Contaminant-by-environment interactive effects on animal behavior in the context of global change: Evidence from avian behavioral ecotoxicology.

The potential for chemical contaminant exposure to interact with other stressors to affect animal behavioral responses to environmental variability is of mounting concern in the context of anthropogenic environmental change. We systematically reviewed the avian literature to evaluate evidence for contaminant-by-environment interactive effects on animal behavior, as birds are prominent models in behavioral ecotoxicology and global change research. We found that only 17 of 156 (10.9 %) avian behavioral ecotoxicological studies have explored contaminant-by-environment interactions. However, 13 (76.5 %) have found evidence for interactive effects, suggesting that contaminant-by-environment interactive effects on behavior are understudied but important. We draw on our review to develop a conceptual framework to understand such interactive effects from a behavioral reaction norm perspective. Our framework highlights four patterns in reaction norm shapes that can underlie contaminant-by-environment interactive effects on behavior, termed exacerbation, inhibition, mitigation and convergence. First, contamination can render individuals unable to maintain critical behaviors across gradients in additional stressors, exacerbating behavioral change (reaction norms steeper) and generating synergy. Second, contamination can inhibit behavioral adjustment to other stressors, antagonizing behavioral plasticity (reaction norms shallower). Third, a second stressor can mitigate (antagonize) toxicological effects of contamination, causing steeper reaction norms in highly contaminated individuals, with improvement of performance upon exposure to additional stress. Fourth, contamination can limit behavioral plasticity in response to permissive conditions, such that performance of more and less contaminated individuals converges under more stressful conditions. Diverse mechanisms might underlie such shape differences in reaction norms, including combined effects of contaminants and other stressors on endocrinology, energy balance, sensory systems, and physiological and cognitive limits. To encourage more research, we outline how the types of contaminant-by-environment interactive effects proposed in our framework might operate across multiple behavioral domains. We conclude by leveraging our review and framework to suggest priorities for future research.