Risk of predation increases susceptibility to parasitism via trait-mediated indirect effects.

Abstract

The presence of natural enemies can cause organisms to change habitat use, foraging behavior, and/or resource allocation in response to a perceived risk, responses that may come at the cost of other fitness-related traits. Since most species encounter multiple natural enemies in nature, defensive behaviors against one attacker may make the focal organism more vulnerable to attack by a different natural enemy. Anti-predator behaviors can lead to trait-mediated indirect effects, such as an increased risk of parasitism and vice versa. Few empirical studies have examined the response of a single focal species to the risk of attack by multiple species. Our experiments provided the cactiphilic fly Drosophila nigrospiracula with opportunities to prioritize either anti-predator (e.g., reduced activity) or anti-parasite behavior (e.g., increased activity) at the cost of increased infection or predation, respectively. We experimentally show that when flies were exposed to ectoparasitic mites, in the presence of predator (jumping spider) cues, flies incurred increased levels of infection compared to flies without predator cues. The mean infection prevalence increased by 80% and the infection intensity increased by 180%. However, the presence of parasite cues had no analogous effect on predation rates, which suggests that flies prioritized predation risk over parasite defense at the cost of increased infection. We provide empirical evidence that the presence of multiple threats can lead to trait-mediated indirect effects, with important consequences for host-parasite and food web dynamics, and the ecology of fear.