Interactions between visitors and Formosan macaques (Macaca cyclopis) at Shou‐Shan Nature Park,Taiwan

Ecotourism involving feeding wildlife has raised public attention and is a controversial issue, especially concerning nonhuman primates. Between July 2002 and April 2005, the behavior of monkeys and tourists was collected through scan samplings, focal samplings and behavior samplings at the Shou‐Shan Nature Park located in Taiwan's second largest city—Kaohsiung. In addition, the number of tourists and monkeys was counted in different hours and places within the park. Four hundred visitors were interviewed using a questionnaire to gather data on sex, age, purpose and frequency of visit to the park. The number of tourists was significantly higher during weekends than in weekdays in all locations. Humans dominated in the initiation of interspecies interactions—the overall ratio of human‐initiated and monkey‐initiated interactions was 2.44:1. Human–monkey conflicts accounted for only 16.4% of the total interactions (n=2,166), and adult human males and adult male macaques participated in higher rates than other age/sex groups in these conflicts. Visitors showed more affiliative behavior (15.9%) than agonistic behavior (8%) toward the macaques. In response to visitors' threat or attack, the Formosan macaques mostly showed submissive behavior with bared teeth, squealed or ran away to avoid confrontation (69.1%)—only few responded with counteraggression (18.7%). This study for the first time provided evidence that food provisioning increased both the frequency and duration of aggression among Formosan macaques (P<0.001). During food provisioning, the average frequency and the duration of agonistic events of macaques were more than 4 times higher compared with those without food provisioning. The average frequency of food provision by tourists was 0.73 times/hr—more than twice the incident that monkeys grabbed the food from tourists (0.34 times/hr). If people refrain from feeding monkeys and destroying the city park's natural vegetation, monkeys can be used to educate public about nature conservation in an urban setting. Am. J. Primatol. 71:214–222, 2009. © 2008 Wiley‐Liss, Inc.     

海南南湾猴岛景区内猕猴与游客接触行为的研究

在世界范围内,观赏和投喂野生猿猴是最常见的野生动物旅游形式之一。其中游客与动物的关系越来越成为动物学、人类学和社会学学者研究关注的热点。游客在娱乐的过程中,存在被猿猴威胁甚至咬伤等问题。对人猴接触行为的客观分析,是提高旅游服务管理和保障游客安全的必要措施。本研究记录了2012-2014年海南南湾猴岛景区内游客与猕猴的接触行为,并分析了景区医务室近两年的游客就诊记录,主要探讨：（1）哪些游客会参与人猴接触,及其游客的认识误区;（2）哪些猕猴会频繁参与人猴接触;（3）哪些原因会引发人猴接触行为。本文旨在了解景区内游客与猿猴的互动关系,探讨游客受伤原因及其解决办法,为完善野生动物旅游的健康发展提供基础资料。     

Human–wildlife conflict: Proximate predictors of aggression between humans and rhesus macaques in India

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co‐inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3‐month study of four free‐ranging populations of rhesus macaques in Dehradun, India from October–December 2012, using event sampling to record all instances of human‐macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human‐primate conflict, and indeed other types of human‐wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other. Am J Phys Anthropol 156:286–294, 2015. © 2014 Wiley Periodicals, Inc.     

Aggression in adult male primates: A comparison of confined Japanese macaques and free-ranging olive baboons

The frequencies and types of adult male aggressive behavior of confined Japanese macaques (Macaca fuscata)and free-ranging olive baboons (Papio anubis)were compared. The baboons, which do not have a mating season, were more aggressive to conspecific males than were the macaques during their nonmating season. The baboons also solicited aid during aggressive encounters more frequently than the macaques. However, during their mating season, the macaques were more aggressive to conspecific females than were the baboons. The macaques were also involved in more triadic sequences of aggression, and the frequency of occurrence of these patterns supported Chase’s theory of dominance hierarchy formation and maintenance. The differences in aggressive behavior appeared to be related to the seasonal reproductive cycle of the macaques.     

