Social risk to infant: The role of kin for maternal visual monitoring in Tibetan macaques.

Maternal monitoring of conspecifics is a crucial anti-predator strategy that also protects infants against risks within the social group. This study examines how maternal characteristics, infant characteristics, mother-infant distance, and the social environment affect maternal monitoring behaviors in free-ranging Tibetan macaques (Macaca thibetana). We observed 12 females with infants and analyzed their visual monitoring patterns. Our findings indicate that maternal rank significantly influences the time allocated to maternal visual monitoring, higher-ranking mothers spending less time than lower-ranking mothers. Maternal experience also played a role in monitoring strategies. Differences in monitoring strategies were observed based on maternal experience: first-time mothers (primiparity) engaged in longer but less frequent monitoring sessions compared to experienced mothers (multiparity). The time and frequency of maternal monitoring decreased as infants aged, and mothers with male infants showed higher levels of monitoring than those with female infants. The distance between mother and infant also affected visual monitoring behavior, with mothers increasing their monitoring levels when infants were nearby (1-5 m), rather than within reach (0-1 m) or beyond nearby (>5 m). Additionally, the presence of kin and non-kin influenced monitoring: as the number of nearby kin increased, monitoring levels decreased, while the presence of more non-kin males led to an increase in monitoring time, and higher-ranking non-kin neighbors increased the frequency of monitoring. These results suggest that Tibetan macaque mothers can adapt their visual monitoring to the social risks faced by their infants, adjusting their strategies to their status and the needs of their offspring.

Gut microbiome is associated with personality traits of free-ranging Tibetan macaques (Macaca thibetana).

Recent studies have emphasized that there is a strong link between the gut microbiome and the brain that affects social behavior and personality in animals. However, the interface between personality and the gut microbiome in wild primates remains poorly understood. Here, we used high-throughput sequencing and ethological methods in primate behavioral ecology to investigate the relationship between gut microbiome and personality in Tibetan macaques (Macaca thibetana). The behavioral assessment results indicated three personality dimensions including socialization, shyness, and anxiety. There was significant variation in alpha diversity only for shyness, with a significantly lower alpha diversity indices (including Shannon, Chao1, and PD) for bold individuals than for shy individuals. Using regression models to control for possible confounding factors, we found that the relative abundance of three genera, Akkermansia, Dialister, and Asteroleplasma, was significantly and positively correlated with the sociability scores in the macaques. In addition, Oscillospiraceae exhibited a positive correlation with scores for Shy Dimension. Furthermore, we found that the predicted functional genes for propionate and pyruvate, porphyrin and chlorophyll metabolic pathways related to animal behavior, were significant enriched in shyness group. We propose that the gut microbiome may play an important role in the formation of personality of Tibetan macaques.

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.

Consistent Individual Differences Drive Collective Movements in a Tibetan Macaque Group.

Collective movement has emerged as a key area of interest in animal behavior. While individual differences are often viewed as a potential threat to group cohesion, growing evidence suggests that these differences can actually influence an animal's behavior as an initiator or follower during collective movements, thereby driving the group's movement and decision-making processes. To resolve the divergence, we asked how personality can affect the dynamics of collective movements in one group of free-ranging Tibetan macaques (Macaca thibetana) in Huangshan, China. We assessed individual personality using principal component analysis and applied the generalized linear mixed model and linear mixed model to examine the influence of personality on decision making during collective movements. Our findings reveled three distinct personality types among Tibetan macaques: sociability, boldness, and anxiousness. Individuals with higher sociability scores and rank, or those with lower anxiousness scores, were more likely to initiate successful collective movements. Older individuals were less successful in initiating movements compared to young adults. Leaders with lower anxiousness scores or higher rank attracted more followers, with females attracting larger groups than males. As for followers, individuals with higher rank tended to join the collective movement earlier. Additionally, individuals with higher sociability or boldness scores had shorter joining latency in collective movement. Finally, there was a longer joining latency for middle-aged adults compared to young adults. These results suggest that individual differences are a potential driver of collective movements. We provide some insights into the relationships between personality and decision making in Tibetan macaques.

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.

Maternal and infantile gut mycobiome during the weaning period in free ranging Tibetan macaques (Macaca thibetana).

