Dong-Po Xia

Grooming Reciprocity in Female Tibetan Macaques Macaca Thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free‐ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques. Am. J. Primatol. 74:569–579, 2012.

Grooming reciprocity in male Tibetan macaques

In several primate species, adult males are reported to compete for access to reproductive partners as well as forming affiliative and cohesive social bonds based on the exchange of goods or services. We hypothesized that among a broad set of fitness‐maximizing strategies, grooming can be used by individual adult males to enhance social relationships through reciprocity and/or through the interchange of grooming for a different but equivalent good or service. We used focal animal sampling and continuously recorded dyadic grooming and agonistic interactions to test a series of predictions regarding male social interactions in a free‐ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China. During the non‐mating season or between males of similar rank throughout the year, grooming effort given was matched by grooming effort received. However, lower ranking males groomed higher ranking males at a greater rate and/or for a longer duration during both the mating and non‐mating periods. We found that higher ranking males directed less aggression towards males with whom they formed a frequent grooming partnership, indicating that grooming received was interchanged for increased social tolerance. These data suggest that individual male Tibetan macaques employ alternative social strategies associated with grooming reciprocity or interchange depending on dominance rank and rates of aggression, and highlight the importance of both biological markets and grooming reciprocity as behavioral mechanisms used by resident adult males to form and maintain affiliative social bonds. Am. J. Primatol. 75:1009–1020, 2013.

Seasonal variation and synchronization of sexual behaviors in free-ranging male Tibetan macaques (Macaca thibetana) at Huangshan, China

Although seasonal breeding has been documented in many non-human primates, it is not clear whether sexual behaviors show seasonal variation among male individuals. To test this hypothesis, the focal animal sampling method and continuous recording were used to investigate seasonal variation and synchronization of sexual behaviors in five male Tibetan macaques (Macaca thibetana) at Mt. Huangshan from Oct 2005 to Sept 2006. Both copulatory and sexually motivated behaviors (i.e., sexual chase, grimace, and sexual-inspection), which were significantly higher in the mating season than non-mating season. Furthermore, seasonal variations of sexual behaviors, including copulatory and sexually motivated behaviors, were synchronized among males. The results shed light on sexual competition and tactics for reproductive success of male M. thibetana and other non-human primates with seasonal breeding.

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.

Collective Movement in the Tibetan Macaques (Macaca thibetana): Early Joiners Write the Rule of the Game

Collective behavior has recently attracted a great deal of interest in both natural and social sciences. While the role of leadership has been closely scrutinized, the rules used by joiners in collective decision making have received far less attention. Two main hypotheses have been proposed concerning these rules: mimetism and quorum. Mimetism predicts that individuals are increasingly likely to join collective behavior as the number of participants increases. It can be further divided into selective mimetism, where relationships among the participants affect the process, and anonymous mimetism, where no such effect exists. Quorum predicts that a collective behavior occurs when the number of participants reaches a threshold. To probe into which rule is used in collective decision making, we conducted a study on the joining process in a group of free-ranging Tibetan macaques (Macaca thibetana) in Huangshan, China using a combination of all-occurrence and focal animal sampling methods. Our results show that the earlier individuals joined movements, the more central a role they occupied among the joining network. We also found that when less than three adults participated in the first five minutes of the joining process, no entire group movement occurred subsequently. When the number of these early joiners ranged from three to six, selective mimetism was used. This means higher rank or closer social affiliation of early joiners could be among the factors of deciding whether to participate in movements by group members. When the number of early joiners reached or exceeded seven, which was the simple majority of the group studied, entire group movement always occurred, meaning that the quorum rule was used. Putting together, Macaca thibetana used a combination of selective mimetism and quorum, and early joiners played a key role in deciding which rule should be used.

Influence of dominance rank and affiliation relationships on self- directed behavior in female Tibetan macaques (Macaca thibetana)

Self-directed behavior (SDB) is characterized as an indicator of anxiety, frustration and stress in nonhuman primates. In this study, we collected self-directed behavior data from one group of free-ranging Tibetan macaques (Macaca thibetana) at Mt. Huangshan, China (September 2012-May 2013) using a combination of behavioral sampling methods including focal animal sampling, behavioral sampling, continuous sampling and instantaneous sampling. Our results showed that females engaged in significantly higher rates of self-directed behavior when they were in proximity to dominant individuals compared to subordinate ones. Conflict losers significantly increased their SDB rates after agonistic episodes, indicating that SDB might also serve as an index of anxiety in M. thibetana. We further found that females significantly increased their SDB rates when focal individual was proximity to weakly affiliation relationship higher rank members than to strongly affiliation relationship higher rank members. If conflicts were not reconciled, the postconflict SDB rates of losers were higher when they stayed with strongly affiliation opponents; if conflicts were reconciled, victims of strongly affiliation relationships opponents engaged in more SDB rates before reconciliation than after reconciliation, while victims of moderately affiliation relationships opponents did not engaged in more SDB rates before reconciliation than after reconciliation. We conclude that both of dominance rank and affiliation relationships might both influence the SDB rates of female Tibetan macaques significantly, suggesting that SDB is not only an index of anxiety in Tibetan macaques, but also can provide a new insight into evaluation of social relationships between individuals.

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.

Ecological footprints and development trends in Hefei, China

Purpose Because natural resource utilization is a predictor of sustainable development, an evaluation of the efficiency of resource utilization is critical for assessing developmental potentiality. The purpose of this paper is to apply three-dimensional (3D) ecological footprint theory to assess the effects of production and consumption on ecological systems in Hefei, China. Design/methodology/approach Using data for Hefei for the period 2005-2014, an ecological footprint model (EFM) was developed to calculate the area’s ecological footprint (EF), ecological carrying (EC) capacity and obtain two indices, namely, footprint depth and size. The relationship between economic development and natural resource utilization was subsequently evaluated based on the calculated ecological deficit and the EF demand per Renminbi 10,000 of gross domestic product (GDP). Findings Over the last decade, Hefei’s EF per capita evidenced a 9.87 percent growth rate, increasing from 1.16 hm2/person in 2005 to 2.70 hm2/person in 2014. EC capacity per capita increased from 0.21 hm2/person in 2005 to 0.36 hm2/person in 2014, evidencing a gradually increasing trend at an average annual growth rate of 6.24 percent. Thus, between 2005 and 2014, the ecological deficit increased annually by three times. The amplification of footprint depth significantly exceeded that of footprint size. Between 2005 and 2014, Hefei’s EF per capita Renminbi 10,000 of GDP decreased annually by 4.68 percent. Thus, energy consumption in Hefei exceeded the natural regeneration capacity of energy resources, with excessive development and resource utilization impacting on the regional ecological system. Practical implications The application of a 3D EFM sheds light on natural resource utilization within regional development. Moreover, footprint depth and size are significant predictors of the impacts of natural resource utilization. These findings will also benefit other countries or cities. Originality/value This is one of the first empirical studies to apply a 3D EFM to evaluate the relationship between natural resource utilization and economic development. Adopting a sustainable development framework, it provides insights into the effects of natural resource utilization in relation to the balance between the natural ecological system and economic development. This has far-reaching implications beyond Hefei and China.

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 macaques 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.