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  • Print publication year: 2015
  • Online publication date: May 2015

2 - The spatio-temporal dynamics of trophic control in large marine ecosystems

from Part II - Ecosystems



The ways in which productivity, stability, population interactions, and community structure are regulated in ecosystems have been a central focus of ecology for over a century. At large spatial scales, major insights into these dynamics have been principally derived from analyses of changes induced from hunting, harvesting, and agricultural practices – so-called “natural experiments.” In terrestrial ecosystems estimates of the fraction of land transformed or degraded by human activity fall within the range of 39 to 75% (Vitousek et al., 1997; Ellis et al., 2010). Equally profound is the reality that up to 75% of the global oceans and in particular the continental shelf, transitional slope water areas, and reef habitats have been strongly impacted by human activity (Halpern et al., 2008).

One of the most widely studied human impacts has been the over-exploitation of large-bodied species. Berger et al. (2001) estimated that the spatial distribution of large mammalian carnivores that once played a dominant role in terrestrial ecosystems has declined by 95–99%. In the global oceans large predatory fish biomass may be as low as 10% of pre-industrial levels (Myers and Worm, 2003). These changes have created a vertical compaction and blunting of the trophic pyramid (Duffy, 2003; Chapter 14, this volume). On a global scale, these losses are attributable to a positive association between body size and sensitivity to population declines experienced by larger species which exhibit a greater susceptibility to decline or collapse as a consequence of their lower population densities, greater times to maturity, lower clutch sizes, and larger home ranges (Schipper et al., 2008). This reduction in the abundance of apex predators has led to abnormally high densities of their former prey in a wide range of ecosystems, which has, in turn, resulted in sometimes catastrophic changes in the ecosystems occupied. This has led some to conclude that large-bodied species are essential to the maintenance of ecosystem structure and stability (Hildrew et al., 2007; Estes et al., 2011).

Anderson, S. C., Lotze, H. K. and Shackell, N. L. (2008). Evaluating the knowledge base for expanding low-trophic-level fisheries in Atlantic Canada. Canadian Journal of Fisheries and Aquatic Sciences, 65, 2553–2571.
Ayón, P., Purca, S. and Guevara-Carrasco, R. (2004). Zooplankton volume trends off Peru between 1964 and 2001. ICES Journal of Marine Science, 61, 478–484.
Bailey, D. M., Ruhl, H. A. and Snith, K. L. (2006). Long-term change in benthopelagic fish abundance in the abyssal northeast Pacific Ocean. Ecology, 87(3), 549–555.
Bakun, A., Babcock, A. and Santora, C. (2009). Regulating a complex adaptive system via its wasp-waist: grappling with ecosystem-based management of the New England herring fishery. ICES Journal of Marine Science, 66, 1768–1775.
Barange, M., Field, J. G., Harris, R. P., Hofmann, E. E. and Perry, R. I. (eds.) (2010). Marine Ecosystems and Global Change. Oxford: Oxford University Press.
Barton, A. D., Pershing, A. J., Litchman, E., et al. (2013). The biogeography of marine plankton traits. Ecology Letters, 16, 522–534.
Baum, J. K. and Worm, B. (2009). Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology, 78, 699–714.
Bax, N. J. (1998). The significance and prediction of predation in marine fisheries. ICES Journal of Marine Science, 55, 997–1030.
Benoît, H. P. and Swain, D. P. (2008). Impacts of environmental change and direct and indirect harvesting effects on the dynamics of a marine fish community. Canadian Journal of Fisheries and Aquatic Sciences, 65, 2088–2104.
Berger, J., Stacey, P. B., Bellis, L. and Johnson, M. P. (2001). A mammalian predator-prey imbalance: grizzly bear and wolf extinction affect avian neotropical migrants. Ecological Applications, 11, 947–960.
