Fallback foods of temperate‐living primates: A case study on snub‐nosed monkeys

Abstract

Only a few primate species thrive in temperate regions characterized by relatively low temperature, low rainfall, low species diversity, high elevation, and especially an extended season of food scarcity during which they suffer from dietary stress. We present data of a case study of dietary strategies and fallback foods in snub-nosed monkeys (Rhinopithecus bieti) in the Samage Forest, Northwest Yunnan, PRC. The snub-nosed monkeys adjusted intake of plant food items corresponding with changes in the phenology of deciduous trees in the forest and specifically showed a strong preference for young leaves in spring. A non-plant food, lichens (Parmeliaceae), featured prominently in the diet throughout the year (annual representation in the diet was about 67%) and became the dominant food item in winter when palatable plant resources were scarce. Additional highly sought winter foods were frost-resistant fruits and winter buds of deciduous hardwoods. The snub-nosed monkeys' choice of lichens as a staple fallback food is likely because of their spatiotemporal consistency in occurrence, nutritional and energetic properties, and the ease with which they can be harvested. Using lichens is a way to mediate effects of seasonal dearth in palatable plant foods and ultimately a key survival strategy. The snub-nosed monkeys' fallback strategy affects various aspects of their biology, e.g., two- and three-dimensional range use and social organization. The higher abundance of lichens at higher altitudes explains the monkeys' tendency to occupy relatively high altitudes in winter despite the prevailing cold. As to social organization, the wide temporal and spatial availability of lichens strongly reduces the ecological costs of grouping, thus allowing for the formation of "super-groups." Usnea lichens, the snub-nosed monkeys' primary dietary component, are known to be highly susceptible to human-induced environmental changes such as air pollution, and a decline of this critical resource base could have devastating effects on the last remaining populations. Within the order Primates, lichenivory is a rare strategy and only found in a few species or populations inhabiting montane areas, i.e., Macaca sylvanus, Colobus angolensis, and Rhinopithecus roxellana. Other temperate-dwelling primates rely mainly on buds and bark as winter fallback foods.

Macaques at the margins: the biogeography and extinction of Macaca sylvanus in Europe

“…As this appears to be a common dietary pattern in temperate primates (Hanya et al, 2011), we can assume that European macaques in the Plio-Pleistocene had similar dietary composition, preferentially incorporating high energy fruits and/or seeds in the diet when available but with more ubiquitous leaves as an important staple. Some modern temperate primates, notably M. sylvanus and the snubnosed monkey R. roxellana, also incorporate significant quantities of lichens into their diets, as a year-round fallback food and a dominant dietary component in winter (Grueter et al, 2009). Not all modern 'feeding' behaviours may have been present in past populations, however.…”

Food Abundance Is the Main Determinant of High-Altitude Range Use in Snub-Nosed Monkeys

“…Temperature and precipitation varied markedly with seasons (for details on climate, see [11]). Several habitat types have been identified at the study site, ranging from subtropical evergreen forest in valleys, pine forest on lower slopes, mixed deciduous, and evergreen conifer forest, with bamboo and rhododendron featuring in the shrub layer.…”

“…Data on monthly dietary composition was gathered via instantaneous group scans at 15 or 30 min intervals. For each scanned individual that was feeding, we recorded the food type, namely, lichens, young leaves, mature leaves, buds, flowers, fruits/seeds, and others (for details, see [11]). …”

“…[12]), this is demonstrably not the case for lichens. Grueter et al [11] have previously shown that arboreal lichen load increases with altitude at Samage, and Li et al [4] have argued that this may be the main reason why the animals stayed at moderately high altitudes in winter and did not descend to lower altitudes. This finding seems highly intuitive and seems to reflect an adaptive strategy, as gaining access to a sufficient amount of fallback foods strongly influences survival chances [13,14].…”

“…It has been firmly established that at least for those populations of R. bieti that live at relatively high latitude, arboreal, and mainly fruticose lichens are a staple fallback food (sensu [9]), eaten throughout the year in large quantities and becoming an essential resource in winter when almost no fruit and no young foliage are available. At Xiaochangdu in Tibet, where the study of Quan et al [6] was conducted, lichens make up 97% of the monkeys' winter diet [10], while at the slightly more productive site at Samage ca 200 km to the south they are 82% [11].…”