Indirect effects in complex ecosystems: recent progress and future challenges
Introduction
Throughout biology, there has been a growing realisation of the need to understand the dynamical interactions among multiple biological components, or biocomplexity (Mervis, 1999). Ecosystems are some of the most obvious complex systems in biology. A fundamental cause of ecosystem complexity is indirect effects, effects of one species on another that only arise in the presence of other species (e. g., Andewartha and Birch, 1984). Consequently, understanding and predicting the behaviour of ecosystems depends on our ability to effectively identify and deal with indirect effects. In this paper, I review some of the recent advances in the study of indirect effects, and outline the future challenges facing studies of indirect effects.
Although the possibility of indirect effects has long been recognized Darwin, 1859, Camerano, 1880, Forbes, 1887, Elton, 1927, interest in them has grown recently because of the widespread application of field experimental methods in ecology. When done in the context of complex natural communities, experiments have often yielded unanticipated results compared to predictions based on pairwise interactions (Sih et al., 1985), and these results are usually most easily explained by indirect effects. The increasing interest in indirect effects can be visualised by the patterns generated by an analysis of ecological papers in the Biological Abstracts database which address indirect effects and related concepts (Fig. 1). Over the past 20 years, the number and fraction of ecological papers on indirect effects have been increasing exponentially, suggesting that this topic has become an important one in ecological research.
Indirect effects can have important implications for ecological study. First, their potential existence complicates experimental interpretation, because multiple pathways of causation are possible (e.g., Connell, 1983, Wootton, 1992). Second, they make implementing conservation and management strategies difficult because the effects of a species loss or an environmental perturbation become difficult to predict a priori (Yodzis, 1988; for some compelling empirical examples, see Estes and Palmisano, 1974, Thrupp, 1990). Therefore, a greater understanding of when they arise, which mechanisms are involved, and how their effects can be predicted is highly desirable.
Section snippets
Terminology
The terminology used in discussing indirect effects has been in a state of flux, as investigators have sought to develop the most useful categorisations and distinctions among these complex interactions Vandermeer, 1969, Miller and Kerfoot, 1987, Wootton, 1993, Menge, 1995, Abrams et al., 1996. A distinction has been made between two basic types of simple indirect effects Vandermeer, 1969, Wootton, 1993, Abrams et al., 1996. First, indirect effects can arise by linking two (or more) direct
Recent results and future challenges
Among the increasing number of studies related to indirect effects (Fig. 1), the vast majority have largely been focused on investigating examples in different systems. Establishing many empirical examples is important to give a sense of the generality of indirect effects, and the range of ways in which they arise. Nevertheless, we will need to move beyond simply documenting indirect effects if substantial progress in grappling with indirect effects is to be made. Therefore, rather than
Acknowledgements
This work was partially supported by a grant from the Andrew W. Mellon Foundation.
References (158)
Distinguishing direct from indirect effects of grazers in intertidal estuarine assemblages
J. Exp. Mar. Biol. Ecol.
(1999)- et al.
Coupling in predator-prey dynamics ratio-dependence
J. Theor. Biol.
(1989) Are there real differences among aquatic and terrestrial food webs?
Trends Ecol. Evol.
(2000)- et al.
Does the activity of cockles, Cerastoderma edule (L.) and lugworms, Arenicola marina L., make Corophium volutator (Pallas) more vulnerable to epibenthic predators: A case of interaction modification?
J. Exp. Mar. Biol. Ecol
(1994) - et al.
Indirect effects in ecological interaction networks I. The chain rule approach
Math. Biosci.
(1995) - et al.
Indirect effects in ecological interaction networks II. The conjugate variable approach
Math. Biosci.
(1995) The impact of loose-lying algal mats and predation by the brown shrimp Crangon crangon (L.) on infaunal prey dispersal and survival
J. Exp. Mar. Biol. Ecol.
(1998)Arguments in favor of higher order interactions
Am. Nat.
(1983)Predators that benefit prey and prey that harm predators: Unusual effects of interacting foraging adaptations
Am. Nat.
(1992)Effect of increased productivity on the abundances of trophic levels
Am. Nat.
(1993)
Implications of dynamically variable traits for identifying, classifying and measuring direct and indirect effects in ecological communities
Am. Nat.
The role of indirect effects in food webs
Sagebrush-grass vegetation dynamics: comparing classical and state-transition models
Ecol. Appl.
Predator responses, prey refuges, and density-dependent mortality of a marine fish
Ecology
The Ecological Web: More on the Distribution and Abundance of Animals
The ecological role of water-column microbes in the sea
Mar. Ecol. Prog. Ser.
How Nature Works: The Science of Self-Organized Criticality
Perturbation experiments in community ecology: theory and practice
Ecology
Strong effects of weak interactions in ecological communities
Nature (Lond.)
Quantifying variation in the strengths of species interactions
Ecology
Higher order interactions in ecological communities: what are they and how can they be detected
Ecology
Consumer versus resource control in freshwater pelagic food webs
Science
The ecology of fear: Optimal foraging, game theory, and trophic interactions
J. Mammal.
Dell'equilibrio dei viventi mercè la reciproca distruzione
Atti dell Reale Accademia delle Scienze di Torino
Testing for higher order interactions
Am. Nat.
The effect of alternative prey on the functional response of Notonecta hoffmani
Ecology
Extending functional response models to include a second prey type: an experimental test
Ecology
Interpreting the results of field experiments: effects of indirect interactions
Oikos
Habitat structural complexity and the interaction between bluegills and their prey
Ecology
Relevance of community structure in assessing indetermanacy of ecological predictions
Ecology
The Origin of Species by Means of Natural Selection
Dynamics of nutrient cycling and food webs
Facilitation on an intertidal mudflat: the effect of siphon nipping by flatfish on burying depth of the bivalve Macoma balthica
Oecologia
Three-way interactions barnacles limpets and algae in a Sonoran desert rocky intertidal zone
Am. Nat.
Interactions among gypsy moths, white-footed mice, and acorns
Ecology
Animal Ecology
Direct and indirect competition between spider mites feeding on grapes
Ecol. Appl.
Interactions between sculpins, net-spinning caddis larvae and midge larvae
Oikos
Sea otters: their role in structuring benthic nearshore communities
Science
Hatch density variation of a generalist arthropod predator: population consequences and community impact
Ecology
The influence of the cockle, Cerastoderma edule, on the macrozoobenthic community of tidal flats in the Wadden Sea
P.S.Z.N.I: Mar. Ecol.
The lake as a microcosm
Bull. Peoria Sci. Ass.
Individual Behavior and Community Dynamics
Fish in offshore kelp forest affect recruitment to intertidal barnacle populations
Science (Washington DC)
Construction and analysis of a large Caribbean foodweb
Ecology
Effects of environmental change on plant species density: comparing predictions with experiments
Ecology
A structural equation model of plant species richness and its application to a coastal wetland
Am. Nat.
On the use of path analysis and related procedures for the investigation of ecological problems
Am. Nat.
The impacts of a nonindigenous marine predator in a California bay
Ecology
Cited by (201)
The propagation of disturbances in ecological networks
2024, Trends in Ecology and EvolutionResilience, indirect effects and cycling in ecological networks
2023, Ecological ModellingInvasive Spartina alterniflora habitat forms high energy fluxes but low food web stability compared to adjacent native vegetated habitats
2023, Journal of Environmental Management