Temporal niche partitioning among sympatric wild and domestic ungulates between warm and cold seasons.

The coexistence of sympatric species with similar ecological niches has been a central issue in ecology. Clarifying the daily activity patterns of sympatric wild ungulates can help understand their temporal niche differentiation and the mechanisms of coexistence, providing information for their conservation. The Baotianman National Nature Reserve in northern China is rich in wild ungulates, but little is known about the daily activity patterns of wild ungulates in the area, making it difficult to develop effective conservation strategies. We studied five representative wild ungulates (i.e. forest musk deer, Chinese goral, Reeve's muntjac, Siberian roe deer, and wild boar) of the region using camera-trapping data, focusing on the seasonal daily activity patterns and effects of seasonal grazing of domestic sheep, to reveal their coexistence based on temporal ecological niche differentiation. Comparative analyses of the seasonal daily activity showed that forest musk deer exhibited a single-peak activity in the warm season. Other ungulates exhibited multipeak activity. All five ungulates differed significantly in daily activity patterns. Notably, wild boar and Reeve's muntjac showed high overlap coefficients between the cold and warm seasons. In both cold and warm seasons, the five wild ungulates and domestic sheep displayed low overlap in their daily activity rhythms potentially indicating temporal ecological niche differentiation. The results suggest that temporal isolation might be a strategy for wild ungulates to avoid domestic sheep and reduce interspecific competition, and that temporal ecological niche differentiation potentially promoted the coexistence among the studied sympatric ungulates. This understanding may provide new insights for the development of targeted conservation strategies.

Behavioral adaptation in an adoptive free-ranging female Tibetan macaque.

Adoption is an important form of allomaternal care in nonhuman primates, with implications for reproductive output and infant survival. Here, we report a kidnapping that became an adoption of a 3-week-old infant by a mother with her own infant in Tibetan macaques (Macaca thibetana). The adoptive mother nursed her "new" infant (allonursing), the first observation of this behavior in the species. The case provided a natural experiment for comparing how a female copes with a heavier burden of care for both her biological infant and another female's infant, compared to mothers caring for only one infant. Our results showed that the adoptive female spent more time foraging and resting, and less time in group social activity compared to females with a single infant. The adoptive female showed more instances of social bridging. Although the duration of post-bridging grooming received from group members decreased, the frequency of such grooming increased. We discuss this adoption with reference to possible factors involved in the evolution of adoption and allonursing behavior in Tibetan macaques.

Current distribution of two species of Chinese macaques (Macaca arctoides and Macaca thibetana) and the possible influence of climate change on future distribution.

Predicting the spatial distribution of species and suitable areas under global climate change could provide a reference for species conservation and long-term management strategies. Macaca thibetana and Macaca arctoides are two endangered species of Chinese macaques. However, limited information is available on their distribution, and their habitat needs lack proper assessment due to complicated taxonomy and less research attention. In recent years, scholars widely used the maximum entropy (MaxEnt) model to predict the impact of global climate and certain environmental factors on species distribution. Therefore, we used the MaxEnt model to predict the spatiotemporal distribution of both macaque species under six climate change scenarios using occurrence and high-resolution ecological data. We identified climatic factors, elevation, and land cover that shape their distribution range and determined shifts in their habitat range. The results demonstrated that temperature range, annual precipitation, forest land cover, and temperature seasonality, including the precipitation of the driest month are the main factors affecting their distribution. Currently, M. thibetana is mainly concentrated in central, eastern, southern, and southwestern China, and M. arctoides is mainly concentrated in three provinces (Yunnan, Guangxi, and Guangdong) in southern China. The MaxEnt model predicted that the suitable habitat for both species will increase with increased greenhouse emission scenarios. We also found that with the further increase in greenhouse emissions M. thibetana is expected to migrate to western China, and M. arctoides is expected to migrate to western or eastern China. This reinterpretation of the distribution of M. thibetana and M. arctoides in China, and predicted potential suitable habitat and possible migration direction, may provide new insights into the future conservation and management of these two species.

