On connecting behavioral responses to HIREC to ecological outcomes: a comment on Wong and Candolin
Wong and Candolin (2015) provide a superb review of ideas and case studies on the ecology and evolution of behavioral responses to human induced rapid environmental change (HIREC) Here, we offer 2 complementary suggestions to help this critically important field move forward. First, faced with innumerable species, aspects of HIREC and types of behavior, how might one choose what to study? Our impression is that many behavioral ecologists, including ourselves, tend to study what we are familiar with. If, however, our goal is to examine behavioral responses to HIREC that have important ecological consequences, we should let the ecology guide us. If, for instance, a goal is to connect behavioral responses to HIREC to community ecology, we suggest focusing on keystone species or ecosystem engineers. As obvious as this may seem, relatively few studies follow this track: a Web of Science search using "environmental change," "behavior," and "keystone species" returned only 3 articles. Our search no doubt missed some relevant articles; still, it appears that looking at behavioral responses to HIREC involving keystone species is a relatively open niche. For population ecology, the classic "limiting factors" tradition asks ecologists to identify (often with experiments) 1) the key limiting factors (here, key aspects of HIREC) that limit success in a given population, 2) in key limiting life history stages (e.g. using elasticity analyses) and to then 3) focus on the key behaviors that influence variation in individual abilities to cope with those key limiting factors (Sih and Gleeson 1995) We thus suggest that behavioral ecologists may benefit by first focusing on significant behaviors in limiting life history stages in keystone species in a community. If HIREC is driven by a combination of 2 factors (e.g. ocean acidification interfering with behavioral responses to an exotic predator) then study behavioral responses to those interacting aspects of HIREC. We recognize that this advice might be annoying at 2 levels. First, it seems obvious of course, focus on what is more important and second, this advice might often be difficult logistically to implement. Still, our sense is that many, including ourselves, might benefit from the reminder to do our best to evaluate ecological importance while choosing a behavior and aspect of HIREC to study, as opposed to simply focusing on what is familiar. Second, we need theory to explain the observed variation in outcomes. Why do some species respond well behaviorally to HIREC, whereas others do not? Why do some prey respond adaptively to exotic predators, whereas other prey do not? Why have some species (or populations) exhibited a plastic shift to breed earlier in the spring with climate change, whereas others have not? Why have some species Scott JM, Rachlow JL, Lackey RT, Pidgorna AB, Aycrigg JL, Feldman GR, Svancara LK, Rupp DA, Stanish DI, Steinhorst RK. 2007. Policy advocacy in science: prevalence, perspectives, and implications for conservation biologists. Conserv Biol. 21:29 35. Sih A. 2013. Understanding variation in behavioral responses to humaninduced rapid environmental change: a conceptual overview. Anim Behav. 85:1077 1088. Wilson EO. 2010. The diversity of life. Harvard: Belknap Press. Wong BBM, Candolin U. 2015. Behavioral responses to changing environments. Behav Ecol. 26:665 673. fallen into evolutionary traps sometimes involving spectacularly maladaptive behaviors, whereas others have not (Robertson et al. 2013) Standard behavioral ecology theory based on optimality theory can do a good job of explaining "smart" responses to HIREC but, by definition, might be less well suited for explaining maladaptive responses. Developing theory on behavioral responses to HIREC starts with a major assumption of optimality theory: past selection pressures have shaped behavioral "rules of thumb" or cue response systems (as examples of previously adaptive traits) After HIREC, however, organisms may continue to rely on these cues, at least initially. Thus, variation in how well organisms (including humans) respond to HIREC can then be explained by whether novel conditions are evolutionarily matched versus mismatched to past conditions. The call is for explicit theory to formalize this idea (see Sih et al. 2011; Sih 2013) We do not have to entirely reinvent the wheel, though: we can use existing behavioral ecology theory to explain variation in previously adaptive behaviors (e.g. cue response thresholds) throughout some ecological parameter space, but then extend existing theory to predict how well organisms should respond when they are exposed to new ecological conditions, assuming that at least initially they retain their previously adaptive (but now possibly maladaptive) cue response systems (e.g. McNamara et al. 2011) Theory can be further extended to address variation in how behavioral responses to HIREC should affect population and community ecology outcomes. A rich body of existing theory predicts how adaptive behavioral responses should affect population dynamics and species interactions (e.g. Abrams 2010) A valuable addition would be to incorporate the "new behavioral ecology theory" predicting both adaptive and maladaptive behavioral responses to HIREC into population/community models. For example, when, according to new behavioral ecology theory do we expect organisms to overavoid humans that actually pose no danger to them, and given predicted negative effects of overavoidance on survival and/or reproduction, how strongly should this impact the population's performance? With interacting species, a key would be the ability of new theory to predict at least qualitative differences among species in their responses to HIREC and how those differences should affect species interactions. For example, with climate change, the goal might be for theory to predict the relative phenological shifts of predators and prey (or 3 trophic levels) and how these would then influence species interactions and, ultimately, ecological dynamics. The key point is that an explicit set of theory on behavioral responses to change should generate predictions on conditions when we expect organisms to respond well or not to HIREC. Case studies can then test predictions that serve to further tune the theory, moving us toward not just a case by case, system specific understanding of responses to HIREC but, potentially, a general understanding that can ideally be used to identify, a priori, situations where organisms are likely to be more versus less vulnerable to HIREC.