Conservation of threatened San Joaquin antelope squirrels: distribution surveys, habitat suitability, and conservation recommendations

The San Joaquin antelope squirrel (Ammospermophilus nelsoni: SJAS) is listed as Threatened pursuant to the California Endangered Species Act due to profound habitat loss throughout its range in the San Joaquin Desert in California. Habitat loss is still occurring and critical needs for SJAS include identifying occupied sites, quantifying optimal habitat conditions, and conserving habitat. Our objectives were to (1) conduct surveys to identify sites where SJAS were present, (2) assess habitat attributes on all survey sites, (3) generate a GIS-based model of SJAS habitat suitability, (4) use the model to determine the quantity and quality of remaining habitat, and (5) use these results to develop conservation recommendations. SJAS were detected on 160 of the 326 sites we surveyed using automated camera stations. Sites with SJAS typically were in arid upland shrub scrub communities where desert saltbush (Atriplex polycarpa) or jointfir (Ephedra californica) were the dominant shrubs, although shrubs need not be present for SJAS to be present. Sites with SJAS usually had relatively sparse ground cover with >10% bare ground and Arabian grass (Schismus arabicus) was the dominant grass. SJAS were more likely to occur on sites where kangaroo rats (Dipodomys spp.) were present and burrow abundance was greater, but SJAS were less likely to be present on sites with California ground squirrels (Otospermophilus beecheyi). Based on our habitat suitability model, an estimated 5,931 km2 of high or moderately high quality habitat and 4,753 km2 of lower quality habitat remain. To conserve SJAS, we recommend (1) conducting additional SJAS surveys on sites not surveyed but with suitable habitat, (2) conserving unprotected lands with suitable habitat, (3) managing vegetation on occupied sites if necessary, (4) restoring disturbed lands to increase suitability for SJAS, and (5) conducting translocations of SJAS to unoccupied sites with suitable habitat.

Potential impact of diphacinone application strategies on secondary exposure risk in a common rodent pest: implications for management of California ground squirrels

Anticoagulant rodenticides are a common tool used to manage rodents in agricultural systems, but they have received increased scrutiny given concerns about secondary exposure in non-target wildlife. Rodenticide application strategy is one factor that influences exposure risk. To understand the impact of application strategy, we tested residues of a first-generation anticoagulant (diphacinone) in liver tissue of radiotransmittered California ground squirrels (Otospermophilus beecheyi) following spot treatments, broadcast applications, and bait station applications in rangelands in central California during summer and autumn 2018–2019. We also documented the amount of bait applied, the mean time from bait application until death, and the proportion of ground squirrels that died belowground. We documented the greatest amount of bait applied via bait stations and the least by broadcast applications. We did not document a difference in diphacinone residues across any application strategy, although survivors had an order of magnitude lower concentration of diphacinone than mortalities, potentially lowering secondary exposure risk. We did not observe any difference among bait delivery methods in time from bait application to death, nor did we identify any impact of seasonality on any of the factors we tested. The vast majority of mortalities occurred belowground (82–91%), likely reducing secondary exposure. Secondary exposure could be further reduced by daily carcass searches. Results from this study better define risk associated with first-generation anticoagulant rodenticide applications, ultimately assisting in development of management programs that minimize non-target exposure.

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

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.

Physiological and behavioral responses to anthropogenic stressors in a human-tolerant mammal

As humans continue to alter natural habitats, many wild animals are facing novel suites of environmental stimuli. These changes, including increased human–wildlife interactions, may exert sublethal impacts on wildlife such as alterations in stress physiology and behavior. California ground squirrels (Otospermophilus beecheyi) occur in human-modified as well as more pristine environments, where they face a variety of anthropogenic and naturally occurring threats. This makes this species a valuable model for examining the effects of diverse challenges on the physiology and behavior of free-living mammals. To explore potential sublethal effects of habitat modification on O. beecheyi, we compared body masses, behaviors, and fecal glucocorticoid metabolite (FGM) levels for free-living squirrels in human-disturbed versus undisturbed habitats. Prior to these analyses, we validated the use of FGMs in this species by exposing captive O. beecheyi to pharmacological and handling challenges; both challenges produced significant increases in FGMs in the study animals. While FGM responses were repeatable within captive individuals, responses by free-living animals were more variable, perhaps reflecting a greater range of life-history traits and environmental conditions within natural populations of squirrels. Animals from our human-disturbed study site had significantly higher FGMs, significantly lower body masses, and were significantly less behaviorally reactive to humans than those from our more pristine study site. Thus, despite frequent exposure of California ground squirrels to human impacts, anthropogenic stressors appear to influence stress physiology and other phenotypic traits in this species. These findings suggest that even human-tolerant mammalian species may experience important sublethal consequences due to human modifications of natural habitats.

Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

Measuring local adaptation can provide insights into how coevolution occurs between predators and prey. Specifically, theory predicts that local adaptation in functionally matched traits of predators and prey will not be detected when coevolution is governed by escalating arms races, whereas it will be present when coevolution occurs through an alternate mechanism of phenotype matching. Here, we analyse local adaptation in venom activity and prey resistance across 12 populations of Northern Pacific rattlesnakes and California ground squirrels, an interaction that has often been described as an arms race. Assays of venom function and squirrel resistance show substantial geographical variation (influenced by site elevation) in both venom metalloproteinase activity and resistance factor effectiveness. We demonstrate local adaptation in the effectiveness of rattlesnake venom to overcoming present squirrel resistance, suggesting that phenotype matching plays a role in the coevolution of these molecular traits. Further, the predator was the locally adapted antagonist in this interaction, arguing that rattlesnakes are evolutionarily ahead of their squirrel prey. Phenotype matching needs to be considered as an important mechanism influencing coevolution between venomous animals and resistant prey.