Building resilience in primate tourism: insights from the COVID-19 pandemic and future directions.

The coronavirus disease 2019 (COVID-19) pandemic revealed the vulnerability of the tourism industry, triggering a call for a structural shift. This study focuses on COVID-19 impacts on primate tourism sites using the resilience-based wildlife tourism study of Jones et al. (2023) as an interpretive framework. Using an online survey, we collected data on impacts, changes, and challenges experienced at primate tourism destinations in various parts of the world. Based on 33 responses, the study found that the most profound impacts were financial, compromising the ability to run facilities and facilitate tourism due mainly to limitation of access to sites for tourists and/or staff/researchers. Seventeen respondents reported that their sites did not make substantial changes in response to the pandemic. This warrants further study to elicit the reasons for the lack of response. It may indicate difficulties in adaptation or implementation due to limited resources or other factors amid COVID-19 pandemic. We suggest that the framework proposed by Jones et al. (2023) has limitations in effectively addressing rapid and extensive repercussions of a disruption such as the COVID-19 pandemic.

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.

Impacts of the COVID-19 pandemic on mammals at tourism destinations: a systematic review.

The COVID-19 outbreak is having an unprecedented effect on human society, but how is it affecting the mammals that people live with? Mammals that were part of tourism experiences are of concern, because they impact on people's health and livelihoods and, since many of them are now dependent on people, we urge consideration of the status of these mammals as a result of the pandemic.We provide a systematic review of the impacts the COVID-19 outbreak has had on mammals in tourism venues. We examine reports of diverse species in various settings responding to changes in their environments that are occurring because of the pandemic.We searched the scholarly literature, preprints, and online news sources using combinations of the search terms 'tourism', 'animals', 'wildlife', 'coronavirus', and 'COVID-19'. We searched Web of Science, SCOPUS, EBSCOHost, JSTOR, bioRxiv, OSFPREPRINTS, GDELT, Google News, and National Public Radio, and analysed a total of 39 news articles, one peer-reviewed article, and six preprints.In total, we identified 92 distinct animal reports representing 48 mammal species. We used an existing tourism classification schema to categorise each article based on the situation reported, with the new addition of one context. We classified 92 separate animal reports in 46 articles into four (of six possible) contexts: mammals as attractions (n = 40 animal reports), mammals as commodities (n = 33), mammals as threats (n = 2), and unusual sightings of mammals (n = 17). Shortage of food, in danger of losing home, having an enriched/relaxed environment, spatial expansion, disease transmission, and poaching are the major impacts or events reported in these contexts.We suggest changes for each context with respect to how people interface with mammals, with the goal of improving the lives of mammals and the people dependent on them.

Human caregivers are integrated social partners for captive chimpanzees.

In a captive environment, it is challenging to ensure the highest level of social and psychological well-being for species with naturally complex social organizations and structures. There is a growing need to meet the social requirements for individuals of these species, especially chimpanzees, housed in zoos, sanctuaries, rehabilitation centers, and laboratories. Complex social interactions and broader social structures can be aptly described via social network analysis. We expand on the literature regarding captive chimpanzee social networks, but uniquely consider their human caregivers as potential social partners. We observed the social interactions between one group of seven chimpanzees (Pan troglodytes) and their caregivers in six behavioral contexts (nearest neighbor, play, aggression, grooming, grooming solicitation, and social vigilance) at Chimpanzee Sanctuary Northwest (USA). By constructing multiple chimpanzee and chimpanzee-caregiver social networks, our results indicate that caregivers are integrated partners in this group's social structure. Additionally, we observed that the type and strength of chimpanzee-caregiver relationships varied between the chimpanzees. These results support the notion that caregivers offer additional opportunities (i.e., beyond those with conspecifics) for captive chimpanzees to construct and maintain meaningful social relationships. Our results show that considerations of captive primate social dynamics should include caregivers as potentially important social partners. Our results also highlight the importance of evaluating individual chimpanzee characteristics when developing philosophies of care and adopting husbandry practices that offer fulfilling social niches. Our findings bear influence on contemporary discussions of interspecies social relationships, captive welfare, health, translocation, and husbandry protocols for captive chimpanzees and other nonhuman primates.

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.

Social connectivity among female Tibetan macaques (Macaca thibetana) increases the speed of collective movements.

Social network analysis provides insights into patterns of group movements in primates, but fewer studies to date have focused on the dynamics of how such movements occur. In this study, we proposed and tested two hypotheses about the influence of sex on social connectivity and group movement in Tibetan macaques (Macaca thibetana): (1) adult females are socially more connected than are adult males and (2) social connectivity facilitates the speed of collective decision-making. We collected data from 128 successful collective movements (≥ 2 individuals followed an initiator within 5 min) over a 2-month period in a group of adult Tibetan macaques at Mt. Huangshan, China. Although high-ranking individuals of both sexes in our dataset were more central in their social network than were low-ranking individuals, our results show that affiliations between females were stronger, with more preferred associations than those between males. Groups with more females reached collective decisions faster than groups with fewer females. We conclude that female Tibetan macaques use their social networks to enhance the speed of collective decision-making, which may have associated fitness benefits.

Comparative Investigations of Social Context-Dependent Dominance in Captive Chimpanzees (Pan troglodytes) and Wild Tibetan Macaques (Macaca thibetana).

