Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants

Abstract

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Risk-Induced Trait Responses and Non-consumptive Effects in Plants and Animals in Response to Their Invertebrate Herbivore and Parasite Natural Enemies

“…As victims, there are certain key biological and ecological similarities in how plants and animals interact with their invertebrate herbivore and parasite enemies, respectivelymore 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 thus far (e.g., Raffel et al, 2008;Buck and Ripple, 2017;Daversa et al, 2021). Considering similarities between plants and animals as victims of predators has been useful for evaluating the timing of defensive investment and fitness loss (Sheriff et al, 2020a). Comparing these two taxa as victims of parasites has also provided a framework for better understanding ecological immunity and infection tolerance (Baucom and de Roode, 2011).…”

“…Secondly, given the sheer number of species represented by invertebrate herbivores and animal parasites (Howe and Jander, 2008), many have a high degree of specificity for particular victims (Bernays and Graham, 1988;Combes, 2001). Last, and most important, consumption by herbivores or parasites of their respective victims is rarely lethal, in contrast to predators of animal prey (Buck and Ripple, 2017;Cortez and Duffy, 2020;Sheriff et al, 2020a). While enemy encounter is likely relatively frequent and prolonged, the nature and capacity for victim damage by herbivores and parasites is limited compared to damage to animal prey caused by predators.…”

“…We thus expect pre-emptive defenses to be more common, and perhaps stronger, for prey than for plants and animal hosts-the latter two victim types have alternative avenues for adaptive responses available to them. In addition, victims that are likely to incur large costs if attacked, such as fitness losses, are predicted to perceive and respond to elevated enemy risk relatively early in the attack sequence compared to organisms with lower proportional cost(s) if attacked (Sheriff et al, 2020a). Plant and animal hosts are more similar in the expectation of delayed timing of a response than either is to prey.…”

“…Plants and animals clearly have different sensory structures and capabilities, yet both may perceive cues related to the risk of attack by herbivores or parasites, respectively, in similar waysjust as for their perception of predators (Sheriff et al, 2020a). These natural enemies may be perceived pre-contact, during physical contact before consumption occurs, or even after some minor attack that has not yet incurred meaningful energetic costs to the victim.…”

“…We have compared plant-herbivore and animal host-parasite systems in terms of victim-enemy interactions toward identifying broad attributes relevant for documenting NCEs-similar to efforts to draw parallels between host-parasite and prey-predator systems (e.g., Raffel et al, 2008;Buck et al, 2018;Daversa et al, 2021), and plant-herbivore and prey-predator systems (Sheriff et al, 2020a). Specifically, we considered plant-herbivore and animal-parasite systems with respect to the victim's ability to perceive enemy risk, the range and magnitude of possible RITRs shown by victims, and whether these responses affect victim fitness or abundance (NCEs).…”