Skip to main content Accessibility help
×
Home

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

  • David Ainley (a1), Grant Ballard (a2), Steve Ackley (a3), Louise K. Blight (a4), Joseph T. Eastman (a5), Steven D. Emslie (a6), Amélie Lescroël (a1), Silvia Olmastroni (a7), Susan E. Townsend (a8), Cynthia T. Tynan (a9), Peter Wilson (a10) and Eric Woehler (a11)...

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.

Copyright

Corresponding author

Footnotes

Hide All

“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”

Footnotes

References

Hide All
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.
Ainley, D.G. 2002a. The Adélie penguin: bellwether of climate change. New York: Columbia University Press, 310 pp.
Ainley, D.G. 2002b. The Ross Sea, Antarctica: where all ecosystem processes still remain for study. CCAMLR Document WG-EMM 02/60. Hobart, Australia.
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.
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.
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.
Barbraud, C. & Weimerskirch, H. 2001. Emperor penguins and climate change. Nature, 411, 183186.
Barbraud, C. & Weimerskirch, H. 2006. Antarctic birds breed later in response to climate change. Proceedings of the National Academy of Science, 103, 62486251.
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.
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.
Beddington, J.R. & May, R.M. 1982. The harvesting of interacting species in a natural ecosystem. Scientific American, November 1982, 6269.
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.
Best, P.B. 1993. Increase rates in severely depleted stocks of baleen whales. ICES Journal of Marine Science, 50, 169186.
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.
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.
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.
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.
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.
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.
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.
Carpenter, S.R. & Kitchell, J.F. 1988. Consumer control of lake productivity. BioScience, 38, 764769.
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.
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.
Croxall, J.P. 1992. Southern Ocean environmental changes: effects on seabird, seal, and whale populations. Philosophical Transactions of the Royal Society, B338, 319328.
Croxall, J.P., Trathan, P.N. & Murphy, E.J. 2002. Environmental change and Antarctic seabird populations. Science, 297, 15101514.
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.
De La Mare, W.K. 1997. Abrupt mid-twentieth century decline in Antarctic sea ice extent from whaling records. Nature, 389, 5760.
Dunlap, R.T. 2006. Why does history matter in ecology. Ecology, 87, 1339.
El-Sayed, S. 1994. Southern Ocean ecology: the BIOMASS perspective. Cambridge: Cambridge University Press, 399 pp.
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.
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.
Frank, K.T., Petrie, B., Choi, J.S. & Leggett, W.C. 2005. Trophic cascades in a formerly cod-dominated ecosystem. Science, 308, 16211623.
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.
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.
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.
Guinet, C. 1992. Comportement de chasse des Orques (Orcinus orca) autour des Iles Crozet. Canadian Journal of Zoology, 70, 16561667.
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.
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.
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.
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.
Jacobs, S. 2006. Observations of change in the Southern Ocean. Philosophical Transactions of the Royal Society, A364, 16571681.
Jacobs, S.S., Guilivi, C.F. & Mele, P.A. 2002. Freshening of the Ross Sea during the late 20th century. Science, 297, 386389.
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.
Jenouvrier, S., Barbraud, C. & Weimerskirch, H. 2005. Long-term contrasted responses to climate of two Antarctic seabird species. Ecology, 86, 28892903.
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.
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.
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.
Kuhn, T.S. 1962. The structure of scientific revolutions. Chicago, IL: University of Chicago Press.
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.
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.
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.
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.
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.
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.
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.
Mills, C.E. 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia, 451, 5568.
Mills, L.S., Soulé, M.E. & Doak, D.F. 1993. The keystone-species concept in ecology and conservation. BioScience, 43, 219224.
Mitchell, B. & Sandbrook, R. 1980. The Management of the Southern Ocean. London: International Institute for Environment and Development, 162 pp.
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.
Myers, R.A. & Worm, B. 2003. Rapid worldwide depletion of predatory fish communities. Nature, 423, 280283.
Nicol, S. 2005. Krill, currents, and sea ice: Euphausia superba and its changing environment. BioScience, 56, 11120.
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.
NSF. 1998. (OEUVRE Ocean Ecology: Understanding and Vision for Research). Workshop Report (www.joss.ucar.edu/joss_psg/project/oce_workshop/oeuvre/report).
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.
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.
Parkinson, C.L. 2002. Trends in the length of the Southern Ocean sea ice season, 1979–99. Annals of Glaciology, 34, 435440.
Pauly, D., Christiansen, V., Dalsgaard, J., Froeser, R. & Torres, F. Jr 1998. Fishing down marine food webs. Science, 279, 860863.
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.
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.
Payne, M.R. 1977. Growth of a fur seal population. Philosophical Transactions of the Royal Society, B279, 6779.
Pitman, R.L. & Ensor, P. 2003. Three forms of killer whales in Antarctic waters. Journal of Cetacean Research and Management, 5, 19.
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.
Prévost, J. 1961. Ecologie du manchot empereur, Aptenodytes forsteri. Expéditions Polaires Françaises, Publication no. 222. Paris: Hermann, 206 pp.
Priddle, J. 1992. Antarctic whales and seals. Cambridge: British Antarctic Survey, 17 pp.
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.
Scheffer, M., Carpenter, S. & De Young, B. 2005. Cascading effects of overfishing marine systems. Trends in Ecology and Evolution, 20, 579581.
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.
Siegel, V. 2005. Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biology, 29, 122.
Smetacek, V. & Nicol, S. 2005. Polar ocean ecosystems in a changing world. Nature, 437, 367368.
Soulé, M.E., Estes, J.A., Miller, B. & Honnold, D.L. 2005. Strongly interacting species: conservation policy, management, and ethics. BioScience, 55, 168176.
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.
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.
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.
Terborgh, J., Feeley, K., Silman, M., Nuňez, P. & Balukjian, B. 2006. Vegetation dynamics of predator-free land bridge islands. Journal of Ecology, 94, 253263.
Xian, W., Kang, B. & Liu, R. 2005. Jellyfish blooms in the Yangtze Estuary. Science, 307, 41.
Verity, P.G. & Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series, 130, 277293.
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.
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.
Wilmers, C.C. & Getz, W.M. 2005. Gray wolves as climate change buffers in Yellowstone. PLoS Biology, 3, 15.
Wilmers, C.C., Sinha, S. & Brede, M. 2002. Examining the effects of species richness on community stability: an assembly model approach. Oikos, 99, 363367.
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.
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.
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.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed