Modelling, 172, 175195.Google Scholar
Hilton, G.M., Thompson, D.R., Sagar, P.M., Cuthbert, R.J., Cherel, Y. & Bury, S.J. 2006. A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin Eudyptes chrysocome. Global Change Biology, 12, 611625.Google Scholar
Jackson, J.B.C. 2006. When ecological pyramids were upside down. In Estes, J.A., Demaster, D.P., Doak, D.F., Williams, T.E. & Brownell, R.L. Jreds. Whales, whaling and ocean ecosystems. Berkeley, CA: University of California Press, 2737.Google Scholar
Jacobs, S. 2006. Observations of change in the Southern Ocean. Philosophical Transactions of the Royal Society, A364, 16571681.Google Scholar
Jacobs, S.S., Guilivi, C.F. & Mele, P.A. 2002. Freshening of the Ross Sea during the late 20th century. Science, 297, 386389.Google Scholar
Jenouvrier, S., Weimerskirch, H., Barbraud, C., Park, Y.-H. & Cazelles, B. 2004. Evidence of a shift in the cyclicity of Antarctic seabird dynamics linked to climate. Proceedings of the Royal Society, B272, 887895.Google Scholar
Jenouvrier, S., Barbraud, C. & Weimerskirch, H. 2005. Long-term contrasted responses to climate of two Antarctic seabird species. Ecology, 86, 28892903.Google Scholar
Kawachuchi, S.O., Kasamatsu, N., Watanabe, S., Odate, T., Fukuchi, M. & Nicol, S. 2005. Sea ice changes inferred from methanesulphonic acid (MSA) variation in East Antarctic ice cores: are krill responsible? Antarctic Science, 17, 211212.Google Scholar
Kasamatsu, N., Kawaguchi, S., Watanabe, S., Odate, T. & Fukuchi, M. 2004. Possible impacts of zooplankton grazing on dimethylsulfide production in the Antarctic Ocean. Canadian Journal of Fisheries and Aquatic Sciences, 61, 736743.Google Scholar
Kock, K.-H. & Everson, I. 1997. Biology and ecology of mackerel icefish, Champsocephalus gunnari: an Antarctic fish lacking hemoglobin. Comparative Biochemistry and Physiology, 118A, 10671077.Google Scholar
Kuhn, T.S. 1962. The structure of scientific revolutions. Chicago, IL: University of Chicago Press.Google Scholar
Laws, R.M. 1977. The significance of vertebrates in the Antarctic marine ecosystem. In Llano, G.A., ed. Adaptations within Antarctic ecosystems. Washington, DC: Smithsonian Institution, 411438.Google Scholar
Loeb, V., Siegel, V., Holm-Hansen, O., Hewitt, R., Fraser, W., Trivelpiece, W. & Trivelpiece, S. 1997. Effects of sea-ice extent on krill or salp dominance on the Antarctic food web. Nature, 387, 897900.Google Scholar
Lynam, C.P., Hay, S.J. & Brierley, A.S. 2005. Jellyfish abundance and climatic variation: contrasting responses in oceanographically distinct regions of the North Sea, and possible implications for fisheries. Journal of the Marine Biological Association of the United Kingdom, 85, 435450.Google Scholar
Lynam, C., Gibbons, M., Axelsen, B., Sparks, C., Coetzee, J., Heywood, B. & Brierley, A. 2006. Jellyfish overtake fish in a heavily fished ecosystem. Current Biology, 16, R492R493.Google Scholar
Lynnes, A.S., Reid, K., Croxall, J.P. & Trathan, P.N. 2002. Conflict or co-existence? Foraging distribution and competition for prey between Adélie and chinstrap penguins. Marine Biology, 141, 11651174.Google Scholar
McMahon, C.R., Bester, M.N., Burton, H.R., Hindell, M.A. & Bradshaw, C.J.A. 2005. Population status, trends and a re-examination of the hypotheses explaining the recent declines of the southern elephant seal Mirounga leonina. Mammal Review, 35, 82100.Google Scholar