Ecotourism Disturbance on an Endemic Endangered Primate in the Huangshan Man and the Biosphere Reserve of China: A Way to Move Forward.

The primary purpose of the Man and the Biosphere Program is the sustainable development of both the economy and nature conservation activities. Although the effectiveness of eco-tourism to reach this goal has been proposed, due to the lack of long-term monitoring data and a model species, there has been no obvious mechanism to evaluate the effectiveness of this policy. This study explored the effectiveness of the sustainable development policy of HMBR based on 30 years data of monitoring the Tibetan macaque, local human population, visitors, and annual ecotourism income in Huangshan by estimating species habitat suitability and the impact of ecotourism. The results showed increases in the income for the local human population, the number of visitors, and annual eco-tourism. Simultaneously, the reserve's Tibetan macaque population size and suitable habitat areas increased. The macaques expanded their habitat to the low-altitude buffer zone (400-800 m), an area with lower eco-tourism disturbance. Scenic spots had a significant negative impact on habitat suitability (the substantially increased contributions of scenic spots from 0.71% to 32.88%). Our results and methods provide a suitable evaluation framework for monitoring the sustainable development and effectiveness of eco-tourism and wildlife conservation in Man and the Biosphere reserves.

Effects of Mother's Dominance Hierarchy on the Development of Social Relationships among Immature Tibetan Macaques.

During a relatively long period of growth, immature individuals rely on their mothers to obtain nutrition, and a good environment for learning social skills needed to cope with complex environments in adulthood. In this study, we collected the behavioral data of Tibetan macaques (Macaca thibetana) to investigate the effects of females' social rank on the development of social relationships among their immature offspring from November to June 2021. The results show that there was no difference in the rate/type of social play and grooming among infants. However, among juveniles and adolescents, the higher their mother's social rank, the higher the rate of social play they participated in, and the more aggressive play they engaged in. Immatures with high-ranking mothers initiated more social play among each other. A similar pattern of playmates was found among juveniles/adolescents with middle-ranking and low-ranking mothers. We also found that immatures preferred immatures with higher-ranking mothers as grooming mates and initiated more grooming with immatures with higher-ranking mothers than with those with lower-ranking mothers. Our study suggests that females' social ranks affect the development of social relationships among their immature offspring. In despotic nonhuman primates, this indicates that the mother's dominance hierarchy would directly or indirectly influence the processes of participating in social interactions and choosing partnerships among immature individuals with age (i.e., infancy, juvenile, and adolescent periods).

Coordination and consensus: the role of compromisers in Tibetan macaques.

Coordination and consensus in collective behavior have attracted a lot of research interest. Although previous studies have investigated the role of compromisers in group consensus, they provide little insight into why compromisers would allow such social arrangements to persist. In this study, the potential relationship between group movements and conflict management in Tibetan macaques in Anhui province, China, was investigated using hierarchical cluster analyses. Some members with higher social centrality or social rank often formed a front-runner cluster during group movements. They had higher leadership success than individuals outside the front-runner cluster. Other members with lower social centrality or social rank often followed the group movements initiated by the front-runner cluster, and thus formed the compromiser cluster. Compromisers' proximity relations with front-runners increased with their following scores to front-runners. Compromisers had fewer events of being attacked when they followed group movements initiated by the front-runners. The compromising process made compromisers lose the choice of direction preference, but it could increase their individual safeties. This trade-off suggests that compromisers play a role of decision-maker in coordination and consensus scenarios among social animals.

Assessing the Influence of Environmental Sources on the Gut Mycobiome of Tibetan Macaques.

