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Community ecology as a framework for predicting contaminant effects

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Most ecosystems receive an assortment of anthropogenic chemicals from the thousands possible, making it important to identify a predictive theory for their direct and indirect effects. Here, we propose that the impacts of contaminants can be simplified and unified under the framework of community ecology. This approach offers predictions of the strength and direction of indirect effects, which species are crucial for propagating these effects, which communities will be sensitive to contaminants, and which contaminants will be most insidious to communities. We discuss insights offered by this approach, potential limitations and extensions, outstanding questions, and its value for integrated pest management, ecological risk assessment, and the development of remediation and ecosystem management strategies.

Introduction

Chemical contaminants are found in most ecosystems, can be major selective forces, can alter ecosystem functions (e.g. [1]), and are regarded as the second greatest threat to aquatic and amphibious species (behind habitat loss) [2]. Despite past environmental catastrophes associated with the pesticide DDT, the number and extent of pesticide applications has reached unprecedented levels [3]. Even recently, contaminants have been associated with reproductive impairment [4], disease emergence [5] and declines of non-targeted species [6].

One reason why we might still be seeing substantial adverse effects of contaminants is because their indirect effects (see Glossary) are often overlooked 7, 8, 9, 10 [Also see special issues in Environmental Toxicology and Chemistry (1996) and Ecological Applications (1997) on indirect effects of contaminants.] Indeed, pesticide and industrial chemical registration decisions in the USA are based largely on tests that cannot directly detect indirect or population-level effects [11]. This is despite continued pleas to shift from the predominantly individual-based approach to toxicology to tests on higher levels of biological organization (reviewed in [9]).

Although the field of ecotoxicology has progressed substantially since the 1962 release of Rachel Carson's seminal book Silent Spring, one statement often still rings true: ‘Chemicals are pre-tested against a few individuals, but not against living communities’ [12]. This is disconcerting because increasing evidence suggests that the indirect effects of pesticides are more common and complex than are their direct effects 7, 8, 9, 13, 14. Furthermore, recent legislation, such as the US Food Quality Protection Act, and a greater emphasis on integrated pest management (IPM) practices are reducing applications of broad-spectrum pesticides and accelerating the development and use of more precisely targeted toxins (e.g. reduced-risk pesticide) [15]. Hence, as direct effects on non-targeted organisms are reduced, indirect effects of pesticides are only expected to become proportionally more common, placing even greater value and urgency for a framework to predict indirect effects of contaminants.

We propose here that community ecology theory can serve as this framework. In particular, because community ecology has a long history of studying indirect effects, generalities have emerged on factors that influence their direction and magnitude. We thus use concepts in community ecology to provide new insights on indirect contaminant effects. We discuss support for, and limitations, extensions and applications of, this community ecology approach, and, in addition, address outstanding questions in ecotoxicology.

Section snippets

A brief historical perspective on ecotoxicology

Early pesticides (e.g. many organochlorine insecticides) had strong, negative, direct impacts on a broad range of species, both target and non-target taxa. Relative to these early pesticides, ‘modern’ pesticides at environmentally common concentrations typically have shorter half-lives, less biomagnification potential, and fewer direct, adverse effects on ‘non-target taxa’ [18] (although further testing of this assumption is required, especially in light of endocrine disruption). From early on,

Contaminants and the paradigms of community ecology

Chemical contaminants have traditionally been considered abiotic stressors and, in many cases, contaminants will be best incorporated into community models as abiotic disturbance. However, contaminant-induced mortality can often be similar to the effects of selective predators (albeit some significant differences; Box 1) 7, 20, 21. Indeed, some ecology texts do not make strong distinctions between abiotic stress and predation (e.g. [17]), and there are cases where it might be more insightful to

Possible extensions

Some researchers have quantified the impacts of contaminants on ecosystem processes but, in general, our knowledge remains scant 1, 21, 55. Increasing evidence links community composition to ecosystem functions [56], suggesting that a promising extension of the community ecology approach is to predict the indirect effects of contaminants on ecosystem processes. Both Odum and Rapport et al. 57, 58 formulated similar expectations for ecosystem responses to stress. Efforts that merge community

Benefits of the approach

We propose that there are three crucial questions that need to be addressed in ecotoxicology: (i) which community types or structures are most sensitive to pollution? (ii) Which species are most threatened by contaminants? and (iii) on which of the tens of thousands of registered chemicals should we focus our attention? Community ecology can facilitate addressing each question because it generates testable predictions regarding which communities will be sensitive to contaminants, which

Acknowledgements

This work was funded by a National Science Foundation grant (DEB 0516227) and USDA grant (NRI Managed Ecosystem 2006–01370) to J.R.R. This article was improved by the thoughts of James Bever, Michelle Boone, Loren Byrne, John Hammond, John Tooker and two anonymous reviewers.

Glossary

Biomagnification
cumulative increase in the concentration of a chemical in successively higher trophic levels generally as a result of predation.
Community stability
tendency of populations to persist with low temporal variability and for community composition to remain constant.
Food-web connectance
observed number of trophic interactions divided by the total number of possible interactions.
Indirect effects
effect on a species mediated by another species or factor.
Intraguild predation
where predators

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