Mikhalev, Y.A., Ivahim, M.H., Savusin, V.P. & Zelenaya, F.E. 1981. The distribution and biology of Killer whales in the Southern Hemisphere. Reports of the International Whaling Commission, 31, 551566.Google Scholar
Mills, C.E. 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia, 451, 5568.Google Scholar
Mills, L.S., Soulé, M.E. & Doak, D.F. 1993. The keystone-species concept in ecology and conservation. BioScience, 43, 219224.Google Scholar
Mitchell, B. & Sandbrook, R. 1980. The Management of the Southern Ocean. London: International Institute for Environment and Development, 162 pp.Google Scholar
Murphy, E.J. 1995. Spatial structure of the Southern Ocean ecosystem: predator-prey linkages in Southern Ocean food webs. Journal of Animal Ecology, 64, 333347.Google Scholar
Myers, R.A. & Worm, B. 2003. Rapid worldwide depletion of predatory fish communities. Nature, 423, 280283.CrossRefGoogle ScholarPubMed
Nicol, S. 2005. Krill, currents, and sea ice: Euphausia superba and its changing environment. BioScience, 56, 11120.Google Scholar
Nicol, S., Pauly, T., Bindoff, N.L., Wright, S., Thiele, D., Hosie, G.W., Strutton, P.G. & Woehler, E. 2000. Ocean circulation off east Antarctica affects ecosystem structure and ice extent. Nature, 406, 504507.Google Scholar
NSF. 1998. (OEUVRE Ocean Ecology: Understanding and Vision for Research). Workshop Report (www.joss.ucar.edu/joss_psg/project/oce_workshop/oeuvre/report).Google Scholar
Pakhomov, E.A. 1997. Feeding and exploitation of the food supply by demersal fishes in the Antarctic part of the Indian Ocean. Journal of Ichthyology, 37, 360380.Google Scholar
Pakhomov, E.A. & Pankratov, S.A. 1992. Feeding of juvenile notothenioid fishes of the Indian Ocean sector of the Antarctic. Journal of Ichthyology, 32, 2837.Google Scholar
Parkinson, C.L. 2002. Trends in the length of the Southern Ocean sea ice season, 1979–99. Annals of Glaciology, 34, 435440.CrossRefGoogle Scholar
Pauly, D., Christiansen, V., Dalsgaard, J., Froeser, R. & Torres, F. Jr 1998. Fishing down marine food webs. Science, 279, 860863.Google Scholar
Pauly, D. & Maclean, J. 2003. In a perfect ocean: the state of fisheries and ecosystems in the North Atlantic Ocean. Washington, DC: Island Press, 175 pp.Google Scholar
Pauly, D., Watson, R. & Alder, J. 2005. Global trends in world fisheries: impacts on marine ecosystems and food security. Philosophical Transactions of the Royal Society, B360, 512.CrossRefGoogle Scholar
Payne, M.R. 1977. Growth of a fur seal population. Philosophical Transactions of the Royal Society, B279, 6779.Google Scholar
Pitman, R.L. & Ensor, P. 2003. Three forms of killer whales in Antarctic waters. Journal of Cetacean Research and Management, 5, 19.Google Scholar
Post, D.M., Conners, M.E. & Goldberg, D.S. 2000. Prey preference by a top predator and the stability of linked food chains. Ecology, 81, 814.Google Scholar
Prévost, J. 1961. Ecologie du manchot empereur, Aptenodytes forsteri. Expéditions Polaires Françaises, Publication no. 222. Paris: Hermann, 206 pp.Google Scholar
Priddle, J. 1992. Antarctic whales and seals. Cambridge: British Antarctic Survey, 17 pp.Google Scholar
Reid, K. & Croxall, J.P. 2001. Environmental response of upper trophic level predators reveals a system change in an Antarctic marine ecosystem. Proceedings of the Royal Society, B268, 377384.Google Scholar