The distribution and availability of microbes in the environment has an important effect on the composition of the gut microbiome of wild vertebrates. However, our current knowledge of gut-environmental interactions is based principally on data from the host bacterial microbiome, rather than on links that establish how and where hosts acquire their gut mycobiome. This complex interaction needs to be clarified. Here, we explored the relationship between the gut fungal communities of Tibetan macaques (Macaca thibetana) and the presence of environmental (plant and soil) fungi at two study sites using the fungal internal transcribed spacer (ITS) and next generation sequencing. Our findings demonstrate that the gut, plant and soil fungal communities in their natural habitat were distinct. We found that at both study sites, the core abundant taxa and ASVs (Amplicon Sequence Variants) of Tibetan macaques' gut mycobiome were present in environmental samples (plant, soil or both). However, the majority of these fungi were characterized by a relatively low abundance in the environment. This pattern implies that the ecology of the gut may select for diverse but rare environmental fungi. Moreover, our data indicates that the gut mycobiome of Tibetan macaques was more similar to the mycobiome of their plant diet than that present in the soil. For example, we found three abundant ASVs (Didymella rosea, Cercospora, and Cladosporium) that were present in the gut and on plants, but not in the soil. Our results highlight a relationship between the gut mycobiome of wild primates and environmental fungi, with plants diets possibly contributing more to seeding the macaque's gut mycobiome than soil fungi.

Social strategies used by dispersing males to integrate into a new group in Tibetan macaques (Macaca thibetana).

In group-living mammals, an individual's fitness depends, in part, on the quality of social relationships it has with others. Among species of nonhuman primates in which one sex is philopatric, individuals of that sex often develop strong social bonds and alliances with closely related kin. Less is known regarding the social processes used by dispersing adults to form stable bonds with nonkin in their new group. From May to December 2009, April to August 2010, September to December 2011, and February to May 2012, we collected data on grooming interactions in wild Tibetan macaques (Macaca thibetana), a female philopatric species, at Mt. Huangshan, China. Our goal was to compare social interactions and bond formation between resident males, recent immigrant males, and resident females. Our results indicate that recent immigrant males formed stable partner relationships with a small number of resident females and groomed these females more frequently or for longer than they received grooming. In contrast, resident males switched female grooming partners more frequently, received more grooming than they gave, and formed relationships with a greater number of female partners. We argue that the ability of recent immigrant male Tibetan macaques to maintain strong and persistent social bonds with a small set of resident adult females is a primary factor that enables them to establish residence in a new multimale-multifemale group. The present study provides new and important insights into the integrated social strategies used by dispersing males and resident females to maintain group stability.

Female behavioral strategies during consortship in Tibetan macaques (Macaca thibetana).

Consortship has been defined as a temporary association between an adult male and an estrous/receptive female. It has been considered as male mating strategies to improve male mating success and potential reproductive success. However, the female roles have been more or less neglected, and thus, less is known about female behavioral strategies during the consortship periods. In this study, during the two consecutive mating seasons, we collected behavioral data of free-ranging Tibetan macaques (Macaca thibetana) habituated in Mt. Huangshan, China, to investigate female behaviors when she was consorted by an adult male. The results showed that (a) females were more likely to approach and exhibit sexual solicitation to their consorting males during the consorted period, and females also exhibited less approach to their nonconsorting males; (b) females exhibited strong responses (either departed distantly or formed affiliative relationships with their consorting male partner) when their consorting males mated with rival females or showed sexual motivation toward rival females; (c) female preferences were positively correlated to the duration of consortships and the frequencies of ejaculation copulations, independent of the social ranks of their consorting male partners. Our results suggested that female strategies played much more important roles in forming and maintaining consortship than previously assumed. It provides new insight into understanding female adaptive strategies to male strategies by forming consortships in multimale-multifemale primate species when males could not identify female's fertile phase accurately.

Sexual Interference Behaviors in Male Adult and Subadult Tibetan Macaques (Macaca thibetana).

