Cold and hungry: combined effects of low temperature and resource scarcity on an edge‐of‐range temperate primate, the golden snub‐nose monkey

Abstract

Both biotic and abiotic factors play important roles in influencing ecological distributions and niche limits. Where biotic and abiotic stressors co‐occur in space and time, homeostatic systems face a scenario in which stressors can compound to impose a challenge that is greater than the sum of the separate factors. We studied the homeostatic strategies of the golden snub‐nosed monkey Rhinopithecus roxellana, a species living in temperate deciduous forests at the edge of the global distribution range for folivorous primates, to cope with the co‐occurrence of cold temperatures and resource scarcity during winter. We discovered that in winter the monkeys experience a dietary energy deficit of 101 kJ mbm−1 d−1 compared with calculated needs, despite increased feeding. This is partly offset by behavioral changes (reduced locomotion and increased resting) and reducing skin temperature by an average of 3.2°C through a cutaneous vasoconstriction to decrease heat loss. However, their major strategy is ingesting surplus energy and accumulating fat reserves when food was not limiting during summer and autumn. Their 14% of body mass lost over the winter represented an energy yield of 102 kJ mbm−1 d−1, which closely matched the calculated winter energy deficit of 101 kJ mbm−1 d−1. However, the latter value assumes that all the 75.41 kJ mbm−1 d−1 of protein ingested in winter was available for energy metabolism. This is almost certainly an over‐estimate, suggesting that the study population was in negative energy balance over the study period. Our study therefore suggests that despite its suit of integrated homeostatic responses, the confluence of low temperatures and resource limitation during winter places this edge‐of‐range primate close the threshold of what is energetically viable. It also provides a framework for quantitative models predicting the vulnerability of temperate primates to global change.

The geometry of resource constraint: An empirical study of the golden snub‐nosed monkey

“…There is, however, also evidence of constraint‐driven variation in intake in our data. In contrast with the captive population, and the heavily supplemented wild monkeys in Guo et al., (2018), the wild monkeys in this study showed only a modest increase in NPE intake in winter, and were energy deficient during that season (Hou, Chapman, Jay, et al, 2020). This suggests that, when possible, macronutrient selection by R. roxellana tracks winter increases in NPE requirements for thermoregulation, but in the wild their capacity to meet those requirements during winter is ecologically constrained.…”

“…Protein leverage has been demonstrated in several species, including humans (Gosby et al., 2011, 2014), mice (Sorensen et al., 2008), grasshoppers Melanoplus differentialis (Le Gall & Behmer, 2014) and flies (Almeida de Carvalho & Mirth, 2017). However, protein leverage cannot on its own explain protein prioritization in R. roxellana because, as discussed above, high NPE intakes in winter were not driven by qualitative constraint forcing the animals to over‐eat NPE, but by an increased requirement for NPE to meet the energetic requirements for thermoregulation in winter (Guo et al., 2018; Hou, Chapman, Jay, et al, 2020). It is likely that the variance in NPE intake across other seasons is likewise driven, at least in part, by seasonal variation in nutrient requirements, rather than by qualitative constraint.…”

“…Body mass for age/sex classes was based on average measurement for adult individuals and juveniles in winter and spring, and we used the averaged body mass in spring and winter to represent the body mass in summer and autumn. Specifically, we weighed animals with a platform scale (EM-60KAL, A&D) and lured the monkeys onto the platform with a small amount of corn (Hou, Chapman, Jay, et al, 2020). We do not have the body mass data of captive monkeys, so we used the weight per size class from data collected for the wild monkeys.…”

“…We used nutritional geometry to analyse 164 full‐day focal animal feeding observations and compare nutritional regulatory responses of a minimally provisioned wild population subject to natural variation in resources with a captive population provided continuous access to a wide variety of wild‐sourced and domesticated foods. Both populations were studied year‐round, enabling us to compare regulatory responses across four seasons, which in the temperate habitat generated substantial variation in resource availability as well as nutritional demands for thermoregulation (Guo et al., 2018; Hou, Chapman, Jay, et al, 2020). At a finer scale, replicate animals were studied within each population and season, enabling us to examine variability between animals, while controlling for season and population.…”

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

“…Thermal demands also result in GSMs requiring twice as much energy during winter compared to the spring. Winter thus presents these monkeys a considerable challenge to extract the required amount of energy from an enforced ultra-high-ber diet [22,23]. Satisfying energetic demands during the winter is partially achieved by increasing daily food consumption [18], but GSMs are also likely to depend heavily on microbial functions to extract su cient nutritional resources from their diets during the winter.…”