Brodeur, R. D., Suchman, C. L., Reese, D. C., Miller, T. W. and Daly, E. A. (2008). Spatial overlap and trophic interactions between pelagic fish and large jellyfish in the northern California Current. Marine Biology, 154, 649–659.
Brooks, J. L. and Dodson, S. I. (1965). Predation, body size, and composition of plankton. Science, 150, 28–35.
Bundy, A. (2005). Structure and functioning of the eastern Scotian Shelf ecosystem before and after the collapse of groundfish stocks in the early 1990s. Canadian Journal of Fisheries and Aquatic Sciences, 62(7), 1453–1473.
Caddy, J. F. and Garibaldi, L. (2000). Apparent changes in the trophic composition of world marine harvests: the perspective from the FAO capture database. Ocean & Coastal Management, 43, 615–655.
Carpenter, S. R., Kitchell, J. F. and Hodgson, J. R. (1985). Cascading trophic interactions and lake productivity. Bioscience, 35, 634–649.
Carr, M. H., Neigel, J. E., Estes, J. A., et al. (2003). Comparing marine and terrestrial ecosystems: implications for the design of coastal marine reserves. Ecological Applications, 13, S90–S107.
Casini, M., Hjelm, J., Molinero, J.-C., et al. (2009). Trophic cascades promote threshold-like shifts in pelagic marine ecosystems. Proceedings of the National Academy of Sciences of the USA, 106, 197–202.
Chassot, E., Mélin, F., Le Pape, O. and Gascuel, D. (2007). Bottom-up control regulates fisheries production at the scale of eco-regions in European seas. Marine Ecology Progress Series, 343, 45–55.
Choi, J. S., Frank, K. T., Leggett, W. C. and Drinkwater, K. (2004). Transition to an alternate state in a continental shelf ecosystem. Canadian Journal of Fisheries and Aquatic Sciences, 61, 505–510.
Christensen, V., Guenette, S., Heymans, J. J., et al. (2003). Hundred-year decline of North Atlantic predatory fishes. Fish and Fisheries, 4, 1–24.
Claireaux, G., Webber, D. M., Lagardère, J.-P. and Kerr, S. R. (2000). Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research, 44, 257–265.
Cury, P. M., Shin, Y.-J., Planque, B., et al. (2008). Ecosystem oceanography for global change in fisheries. Trends in Ecology and Evolution, 23(6), 338–346.
Daan, N., Gislason, H., Pope, J. G. and Rice, J. C. (2005). Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES Journal of Marine Science, 62, 177–188.
Darimont, C. T., Carlson, S. M., Kinnison, M. T., et al. (2009). Human predators outpace other agents of trait change in the wild. Proceedings of the National Academy of Sciences of the USA, 106, 952–954.
Daskalov, G. M., Grishin, A. N., Rodionov, S. and Mihneva, V. (2007). Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proceedings of the National Academy of Sciences of the USA, 104, 10518–10523.
deYoung, B., Heath, M., Werner, F., et al. (2004). Challenges of modelling ocean basin ecosystems. Science, 304, 1463–1466.
Doney, S. C., Ruckelshaus, M., Duffy, J. E., et al. (2012). Climate change impacts on marine ecosystems. Annual Reviews of Marine Science, 4, 11–37.
Drinkwater, K. F. (2006). The regime shift of the 1920s and 1930s in the North Atlantic. Progress in Oceanography, 68, 134–151.
Duarte, C. M., Holmer, M., Olsen, Y., et al. (2009). Will the oceans help feed humanity? BioScience, 59, 967–976.
Duffy, J. E. (2002). Biodiversity and ecosystem function: the consumer connection. Oikos, 99, 201–219.
Duffy, J. E. (2003). Biodiversity loss, trophic skew and ecosystem functioning. Ecology Letters, 6, 680–687.
Eliasen, K., Reinert, J., Gaard, E., et al. (2011). Sandeel as a link between primary production and higher trophic levels on the Faroe shelf. Marine Ecology Progress Series, 438, 185–194.
