Heterogeneity in risk‐sensitive allocation of somatic reserves in a long‐lived mammal

Abstract

Food quality and availability, when combined with energetic demands in seasonal environments, shape resource acquisition and allocation by animals and hold consequences for life‐history strategies. In long‐lived species with extensive maternal care, regulation of somatic reserves of energy and protein can occur in a risk‐sensitive manner, wherein resources are preferentially allocated to support survival at the cost of investment in reproduction. We investigated how Rocky Mountain bighorn sheep (Ovis canadensis), an alpine mammal in a highly seasonal environment, allocates somatic reserves across seasons. In accordance with the hypothesis of risk‐sensitive resource allocation, we expected accretion and catabolism of somatic reserves to be regulated relative to preseason nutritional state, reproductive state, and variation among populations in accordance with local environmental conditions. To test that hypothesis, we monitored seasonal changes in percent ingesta‐free body fat (IFBFat) and ingesta‐free, fat‐free body mass (IFFFBMass) in three populations of bighorn sheep in northwest Wyoming between 2015 and 2019 through repeated captures of female sheep in December and March of each year in a longitudinal study design. Regulation of somatic reserves was risk‐sensitive and varied relative to the amount of somatic reserves an animal had at the beginning of the season. Regulation of fat reserves was sensitive to reproductive state and differed by population, particularly over the summer. In one population with low rates of recruitment of young, sheep that recruited offspring lost fat over the summer in contrast to the other two populations where sheep that recruited gained fat. And yet, all populations exhibited similar changes in fat catabolism and risk sensitivity over winter. The magnitude of body fat and mass change across seasons may be indicative of sufficiency of seasonal ranges to meet energetic demands of survival and reproduction. Risk‐sensitive allocation of resources was pervasive, suggesting nutritional underpinnings are foundational to behavior, vital rates, and, ultimately, population dynamics. For species living in alpine environments, risk‐sensitive resource allocation may be essential to balance investment in reproduction with ensuring survival.

Survival of the fattest: How body fat and migration influence survival in highly seasonal environments

“…reproduction versus fat stores) over summer and thus, what fat levels are attained leading into winter (Bårdsen et al, 2008;Monteith et al, 2013;Smiley et al, 2022).…”

“…For animals less apt to switch their migratory tactic, selective pressures should affect how energy is allocated (i.e. reproduction versus fat stores) over summer and thus, what fat levels are attained leading into winter (Bårdsen et al, 2008; Monteith et al, 2013; Smiley et al, 2022).…”

“…Few animals classified as residents (n = 5) died before the time that most migrations typically occur, thus any bias associated with this type of misclassification likely is small. Additionally, we only had one measurement of body fat for each individual and did not have recruitment data, which prevented us from conducting longitudinal analyses with body fat and recruitment that undoubtedly would provide greater insights into life-history strategies and trade-offs (Monteith et al, 2013(Monteith et al, , 2014Smiley et al, 2022). Nonetheless, vacillating migration appears to be a highly successful tactic where it can be employed and may allow individuals to experience the best of both migrant and resident environments.…”

“…lactation, growth). Generally, skinnier animals accrete more fat over summer than fatter animals (Cook et al, 2013; Monteith et al, 2013; Smiley et al, 2022) and lactating females with elevated requirements for milk production often are less able to meet nutritional requirements, including those for fat accretion, than non‐lactating animals (Cook et al, 2013; Denryter et al, 2020; Stephenson et al, 2020). The exogenous nutritional environment also exerts important constraints on fat accretion regardless of the endogenous environment of the animal.…”

Maternal effects and the legacy of extreme environmental events for wild mammals

“…Particularly in temperate environments with harsh conditions and severe limitation of resources for extended periods, animals rely heavily on energy stored as fat during winter when resources are scarce (Mautz, 1978; Parker et al, 2009). In seasonal environments, the pattern of fat accumulation and depletion is closely synchronized to their environment and availability of resources (Smiley, Wagler, et al, 2022). Nevertheless, to survive when severe environmental conditions result in an unanticipated but necessary depletion in fat reserves, animals that persist are faced with severe consequences for reproduction that can span years or even generations.…”