Direct and indirect effects of chemical contaminants on the behaviour, ecology and evolution of wildlife

Abstract

Chemical contaminants (e.g. metals, pesticides, pharmaceuticals) are changing ecosystems via effects on wildlife. Indeed, recent work explicitly performed under environmentally realistic conditions reveals that chemical contaminants can have both direct and indirect effects at multiple levels of organization by influencing animal behaviour. Altered behaviour reflects multiple physiological changes and links individual- to population-level processes, thereby representing a sensitive tool for holistically assessing impacts of environmentally relevant contaminant concentrations. Here, we show that even if direct effects of contaminants on behavioural responses are reasonably well documented, there are significant knowledge gaps in understanding both the plasticity (i.e. individual variation) and evolution of contaminant-induced behavioural changes. We explore implications of multi-level processes by developing a conceptual framework that integrates direct and indirect effects on behaviour under environmentally realistic contexts. Our framework illustrates how sublethal behavioural effects of contaminants can be both negative and positive, varying dynamically within the same individuals and populations. This is because linkages within communities will act indirectly to alter and even magnify contaminant-induced effects. Given the increasing pressure on wildlife and ecosystems from chemical pollution, we argue there is a need to incorporate existing knowledge in ecology and evolution to improve ecological hazard and risk assessments.

Keywords: behavioural ecology; endocrine-disrupting chemicals; plasticity; predator-prey dynamics; sublethal.

Figure 1.

Outline of our conceptual framework modelling the direct and indirect effects of a chemical contaminant using predator–prey dynamics as a case study. Two predatory species (A and B) are exposed to a chemical contaminant. (a) State 1 shows initial changes to species in the food web at the individual and community levels; (b) state 2 includes feedback loops, which show dynamic interactions between species in time and space. Increases and decreases in population size for each species are indicated by arrows. The solid arrows indicate direct effects, dashed arrows indirect effects, dotted arrows nutrient cycling and blue arrows species interactions.

Figure 2.

Implementation plan suggesting methodological approaches for utilizing our conceptual framework to identify the routes by which animal behaviour is affected by chemical contaminants. For each level of biological organization (individual, species, community and ecosystem), we highlight some of the factors that should or could be quantified or experimentally manipulated.

Figure 3.

The distribution of expressions of a trait (here, activity) in two populations from environments with different levels of predation risk. (a) Population collected from the field (high predation); (b) laboratory-bred population (low predation). Black arrows illustrate the potential for contaminant-induced increases in activity in the populations (the longer the arrow, the greater the potential change).