Gut microbiome is critical to the health of mammals. Many previous studies have revealed the gut bacterial microbiomes of mother and infant changed significantly during the weaning period. However, little is known concerning the gut mycobiome of wild primates. Here, we examined the variations on gut mycobiome between weaning and post-weaning for both mother and infant in wild-living Tibetan macaques (Macaca thibetana). Our results showed that the gut mycobiomes of mother and infant were dominated by two phyla Ascomycota and Basidiomycota. For both mother and infant, the ASV richness of gut mycobiome remained relatively steady from weaning to post-weaning periods, while the Shannon indexes increased significant in weaning compared to post-weaning periods. However, no significant difference between mother and infant ASV richness and Shannon indexes during weaning and post-weaning periods respectively. Compared to mothers, we found that much more known taxa of gut fungi were enriched in weaning or post-weaning periods of infants. In particular, we found that the dominant genus Aspergillus was enriched in infants during weaning period. Furthermore, we found that the relative abundance of plant pathogens were significantly higher in the post-weaning period than in the weaning period for infants. Our results indicated that weaning events could affect the gut mycobiome significantly for both mothers and infant in Tibetan macaques, which had a stronger effect on the gut mycobiome of infant monkeys than on their mothers.

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.

Effects of captive and primate-focused tourism on the gut microbiome of Tibetan macaques.

Documenting the effects of anthropogenic activities on the gut microbiome of wild animals is important to their conservation practices. Captivity and ecotourism are generally considered two common anthropogenic disturbances on the health of nonhuman primates. Here, we examined the divergences of gut microbiome in different environments of Tibetan macaques. Our results showed that there were no significant differences in the alpha diversity, predominant families and genera of gut microbiomes between wild and tourist groups. However, these indexes decreased significantly in the captive individuals. In addition, the significant differences of beta diversity and community compositions between wild and tourism groups also were detected. In particular, higher potential pathogenic and predicted KEGG pathway of drug resistance (antimicrobial) were detected in the gut microbiome of individuals in captive environment. Our results indicated that living in the wild are beneficial to maintaining gut microbial diversity of Tibetan macaques, while captivity environment is harmful to the health of this macaque. Exploring ways to restore the native gut microbiome and its diversity of captive individual should pay more attention to in the future studies.

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.

Captivity Is Associated With Gut Mycobiome Composition in Tibetan Macaques (Macaca thibetana).

Although recent studies have revealed that gut fungi may play an important functional role in animal biology and health, little is known concerning the effects of anthropogenic pressures on the gut mycobiome. Here, we examined differences of the gut mycobiome in wild and captive populations of Tibetan macaques (Macaca thibetana) targeting the fungal internal transcribed spacer (ITS) and using next generation sequencing. Our findings demonstrate that the diversity, composition, and functional guild of the Tibetan macaque gut mycobiome differ across populations living in different habitats. We found that Tibetan macaques translocated from the wild into a captive setting for a period of 1 year, were characterized by a reduction in fungal diversity and an increase in the abundance of potential gut fungal pathogens compared to wild individuals. Furthermore, we found that the relative abundance of two main fungal guilds of plant pathogens and ectomycorrhizal fungi was significantly lower in captive individuals compared to those living in the wild. Our results highlight that, in addition to bacteria, gut fungi vary significantly among individuals living in captive and wild settings. However, given limited data on the functional role that fungi play in the host's gut, as well as the degree to which a host's mycobiome is seeded from fungi in the soil or ingested during the consumption of plant and animal foods, controlled studies are needed to better understand the role of the local environment in seeding the mycobiome.

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.

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.

Variation of Gut Microbiome in Free-Ranging Female Tibetan Macaques (Macaca thibetana) across Different Reproductive States.

The gut microbiome is expected to adapt to the varying energetic and nutritional pressures in females of different reproductive states. Changes in the gut microbiome may lead to varying nutrient utilizing efficiency in pregnant and lactating female primates. In this study, we examined variation in the gut bacterial community composition of wild female Tibetan macaques (Macaca thibetana) across different reproductive states (cycling, pregnancy and lactation). Fecal samples (n = 25) were collected from ten adult females harvested across different reproductive states. Gut microbial community composition and potential functions were assessed using 16 S rRNA gene sequences. We found significant changes in gut bacterial taxonomic composition, structure and their potential functions in different reproductive states of our study species. In particular, the relative abundance of Proteobacteria increased significantly during pregnancy and lactation. In addition, the relative abundance of Succinivibrionaceae and Succinivibrio (Succinivibrionaceae) were overrepresented in pregnant females, whereas Bifidobacteriaceae and Bifidobacterium (Bifidobacteriaceae) were overrepresented in lactating females. Furthermore, the relative abundance of predicted functional genes of several metabolic pathways related to host's energy and nutrition, such as metabolism of carbohydrates, cofactors and vitamins, glycans and other amino acids, were enriched in pregnancy and lactation. Our findings suggest that changes in the gut microbiome may play an important role in meeting the energetic needs of pregnant and lactating Tibetan macaques. Future studies of the "microbial reproductive ecology" of primates that incorporate food availability, reproductive seasonality, female reproductive physiology and gut inflammation are warranted.

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.