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

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.

The benefits of being dominant: health correlates of male social rank and age in a marmot

“…Support for the immunocompetence handicap hypothesis is consistent with the hypothesis that chronic stressors can induce a rise in GC levels and this hormonal response compromises vertebrate immune systems ( Davis et al 2008 ). The elevated GC levels due to environmental stresses are also known to suppress the immune function of individuals by changing the leukocyte component of many vertebrates such as increasing the ratio of heterophils or neutrophils to lymphocytes ( Davis et al 2008 ), which increase the pathogen and parasite burden or reduce resistance to toxins ( Holding et al 2020 ). For example, an adverse effect of reduced health is also associated with higher parasite burden as well as more prominent secondary sexual characteristics in the lacertid lizard ( Psammodromus algirusi ; Salvador et al 1996 ) and red grouse ( Trrichostonglys lenuis ; Mougeot et al 2006 ), respectively.…”

Sensory integration of danger and safety cues may explain the fear of a quiet coyote

“…Another major finding of our study was that individuals were consistent in their behavioural reactivity—but not in their time spent near stimuli—across treatments. This finding adds to our growing understanding of the consistent individual differences in California ground squirrels [36,63,75,78] and other animals [76,110,111]. More broadly, given that individuals residing at the human-impacted site were also consistently most reactive to predator cues, future studies should investigate the extent to which fear of predators generalizes to fearfulness of other dangers, including humans [112].…”

“…Animals at the disturbed site are generally less reactive to humans, have higher glucocorticoid levels, and are in poorer body condition than those residing at the relatively pristine site [69,77]. Moreover, ground squirrels at our study sites have consistent individual differences in behaviour across time and contexts [36,63,75,78].…”

“…We focused on the free-living California ground squirrel (Otospermophilus beecheyi), an endemic in California grasslands that is a major prey species for northern Pacific rattlesnakes (Crotalus oreganus), birds of prey and coyotes (Canis latrans) [34]. California ground squirrels represent a textbook example of a species that produces a suite of multimodal, anti-predator signals-alarm calls (acoustic), tail-flagging (visual) and infrared heat (electromagnetic) [35][36][37][38][39]. They also respond to conspecific alarm calls [40][41][42].…”

Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey

“…Individuals with high levels of SVMPI proteins in their serum can survive an envenomation that would rapidly immobilize or kill non‐resistant mammals (Biardi, 2008). Yet, there is significant variation among both populations and species in SVMPI composition and function (Biardi, 2008; Perales et al., 2005), suggesting that fitness trade‐offs associated with particularly resistant phenotypes exist (Holding et al., 2020). For example, California Ground Squirrel populations studied across geographic space show a high degree of intraspecific variation in SVMP resistance (Holding, Biardi, et al., 2016; Poran et al., 1987), whereas species specificity in SVMPI function manifests when allopatric snake and rodent species are tested against one another (Pomento et al., 2016).…”