Dispersal,nepotism, and primate social behavior

High degrees of relatedness within primate social groups are thought to promote the evolution of altruistic behavior via kin selection. Dispersal, for whatever reason, should limit opportunities for nepotistic behaviors. Conversely, emigration is usually attributed to the avoidance of inbreeding depression. Actual dispersal patterns may result from a balance of these forces. Systematic behavioral differences are expected between taxa that differ in such patterns. In fact, comparisons of (a) colobines vs. cercopithecines, (b) bonnet, stumptailed, and Barbary macaques vs. Japanese and rhesus macaques, and (c) red vs. mantled howler monkeys yield a perplexing blend of unexplained differences and unmet theoretical expectations. Kin selection may be less important than generally believed, and/or methodological standardization more so.     

Temperament in Rhesus,Long‐Tailed,and Pigtailed Macaques Varies by Species and Sex

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey—rhesus (Macaca mulatta), long‐tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques—using cage‐front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early‐life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long‐tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species’ social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male–male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species‐typical behaviors adaptive. Our results suggest that adaptive species‐level social differences may be encoded in individual‐level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303‐313, 2013. © 2012 Wiley Periodicals, Inc.     

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.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata)

It is predicted that variation in intergroup relationships in group living primates reflects the cost and benefit of resource defense. We tested the applicability of the model by examining population difference, group difference, and seasonal difference in behaviors during intergroup encounters in two populations of Japanese macaques (Macaca fuscata), one of six groups from Yakushima Island, and the other of three groups from Kinkazan Island. We found that the nature of intergroup encounter varied with group identity, reproductive seasonality, and population. Yakushima groups showed aggressive behaviors more frequently than did Kinkazan groups and the difference was consistent with the food competition model, both because of the involvement of females, and because home ranges were smaller on Yakushima than on Kinkazan, and thus more defensive. Both sexes of animals participated in aggressive interactions, but males were more aggressive than females. Furthermore, Yakushima population showed more agonistic intergroup behaviors during the mating season than the non-mating season. Also during the encounters, intergroup mating was observed, but only in Yakushima. It is concluded that intergroup relationships reflect the mate guarding behavior by group males. However, the agonistic relationship during non-mating season, especially that of among females, is also consistent with the food competition model. It is also noted that males' behavior toward other groups can also be interpreted as a form of investigative behavior before possible transfer into a new group.     

Postconflict Affiliation Between Former Opponents in Macaca thibetana on Mt. Huangshan, China

We describe basic patterns of postconflict affiliation between former opponents within a group of wild, provisioned Tibetan macaques Macaca thibetana on Mt. Huangshan, China. Like most primates studied to date, Tibetan macaques reconciled, i.e., overall they engaged in affiliative interaction with opponents at higher rates immediately after an aggressive conflict than at other times. Probabilities of affiliation were enhanced ≤30 s after the end of hostilities. However when we examined sex partner combinations separately, we found unequivocal evidence for reconciliation only for male-male dyads. Tolerant interaction among other partner combinations apparently was not disrupted after a conflict, presumably obviating the need to reconcile. One aspect of reconciliation among males was consistent with other indications of a despotic dominance style: aggressors initiated a higher proportion of affiliative interactions after a conflict than at other times. Another aspect of reconciliation was more typical of relaxed dominance styles: males used specialized behaviors (embraces and same-sex mounts) disproportionately to reconcile. We also found inconsistent evidence for the valuable relationship hypothesis; probabilities of reconciliation were enhanced for male-male dyads with the closest affiliative relationships, but not for those that displayed the most tolerance or mutual agonistic support. We discuss reconciliation and other aspects of conflict management among males in the context of a group with nearly even sex ratios and high male-male mating competition.     

