Behavioral variation and flexibility of snub-nosed monkeys (Rhinopithecus spp.)
This dissertation aimed to better understand the behavioral variation and behavioral flexibility of snub-nosed monkeys (Rhinopithecus spp.). Most snub-nosed monkey populations live in high-elevation habitats (exceeding 2,000 m above sea level) characterized by colder and drier climates, stronger seasonality, and a lower abundance of vegetation (including their preferred young leafy foods) than similar habitats at lower elevations. Snub-nosed monkeys are part of the colobine subfamily, which typically engage in time-minimizing behaviors that prioritize energy conservation (i.e. resting) over energy acquisition (i.e. feeding or moving). However, it is possible that snub-nosed monkeys must engage in energy-maximizing behaviors that prioritize energy acquisition over energy conservation to obtain enough energy to survive in the extreme conditions of their high-elevation habitats.
Methods and Main Results
Snub-nosed monkey populations display energy-maximizing behaviors at higher elevations and in colder climates.
We conducted a web-based search of studies quantifying the activity budgets of colobine monkeys, and extracted information on the geography and climates at each study site along with behavioral data collected on the activity budgets. We ran phylogenetic generalized least squares (PGLS) regressions to determine the influence of geography (elevation, latitude) and climate (precipitation, temperature) on each category within colobine activity budgets. Applying best subsets selection, we generated models for all possible combinations of our geographic and climatic variables, and used model averaging to calculate model-averaged estimates for the best fitting models. Because colobines vary greatly in the range of habitat conditions they occupy, we also evaluated the influence of intra-generic variation within our models by running simple linear models using the significantly correlated pairs of variables from our averaged PGLS models. We first ran these models using subsets of our dataset containing the four most common genera within our full data set (Colobus, Piliocolobus, Trachypithecus, and Rhinopithecus).
We found that colobines living at higher elevations spent a higher proportion of their activity budgets engaged in feeding behaviors and a correspondingly lower proportion in resting behaviors. However, when we analyzed each genus separately, the effect of elevation and temperature on feeding appeared to be attributed to the higher elevations and lower temperatures at which snub-nosed monkeys occurred (Figure 1). Specifically, snub-nosed monkeys spent significantly more time feeding at higher elevations than at lower elevations and at lower temperatures than at higher temperatures. By contrast, there were no effects on feeding times in the other genera when examined separately for elevation or temperature.
Figure 1. Results of simple linear regressions between feeding and elevation (A), and feeding and temperature (B), across four colobine genera (red square: Colobus; green circle: Piliocolobus; blue triangle: Rhinopithecus; purple diamond: Trachypithecus). 95% confidence intervals for each regression line are depicted in gray.
Elevation use impacts behavioral and dietary flexibility in black-and-white snub-nosed monkeys.
We collected data on the activities and diets of an isolated black-and-white snub-nosed monkey (R. bieti) population at Mt. Lasha, Yunnan Province, China, between 2008 and 2016. We also recorded the latitude, longitude, and elevation of the population and collected climatic data for the field site. Data were then subsampled to ensure that analyzed activities came from nearly complete daylength periods of observation and minimized biases in observation duration or timing. We ran a series of Linear Mixed Models (LMMs) to assess the variation in black-and-white snub-nosed monkey feeding time across months and seasons, and Generalized Linear Models (GLMs) to assess this within the winter, spring, and fall. For each LMM and GLM, we used time spent feeding as our explanatory effect, mean elevation and temperature as our main fixed effects, and year as our random effect. We also ran a series of Spearman correlations to assess the relationships between time spent feeding on important food items (leaves and lichen) and elevation use between months, between seasons, and within the winter, spring, and fall months.
We found that black-and-white snub-nosed monkeys spent less time feeding in months and seasons when ranging at higher elevations than at lower elevations (Figure 2). We found no significant relationship between elevation use and feeding time within seasons. While black-and-white snub-nosed monkeys spent more time feeding in months with colder temperatures, we found no significant relationship between temperature and feeding time either between or within seasons. Across dietary categories, we found that only lichen consumption correlated with black-and-white snub-nosed monkey monthly and seasonal elevation usage (Figure 3).
