Seasonal variation in diet and nutrition of the northern‐most population of Rhinopithecus roxellana

Abstract

There is a great deal of spatial and temporal variation in the availability and nutritional quality of foods eaten by animals, particularly in temperate regions where winter brings lengthy periods of leaf and fruit scarcity. We analyzed the availability, dietary composition, and macronutrients of the foods eaten by the northern-most golden snub-nosed monkey (Rhinopithecus roxellana) population in the Qinling Mountains, China to understand food choice in a highly seasonal environment dominated by deciduous trees. During the warm months between April and November, leaves are consumed in proportion to their availability, while during the leaf-scarce months between December and March, bark and leaf/flower buds comprise most of their diet. When leaves dominated their diet, golden snub-nosed monkeys preferentially selected leaves with higher ratios of crude protein to acid detergent fiber. While when leaves were less available, bark and leaf/flower buds that were high in nonstructural carbohydrates and energy, and low in acid detergent fiber were selected. Southern populations of golden snub-nosed monkey can turn to eating lichen, however, the population studied here in this lichen-absent area have adapted to their cool deciduous habitat by instead consuming buds and bark. Carbohydrate and energy rich foods appear to be the critical resources required for the persistence of this species in temperate habitat. The dietary flexibility of these monkeys, both among seasons and populations, likely contributes to their wide distribution over a range of habitats and environments.

Cafeteria‐style feeding trials provide new insights into the diet and nutritional strategies of the black snub‐nosed monkey (Rhinopithecus strykeri): Implications for conservation

“…These values are generally similar to those reported for R. brelichi (NDF: 46% in summer/autumn; Bleisch et al, 1998) and R. roxellana (NDF: 32.23% in spring; Hou, 2018), but higher than those reported for R. bieti (NDF: 34.17% in autumn; Huang et al, 2010). The protein‐to‐fiber ratio of food items consumed by R. strykeri in our study was higher than for nonconsumed items, which is consistent with previous findings for African and Asian colobines ( Procolobus badius, C. guereza , Wasserman & Chapman, 2003; Presbytis rubicunda , Hanya & Bernard, 2015; R. bieti ; Huang et al, 2010; and R. roxellana , Hou et al, 2018). However, the fiber content of leaves consumed by R. avunculus in Khau Ca (ADF; Lan Anh et al, 2014), R. bieti in the Longma Mountains (NDF; Huang et al, 2010), R. roxellana in Shennongjia (Crude Fiber; Liu, Stanford, Yang, Yao, & Li, 2013; ADF, Li, 2015), R. roxellana in the Qingling mountains (NDF & ADF, Hou, 2018), and R. brelichi in Fanjingshan (NDF, ADF, and lignin; Bleisch et al, 1998) did not differ from that of nonconsumed leaves.…”

“…Wild R. strykeri , similar to R. avunculus and R. brelichi , may switch to evergreen leaves when other resources are less available (Dong, 2012; Xiang, Liang, Nie, & Li, 2012). This dietary adjustment is similar to that reported for other Rhinopithecus species that exploit foods high in carbohydrates and energy (e.g., evergreen leaves, lichen, bark, seeds, and buds) during the cold winter months ( R. bieti : Grueter et al, 2009; R. roxellena : Guo, Li, & Watanabe, 2007; Hou et al, 2018; Liu et al, 2013). In the case of R. roxellena , increased energy consumption during the winter has been shown to offset the increased costs needed to remain thermoneutral when winter temperatures drop below 0°C (Guo et al, 2018).…”

“…Huang (2014) reported that NDF digestibility by captive golden snub‐nosed monkeys was 74.3% based on feeding experiments conducted on five adult males. As per Conklin‐Brittain, Knott, and Wrangham (2006), we used a value of 12 kJ/g of available energy/g fiber after subtracting 4 kJ/g consumed by anaerobic microbes to calculate the physiological fuel value of NDF, which was 12 × 0.743 = 9 kJ/g (Chen et al, 2018; Hou et al, 2018). We calculated the ME of each food item per 100 g using standard conversion factors (CP 17 kJ/g, CL 37 kJ/g, TNC 16 kJ/g, and NDF 9 kJ/g; Conklin‐Brittain et al, 2006) and the formula: ME kJ = 100 g × CP% × 17 kJ/g + 100 g × CL% × 37 kJ/g + 100 g × TNC% × 16 kJ/g + 100 g × NDF% × 9 kJ/g.…”

“…Snub‐nosed monkeys ( Rhinopithecus ) represent an endangered genus of Asian colobines with four of the five extant species native to China (Meyer et al, 2017). As in the case of other colobine monkeys, Rhinopithecus have an elongated, multichambered, low‐acid forestomach that contains a diverse microbiota required to assist in the fermentation of difficult‐to‐digest foods that contain high levels of structural carbohydrates and secondary compounds, such as mature leaves, twigs, tree bark, winter buds, and lichen (Davies & Oates, 1994; Hou et al, 2018; Zhou et al, 2014). Snub‐nosed monkeys inhabit a wide range of tropical and alpine forest environments ranging from 600 to 4,600 m in elevation (Kirkpatrick & Grueter, 2010).…”

“…Snub‐nosed monkeys inhabit a wide range of tropical and alpine forest environments ranging from 600 to 4,600 m in elevation (Kirkpatrick & Grueter, 2010). Studies of the diet and nutritional ecology of four snub‐nosed monkey species ( R. bieti, R. roxellana, R. brelichi , and R. avunculus ) indicate that individuals prioritize nutrients while limiting their intake of plant secondary metabolites (Bleisch, Liu, Dierenfeld, & Xie, 1998; Hou et al, 2018; Lan Anh, Dang, Huan, & Duc, 2014; Zhang et al, 2013). For example, wild black‐and‐white snub‐nosed monkeys ( R. bieti ) were found to consume leaves that were higher in protein and phosphorus and lower in tannins than not consumed leaves (Zhang et al, 2013).…”