Coprophagy-related interspecific nocturnal interactions between Japanese macaques (<Emphasis Type="Italic">Macaca fuscata yakui</Emphasis>) and sika deer (<Emphasis Type="Italic">Cervus nippon yakushimae</Emphasis>)

The influence of sympatric large animals on the sleeping behavior of primates in the wild is still largely unknown. In this study, we observed behaviors of wild Japanese macaques (Macaca fuscata yakui) at their sleeping sites, using a highly sensitive video camera. We found evidence of nocturnal interspecific interactions, such as agonistic interactions, between Japanese macaques and sika deer (Cervus nippon yakushimae). Deer approached sleeping clusters of macaques, which slept on the ground, to eat their feces or unidentified materials near the sleeping clusters, and as a result, the macaques were often quickly displaced from their sleeping site. There was a significant difference in the occurrence of macaque–deer agonistic interactions between seasons. Our results suggested that the size of the sleeping cluster, the number of adult macaques in the cluster, and the existence of adult males in the cluster did not influence the occurrence of the agonistic interactions. Finally, we discuss the influence of this interaction on macaques and speculate on the influential factors leading to nocturnal coprophagy of macaques’ feces by deer.     

Successive aggression: another pattern of polyadic aggressive interactions in a captive group of Japanese macaques

Several patterns of polyadic aggressive interactions have been previously reported. Here, we describe another pattern of polyadic interactions in a captive group of Japanese macaques (Macaca fuscata fuscata) that we designate as "successive aggression". We defined successive aggression as aggression by the original actor toward a second recipient within a very short time interval after the initial aggression toward the first recipient. We compared the patterns and characteristics of successive aggression to those of redirection. Among 2,698 recorded aggressive interactions, 80 involved successive aggressions and 75 were classified as redirections. Females, especially adult females, performed and received more successive aggression, whereas males, especially adult males, performed and received more redirection. Successive aggression often occurred when the first recipient exhibited counter-aggression. Successive aggression was then directed toward an individual related to the first recipient, such as the mother, offspring or sibling. The targets of redirection were not relatives of the first recipient in most cases, but were clearly subordinate individuals. The dominance relationships among the aggressor, the first recipient and the second recipients were usually non-linear for successive aggression, but were linear for most cases of redirection. These results suggest that monkeys can anticipate possible opponents who may intervene in ongoing aggressive interactions and suppress them, even though they are not yet hostile toward these individuals. Successive aggression may function to establish and maintain dominance relationships among matrilineal groups through repeated confirmations.     

Tourism and Infant-Directed Aggression in Tibetan Macaques (Macaca thibetana) at Mt. Huangshan,China

ABSTRACT

Previous studies of habituated Tibetan macaques (Macaca thibetana) at Mt. Huangshan, China demonstrated the negative impact that some tourism management strategies had on monkeys' annual infant mortality, but data on precise causes and perpetrators of infant injuries were not available. We worked at the same site and recorded rates of aggression that older monkeys directed toward group infants as a function of tourist numbers and proximity. We found a negative correlation between the number of people on the viewing platform and the frequency of monkeys' aggression toward the group's infants, but the effect is slight. We noted that infant-directed aggression (IDA) was more likely to occur in the provisioning zone where tourists bounded the monkeys on two sides, despite the fact that infants spent very little time in that location. The alpha and beta males engaged in more IDA than expected, while the other three adult males, adult females, and juveniles exhibited less IDA than expected. Males' IDA included biting, chasing, grabbing, and pushing. Adult females bit and grabbed mostly their own infants in the contexts of punishment and weaning. Juveniles' IDA was uncommon and consisted mostly of open-mouth threats. To minimize the severity and frequency of male-toinfant IDA, we recommend that sections of the tourist viewing platform be closed off so that tourists do not surround the monkeys, particularly when infants are near the viewing platforms and tourist numbers are few. The rule against tourists feeding monkeys should also be strictly enforced, so that altercations between the highest-ranked males and other group members, particularly infants, are less likely to occur.     

Grooming relationships of adolescent orphans in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama: a comparison among orphans with sisters, orphans without sisters, and females with a surviving mother

