Abstract
Predators kill and consume prey, but also scare living prey. Fitness of prey can be reduced by direct killing and consumption, but also by non-consumptive effects (NCEs) if prey show costly risk-induced trait responses (RITRs) to predators, which are meant to reduce predation risk. Recently, similarities between predators and parasites as natural enemies have been recognized, including their potential to cause victim RITRs and NCEs. However, plant-herbivore and animal host-parasite associations might be more comparable as victim-enemy systems in this context than either is to prey-predator systems. This is because plant herbivores and animal parasites are often invertebrate species that are typically smaller than their victims, generally cause lower lethality, and allow for further defensive responses by victims after consumption begins. Invertebrate herbivores can cause diverse RITRs in plants through various means, and animals also exhibit assorted RITRs to increased parasitism risk. This synthesis aims to broadly compare these two enemy-victim systems by highlighting the ways in which plants and animals perceive threat and respond with a range of induced victim trait responses that can provide pre-emptive defense against invertebrate enemies. We also review evidence that RITRs are costly in terms of reducing victim fitness or abundance, demonstrating how work with one victim-enemy system can inform the other with respect to the frequency and magnitude of RITRs and possible NCEs. We particularly highlight gaps in our knowledge about plant and animal host responses to their invertebrate enemies that may guide directions for future research. Comparing how potential plant and animal victims respond pre-emptively to the threat of consumptionviaRITRs will help to advance our understanding of natural enemy ecology and may have utility for pest and disease control.
Highlights
On the surface, a tomato plant reacting to the presence of a hungry hornworm caterpillar and a squirrel to that of ticks in the vicinity might seem to have little in common
Prey will often avoid foraging in areas, or at times, with high predation risk, and predator exposure can elevate levels of hormones in prey that are associated with a stress response (e.g., Dahl et al, 2012)
Prey-predator systems have been the primary focus for non-consumptive effects (NCEs) and trait-mediated indirect effects (TMIEs), but there are growing efforts to synthesize this area by considering other natural enemies, such as parasites and pathogens (e.g., Raffel et al, 2008; Buck et al, 2018; Weinstein et al, 2018a; Daversa et al, 2021)
Summary
A tomato plant reacting to the presence of a hungry hornworm caterpillar and a squirrel to that of ticks in the vicinity might seem to have little in common. There are certain key biological and ecological similarities in how plants and animals interact with their invertebrate herbivore and parasite enemies, respectively— more so than either of these compared to prey and predators, even though comparisons between the latter and host-parasite associations have been the primary focus far (e.g., Raffel et al, 2008; Buck and Ripple, 2017; Daversa et al, 2021). The allocation costs associated with phenotypic plasticity in traits related to victim resistance are central to evaluating NCEs (Peacor et al, 2020) Because both of these victim types may face trade-offs between investments in resistance and tolerance, this could constrain enemy riskinduced pre-emptive defenses compared to those of animal prey in response to predators. We briefly consider the potential for TMIEs in both victim-enemy systems
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