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Daily foraging activity of an imperiled ground squirrel: effects of hibernation, thermal environment, body condition, and conspecific density

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Austin Z. T. Allison
Austin Z. T. Allison
Austin Z. T. Allison
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Courtney Conway at University of Idaho
Courtney Conway
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Abstract and Figures

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.
We placed 5 radio collars equipped with geolocators in different positions relative to the entrance of a northern Idaho ground squirrel nest burrow (a) for 24 h on a cloudless day in summer 2020 to determine the threshold for classifying a squirrel as above or below ground during a given sampling interval. We placed a 6th geolocator ~ 100 m away in full shade to account for cloudy days and squirrels foraging in shade. The geolocators at 0 cm (burrow mouth) and 5 cm below the nest burrow entrance recorded values ≥ 1000 lx (horizontal dashed line) on 22% and 7% of sampling intervals from 8:00 to 20:00 MDT and the 2 geolocators > 5 cm below the entrance never recorded values ≥ 1000 lx (b). Conversely, the shaded and non-shaded aboveground geolocators recorded values ≥ 1000 lx on 97% and 100% of sampling intervals from 8:00 to 20:00 MDT. We therefore used 1000 lx as the threshold to determine whether a squirrel was above (≥ 1000 lx) or below (< 1000 lx) ground for geolocator readings we obtained from free-ranging squirrels
We placed 5 radio collars equipped with geolocators in different positions relative to the entrance of a northern Idaho ground squirrel nest burrow (a) for 24 h on a cloudless day in summer 2020 to determine the threshold for classifying a squirrel as above or below ground during a given sampling interval. We placed a 6th geolocator ~ 100 m away in full shade to account for cloudy days and squirrels foraging in shade. The geolocators at 0 cm (burrow mouth) and 5 cm below the nest burrow entrance recorded values ≥ 1000 lx (horizontal dashed line) on 22% and 7% of sampling intervals from 8:00 to 20:00 MDT and the 2 geolocators > 5 cm below the entrance never recorded values ≥ 1000 lx (b). Conversely, the shaded and non-shaded aboveground geolocators recorded values ≥ 1000 lx on 97% and 100% of sampling intervals from 8:00 to 20:00 MDT. We therefore used 1000 lx as the threshold to determine whether a squirrel was above (≥ 1000 lx) or below (< 1000 lx) ground for geolocator readings we obtained from free-ranging squirrels
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Aboveground (i.e., foraging) activity (± 95% CI) of northern Idaho ground squirrels was highest during mid-morning hours and lowest in the hours immediately after sunrise and before sunset (a); x-axis is proportional time of day for daylight hours, which accounts for changes in daylength across the active season (i.e., 0.5 = solar noon). Julian day (b), body condition (b), and conspecific density (c) influenced aboveground activity (± 95% CI) of northern Idaho grounds during daylight hours. Thermal conditions—ambient aboveground temperature (d), ambient aboveground solar radiation (d), and daily precipitation (e)—also influenced aboveground activity (± 95% CI) of northern Idaho ground squirrels during daylight hours. We generated these partial effects plots from model-averaged parameter estimates from the top generalized linear mixed-effects models designed to explain variation in northern Idaho ground squirrel aboveground activity. All models included data from 1142 squirrel days and 211,128 sampling intervals derived from 59 geolocator-equipped, free-ranging adult squirrels during summer 2017 through spring 2020
Aboveground (i.e., foraging) activity (± 95% CI) of northern Idaho ground squirrels was highest during mid-morning hours and lowest in the hours immediately after sunrise and before sunset (a); x-axis is proportional time of day for daylight hours, which accounts for changes in daylength across the active season (i.e., 0.5 = solar noon). Julian day (b), body condition (b), and conspecific density (c) influenced aboveground activity (± 95% CI) of northern Idaho grounds during daylight hours. Thermal conditions—ambient aboveground temperature (d), ambient aboveground solar radiation (d), and daily precipitation (e)—also influenced aboveground activity (± 95% CI) of northern Idaho ground squirrels during daylight hours. We generated these partial effects plots from model-averaged parameter estimates from the top generalized linear mixed-effects models designed to explain variation in northern Idaho ground squirrel aboveground activity. All models included data from 1142 squirrel days and 211,128 sampling intervals derived from 59 geolocator-equipped, free-ranging adult squirrels during summer 2017 through spring 2020
… 
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https://doi.org/10.1007/s00265-022-03142-4
ORIGINAL ARTICLE
Daily foraging activity ofanimperiled ground squirrel: effects
ofhibernation, thermal environment, body condition, andconspecific
density
AustinZ.T.Allison1 · CourtneyJ.Conway2
Received: 5 October 2021 / Revised: 25 January 2022 / Accepted: 27 January 2022 / Published online: 7 February 2022
This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2022, corrected publication 2022
Abstract
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 forag-
ing 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 squir-
rel 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.