Theoretical definitions of dominance, how dominance is structured and organized in nature, and how dominance is measured have varied as investigators seek to classify and organize social systems in gregarious species. Given the variability in behavioral measures and statistical methods used to derive dominance rankings, we conducted a comparative analysis of dominance using existing statistical techniques to analyze dominance ranks, social context-dependent dominance structures, the reliability of statistical analyses, and rank predictability of dominance structures on other social behaviors. We investigated these topics using behavioral data from captive chimpanzees (Pan troglodytes) and wild Tibetan macaques (Macaca thibetana). We used a combination of all-occurrence, focal-animal, and instantaneous scan sampling to collect social, agonistic, and associative data from both species. We analyzed our data to derive dominance ranks, test rank reliability, and assess cross-context predictability using various statistical analyses. Our results indicate context-dependent dominance and individual social roles in the captive chimpanzee group, one broadly defined dominance structure in the Tibetan macaque group, and high within-context analysis reliability but little cross-context predictability. Overall, we suggest this approach is preferable over investigations of dominance where only a few behavioral metrics and statistical analyses are utilized with little consideration of rank reliability or cross-context predictability.

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.

Playing it cool: Characterizing social play, bout termination, and candidate play signals of juvenile and infant Tibetan macaques (Macaca thibetana).

Play behaviors and signals during playful interactions with juvenile conspecifics are important for both the social and cognitive development of young animals. The social organization of a species can also influence juvenile social play. We examined the relationships among play behaviors, candidate play signals, and play bout termination in Tibetan macaques (Macaca thibetana) during juvenile and infant social play to characterize the species play style. As Tibetan macaques are despotic and live in groups with strict linear dominance hierarchies and infrequent reconciliation, we predicted that play would be at risk of misinterpretation by both the individuals engaged in the play bout and by those watching, possibly leading to injury of the players. Animals living in such societies might need to frequently and clearly signal playful intent to play partners and other group members to avoid aggressive outcomes. We gathered video data on 21 individually-identified juvenile and infant macaques (one month to five years of age) from the Valley of the Wild Monkeys, Mt. Huangshan, China. We used all-occurrence sampling to record play behaviors and candidate play signals based on an ethogram. We predicted that play groups would use multiple candidate play signals in a variety of contexts and in association with the number of audience members in proximity to the players and play bout length. In the 283 playful interactions we scored, juvenile and infant macaques used multiple body and facial candidate play signals. Our data showed that juvenile and infant Tibetan macaques use a versatile repertoire of play behaviors and signals to sustain play.

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.

The vocal repertoire of Tibetan macaques (Macaca thibetana): A quantitative classification.

Vocal repertoires are basic and essential components for describing vocal communication in animals. Studying the entire suite of vocal signals aids investigations on the variation of acoustic structure across social contexts, comparisons on the complexity of communication systems across taxa, and in exploration of the evolutionary origins of species-specific vocalizations. Here, we describe the vocal repertoire of the largest species in the macaque genus, Macaca thibetana. We extracted thirty acoustic parameters from call recordings. Post hoc validation through quantitative analyses of the a priori repertoire classified eleven call types: coo, squawk, squeal, noisy scream, growl, bark, compound squeak, leap coo, weeping, modulated tonal scream, and pant. In comparison to the rest of the genus, Tibetan macaques uttered a wider array of vocalizations in the context of copulations. Previous reports did not include modulated tonal screams and pants during harassment of copulatory dyads. Furthermore, in comparison to the rest of the genus, Tibetan macaque females emit acoustically distinct copulation calls. The vocal repertoire of Tibetan macaques contributes to the literature on the emergence of species-specific calls in the genus Macaca with potential insights from social, reproductive, and ecological comparisons across species. Am. J. Primatol. 78:937-949, 2016. © 2016 Wiley Periodicals, Inc.

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.

Park Rangers' Behaviors and Their Effects on Tourists and Tibetan Macaques (Macaca thibetana) at Mt. Huangshan, China.

Previous studies have reported the negative impacts of tourism on nonhuman primates (NHPs) and tourists and advocated the improvement of tourism management, yet what constitutes good quality management remains unclear. We explored whether rates of macaque aggression and self-directed behaviors (SDBs) differed under the supervision of two park ranger teams at the Valley of the Wild Monkeys (VWM) in Mt. Huangshan, Anhui Province, China. The two ranger teams provisioned and managed a group of macaques on an alternating monthly basis. Monkey, tourist and ranger behaviors were collected from August 16-September 30, 2012. Macaque aggression and SDB rates did not differ significantly under the management of the two teams. Overall, there was little intervention in tourist-macaque interactions by park rangers, and even when rangers discouraged tourists' undesirable behaviors, tourist interactions with monkeys persisted. Furthermore, only one or sometimes two park rangers managed monkeys and tourists, and rangers established dominance over the monkeys to control them. In order to effectively manage tourists and monkeys by a single park ranger, we recommend that rangers: (1) prohibit tourists from feeding; (2) move around the viewing platform more frequently; and (3) limit the number of tourists each visiting session.

Sleeping site selection by agile gibbons: the influence of tree stability, fruit availability and predation risk.

Primates spend a significant proportion of their lives at sleeping sites: the selection of a secure and stable sleeping tree can be crucial for individual survival and fitness. We measured key characteristics of all tree species in which agile gibbons slept, including exposure of the tree crown, root system, height, species and presence of food. Gibbons most frequently slept in Dipterocarpaceae and Fabaceae trees and preferentially chose trees taller than average, slept above the mean canopy height and showed a preference for liana-free trees. These choices could reflect avoidance of competition with other frugivores, but we argue these choices reflect gibbons prioritizing avoidance of predation. The results highlight that gibbons are actively selecting and rejecting sleeping trees based on several characteristics. The importance of the presence of large trees for food is noted and provides insight into gibbon antipredatory behaviour.

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.