R EPORTS by the National Health and Environmental Effects drugs for disorders of heart, lung, and blood. This Materials and Methods Research Laboratory, U.S. Environmental Protection work was supported by NIH ES012496 (J.S.S.) and Figs. S1 and S2 Agency. Approval does not signify that the contents HL004171 (L.G.Q.), and by an award to J.S.S. from References and Notes necessarily reflect the views and policies of the U.S. the Sandler Program for Asthma Research. We thank EPA, nor does mention of trade names or commer- N. Coates and W. M. Foster for their assistance. 3 December 2004; accepted 26 April 2005 cial products constitute endorsement or recommen- Published online 26 May 2005; dation for use. J.S.S. is a paid consultant to Nitrox Supporting Online Material 10.1126/science.1108228 LLC, a biotechnology company developing NO-based www.sciencemag.org/cgi/content/full/1108228/DC1 Include this information when citing this paper. (Merluccius bilinearis), pollock (Pollachius Trophic Cascades in a Formerly virens), cusk (Brosme brosme), redfish (Sebastes sp.), American plaice (Hippoglossoides Cod-Dominated Ecosystem platessoides), yellowtail flounder (Limanda ferruginea), thorny skate (Raja radiata), and Kenneth T. Frank,1* Brian Petrie,1 Jae S. Choi,1,2 William C. Leggett2 winter skate (Raja ocellata). The transition occurred during the mid-1980s and early Removal of top predators from ecosystems can result in cascading effects 1990s and resulted in the virtual elimination through the trophic levels below, completely restructuring the food web. of the ecosystem-structuring role of the large- Cascades have been observed in small-scale or simple food webs, but not in bodied predators that had dominated for cen- large, complex, open-ocean ecosystems. Using data spanning many decades turies (14). The abundance of small pelagic from a once cod-dominated northwest Atlantic ecosystem, we demonstrate fishes and benthic macroinvertebrates [pre- a trophic cascade in a large marine ecosystem. Several cod stocks in other dominantly northern snow crab (Chionoecetes geographic areas have also collapsed without recovery, suggesting the exis- opilio) and northern shrimp (Pandalus bo- tence of trophic cascades in these systems. realis)^, once among the primary prey of the benthic fish community (supporting text), in- Trophic cascades, defined by (i) top-down because of exploitation, should provide the creased markedly following the benthic fish control of community structure by predators most definitive tests of the trophic cascade hy- collapse (Fig. 1B). The correlations between and (ii) conspicuous indirect effects two or pothesis, yet none were found. Reid et al.(5) the benthic fish biomass and small pelagic more links distant from the primary one, found no evidence of trophic cascades in the fishes (r 0 j0.61, n 0 33 years), snow crab have been intensively researched and contro- heavily exploited North Sea, nor did Micheli_s (r 0 j0.70, n 0 24), and shrimp abundances versial for decades (1, 2). The existence of (11) meta-analysis of 20 open marine sys- (r 0 j0.76, n 0 24) were negative. top-down control of ecosystem structure (im- tems. However, Worm and Myers_s(12) meta- Consistent with the second criterion of plied by trophic cascades) creates opportuni- analysis of nine continental shelf ecosystems trophic cascades, there were conspicuous ties for the understanding and manipulation/ revealed large increases in macroinvertebrate indirect effects resulting from removal of the management of exploited ecosystems, because populations following declines in cod (Gadus top predator. As predicted, the correlation exploitation is generally focused on top pred- morhua) stocks. Although their findings do between the time series of the benthic fish ators (3, 4). From a theoretical perspective, not provide evidence of a trophic cascade, they community (landings) and large (92mm),her- the spatiotemporal balance between the Btop- suggest the potential for predation-induced bivorous zooplankton was positive (r 0 0.45, down[ (predator dominated) and Bbottom-up[ top-down effects in large marine ecosystems. n 0 23), and that for phytoplankton was neg- (nutrient driven) regulation of ecosystems pro- Estes et al.(9) found evidence of a four-level ative (r 0 j0.72, n 0 24). These relation- vides a foundation for understanding their cascade consisting of killer whales, sea otters, ships remained equally strong when survey structure, function, and evolution (5). sea urchins, and kelp. However, their time se- estimates of groundfish biomass were used Most ecosystems for which trophic cas- ries were limited and the changes in killer in place of landings (13). cades have been shown feature one or more whale abundance were unknown. Thus, the The herbivorous zooplankton abundance of the following: low species diversity, simple evidence for trophic cascades in open ocean series revealed strong evidence of a transition food webs, and small geographic size (6, 7); systems is equivocal. from high to low abundance of large-bodied examples from more complex ecosystems Here we provide evidence