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Sex and age class influenced northern Idaho ground squirrel hibernation (a) immergence date (Julian day), (b) emergence date (Julian day) and (c) duration (number of days), providing support for the predation avoidance and sexual selection hypotheses. Sample sizes are included above 95% CI. Marginal effects were derived from the top linear mixed‐effects models designed to explain intraspecific variation in each response variable (i.e. the three hibernation behaviours).
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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 anima...
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... A larger amount of stored fat has been shown in different mammals to enable a more flexible use of heterothermy, as an adaptation to unpredictable environmental conditions, predator avoidance or reproductive strategies (Allison et al., 2023;Bieber et al., 2013;Zervanos et al., 2013). The use of daily (< 24 h) or prolonged torpor (>24 h) or even hibernation for several weeks was already reported in six of the 19 different mouse lemur species (Blanco et al., , 2018Dausmann and Warnecke, 2016). ...
... jonahi and M. simmonsi (Andriambeloson et al., 2020;this study), and (2) that modern distributions are a relic of historical colonization and habitat suitability (Dausmann and Warnecke, 2015;Nowack and Dausmann, 2016). The capacity to deposit larger amounts of fat may generally provide a higher flexibility to persist under unpredictable environmental conditions (Allison et al., 2023;Bieber et al., 2013;Blanco et al., 2018;Dausmann, 2014;Wright, 1999;Zervanos et al., 2013). The paleoclimatic oscillations of the Pleistocene, during which the diversification of the genus Microcebus likely happened (van Elst et al., 2024;Yoder et al., 2016), were characterized by an exceptional unpredictability (Hofreiter and Stewart, 2009;Lupien et al., 2020) During a glacial maximum, increased aridity and lower annual mean temperatures in the tropics have led to a contraction of forests to areas still receiving sufficient water supply (Gasse and Van Campo, 2001;Teixeira et al., 2021;Wilmé et al., 2006). ...
Species distributions are shaped by complex biotic and abiotic interactions. We studied major ecological drivers of the distribution of four cryptic mouse lemur species (Microcebus spp.) in northeastern Madagascar, across sympatric and allopatric ranges. Using structural habitat characteristics, adaptability to habitat degradation, bioclimatic niches, and morphology, we estimated n-dimensional hypervolumes of niche sizes and overlaps. Annual body mass variability was analyzed as an indicator of heterothermy, a potential indicator for ecological plasticity.
M. jonahi and M. simmonsi were found almost equally often in forest- and fallow-derived habitats (52% and 58%, respectively), while M. lehilahytsara predominantly occupied fallow habitats (71%), likely driven by the coexistence with other species. M. lehilahytsara exhibited the largest niche and range size, followed by M. jonahi and M. simmonsi. In contrast, M. macarthurii was restricted to a narrow niche and range. M. jonahi and M. simmonsi displayed significant fat deposition before the austral winter, indicating heterothermy as an adaptation to unpredictable environmental conditions. These species were only found in allopatry, likely due to competition for critical resources like sleeping sites. The smaller M. lehilahytsara coexisted with M. jonahi and M. macarthurii potentially by adjusting its niche to avoid competition with these larger-bodied species.
We hypothesize that heterothermy allowed M. jonahi, M. simmonsi, and M. macarthurii to persist in lowlands during Pleistocene climatic challenges but that it did not promote coexistence. In contrast, M. lehilahytsara may have lost lowland distributions due to a lower ability to store fat. Our findings require further testing but provide a plausible explanation for a complex distributional pattern of sympatric and allopatric occurrences.
... In a recent study, predation avoidance and sexual selection received support for explaining intraspecific variation in hibernation phenology in the northern Idaho ground squirrel (Urocitellus brunneus, Allison et al., 2023) Males often emerged from dormancy and arrived at mating sites some days or weeks before females (termed 'protandry'), and mating occurred shortly after female emergenced from dormancy. Sexual selection may favor a life history in which relatively early-emerging males benefit from greater reproductive success (the 'mating opportunity hypothesis, ' Morbey and Ydenberg, 2001). ...
Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.
... In a recent study, predation avoidance and sexual selection received support for explaining intraspecific variation in hibernation phenology in the northern Idaho ground squirrel (Urocitellus brunneus, Allison et al., 2023) Males often emerged from dormancy and arrived at mating sites some days or weeks before females (termed 'protandry'), and mating occurred shortly after female emergenced from dormancy. Sexual selection may favor a life history in which relatively early-emerging males benefit from greater reproductive success (the 'mating opportunity hypothesis, ' Morbey and Ydenberg, 2001). ...