The present study examined grooming relationships of adolescent females in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama. To assess whether the loss of the mother influenced the grooming relationships of adolescent females (5–7 years old), we compared the time spent in grooming interactions and the number of grooming partners among the following three groups: 6 adolescent orphans with sisters, 9 adolescent orphans without sisters, and 11 adolescent non-orphans with surviving mothers. In Japanese macaques, grooming most frequently occurs between mothers and their daughters. Therefore, it is expected that if the mother is lost, orphans will devote less time to grooming interactions than non-orphans. However, the time spent in overall grooming interactions did not differ among the three groups. While non-orphans maintained grooming relationships with their mothers, orphans acquired alternative grooming relationships with other group members. Orphans adopted two kinds of tactics to compensate for the loss of the mother. First, adolescent orphans with sisters developed more affiliative grooming relationships with their sisters than non-orphans with sisters. Secondly, adolescent orphans without sisters spent more time in grooming interactions with same-aged females and non-related adult females. Moreover, regarding grooming interactions with same-aged females and non-related adult females, orphans without sisters had a larger number of grooming partners than non-orphans. These results indicate that adolescent females have enough flexibility to develop their grooming network after the loss of their mothers, and that the lack of mother and sisters might accelerate socialization of adolescent females and enable them to be integrated in reciprocal adult grooming relationships.     

Changes in the social structure of two groups of stumptail macaques (Macaca arctoides)

Two previously studied groups of stumptail macaques were restudied to investigate stabilities and instabilities within group structures. Frequency data for nonsocial and dyad behaviors were collected. While there was considerable group stability, several important changes occurred. The most noteworthy group changes were in grooming and playing. Individual changes centered upon females. The first and fourth ranking females of one group switched dominance positions. The roots of this reversal were minimally reflected by aggressive and submissive interactions, and more fully exposed by quiet association patterns such as grooming, huddling, and sitting together. Increased frequencies of huddling, touching, and approaching indicated that the lowest ranking female of each group moved closer to other group members. There was no hint of this change in agonistic interactions.     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.     

Qualitative Assessment of Macaque Tourist Sites in Padangtegal,Bali, Indonesia,and the Upper Rock Nature Reserve,Gibraltar

Human tourists share space with, touch, feed, and otherwise interact with Macaca at multiple locations. Across Asia and stretching to Gibraltar and Northern Africa, macaques form a substantial tourist attraction as their ranges become increasingly coincident with human use zones. Residing in or as tourist attractions, macaques frequently generate economic benefits to local humans and compete with them for habitat and specific resources. In addition, health conflicts may emerge from increased overlap and interactions between humans and macaques. There is only a handful of studies on the impact, structure, context, and cultural ecology of macaque tourist sites. We provide a general overview of 2 macaque tourist sites, one in Padangtegal, Bali, Indonesia and one in Gibraltar. Qualitative assessment reveals variability in behavioral, ecological, economic, and politically relevant facets of macaque tourism. Specifically, differences in aggression during interactions, potential health dangers, economic factors, and local human perceptions between Padangtegal and Gibraltar suggest that qualitative assessments can assist in our construction of broader models and conceptualizations of the interaction context.     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.     

Causes of obesity in captive cynomolgus macaques: influence of body condition, social and management factors on behaviour around feeding

Similar to other primate species, captive cynomolgus macaques (Macaca fascicularis) are prone to becoming overweight. The relationship between body condition and feeding behaviour in group-housed animals has not been reported. This study evaluated the effect of daily feeding routines on behaviour patterns in cynomolgus macaques to determine whether overweight macaques displayed different behaviours and activity levels. In this prospective observational study, 16 macaques (m = 4, f = 12) from four separate troops (n = 4 per troop) were selected from a colony of 165 animals. Observational data were collected over six months during morning and afternoon feedings by scan sampling. Behaviours of interest included foraging, eating, aggressive and positive social interactions, inactivity and physical activities. Multivariable mixed logistic regression modelling was used for data analysis. Results indicated that overweight animals were more likely to be inactive, dominant animals had increased probabilities of eating compared with non-dominants, and aggressive behaviours were more likely to occur in the morning and before feeding, suggesting feeding anticipation. Positive social interaction before feeding was seen and may be a strategy used to avoid aggressive encounters around food resources. Individual animal caregivers had an unintentional impact on behaviour, as decreased eating and an increase in inactivity were noted when certain individuals fed animals. These findings illustrate the complexities of feeding group-housed cynomolgus macaques to avoid overweight body condition. Feeding routines may require more care and attention to distribute food in a way that ensures equitable food intake among troop animals, while not disturbing group cohesion.