Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels.

Matthew L Holding,Jennifer E Smith,Rulon W Clark,Breanna J Putman,Lauren M Kong

doi:10.3390/toxins12100617

Abstract

Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of “stress”), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator–prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey.

Highlights

Predator–prey interactions are often prolonged, dynamic encounters involving an array of traits expressed by both parties
We evaluated two alternative hypotheses for the connection between ground squirrel physiology and multi-trait defenses against snake predation: (1) a “resistance facilitates boldness” hypothesis where venom resistance directly predicts risky behavior during snake encounters or (2) a “shared physiological correlates” hypothesis where venom resistance and risky behavior are integrated via shared physiological mediators but do not directly affect each other
Assuming this effect and a causal relationship between corticosterone and venom resistance, our sampling of asize and a causal relationship between corticosterone and venom resistance, and given our sampling to 181 ng/g fecal glucocorticoid metabolite (FGM) concentration, the potential exists for changes in corticosterone concentrationsof toa 51 to 181 ng/gresistance

Summary

Introduction

Predator–prey interactions are often prolonged, dynamic encounters involving an array of traits expressed by both parties. Traits shaped by natural selection in this fashion can be potentiated and/or constrained by phenotypic integration, with sets of traits predisposed to correlations within individuals, populations, or species (for review, see [9]). Integration in this context is related to the concept of behavioral syndromes, which focuses more narrowly on correlated suites of behavior [10]. In response to predator attacks, other traits such as morphological or physiological defenses are exposed to selection, and their effectiveness may be modulated by behavioral phenotypes [14,15]. Modeling the relationships among distinct traits, as well as their potential physiological underpinnings, can identify both the strength and form of phenotypic integration in antipredator traits [16]

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Discussion

Conclusion