Male nonhuman primate sexual interference, which includes copulation interruption and copulation harassment, has been related to reproductive success, but its significance has been challenging to test. Copulation interruption results in the termination of a copulation before ejaculation, whereas copulation harassment does not. We conducted this study using the all-occurrence behavior sampling method on sexual interference behaviors of seven adult and four subadult male Tibetan macaques (Macaca thibetana) in mating and non-mating seasons at Mt. Huangshan, China, from August 2016 to May 2017. Our results showed that males' individual proportion of copulation interruption and harassment was higher during the mating season than during the non-mating season. In addition, dominant males more often performed interruption, whereas subordinate males more often performed harassment. We found no difference in the individual proportion of copulation interruption or harassment between adult and subadult males. Adult and subadult males both directed copulation interruption and harassment more often toward the mating male than toward the mating female. Lastly, the post-ejaculation phase of copulation was shorter when copulation harassment occurred than when it did not. Our results suggest that sexual interference may be an important mating tactic that adult and subadult males use in male-male sexual competition.

Sex-Specific Variation of Social Play in Wild Immature Tibetan Macaques, Macaca thibetana.

Theories proposed to explain social play have centered on its function in establishing social relationships critical for adulthood, its function in developing motor skills needed to survive, and promoting cognitive development and social learning. In this study, we compared variations in social play among infant and juvenile male and female Macaca thibetana. Given that this species is characterized by female philopatry and male dispersal, we hypothesized that immature females use social play as a mechanism to develop bonds that persist through adulthood whereas immature males use play to develop social skills needed to successfully enter new groups. The results indicated that social play steadily increased during the infant period and peaked at approximately 12 months of age. There were no significant differences in the frequency or types of social play exhibited between infant males and infant females. During the juvenile period, however, social play was found to decrease with age, with males engaging in social play more frequently than juvenile females. Moreover, whereas juvenile males engaged in more aggressive forms of play, juvenile females engaged in more affiliative forms of play. In addition, juvenile females engaged in higher rates of grooming than juvenile males. These results provide evidence of sex-specific differences and imply the functional variation of social play in Tibetan macaques, with immature males using social play to develop skills needed to enter and enhanced their dominance rank in a new social group and immature females using social play to develop long-term same-sex social bonds in their natal group.

Publisher Correction: The prospect of rising in rank is key to long-term stability in Tibetan macaque society.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Infant attraction: why social bridging matters for female leadership in Tibetan macaques.

Leadership is a key issue in the study of collective behavior in social animals. Affiliation-leadership models predict that dyadic partner preferences based on grooming relationships or alliance formation positively affect an individual's decision to follow or support a conspecific. In the case of many primate species, females without young infants are attracted to mother-infant dyads. However, the effects of mother-infant-female associations on affiliation-leadership models remain less clear. In free-ranging Tibetan macaques Macaca thibetana, we used social network analysis to examine the importance of "mother-infant-adult female" social bridging events as a predictor of who leads and who follows during group movement. Social bridging is a common behavior in Tibetan macaques and occurs when 2 adults, generally females, engage in coordinated infant handling. Using eigenvector centrality coefficients of social bridging as a measure of social affiliation, we found that among lactating females, initiating bridging behavior with another female played a significant role in leadership success, with the assisting female following the mother during group movement. Among nonlactating females, this was not the case. Our results indicate that infant attraction can be a strong trigger in collective action and directing group movement in Tibetan macaques and provides benefits to mothers who require helpers and social support in order to ensure the safety of their infants. Our study provides new insights into the importance of the third-party effect in rethinking affiliation-leadership models in group-living animals.

Grooming networks reveal intra- and intersexual social relationships in Macaca thibetana.

The analysis of grooming networks is a powerful tool to examine individual social and sexual relationships and how these relationships change over time. In this study, we investigated the seasonal dynamics of intra- and intersexual social relationships in Tibetan macaques (Macaca thibetana) based on grooming interactions. Similar to other female philopatric and male dispersal primates, female Tibetan macaques form the core of the social group with higher values of centralities, compared to the males who tend to be distributed on the periphery of the grooming network. The results of this study indicate that females formed stable clusters with maternal kin-related female partners both during the mating and non-mating season. Males were not included in the females' clusters during the mating season, however, during the non-mating season high-ranking males joined females to form loosely connected clusters. Male-female clustering was associated with the frequency of grooming (bouts per hour) rather than grooming duration (bout length). Our results illustrate that Tibetan macaque social networks fluctuate in response to reproductive seasonality and appear to play a role in mating choice and male reproductive success. Moreover, our results indicate that the frequency of grooming interactions might be more effective than the duration of grooming interactions in establishing cluster pattern on group level. It appears that changes in male mating strategies may drive these shifting social relationships and networks. Future studies on Tibetan macaques will need to investigate the degree to which changes in male grooming strategies directly correlate with male reproductive success.

