Abstract
Fear of natural enemies in non-human animals is a concept dating back to the time of Darwin. Now recognized as a nonconsumptive effect, the ecological and evolutionary impact of fear has been studied in a number of predator-prey systems within the last few decades. However, comparatively little consideration has been given to the nonconsumptive effects that parasites have on their hosts, which have evolved behaviors to avoid parasites, impacting habitat selection, mate choice, and foraging activity. These avoidance behaviors create a “landscape of disgust”, wherein hosts navigate to avoid parasites, akin to the “landscape of fear” in prey. Evolutionarily speaking, however, predators and parasites are but two examples of natural enemies. Pathogens, parasites, predators, and parasitoids, among others, each exert their own fitness cost on the victims they attack. Since animals likely evolve in the presence of multiple natural enemies, they must adopt a range of avoidance behaviors to navigate through the resulting “landscape of peril”. Therefore, in line with recent efforts to combine the landscapes of fear and disgust, we offer a theoretical framework to better understand the impacts of natural enemies on the evolution of trait-mediated avoidance behaviors in animals. More precisely, we look at how victims may evolve to allocate energy optimally among distinct avoidance behaviors under the selective pressures imposed by different types of natural enemy. This framework is then put into the more realistic context of a food web, which highlights the impact of trophic interactions and trophic level on the evolution of avoidance behaviors.
Highlights
When imagining a pride of lions chasing down an antelope in sub-Saharan Africa, few would consider that these apex predators have any enemies of their own
There are exceptions to this, but on an evolutionary timescale, we argue that this dichotomy represents a strong selective pressure exerted by enemies on the evolution of avoidance behaviors in victims
All species likely evolve under the selective pressures imposed by enemies and have to adapt in order to safely navigate through their environment with the use of avoidance behaviors
Summary
When imagining a pride of lions chasing down an antelope in sub-Saharan Africa, few would consider that these apex predators have any enemies of their own. The Integrated Landscape of Peril enemies ( referred to as enemies) Following this assumption, we would expect lions to have evolved traits that reduce the probability of acquiring parasites, such as avoiding the carcasses of conspecifics and other carnivores even though they represent an easy energy source (Moléon et al, 2017). By illustrating how victims may evolve to detect enemy cues and invest their resources into avoidance behaviors to navigate safely through the landscape of peril, we can predict how animals allocate energy for optimal survival. This depends on the selective pressures or risk imposed by enemies, which can be measured with abundance, lethality, or species richness (Bordes and Morand, 2009). We provide a theoretical backdrop for the evolution of avoidance behaviors in animals subjected to the selective pressures imposed by one or more types of enemy
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