Review
Predicting ecological consequences of marine top predator declines

https://doi.org/10.1016/j.tree.2008.01.003Get rights and content

Recent studies document unprecedented declines in marine top predators that can initiate trophic cascades. Predicting the wider ecological consequences of these declines requires understanding how predators influence communities by inflicting mortality on prey and inducing behavioral modifications (risk effects). Both mechanisms are important in marine communities, and a sole focus on the effects of predator-inflicted mortality might severely underestimate the importance of predators. We outline direct and indirect consequences of marine predator declines and propose an integrated predictive framework that includes risk effects, which appear to be strongest for long-lived prey species and when resources are abundant. We conclude that marine predators should be managed for the maintenance of both density- and risk-driven ecological processes, and not demographic persistence alone.

Section snippets

Declines in marine top predators

Predators that occupy high trophic levels in marine habitats, including marine mammals, large teleosts and sharks, have been declining worldwide at a rapid pace 1, 2, 3, 4. Recent estimates suggest that populations of large sharks have declined regionally by 90% or more 3, 5. The status of large tuna, billfish and groundfish [2] and reef-associated predators in human-impacted areas [6] is equally dire. Although the magnitude of some declines is debated, few researchers doubt the generality of

Marine communities change when top predators decline

Predicting the ecological consequences of reductions in top predators is, in essence, an inquiry into the importance of top-down processes. From groundbreaking work on rocky intertidal shores [8] to the documentation of the keystone role of sea otters in kelp forests [9] and studies of the indirect effects of bird predation [10], among many other examples, there is little doubt that predators have a fundamental influence on the structure and function of marine communities. Hence, widespread

The importance of risk effects

Researchers of marine systems involving large-bodied predators often implicitly assume that trophic cascades occur via direct predation (so-called lethal effects) on mesoconsumers. Using this framework, the effects of predation could be fully quantified based on the diets, metabolic rates and abundances of predators and data on prey population dynamics [18]. Declines in top predator abundance should release mesoconsumers from predation and indirectly increase the mortality rate of resource

Risk effects of marine top predators

The influence of marine top predators such as tuna, sharks and marine mammals on the behavior of mesoconsumers has not yet been evaluated comprehensively [32], and few studies measure the indirect community effects that might arise from these interactions. However, those studies that have done so suggest that risk effects likely are common and might be transmitted to lower trophic levels. For example, the presence of New Zealand fur seals Arctocephalus forsteri causes a temperate reef fish

Identifying key interactions and species

Considering risk effects raises interesting questions that are relevant to understanding the ecological consequences of removing marine top predators. First, what factors influence the relative importance of risk effects and those of direct predation? Second, which top predators are most likely to have disproportionate effects on their communities (through both mechanisms) relative to their abundance (i.e. are keystone species, sensu [42])? Small-scale experiments and field studies in

Toward a predictive framework

Recent studies suggest that marine top predators can exert considerable effects on their prey that can cascade through marine communities. These overall effects might not be caused solely by direct predation; rather, risk effects can contribute a large component of overall predator effects. In most cases, therefore, predictions about how communities will respond to marine predator declines should be improved by an understanding of risk effects and behaviorally mediated indirect interactions.

Acknowledgements

We thank Pieter Folkens, Lindsay Marshall, Elliott Lee Hazen and Roger Hall (http://inkart.net) for artwork and photos. Julia Baum, Craig Layman, Ray Heithaus, Jim Estes and four anonymous reviewers provided helpful comments. This work was supported by NSF grant OCE-0526065 to M.R.H., a Lenfest Ocean's Program grant to B.W. and North Pacific Research Board and Prince William Sound Science Center grants to A.F.

Glossary

Behaviorally mediated indirect interaction
occurs when changes in the abundance of one species results in a change in the behavior of a second species (a risk effect) that in turn influences a third species.
Density-mediated indirect interaction
occurs when changes in the abundance of one species affect the density of another species through direct predation, which in turn changes densities of a third species.
Direct predation effect
effects of predator-inflicted mortality on prey populations.

References (70)

  • R.A. Myers et al.

    Rapid worldwide depletion of predatory fish communities

    Nature

    (2003)
  • J.K. Baum

    Collapse and conservation of shark populations in the northwest Atlantic

    Science

    (2003)
  • D. Pauly

    Fishing down marine food webs

    Science

    (1998)
  • R.A. Myers

    Cascading effects of the loss of apex predatory sharks from a coastal ocean

    Science

    (2007)
  • A.M. Friedlander et al.

    Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators

    Mar. Ecol. Prog. Ser.

    (2002)
  • R.T. Paine

    Food webs: linkage, interaction strength and community infrastructure

    J. Anim. Ecol.

    (1980)
  • J.A. Estes et al.

    Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm

    Ecol. Monogr.

    (1995)
  • J.T. Wootton

    Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications

    Am. Nat.

    (1993)
  • P. Ward et al.

    Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing

    Ecology

    (2005)
  • E.T. Borer

    What determines the strength of a trophic cascade?

    Ecology

    (2005)
  • B. Worm et al.

    Meta-analysis of cod-shrimp interactions reveals top-down control in oceanic food webs

    Ecology

    (2003)
  • K.T. Frank

    Trophic cascades in a formerly cod-dominated ecosystem

    Science

    (2005)
  • N.K. Dulvy

    Coral reef cascades and the indirect effects of predator removal by exploitation

    Ecol. Lett.

    (2004)
  • J.A. Estes

    Killer whale predation on sea otters linking oceanic and nearshore ecosystems

    Science

    (1998)
  • T.M. Williams

    Killer appetites: assessing the role of predators in ecological communities

    Ecology

    (2004)
  • J.S. Brown et al.

    Hazardous duty pay and the foraging cost of predation

    Ecol. Lett.

    (2004)
  • S.L. Lima et al.

    Behavioral decisions made under the risk of predation: a review and prospectus

    Can. J. Zool.

    (1990)
  • W. Lampert

    The adaptive significance of diel vertical migration of zooplankton

    Func. Ecol.

    (1989)
  • E.E. Werner et al.

    A review of trait-mediated indirect interactions in ecological communities

    Ecology

    (2003)
  • E.L. Preisser

    Scared to death? The effects of intimidation and consumption in predator-prey interactions

    Ecology

    (2005)
  • O.J. Schmitz

    Trophic cascades: the primacy of trait-mediated indirect interactions

    Ecol. Lett.

    (2004)
  • S. Creel

    Predation risk affects reproductive physiology and demography of elk

    Science

    (2007)
  • C. Walters et al.

    Recruitment limitation as a consequence of natural selection for use of restricted feeding habitats and predation risk taking by juvenile fishes

    Can. J. Fish. Aquat. Sci.

    (1993)
  • G.C. Trussel

    Habitat effects on the relative importance of trait- and density-mediated indirect interactions

    Ecol. Lett.

    (2006)
  • Cited by (1003)

    View all citing articles on Scopus
    View full text