Interchange between grooming and infant handling in female Tibetan macaques (Macaca thibetana).

In some nonhuman primates, infants function as a social tool that can bridge relationships among group members. Infants are a desired commodity for group members, and mothers control access to them. The biological market theory suggests that grooming is widespread and represents a commodity that can be exchanged for infant handling. As a limited resource, however, the extent to which infants are interchanged between mothers (females with an infant) and non-mothers (potential handlers, females without an infant) remains unclear. In this study, we collected behavioral data to investigate the relationship between grooming and infant handling in free-ranging Tibetan macaques (Macaca thibetana) at Mt. Huangshan, China. Our results showed that females with infants received more grooming than females without infants. After her infant was handled, mother females received more grooming than they did during daily grooming interactions. However, with the increasing number of infants within the social group, both the grooming that mothers received and the grooming that non-mothers invested for handling infants decreased. We also found that non-mothers invested more time in grooming to gain access to younger infants than older infants. Our results provide evidence that infants are social commodities for both mother and non-mother females. Mothers use infants for obtain grooming and non-mothers use grooming to gain access to infants. The current study implies a bidirectional and complex interchange pattern between grooming and infant handling to compensate for the dyadic grooming disparity in non-human primates.

Bridging may help young female Tibetan macaques Macaca thibetana learn to be a mother.

Attraction to infants is a common feature of non-human primates. Frequent affiliative male-infant interactions have been observed in many multimale, multifemale groups of macaques, including a behaviour termed 'bridging' in which two male macaques simultaneously lift an infant. This behaviour has been suggested to serve as a positive affiliative interaction between the adult or subadult males. Female macaques display bridging in the same manner as males, but the function of this behaviour to females remains unknown. In this study, we examined evidence for the function and evolution of bridging in female Tibetan macaques within the framework of three hypotheses: the learning to mother, a side-effect of selection for appropriate maternal care, and alliance formation hypotheses. Our results showed that subadult females initiated more bridging than adult females. Females preferred to use infants for bridging when the infants were less than four weeks old. Female frequency of received bridging with higher-ranking females was not significantly different from their frequency of received bridging with lower-ranking females. Bridging frequency was not significantly different between dyads composed of related and unrelated females. Additionally, post-bridging grooming frequency was significantly higher than nonbridging grooming interactions, suggesting a social function for bridging. The results of our study supported the 'learning to mother' hypothesis, suggesting that bridging among female intrasexual dyads is a multi-functional, complex and differential evolutionary process.

Season, age, and sex affect the fecal mycobiota of free-ranging Tibetan macaques (Macaca thibetana).

Recent studies highlight that the gut mycobiota play essential roles in mammalian metabolic and immune systems, but to date we lack information on the forces that naturally shape the gut mycobiota of wild primates. To investigate the contributions of host and environmental factors in the taxonomic variation of the gut mycobiota, we examined the effects of age, sex, and season on the fecal mycobiota in wild-living Tibetan macaques (Macaca thibetana). Using next generation sequencing and a longitudinal set of fecal samples collected over 1 year, we identified a set of core fungal taxa present in the Tibetan macaque's fecal samples. The predominant genera Aspergillus and Penicillium, which promote the digestion of cellulose and hemicellulose in herbivorous mammals, were detected in this study. Similar to humans, we found age and sex effects on the macaques' fecal mycobiota. We also found that both fecal fungal composition and diversity (alpha and beta diversity) varied significantly by season. In particular, the Penicillium enriched mycobiota in summer samples may aid in the digestion of cellulose and hemicellulose present in mature leaves. The high alpha diversity detected in Tibetan macaques' winter fecal samples may facilitate a diet rich in fiber ingested during this season. We propose that the gut mycobiota play an important role in the macaques' ability to adapt to seasonal fluctuations in food availability and nutrient content.