Ellis, E. C., Goldewijk, K. K., Siebert, S., Lightman, D. and Ramankutty, N. (2010). Anthropogenic transformation of the biomes, 1700 to 2000. Global Ecology and Biogeography, 19, 589–606.
Elton, C. (1927). Animal Ecology. London: Sidwick and Jackson.
Eriksson, B. K., Lunggren, L., Sandstrom, A., et al. (2009). Declines in predatory fish promote bloom-forming macroalgae. Ecological Applications, 19, 1975–1988.
Estes, J. A., Terborgh, J., Brashares, J. S., et al. (2011). Trophic downgrading of planet Earth. Science, 333, 301–306.
Fauchald, P. (2010). Predator-prey reversal: a possible mechanism for ecosystem hysteresis in the North Sea. Ecology, 91, 2191–2197.
Finenko, Z. Z., Piontkovski, S. A., Williams, R. and Mishonov, A. V. (2003). Variability of phytoplankton and mesozooplankton biomass in the subtropical and tropical Atlantic Ocean. Marine Ecology Progress Series, 250, 125–144.
Finkel, Z. V., Beardall, J., Flynn, K. J., et al. (2010). Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research, 32, 119–137.
Finni, T., Kononen, K., Olsonen, R. and Wallström, K. (2001). The history of cyanobacterial blooms in the Baltic Sea. Ambio 30, 172–178.
Fisher, J. A. D., Frank, K. T., Petrie, B., Leggett, W. C. and Shackell, N. L. (2008). Temporal dynamics within a contemporary latitudinal diversity gradient. Ecology Letters, 11, 883–897.
Fisher, J. A. D., Frank, K. T. and Leggett, W. C. (2010a). Breaking Bergmann's rule: truncation of Northwest Atlantic marine fish body sizes. Ecology, 91, 2499–2505.
Fisher, J. A. D., Frank, K. T. and Leggett, W. C. (2010b). Global variation in marine fish body size and its role in biodiversity-ecosystem functioning. Marine Ecology Progress Series, 405, 1–13.
Fogarty, M. J. and Murawski, S. A. (1998). Large-scale disturbance and the structure of marine systems: fishery impacts on Georges Bank. Ecological Applications, 8: S6–S22.
Frank, K. T., Petrie, B., Choi, J. S. and Leggett, W. C. (2005). Trophic cascades in a formerly cod-dominated ecosystem. Science, 308, 1621–1623.
Frank, K. T., Petrie, B., Shackell, N. L. and Choi, J. S. (2006). Reconciling differences in trophic control in mid-latitude marine ecosystems. Ecology Letters, 9, 1096–1105.
Frank, K. T., Petrie, B. and Shackell, N. L. (2007). The ups and downs of trophic control in continental shelf ecosystems. Trends in Ecology and Evolution, 22(5), 236–242.
Frank, K. T., Petrie, B., Fisher, J. A. D. and Leggett, W. C. (2011). Transient dynamics of an altered large marine ecosystem. Nature, 477, 86–89.
Franks, P. J. (2002). NPZ models of plankton dynamics: their construction, coupling to physics, and application. Journal of Oceanography, 58, 379–387.
Frederiksen, M., Edwards, M., Richardson, A. J., Halliday, N. C. and Wanless, S. (2006). From plankton to top predators: bottom-up control of a marine food web across four trophic levels. Journal of Animal Ecology, 75, 1259–1268.
Fréon, P., Barange, M.Arístegui, J. and McIntyre, A. D. (2009). Eastern boundary upwelling ecosystems: integrative and comparative approaches. Progress in Oceanography, 83, 1–14.
Gerber, L. R., Morissette, L. and Pauly, D. (2009). Should whales be culled to increase fishery yield? Science, 323, 880–881.
Gislason, H., Sinclair, M., Sainsbury, K. and O'Boyle, R. N. (2000). Symposium overview: incorporating ecosystem objectives within fisheries management. ICES Journal of Marine Science, 57, 468–475.
