Consumption of underground storage organs is associated with improved energetic status in a graminivorous primate.

Early hominin species likely had access to open, grassy habitats where periodic reliance on underground storage organs (USOs) is hypothesized to have played a crucial dietary role. As the only living graminivorous primate today, geladas (Theropithecus gelada) provide a unique perspective for understanding the energetic consequences of seasonal consumption of USOs. Geladas rely heavily on above-ground grasses throughout the year, but when grass is seasonally less available, they feed more on USOs. To assess whether USOs fit the definition of fallback foods (i.e., foods that are difficult to access, less preferred, or both), we examined how foraging effort (measured via time spent feeding and moving) and energetic status (measured via urinary C-peptide) fluctuated during seasonal dietary changes in a population of wild geladas in the Simien Mountains National Park, Ethiopia. If, indeed, USOs are fallback foods, we predicted an increase in foraging effort and a decline in energetic status during the dry season, when geladas rely more heavily on USOs. We collected behavioral and physiological data from 13 adult gelada males across a 13-month period. As expected, we found that male geladas spent more time moving during drier months. However, counter to the hypothesis that USOs are fallback foods in geladas, urinary C-peptide concentrations were significantly higher during the dry season. We suggest that USOs may represent an energy-rich food item for geladas, but it remains unclear why USOs are not consumed year-round. Future work is needed to better understand seasonal variation in the availability, nutrient content, and digestibility of USOs. However, results indicate that exploiting USOs seasonally could have been a valuable dietary strategy for the evolutionary success of early hominins.

Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas.

BACKGROUND: Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. RESULTS: Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. CONCLUSION: Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. Video abstract.

Characteristics of alpha males in Nepal gray langurs.

In species with strong male-male competition, access to females in multimale-multifemale groups is usually regulated via a dominance hierarchy. The highest ranking (alpha) male often has priority of access and sires most offspring. The alpha male can change in three basic ways: (i) a recent immigrant or a resident challenges and becomes the new alpha; (ii) formation of a new group; (iii) succession-becoming alpha after higher ranking males have left. When, in a given primate population, the alpha male changes in different ways, two questions arise: (a) which is the most successful tactic and (b) do male attributes, such as age, aggressiveness or propensity to commit infanticide, affect the outcome? We examined these questions in the seasonally breeding Nepal gray langurs (Semnopithecus schistaceus) at Ramnagar, where new alpha males were either recent immigrants or residents. Success was measured as alpha tenure, residency duration, and the number of offspring sired (paternity exclusion based on DNA analysis, 28 infants). We documented 12 alpha-male tenures across two multimale-multifemale groups between 1991 and 1997. The predominant mode of change was the immigrant tactic. Age had no effect perhaps because alpha males were among the youngest adult males in their group. As expected, infanticidal males performed similarly to non-infanticidal ones. Alpha tenure was highly variable and longer for immigrant alphas and hyper-aggressive ones. However, none of the tactics or attributes examined resulted in significantly longer residencies or more offspring, likely because of the timing of immigrations and stochastic effects (i.e., the number of conceptions occurring per alpha tenure). The influence of female mate choice on male reproductive success requires further investigation. Furthermore, it remains to be examined why resident alpha males-with their presumed better knowledge of their opponents -performed so poorly. Am. J. Primatol. 79:e22437, 2017. © 2015 Wiley Periodicals, Inc.

Dominance relationships in male Nepal gray langurs (Semnopithecus schistaceus).

OBJECTIVES: Reproductive skew is proposed to link to despotism in dominance hierarchies. While studies illustrating male skew are plentiful, demonstrating the link to despotism is rare. Likewise, it is often unknown which factors (e.g., resource holding potential, age, physical condition) affect a male's dominance rank. Here we investigated correlates of male rank and hierarchy characteristics in Nepal gray langurs (Semnopithecus schistaceus), a population with high male reproductive skew, and compared the results to other multi-male groups of nonhuman primates. METHODS: We collected dyadic displacement interactions from two groups (mean 3.0 and 4.1 adult males) for five years each. We assessed dominance ranks for demographically stable phases (n = 11, n = 28) and analyzed the effects of age and physical condition through linear mixed models (LMM). We analyzed hierarchy characteristics via the program MatMan. We used data from 27 primate groups (cercopithecines, colobines, hominoids) as a comparative sample. RESULTS: The highest ranks were attained by adults in one group (LMM, P < 0.091) and by young adults in the other group (LMM, P < 0.001). With some exceptions, rank was highest for males with higher physical condition scores (LMM, P < 0.05). Hierarchies had high directional consistency (mean > 0.93) and linearity (mean >0.81) and were relatively steep (mean >0.66) when compared with other species. DISCUSSION: Dominance rank followed a pattern predicted by resource holding potential, but other individual attributes and group composition also seemed important. As predicted, hierarchy characteristics indicated a despotic system in line with the strong reproductive skew. Across primates, however, the degree of despotism did not appear to match the degree of reproductive skew. Am J Phys Anthropol 160:208-219, 2016. © 2016 Wiley Periodicals, Inc.