Seasonal animal dormancy, hibernation or diapause, is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Other survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the “life-history” hypothesis), but comparative tests across animal species are not yet available. Under this hypothesis, dormancy phenology is influenced by a trade-off between reproductive advantages of being active and survival benefits of dormancy. Within a species, males and females differ in the amount of time and energy they invest in reproduction. Thus, the trade-off between reproduction and survival may be reflected by within-species sex differences in the phenology of dormancy. To examine this hypothesis, we used two complementary approaches: (i) a set of phylogenetic comparative analyses on mammals (mainly holarctic rodents), and (ii) a comparison between endotherm and ectotherm dormancy, via analyses of endotherms (including mainly holoarctic rodents) and the existing literature on ectotherms. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life history hypotheses, sex differences in emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that, low temperature and precipitation as well as smaller body mass influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy (invertebrates and reptiles) may be 1) less temperature dependent than previously thought and 2) associated with trade-offs consistent with the life history hypothesis. Dormancy in some endotherms and ectotherms show staggered phenology with respect to the growing season (earlier emergence and immergence than expected) which illustrates the selection pressure exerted by the trade-off between reproduction (earlier emergence than expected) and adult survival (earlier immergence than expected). Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously appreciated.
... However, individuals often enter a potentiation phase near the conclusion of seasonal hibernation that marks the transition from dormancy to activity and is characterized by shorter torpor bouts and longer arousal bouts (Geiser et al. 1990;Ruf and Geiser 2015;Williams et al. 2017a;Wilsterman et al. 2021). Although hibernation phenology is often assumed to be determined by ambient temperature and food availability (Humphries et al. 2003), optimal hibernation phenology balances trade-offs among these and several other selection pressures to maximize individual fitness (Michener 1983;Allison et al. 2023;Ruf and Bieber 2023). Indeed, predation risk and reproductive requirements often explain more intraspecific variation in hibernation phenology than thermal tolerance or food limitation (Stawski and Geiser 2010;Bieber et al. 2014;Williams et al. 2017a;Allison et al. 2023). ...
... Although hibernation phenology is often assumed to be determined by ambient temperature and food availability (Humphries et al. 2003), optimal hibernation phenology balances trade-offs among these and several other selection pressures to maximize individual fitness (Michener 1983;Allison et al. 2023;Ruf and Bieber 2023). Indeed, predation risk and reproductive requirements often explain more intraspecific variation in hibernation phenology than thermal tolerance or food limitation (Stawski and Geiser 2010;Bieber et al. 2014;Williams et al. 2017a;Allison et al. 2023). ...
... Testosterone production inhibits torpor expression, resulting in earlier emergence from hibernation than is energetically optimal in males but allowing phenological synchrony between the sexes (i.e., simultaneous reproductive maturation ;Lee 1990;Richter et al. 2017). However, many species shift hibernation phenology (especially hibernation termination and emergence timing; table S1) in response to environmental variation (e.g., ambient temperature and snowmelt ;Michener 1977;Murie and Harris 1982;Inouye et al. 2000;Lane et al. 2012;Williams et al. 2017a;Kucheravy 2021;Allison et al. 2023;Chmura et al. 2023;Thompson et al. 2023). Given these patterns, male hibernators might be expected to plastically modulate emergence timing to maximize their status within intrasexual breeding hierarchies (e.g., by claiming and defending breeding territories) while avoiding starvation and maintaining reproductive synchrony with later-emerging females (i.e., emerging sufficiently early to establish spermatogenesis before female emergence from hibernacula; Thompson et al. 2023). ...
... The northern Idaho ground squirrel is a semi-fossorial mammal endemic to a 1600-km 2 area in western Idaho, USA. These small squirrels (adults weigh 100-300 g) are obligate hibernators, spending 8-10 months hibernating underground each year-mid-July to early April on average (Allison, Conway, & Morris, 2023;. The squirrels live in aggregations during the active season, often inhabiting xeric, rocky openings embedded within an otherwise forested landscape (Goldberg, Conway, Evans Mack, & Burak, 2020;Helmstetter et al., 2021). ...