Gonzalez, A. and Loreau, M. (2009). The causes and consequences of compensatory dynamics in ecological communities. Annual Review of Ecology Evolution and Systematics, 40, 393–414.
Hairston, N. G., Smith, F. E. and Slobodkin, L. B. (1960). Community structure, population control, and competition. American Naturalist, 94, 421–425.
Halpern, B. S., Walbridge, S., Selkoe, K. A., et al. (2008). A global map of human impact on marine ecosystems. Science, 319, 948–952.
Head, E. J. H. and Sameoto, D. D. (2007). Inter-decadal variability in zooplankton and phytoplankton abundance on the Newfoundland and Scotian shelves. Deep-Sea Research II, 57, 2686–2701.
Heath, M. R., Speirs, D. C. and Steele, J. H. (2013). Understanding patterns and processes in models of trophic cascades. Ecology Letters doi:10.1111/ele.12200
Heck, K. L. Jr. and Valentine, J. F. (2007). The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts, 30, 371–381.
Hensen, V. (1887). Ueber die Bestimmung des Plankton's oder des im Meere treibenden Materials an Pflanzen und Tieren. Kommission zur wiss. Untersuchung der deutschen Meere, in Kiel, 1882–1886, Bericht 5, Vols. 12–16, pp. 1–107. Schmidt and Klaunig.
Hilborn, R. and Walters, C. J. (1992). Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty. Norwell, MA: Kluwer Academic Publishers.
Hildrew, A., Raffaelli, D. and Edmonds-Brown, R. (2007). Body Size: The Structure and Function of Aquatic Ecosystems. Cambridge, UK: Cambridge University Press.
Johannesen, E., Ingvaldsen, R. B., Bogstad, B., et al. (2012). Changes in Barents Sea ecosystem state, 1970–2009: climate fluctuations, human impact, and trophic interactions. ICES Journal of Marine Science, 69(5), 880–889.
Johnson, N. A., Campbell, J. W., Moore, T. S., et al. (2007). The relationship between the standing stock of the deep-sea macrobenthos and surface production in the western North Atlantic. Deep-Sea Research I, 54, 1350–1360.
Kemp, W. M., Boynton, W. R., Adolf, J. E., et al. (2005). Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Maine Ecology Progress Series, 303, 1–29.
Knowlton, N. (2004). Multiple stable states and the conservation of marine ecosystems. Progress in Oceanography, 60, 387–396.
Köster, F. W. and Möllmann, C. (2000). Trophodynamic control by clupeid predators on recruitment success in Baltic cod? ICES Journal of Marine Science, 57, 310–323.
Laptikhovsky, V., Arkhipkin, A. and Brickle, P. (2013). From small bycatch to main commercial species: explosion of stocks of rock cod Patagonotothen ramsayi (Regan) in the southwest Atlantic. Fisheries Research, 147, 399–403.
Legendre, L. and Michaud, J. (1998). Flux of biogenic carbon in oceans: size-dependent regulation by pelagic food webs. Marine Ecology Progress Series, 164, 1–11.
Llope, M., Licandro, P., Chan, K.-S. and Stenseth, N. C. (2012). Spatial variability of the plankton trophic interaction in the North Sea: a new feature after the early 1970s. Global Change Biology, 18, 106–117.
Lynman, C. P., Gibbons, M. J., Axelsen, B. E., et al. (2006). Jellyfish overtake fish in a heavily fished ecosystem. Current Biology, 16, R492–493.
Manning, F. (2012). The sustainable management of grey seal populations: a path toward the recovery of cod and other groundfish stocks. Report of the Standing Senate Committee on Fisheries and Oceans. 42 pp.
McCann, K. S., Rasmussen, J. B. and Umbanhowar, J. (2005). The dynamics of spatially coupled food webs. Ecology Letters, 8, 513–523.
Micheli, F. (1999). Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystem. Science, 285, 1396–1398.