of a trophic cas- species from the 1960s and 1970s to the 1990s exist (8, 9). This restricted subset of ecologi- cade in the large eastern Scotian Shelf eco- and beyond (Fig. 1C). This finding is consist- cal types characterizes many freshwater eco- system off Nova Scotia, Canada (Fig. 1) (13). ent with the enhanced role of size-selective systems, which constitute most aquatic-based The cascade involved four trophic levels and predation on zooplankton by pelagic fishes examples of trophic cascades (6). Marine con- nutrients and was driven by changes in the and early-life stages of shrimp and crab. The tinental shelf ecosystems, which generally abundance of large predators (primarily cod) abundance of small-bodied (G2 mm) zooplank- have large spatial scales, high species diver- of fish and macroinvertebrates, thereby meet- ton remained similar throughout the study sity, and food web complexity, have not yet ing the requirements of top-down control and period (Fig. 1C). The phytoplankton record revealed unequivocal evidence of trophic cas- indirect effects with multiple links (1). More- (Fig. 1D) revealed a reciprocal pattern: Abun- cades. Steele and Collie (10) reasoned that over, the cascading effects involved the entire dances were low in the 1960s and 1970s and continental shelf ecosystems, with their mas- community, rather than only a subset of the high in the 1990s and beyond. Plankton data sive changes in predatory fish populations species that occupy each of the affected troph- ancillary to the continuous plankton recorder ic levels. data (13) revealed a 45% greater abundance 1Department of Fisheries and Oceans, Bedford Consistent with the first criterion of troph- of large zooplankton during the early 1980s Institute of Oceanography, Ocean Sciences Division, ic cascades, the system changes were driven relative to the late 1990s (Fig. 1C). In con- Post Office Box 1006, Dartmouth, Nova Scotia, B2Y 2 by the collapse of the benthic fish community trast, chlorophyll levels were higher in the 4A2, Canada. Department of Biology, Queen’s Uni- versity, 74 University Avenue, Kingston, Ontario, K7L (Fig. 1A). In addition to cod, several other 1990s relative to the 1980s, but the differences 3N6, Canada. commercially exploited species declined, in- were slight (Fig. 1D). Finally, nitrate concen- *To whom correspondence should be addressed. cluding haddock (Melanogrammus aeglefinus), trations, a major limiting factor in marine E-mail: [email protected] white hake (Urophycis tenuis), silver hake systems, showed the expected reciprocal re- www.sciencemag.org SCIENCE VOL 308 10 JUNE 2005 1621 R EPORTS sponse to changes in phytoplankton abundance was positive and nearly constant from 1970 directed fishing of the dominant benthic fish (Fig. 1D). to the mid-1980s, featured a linear transition species (cod, haddock, and pollock) in 1993, The predatory impact of the expanding from the mid-1980s to negative values in the and development of new fisheries designed grey seal (Halichoerus grypus) population early 1990s, and remained negative and nearly to divert fishing mortality away from the re- (13) on the resident cod stock was minor constant since then. Initially (1970 to 1986), maining benthic fish species. In 1995, senti- (Fig. 1A) (15). Seals appear to have bene- benthic fish, possessing good physiological nel surveys, supplementing existing scientific fited from the cod collapse, which released condition, high growth rates, and supporting a surveys, were instituted to monitor and docu- their forage base (small pelagic fish and ben- 9100 Â 103 metric tons (kt) commercial fish- ment the anticipated recovery. thic invertebrates) from predation. A strong ery, dominated; the current period (post-1990) Whether the recent ecosystem changes are positive correlation between the abundances is a pelagic fish/macroinvertebrate–dominated reversible is an open question. Other factors, of small pelagics and grey seals (r 0 0.70, n 0 system characterized by poor benthic fish pro- both intrinsic and extrinsic, were associated 33) and the ongoing exponential rate of in- ductivity, a G50-kt benthic fish fishery, and a with the ecosystem changes. For example, the crease in the seal population (16) support small (G50 kt), but increasing, macroinverte- expected inverse and reversible relationship this claim. brate fishery directed at shrimp and snow crab. between fishing mortality and cod biomass Principal component analysis of the se- Several management measures designed to re- (13) that characterized the 1960 to early 1990 ries that we used (Fig. 1) and of other biotic, verse the trend and restore the system to its period does not hold after 1993 despite the abiotic, and human variables conducted by earlier state have failed. The actions taken near-elimination of exploitation (Fig. 2A). Choi et al.(17) has provided statistical evi- included establishment of a fishing closure Physical environmental changes may have dence and a concise assessment of the change on two major offshore banks in 1987 that en- contributed to the restructuring of the food in ecosystem structure.