Signicance statement
Acquiring food is a vital task for wild animals, but foraging can be dangerous. Hibernation imposes annual energetic require-
ments 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 spe-
cies. 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.
Keywords Optimal foraging· Risk sensitivity· State dependence· Hibernation· Geolocator· Ground squirrel
Introduction
Obtaining sufficient food is arguably the most important task
free-ranging animals confront each day. Foraging decisions
are, however, more nuanced than merely maximizing food
intake, and herbivorous animals face trade-offs regarding
Communicated by A. G. Ophir
* Austin Z. T. Allison
aallison@uidaho.edu
Extended author information available on the last page of the article
Behavioral Ecology and Sociobiology (2022) 76: 28
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... The northern Idaho ground squirrel is a small-bodied, semifossorial rodent endemic to west-central Idaho. Adult female body mass ranges seasonally from ∼100 g at hibernation emergence in spring to ∼180 g at hibernation immergence in summer; adult male body mass ranges from ∼120 g at hibernation emergence in spring to ∼270 g at hibernation immergence in summer (Allison and Conway 2022). These rare squirrels are listed as federally threatened under the US Endangered Species Act due to population declines in the twentieth century (US Fish and Wildlife Service 2000; Sherman and Runge 2002;Yensen and Dyni 2020). ...
... To test the surface assessment hypothesis, we captured northern Idaho ground squirrels in baited Tomahawk traps (Tomahawk Live Trap, Hazelhurst, WI) and via focal animal trapping (Allison and Conway 2022). We attached VHF radio collars (Holohil Systems, Ottawa, Ontario; Lotek, Newmarket, Ontario) and geolocators (Migrate Technology, Cambridge) to 207 adult (≥1 yr old in the year they were collared) squirrels (92 males and 115 females; table S3). ...
... We attached VHF radio collars (Holohil Systems, Ottawa, Ontario; Lotek, Newmarket, Ontario) and geolocators (Migrate Technology, Cambridge) to 207 adult (≥1 yr old in the year they were collared) squirrels (92 males and 115 females; table S3). Geolocators recorded the maximum ambient light intensity during 5-min intervals, allowing us to ascertain whether a squirrel emerged aboveground during a given 5-min sampling interval Allison and Conway 2022). We considered any light intensity reading 10 lux to indicate that a squirrel had emerged to the surface because northern Idaho ground squirrels plug hibernacula such that no light penetrates the burrow system until the squirrel surfaces. ...
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... However, population declines within that limited historical range are often attributed to encroachment by woody vegetation into the meadows and scablands the squirrels inhabit during their active season (Gavin et al., 1999;Sherman & Runge, 2002). Additional potential threats to northern Idaho ground squirrel populations include land conversion for human use (Yensen & Dyni, 2020), invasive pathogens , and climate change (Allison & Conway, 2022). ...
... We set 30 traps in a grid at each site each trapping day, with traps placed at burrow entrances. We also captured northern Idaho ground squirrels in nonbaited 'focal' traps to increase captures of these rare squirrels (Allison & Conway, 2022;Goldberg, Conway, Evans Mack, & Burak, 2020). We trapped 6-10 h per trapping day (depending on weather conditions) and checked traps for captured animals every 30-60 min. ...
... Habitat selection resulting from the competitive asymmetry we documented is a likely explanation for the coexistence of northern Idaho ground squirrels and Columbian ground squirrels (Morris, 2003;Rosenzweig, 1981Rosenzweig, , 1991. We expect that these squirrel species share preferred habitat given that ground squirrels must dig burrows for thermal shelter (Allison & Conway, 2022;Williams et al., 2016) and to provide refuge from predators (Allison & Conway, 2022;Holmes, 1984;Thorson et al., 1998), and the two species have overlapping herbivorous diets (Dyni & Yensen, 1996;Goldberg, Conway, Tank, et al., 2020;Yensen et al., 2018). Mesic meadows may represent the highest-quality habitat for both species in our system. ...
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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.
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... Because daily survival probability in northern Idaho ground squirrels is higher during hibernation than the active season (Allison et al., in review)-as is the case in most hibernators (Turbill et al., 2011)-squirrels may navigate life-history trade-offs by optimizing hibernation phenology to maximize fitness (Bieber et al., 2018;Constant et al., 2020;Hoelzl et al., 2015;Michener, 1977). The most likely explanation for the stark difference in daily survival probability between the active season and hibernation is differential predation risk associated with seasonal differences in above-ground activity (Allison & Conway, 2022;Constant et al., 2020;Turbill et al., 2011;Turbill & Stojanovski, 2018). Thus, optimal foraging theory predicts that squirrels modulate immergence timing, dependent on their energetic state, to annually balance the costs (e.g. ...