Scheffer, M., Carpenter, S. & De Young, B. 2005. Cascading effects of overfishing marine systems. Trends in Ecology and Evolution, 20, 579581.Google Scholar
Schindler, D.E., Essington, T.E., Kitchell, J.F., Boggs, C. & Hilborn, R. 2002. Sharks and tunas: fisheries impacts on predators with contrasting life histories. Ecological Applications, 12, 735748.Google Scholar
Siegel, V. 2005. Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biology, 29, 122.Google Scholar
Smetacek, V. & Nicol, S. 2005. Polar ocean ecosystems in a changing world. Nature, 437, 367368.Google Scholar
Soulé, M.E., Estes, J.A., Miller, B. & Honnold, D.L. 2005. Strongly interacting species: conservation policy, management, and ethics. BioScience, 55, 168176.CrossRefGoogle Scholar
Smith, R.C., Domack, E., Emslie, S., Fraser, W., Ainley, D.G., Baker, K., Kennett, J., Leventer, A., Stammerjohn, S., Mosley-Thompson, E. & Vernet, M. 1999. Marine ecosystem sensitivity to climate change. BioScience, 49, 393404.Google Scholar
Springer, A.M., Estes, J.A., Van Vliet, G.B., Williams, T.M., Doak, D.F., Danner, E.M., Forney, K.A. & Pfister, B. 2003. Sequential megafaunal collapse in the North Pacific Ocean: an ongoing legacy of industrial whaling? Proceedings of the National Academy of Sciences, 100, 12223–12 228.CrossRefGoogle ScholarPubMed
Taylor, R.H. & Wilson, P.R. 1990. Recent increase and southern expansion of Adélie penguin populations in the Ross Sea, Antarctica, related to climate warming. New Zealand Journal of Ecology, 14, 2529.Google Scholar
Terborgh, J., Feeley, K., Silman, M., Nuňez, P. & Balukjian, B. 2006. Vegetation dynamics of predator-free land bridge islands. Journal of Ecology, 94, 253263.Google Scholar
Xian, W., Kang, B. & Liu, R. 2005. Jellyfish blooms in the Yangtze Estuary. Science, 307, 41.Google Scholar
Verity, P.G. & Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series, 130, 277293.Google Scholar
Weimerskirch, H., Inchausti, P., Guinet, C. & Barbraud, C. 2003. Trends in bird and seal populations as indicators of a system shift in the Southern Ocean. Antarctic Science, 15, 249256.Google Scholar
Williams, T.M., Estes, J.A., Doak, D.F. & Springer, A.M. 2004. Killer appetites: assessing the role of predators in ecological communities. Ecology, 85, 33733384.Google Scholar
Wilmers, C.C. & Getz, W.M. 2005. Gray wolves as climate change buffers in Yellowstone. PLoS Biology, 3, 15.Google Scholar
Wilmers, C.C., Sinha, S. & Brede, M. 2002. Examining the effects of species richness on community stability: an assembly model approach. Oikos, 99, 363367.Google Scholar
Wilson, P.R., Ainley, D.G., Nur, N., Jacobs, S.S., Barton, K.J., Ballard, G. & Comiso, J.C. 2001. Adélie penguin population change in the Pacific sector of Antarctica: relation to sea-ice extent and the Antarctic Circumpolar Current. Marine Ecology Progress Series, 213, 301309.CrossRefGoogle Scholar
Woehler, E.J., Cooper, J., Croxall, J.P., Fraser, W.R., Kooyman, G.L., Miller, G.D., Nel, D.C., Patterson, D.L., Peter, H.-U., Ribic, C.A., Salwick, K., Trivelpiece, W.R. & Weirmirskirch, H. 2001. A statistical assessment of the status and trends of Antarctic and Subantarctic seabirds. Cambridge: SCAR, 45 pp.Google Scholar
Zwally, H.J., Comiso, J.C., Parkinson, C.L., Cavalieri, D.J. & Gloersen, P. 2002. Variability of Antarctic sea ice 1979–1998. Journal of Geophysical Research, 107, doi: 10.1029/2000JC000733.CrossRefGoogle Scholar