Figure 2. Relationship between the amount of time R. bieti spent feeding across mean monthly (A) and seasonal (B) elevations. Colored circles indicate samples collected in the winter (red), spring (green), summer (blue), and fall (purple). 95% confidence intervals are depicted in gray.
Specifically, black-and-white snub-nosed monkeys spent more time feeding on lichen when ranging across higher elevations than when ranging across lower elevations. Within seasons, however, we found that only time spent feeding on leaves, rather than lichen, correlated with elevation use. In the spring, black-and-white snub-nosed monkeys spent more time feeding on leaves when ranging at higher elevations compared with when ranging at lower elevations (Figure 3).
Figure 3. Relationship between the amount of time R. bieti spent feeding on lichen across mean monthly (A) and seasonal (B) elevations, and feeding on leaves across mean monthly elevations in the spring (C). Colored circles indicate samples collected in the winter (red), spring (green), summer (blue), and fall (purple). 95% confidence intervals are depicted in gray.
Black-and-white snub-nosed monkeys display differences in behavioral flexibility among age-sex classes.
Using the same data collected at Mt. Lasha, we conducted behavioral analyses among and within three age-sex classes: juveniles, adult females, and adult males. We ran a series of Linear Mixed Models (LMMs) to assess the effects of age-sex class, temperature, and the interaction between age-sex class and temperature (fixed effects) on monthly variation in each component of the black-and-white snub-nosed monkey activity budget and Generalized Linear Mixed Models (GLMMs) with negative binomial link functions to assess the impacts of these fixed effects on monthly variation in the major components of their diet (leaves and lichen), with year as a random effect in all models.
All activities significantly differed by age-sex class. Juveniles spent more time moving, more time socializing, and less time resting than adults, and adult females spent more time feeding, more time moving, and less time resting than adult males. Juveniles also spent less time feeding than adult females. At colder temperatures, black-and-white snub-nosed monkeys spent significantly more time feeding, less time moving, and less time resting than at warmer temperatures (Figure 4). When we analyzed each age-sex class separately, we found no significant effects of temperature on the time spent feeding or socializing. However, all age-sex classes spent less time moving and adults spent less time resting at colder temperatures than at warmer temperatures.
Figure 4. Relationship between mean monthly temperature and time R. bieti spent feeding (A, B), moving (C, D), and resting (E, F) for the whole population (black) and for each age-sex class (red: adult male; green: adult female; blue: juvenile). 95% confidence intervals are depicted in gray.
Conclusions and Conservation Implications
1) Snub-nosed monkey feeding behaviors may uniquely reflect a response to their extreme habitats. However, the degree of behavioral variation displayed among populations is not consistent with the degree of flexibility displayed within populations. Given that behavioral variation and behavioral flexibility are measured at different scales and can be driven by different factors, both should be considered in future studies of primate behavior, especially for primates living in extreme conditions. While snub-nosed monkeys appear highly resilient to environmental change, future studies should also consider the limitations of this resilience to anthropogenic disturbance.
2) Young leaves and lichen are both important dietary items for black-and-white snub-nosed monkeys. Young leaves are prioritized in the spring when they are most widely available, and lichen sustains these monkeys for the remainder of the year, when other foods are largely unavailable or absent. Given lichens’ slow regeneration time, sensitivity to environmental contaminants and climate change, and harvesting by local residents for food, we recommend that managing and protecting lichen is a priority for black-and-white snub-nosed monkey conservation efforts.
3) Overall, smaller age-sex classes spend more time active than larger age-sex classes, indicative of their greater energy and nutrient requirements relative to body mass. However, that adult females spend the most time feeding may reflect their greater energy needs for reproduction. While temperature affects variation in time spent feeding at the population level, it does not affect such variation within each age-sex class suggesting that individuals may have different feeding strategies throughout the year based on age or sex-related factors. That we only found an effect of temperature on variation in time spent resting within adults suggests that juveniles may be unable to sacrifice their already limited resting time to engage in more active behaviors when temperatures decrease. Conservation efforts targeting whole populations may therefore overlook the needs of adult females (potentially limited in feeding time) or juveniles (potentially limited in resting time). We recommend that managers closely monitor the behaviors, diets, and overall health of adult females and juveniles to decide how to best protect this species from population decline.