... After mating, Northern Idaho ground squirrels spend the remainder of the active season foraging to attain energetic reserves to rear young and survive their long annual hibernation period (Allison & Conway, 2022). The squirrels experience high levels of predation during the active season (Yensen & Sherman, 1997), which we frequently documented at our study sites. ...
... Geolocators sampled ambient light intensity every minute and recorded the maximum value across 5-min sampling intervals. Light intensity data allowed us to determine when a squirrel immerged into and emerged from a hibernaculum to the nearest 5 min (Allison & Conway, 2022). Geolocators also sampled and recorded temperature every 15 min, which provided ground squirrel skin temperature during hibernation. ...
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... Biologging data can be used to explore the complex relationships between behavior and body condition (Amo et al., 2007;Beale & Monaghan, 2004;Ransom et al., 2010). With our limited sample size, we documented that all gray whales with a BAI below average (i.e., less than median PCFG gray whale BAI of $26) consistently made more foraging dives than search or transit, which aligns with previous work that found individuals in poorer body condition spent more time foraging (Allison & Conway, 2022;Ransom et al., 2010;Skogland & Grøvan, 1988;Stawski & Geiser, 2010). Body condition may also play a role in how animals respond behaviorally to disturbances, as a recent meta-analysis shows that individuals in poorer body condition are more likely to exhibit high-risk behaviors (Moran et al., 2021) that potentially increases their exposure to disturbances. ...
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... Models with the lowest AICc are indicated in bold. 'Mean NDVI' corresponds to the estimated vegetation biomass over the active season of ground squirrels 2008; Idaho ground squirrel, Urocitellus brunneus, Allison and Conway 2022). Similarly, the reproductive success of reindeer (Rangifer tarandus) has been shown to respond both to population density and vegetation green-up (Tveraa et al. 2013). ...
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... Energy regulation is a key factor in animal life histories (Brown et al., 2004). Energy acquisition and expenditure can be strongly influenced by weather conditions either via effects on foraging resources (modifications of resource availability and acquisition; Allison and Conway, 2022) or via effects on animal behavior (e.g. foraging behavior) and metabolism (e.g. ...
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Article
  • Jul 2021
Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels (Urocitellus brunneus – NIDGS, and U. endemicus - SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single-nucleotide polymorphisms (SNPs) from buccal swabs with restriction site-associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both theinter- and intraspecific level, and identified putatively adaptive SNPs using population structure outlier detection and genotype-environment association (GEA) analyses. At the interspecific level, we detected a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation putatively linked to torpor patterns. At the intraspecific level, we found evidence of both neutral and adaptive differentiation. For NIDGS, elevation appears to be the main driver of adaptive differentiation, while neutral variation patterns match and expand information on the low connectivity between some populations identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected natural geographic barriers, while adaptive variation reflected differences in land cover and temperature, as well as elevation. These results clearly highlight the roles of neutral and adaptive processes for understanding the complexity of the processes leading to species and population differentiation, which can have important conservation implications in susceptible and threatened species.
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Hibernation behavior of a federally threatened ground squirrel: Climate change and habitat selection implications
Article
  • Apr 2021
Hibernation is an adaptation to survive periods of stress, from food limitation or harsh thermal conditions. A key question in contemporary ecology is whether rare, range-restricted species can change their behavior in response to climate change (i.e., through behavioral plasticity). The northern Idaho ground squirrel, Urocitellus brunneus (A. H. Howell, 1928), is a federally threatened species that hibernates for approximately 8 months per year within the bounds of its small range in central Idaho, USA. Changes in temperature, snow accumulation, and summer precipitation, all brought about as a result of climate change, may reduce survival or fecundity of northern Idaho ground squirrels if they cannot adapt to these climate changes. Hibernating species can respond to climate-change-induced thermal challenges in two ways: change their hibernation physiology and behavior (i.e., emergence date or number of torpor bouts) or alter their environment (i.e., change hibernacula depth or location). We explored a suite of intrinsic and extrinsic factors to document the extent to which they influenced hibernation behavior of northern Idaho ground squirrels. Emergence date was positively associated with snowpack and negatively associated with mean winter temperature. Mean minimum skin temperature was negatively associated with canopy closure and slope of a squirrel's hibernaculum. Duration of the heterothermal period, number of euthermic bouts, and total time spent euthermic were positively associated with body mass. Immergence date and duration of the longest torpor bout were negatively associated with body mass. Warmer temperatures and less snow accumulation in the winter-caused by climate change-likely will cause altered emergence dates. Our results suggest that any future climate-induced changes in snowfall, ambient temperature, food availability, or habitat likely will impact survival of this rare ground squirrel, because such changes will cause changes in hibernation behavior, percent mass loss during hibernation, and duration of the active season when small mammals are more susceptible to predation.
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