Austin Z. T. Allison’s research while affiliated with Colorado State University and other places

The acute-phase response (APR) is an adaptive emergency life-history stage, wherein vertebrates exhibit fever and anorexia to survive an infection. However, induced immune responses are energetically costly, and sick animals may reduce physical activity to compensate. Tests of this predicted energetic trade-off in free-ranging animals are rare due to difficulties in measuring individual physiology and behaviour under immune challenge in natural settings. However, recent advances in biologging technology now make such studies possible. We surgically implanted heart rate/temperature loggers in free-ranging adult male Arctic ground squirrels, fitted the squirrels with collar-mounted accelerometers and light/temperature loggers, and injected animals with lipopolysaccharide (LPS) to simulate an immune challenge. LPS-injected squirrels exhibited approximately 1°C overnight fevers accompanied by slightly elevated (10 bpm) heart rates; LPS-injected squirrels also spent 19% less of their time aboveground the following day and reduced overall movement by 40% compared with saline-injected controls. Thus, we found support for an energetic trade-off between functional immune responses (fever and anorexia) and lethargic sickness behaviour within the APR of a free-ranging mammal. Moreover, our results suggest animal-borne devices can play an important role in future studies of vertebrate immunity and disease dynamics.

Ecologists have studied the role of interspecific competition in structuring ecological communities for decades. Differential weather effects on animal competitors may be a particularly important factor contributing to the outcome of competitive interactions, though few studies have tested this hypothesis in free‐ranging animals. Specifically, weather might influence competitive dynamics by altering competitor densities and/or per‐capita competitive effects on demographic vital rates. We used a 9‐year data set of marked individuals to test for direct and interactive effects of weather and competitor density on survival probability in two coexisting mammalian congeners: Columbian ground squirrels (Urocitellus columbianus) and northern Idaho ground squirrels (Urocitellus brunneus). Ambient temperature and precipitation influenced survival probability in both species, but the effects of weather differed between the two species. Moreover, density of the larger Columbian ground squirrel negatively impacted survival probability in the smaller northern Idaho ground squirrel (but not vice versa), and the strength of the negative effect was exacerbated by precipitation. That is, cooler, wetter conditions benefited the larger competitor to the detriment of the smaller species. Our results suggest weather‐driven environmental variation influences the competitive equilibrium between ecologically similar mammals of differential body size. Whether future climate change leads to the competitive exclusion of either species will likely depend on the mechanism(s) explaining the coexistence of these competing species. Divergent body size and, hence, differences in thermal tolerance and giving up densities offer potential explanations for the weather‐dependent competitive asymmetry we documented, especially if the larger species competitively excludes the smaller species from habitat patches of shared preference via interference.

Hibernation is a remarkable behaviour deployed by a diverse array of endotherms within many clades that greatly reduces metabolic need, but also has somatic costs. Hibernation in modern endotherms is often assumed to be an adaptation allowing animals to avoid extreme thermal conditions or food shortages in seasonal environments. However, many animals hibernate when foraging conditions are energetically profitable, suggesting other causal factors influence hibernation behaviour. Understanding the selection pressures responsible for intraspecific variation in the timing and duration of hibernation can help elucidate the relative evolutionary influences of the ultimate ecological causes of hibernation. We tested four previously proposed mechanistic hypotheses to explain intraspecific variation in hibernation phenology in the federally threatened northern Idaho ground squirrel (Urocitellus brunneus): (1) thermal tolerance, (2) food limitation, (3) predation avoidance and (4) sexual selection. The predation avoidance and sexual selection hypotheses received the most support, although we also found some support for the thermal tolerance and food limitation hypotheses. Heavy squirrels increased hibernation duration regardless of environmental conditions, as predicted solely by the predation avoidance hypothesis. Reproductive males emerged from hibernation earlier in spring than other sex–age classes, a pattern predicted by the sexual selection hypothesis. Temperature and food availability explained a much smaller amount of the variation in hibernation behaviour, only partially supporting predictions of the thermal tolerance and food limitation hypotheses. Our results indicate that animals navigate life‐history trade‐offs between energetic allocation to survival and reproduction via state‐dependent optimization of hibernation phenology. Consequently, any future environmental changes that influence body condition will have implications for population ecology and life‐history evolution of hibernating animals due to stark differences in daily survival probability between hibernation and the active season. Read the free Plain Language Summary for this article on the Journal blog.

Food acquisition is among the most important tasks faced by free-ranging animals. Predation and thermal risks, however, can make foraging a costly endeavor and foraging can preclude other important activities. Moreover, seasonal life cycle events such as hibernation impose energetic thresholds and time constraints on foraging. These factors interact with an animal’s endogenous state to influence foraging behavior. We tested a suite of predictions based on foraging theory to explore the effects of thermal environment, body condition, and conspecific density on aboveground activity (which is primarily foraging activity) of the northern Idaho ground squirrel (Urocitellus brunneus), an imperiled rodent that hibernates for 9 months each year. We took advantage of the squirrels’ semi-fossorial lifestyle to document daily aboveground activity by attaching geolocators to squirrels. We modeled squirrel activity with generalized linear mixed-effects models to document the relative importance of thermal environment, body condition, and conspecific density for daily aboveground activity. Aboveground activity by northern Idaho ground squirrels increased throughout their active season and leaner squirrels increased their activity more than heavier squirrels as residual foraging opportunities diminished. Thermal conditions also influenced squirrel activity: squirrels spent less time above ground during extreme temperatures and on days with significant precipitation. Aboveground activity of northern Idaho ground squirrels largely adhered to predictions of risk-sensitive and state-dependent foraging theory. Management actions that enhance forage will likely improve the probability of recovery for this federally threatened species by minimizing trade-offs squirrels need to make to acquire sufficient food to survive hibernation and reproduce in subsequent years. Significance statement Acquiring food is a vital task for wild animals, but foraging can be dangerous. Hibernation imposes annual energetic requirements animals must meet within a short time when food is available and the animal is active. Hibernating species, therefore, must navigate trade-offs among foraging, predation risk, and thermal intolerance. We investigated how these pressures influence daily foraging activity of the northern Idaho ground squirrel (Urocitellus brunneus), a federally threatened species. Ground squirrels forage above ground during the active season and retreat to burrows to avoid predation and extreme weather but accept greater risks to forage as hibernation approaches. Additionally, lean squirrels with high energetic needs forage more than heavy squirrels, exposing lean squirrels to higher predation risk. Improving forage may improve recovery odds for this imperiled species by allowing squirrels to reduce their mortality risk.