Micheli, F., Benedetti-Cecchi, L., Gambaccini, S., et al. (2005). Cascading human impacts, marine protected areas, and the structure of Mediterranean reef assemblages. Ecological Monographs, 75, 81–102.
Minto, C. and Worm, B. (2012). Interactions between small pelagic fish and young cod across the North Atlantic. Ecology, 93, 2139–2154.
Möllmann, C., Müller-Karulis, B., Kornilovs, G. and St. John, M. (2008). Effects of climate and overfishing on zooplankton dynamics and ecosystem structure: regime shift, trophic cascade, and feedback loops in a simple ecosystem. ICES Journal of Marine Scence, 65, 302–310.
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. and Worm, B. (2011). How many species are there on Earth and in the ocean? PLoS Biology, 9(8), e1001127.
Myers, R. A., Mertz, G. and Fowlow, P. S. (1997). Maximum population growth rates and recovery times for Atlantic cod, Gadus morhua. Fishery Bulletin, 95, 762–772.
Myers, R. A. and Worm, B. (2003). Rapid worldwide depletion of predatory fish communities. Nature, 423, 280–283.
Myers, R. A. and Worm, B. (2005). Extinction, survival, or recovery of large predatory fish. Philosophical Transactions of the Royal Society, Series B, 360, 13–20.
Nixon, S. W. (1988). Physical energy inputs and the comparative ecology of lake and marine ecosystems. Limnology and Oceanography, 33, 1005–1025.
Österblom, H., Casini, M., Olsson, O. and Bignert, A. (2006). Fish, seabirds and trophic cascades in the Baltic Sea. Marine Ecology Progress Series, 323, 233–238.
Österblom, H., Olsson, O., Blenckner, T. and Furness, R. W. (2008). Junk-food in marine ecosystems. Oikos, 117, 967–977.
Paine, R. T. (1980). Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology, 49, 667–685.
Pauly, D., Christensen, V., Guenette, S., et al. (2002). Towards sustainability in world fisheries. Nature, 418, 689–695.
Pershing, A. J., Head, E. H., Greene, C. H. and Jossi, J. W. (2010). Pattern and scale of variability among Northwest Atlantic shelf plankton communities. Journal of Plankton Research, 32, 1661–1674.
Peterson, W. T. and Schwing, F. B. (2003). A new climate regime in northeast Pacific ecosystems. Geophysical Resarch Letters, 30(17), 1896.
Petrie, B., Frank, K. T., Shackell, N. L. and Leggett, W. C. (2009). Structure and stability in exploited marine ecosystems: quantifying critical transitions. Fisheries Oceanography, 18(2), 83–101.
Polis, G. A., Sears, A. L. W., Huxel, G. R., Strong, D. R. and Maron, J. (2000). When is a trophic cascade a trophic cascade? Trends in Ecology and Evolution, 15(11), 473–475.
Reid, P. C., Battle, E. J. V., Batten, S. D. and Brander, K. M. (2000). Impacts of fisheries on plankton community structure. ICES Journal of Marine Science, 57, 495–502.
Richardson, A. J. and Schoeman, D. S. (2004). Climate impact on plankton ecosystems in the Northeast Atlantic. Science, 305, 1609–1612.
Richardson, A. J., Bakun, A., Hays, G. C. and Gibbons, M. J. (2009). The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends in Ecology and Evolution, 24(6), 312–322.
Ritchie, E. G. and Johnson, C. N. (2009). Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters, 12, 982–998.
Romanuk, T. N., Hayward, A. and Hutchings, J. A. (2011). Trophic level scales positively with body size in fishes. Global Ecology and Biogeography, 20, 231–240.
Salomon, A. K., Gaichas, S. K., Shears, N. T., et al. (2010). Key features and context-dependence of fishery-induced trophic cascades. Conservation Biology, 24(2), 382–394.