The prospect of rising in rank is key to long-term stability in Tibetan macaque society.

One of the most fundamental questions in behavioural biology is why societies can persist for a long period of time. While researchers in animal behaviour have been hindered by a lack of an aggregate measure (such as social mobility) to quantify the dynamics of animal societies, researchers in social sciences have been challenged by the complexity and diversity of human societies. As a result, direct empirical evidence is still lacking for the hypothesized causal relationship between social mobility and social stability. Here we attempt to fill the void by examining a much simpler society in the Tibetan macaque (Macaca thibetana), which we have tracked for 30 consecutive years. By testing two group-level hypotheses based on benefit-cost analysis and social stratification, we show the first quantitative evidence that an annual 2-to-1 stay/change ratio in the hierarchy with a 3-to-1 upward/downward ratio in intragenerational social mobility provides a substantive expected benefit for adult members to stay in the group and wait for their chances to advance. Furthermore, using a Markov transition matrix constructed from empirical data, we demonstrate that the 3-to-1 upward/downward ratio could lead to long-term structural stability in Tibetan macaque society.

Marked variation between winter and spring gut microbiota in free-ranging Tibetan Macaques (Macaca thibetana).

Variation in the availability and distribution of food resources is a strong selective pressure on wild primates. We explored variation in Tibetan macaque gut microbiota composition during winter and spring seasons. Our results showed that gut microbial composition and diversity varied by season. In winter, the genus Succinivibrio, which promotes the digestion of cellulose and hemicellulose, was significantly increased. In spring, the abundance of the genus Prevotella, which is associated with digestion of carbohydrates and simple sugars, was significantly increased. PICRUSt analysis revealed that the predicted metagenomes related to the glycan biosynthesis and metabolic pathway was significantly increased in winter samples, which would aid in the digestion of glycan extracted from cellulose and hemicellulose. The predicted metagenomes related to carbohydrate and energy metabolic pathways were significantly increased in spring samples, which could facilitate a monkey's recovery from acute energy loss experienced during winter. We propose that shifts in the composition and function of the gut microbiota provide a buffer against seasonal fluctuations in energy and nutrient intake, thus enabling these primates to adapt to variations in food supply and quality.

Social rank versus affiliation: Which is more closely related to leadership of group movements in Tibetan macaques (Macaca thibetana)?

Research on leadership is a critical step for understanding collective decision making. However, only 4 of the 22 extant macaque species have been examined for the impact of social rank and affiliation on the initiation of collective movement. It is far from clear whether such impact exists and, if so, how it works among other macaques. To answer these questions, we investigated free-ranging, Tibetan macaques' (Macaca thibetana) group departures from a provisioning area and tested two alternative hypotheses: personal versus distributed leadership. Personal leadership predicts that a single, highest ranking individual initiates the most group movements, whereas distributed leadership predicts that different members lead the group on different occasions and affiliative individuals have more initiations. We recorded how often and how successfully adults initiated group movements from a provisioning area into the forest, and related these variables to the duration of interindividual proximity and grooming time in the forest. All adults initiated group movements, but did so variably. Social rank was related neither to the number of successful initiations nor to the success ratio of initiations. By contrast, eigenvector centrality based on proximity relations was positively correlated with the number and ratio of successful initiations. Moreover, successful initiations were positively correlated with social grooming. Overall, Tibetan macaques showed a pattern of distributed leadership. Our study demonstrated the relationship between social affiliation and individual leadership in a macaque society. Am. J. Primatol. 78:816-824, 2016. © 2016 Wiley Periodicals, Inc.