... Precipitation fell primarily as snow during the winter months when squirrels were hibernating. Snowmelt date is positively correlated with northern Idaho ground squirrel and Columbian ground squirrel emergence from hibernation (Allison, Conway, & Morris, 2023;Lane et al., 2012), and winter snowpack provides water for rapid spring green-up of the squirrels' preferred foods. Winter snowfall and the timing of spring snowmelt varied annually and likely influenced the magnitude and duration of the seasonal pulse in food availability for ground squirrels. ...
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.
Phenology is often thought to evolve mainly in response to food availability, yet recent studies have focused on predation. Predation may explain apparent mismatches between phenology and resources. One type of phenological response to predation involves shifting phenology from a period of high to low predation (i.e., a safe‐period strategy). This strategy presupposes variation in predation over time due to environmental factors such as the number or diversity of predators. Predation varies not only over time but also among different activities like reproduction and dormancy. Alternative activities involve alternative behavioral or physiological states, and different locations where they take place influencing predation risk. Phenological responses to predation may involve shifting from a high risk activity to a safer one, resulting in increased survival (i.e., a «safe‐activity» strategy). This strategy may theoretically evolve under environmental conditions associated with constant predation over time, but assumes variation in predation among activities. Safe‐period and safe‐activity strategies are not mutually exclusive, but assume different conditions for their evolution. On the basis of a literature review, our goal was to: (1) propose a classification of phenological responses to predation according to their evolutionary context, including mean population responses and interindividual differences (degree of synchrony); (2) to show how these two strategies may explain the lack of support for the idea that phenology responds primarily to food availability; and (3) to propose several approaches for testing the influence of predation on phenology. Our review highlights the relevance of studying phenology on multiple scales, thereby integrating several interspecific interactions (communities scales) and multiple activities (annual scale), and studying synchronicity and the pace‐of‐life (inter‐individual scale).
The magnitude of many kinds of biological structures and processes scale with organismal size, often in regular ways that can be described by power functions. Traditionally, many of these “biological scaling” relationships have been explained based on internal geometric, physical, and energetic constraints according to universal natural laws, such as the “surface law” and “3/4‐power law”. However, during the last three decades it has become increasingly apparent that biological scaling relationships vary greatly in response to various external (environmental) factors. In this review, I propose and provide several lines of evidence supporting a new ecological perspective that I call the “mortality theory of ecology” (MorTE). According to this viewpoint, mortality imposes time limits on the growth, development, and reproduction of organisms. Accordingly, small, vulnerable organisms subject to high mortality due to predation and other environmental hazards have evolved faster, shorter lives than larger, more protected organisms. A MorTE also includes various corollary, size‐related internal and external causative factors (e.g. intraspecific resource competition, geometric surface area to volume effects on resource supply/transport and the protection of internal tissues from environmental hazards, internal homeostatic regulatory systems, incidence of pathogens and parasites, etc.) that impact the scaling of life. A mortality‐centred approach successfully predicts the ranges of body‐mass scaling slopes observed for many kinds of biological and ecological traits. Furthermore, I argue that mortality rate should be considered the ultimate (evolutionary) driver of the scaling of life, that is expressed in the context of other proximate (functional) drivers such as information‐based biological regulation and spatial (geometric) and energetic (metabolic) constraints.
Seasonal animal dormancy, hibernation or diapause, is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year. However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy over time, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Other survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the “life-history” hypothesis), but comparative tests across animal species are not yet available. Under this hypothesis, dormancy phenology is influenced by a trade-off between the reproductive advantages of being active and the survival benefits of being in dormancy. Thus, species may emerge from dormancy when reproductive benefits occur, regardless of the environmental conditions for obtaining energy. Species may go into dormancy when these environmental conditions would allow continued activity, if there were benefits from reduced predation or competition. Within a species, males and females differ in the amount of time and energy they invest in reproduction. Thus, the trade-off between reproduction and survival may be reflected in sex differences in phenology of dormancy.
Using a phylogenetic comparative method applied to more than 20 hibernating mammalian species, we predicted that differences between the sexes in hibernation phenology should be associated with differences in reproductive investment, regardless of energetic status. Consistent with the life-history hypothesis, the sex that spent the less time in activities directly associated with reproduction (e.g. testicular maturation, gestation) or indirectly (e.g. recovery from reproductive stress) spent more time in hibernation. This was not expected if hibernation phenology were solely influenced by energetic constraints. Moreover, hibernation sometimes took place at times when the environment would allow the maintenance of a positive energy balance. We also compiled, initial evidence consistent with the life history hypothesis to explain the dormancy phenology of ectotherms (invertebrates and reptiles). Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously appreciated.
Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.