Savenkoff, C., Swain, D. P., Hanson, J. M., et al. (2007). Effects of fishing and predation in a heavily exploited ecosystem: comparing periods before and after the collapse of groundfish in the southern Gulf of St. Lawrence (Canada). Ecological Modeling, 204, 115–128.
Schipper, J., Chanson, J. S., Chiozza, F., et al. (2008). The status of the world's land and marine mammals: diversity, threat, and knowledge. Science, 322, 225–230.
Shackell, N. L. and Frank, K. T. (2007). Compensation in exploited marine fish communities on the Scotian Shelf, Canada. Marine Ecology Progress Series, 336, 235–247.
Shackell, N. L., Frank, K. T., Fisher, J. A. D., Petrie, B. and Leggett, W. C. (2010). Decline in top predator body size and changing climate alter trophic structure in an oceanic ecosystem. Proceedings of the Royal Society, Series B, 277, 1353–1360.
Shears, N. T., Babcock, R. C. and Salomon, A. K. (2008). Context-dependent effects of fishing: variation in trophic cascades across environmental gradients. Ecological Applications, 18, 1860–1873.
Shurin, J. B., Borer, E. T., Seabloom, E. W., et al. (2002). A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters, 5, 785–791.
Sinclair, A. R. E. and Krebs, C. J. (2002). Complex numerical responses to top-down and bottom-up processes in vertebrate populations. Philosophical Transactions of the Royal Society of London Series B, 357, 1221–1231.
Steele, J. H. (1998). Regime shifts in marine ecosystems. Ecological Applications, 8, S33–S36.
Strong, D. R. (1992). Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology, 73, 747–754.
Strong, D. R. and Frank, K. T. (2010). Human involvement in food webs. Annual Review of Environmental Resources, 35, 1–23.
Swain, D. P. and Mohn, R. K. (2012). Forage fish and the factors governing recovery of Atlantic cod (Gadus morhua) on the eastern Scotian Shelf. Canadian Journal of Fisheries and Aquatic Sciences, 69, 997–1001.
Swain, D. P. and Sinclair, A. F. (2000). Pelagic fishes and the cod recruitment dilemma in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1321–1325.
Tremblay-Boyer, L., Gascuel, D., Watson, R., Christensen, V. and Pauly, D. (2011). Modelling the effects of fishing on the biomass of the world's oceans from 1950 to 2006. Marine Ecology Progress Series, 442, 169–185.
Turner, J. T. and Granéli, E. (2006). “Top-down” predation control on marine harmful algae. In Ecology of Harmful Algae. Ecological Studies, Vol. 189. Berlin Heidelberg: Springer-Verlag, pp. 355–366.
Verity, P. G. (1998). Why is relating plankton community structure to pelagic production so problematic? South African Journal of Marine Science, 19, 333–338.
Verity, P. G. and Smetacek, V. (1996). Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series, 130, 277–293.
Vitousek, P. M., Mooney, H. A., Lubchenco, J. and Melillo, J. M. (1997). Human domination of earth's ecosystems. Science, 277, 494–499.
Walters, C. and Kitchell, J. F. (2001). Cultivation/depensation effects on juvenile survival and recruitment: implications for the theory of fishing. Canadian Journal of Fisheries and Aquatic Sciences, 58, 39–50.
Ware, D. M. and Thompson, R. E. (2005). Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science, 308, 1280–1284.
Webb, T. J., Berghe, E. V. and O'Dor, R. (2010). Biodiversity's big wet secret: the global distribution of marine biological records reveals chronic under-exploration of the deep pelagic ocean. PLoS One, 5(8), e10223.
White, T. C. R. (1978). The importance of a relative shortage of food in animal ecology. Oecologia, 33, 71–86.
Worm, B. and Myers, R. A. (2003). Meta-analysis of cod-shrimp interactions reveals top-down control in oceanic food webs. Ecology, 84, 162–173.
Yodzis, P. (2001). Must top predators be culled for the sake of fisheries?Trends in Ecology and Evolution, 16, 78–84.