Intraspecies variation in dominance style of Macaca fuscata

Knowledge of intraspecific variation is important to test the evolutionary basis of covariation in primate social systems, yet few reports have focused on it, even in the best-studied species of the Macaca genus. We conducted a comparative study of the dominance styles among three provisioned, free-ranging groups of Japanese macaques at Shodoshima Island, Takasakiyama Mountain and Shiga Heights, and collected standard data on aggressive and affiliative behavior during a period of 5 years. Our data in the Takasakiyama and Shiga groups support previous studies showing that Japanese macaques typically have despotic social relations; nevertheless, our data in the Shodoshima group are inconsistent with the norm. The social traits of Shodoshima monkeys suggested that: (1) their dominance style is neither despotic nor tolerant but is intermediate between the two traits; (2) some measures of dominance style, e.g., frequency and duration of social interactions, covary as a set of tolerant traits in Shodoshima monkeys. This study suggests broad intraspecific variation of dominance style in Japanese macaques as can be seen in some other primate species.     

The function of teeth chattering in male Barbary macaques (Macaca sylvanus)

Teeth chattering is seen in many primate species and has been proposed to have a range of social functions. This observational study tested specific hypotheses relating to the function of teeth chattering in a semi-free-ranging group of Barbary macaques, Macaca sylvanus. During focal watches of males, the outcome of male-male dyadic social interactions in which teeth chattering was present or absent was compared. Using these data, we tested the predictions of four hypotheses: teeth chattering functions as a signal of submission, appeasement, affiliation or reassurance. Support was found for all four hypotheses. In addition, in some contexts, an exchange of teeth chattering appeared to have a greater impact on the outcome of interactions than one male alone giving this signal. These findings suggest that teeth chattering serves an important role in coordinating the social interactions of male Barbary macaques.     

Ground substrate affects activity budgets and hair loss in outdoor captive groups of rhesus macaques (Macaca mulatta)

How the captive environment influences the behavior of animals is relevant to the well-being of captive animals. Captivity diverges from the natural environment in many ways, and one goal of enrichment practices is to encourage species-typical behavior in these unnatural environments. This study investigated the influence of grass vs. gravel substrate on activity budgets and degree of hair loss in seven groups of captive rhesus macaques housed in outdoor enclosures at the California National Primate Research Center. Groups having grass substrate spent a greater proportion of their time foraging and a smaller proportion of time grooming compared with groups having gravel substrate. Increased time spent grooming in gravel enclosures may have contributed to significantly greater hair loss in those enclosures. A causal relationship between ground substrate on foraging and grooming, and therefore hair loss, is strengthened by similar changes in activity budgets and hair loss in a single group that was moved from gravel to grass substrate halfway through the study. These results add to growing evidence that substrate type in captivity is important to consider because it affects animal well-being. In particular, these results reveal that grass substrate is more effective than gravel in stimulating foraging and reducing allo-grooming to levels that are comparable to wild populations, and enable animals to maintain healthier coats.     

Extra-large cluster formation by Japanese macaques (Macaca fuscata) on Shodoshima Island, central Japan, and related factors

Japanese macaques on Shodoshima Island habitually form very large rest clusters, in which 50+ or even 100+ individuals huddle together. This behavior is not seen in any other populations of the species. Mean cluster sizes of two groups of Shodoshima monkeys are three and four in summer and 17 and 16 in winter, respectively. A maximum of 137 individuals have been seen to huddle in one cluster. It is difficult to explain the extra large clusters on Shodoshima only as an adaptive behavior against cold, since Shodoshima is relatively warm in the range of habitats for Japanese macaques. Compared with other groups of Japanese macaques, Shodoshima monkeys show: more frequent affinitive interactions, shorter inter-individual distance, more frequent ignoring of exclusion, more frequent aggression, less intense aggression, and more frequent counter-aggression. These characteristics suggest that the Japanese macaques on Shodoshima have relaxed dominant relations. The specific social organization of Shodoshima monkeys may sustain the formation of extra large clusters. Inter-group comparisons suggest that the social structure of Japanese macaques might be highly plastic, and that Shodoshima monkeys have less despotic, more tolerant social relations than typically reported for this species.     

Demodex spp. in the hair follicles of rhesus macaques (Macaca mulatta)

The perineal or perineal and facial skin were evaluated on 53 rhesus macaques as part of a necropsy protocol. Microscopic evaluation of H & E stained skin sections revealed 19 animals positive for Demodex spp. Mites were seen within all portions of the hair follicles. Infestation varied from minimal to severe. Mites were found in macaques of all ages and in both sexes. Reaction to the mites ranged from no reaction, to minimal follicular epidermal hyperplasia to furunculosis. Immune status of the animal did not determine infestation but immune compromised macaques had more severe lesions. This is the first known report of Demodex spp. in rhesus macaques.     

Social Tolerance in Wild Female Crested Macaques (Macaca nigra) in Tangkoko‐Batuangus Nature Reserve,Sulawesi, Indonesia

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared‐teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared‐teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females’ social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems. Am. J. Primatol. 75:361‐375, 2013. © 2013 Wiley Periodicals, Inc.     

Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (<Emphasis Type="Italic">Macaca fascicularis umbrosus</Emphasis>)

Macaques possess a repertoire of extractive foraging techniques that range from complex manipulation to tool-aided behaviors, to access food items that increase their foraging efficiency substantially. However, the complexity and composition of such techniques vary considerably between species and even between populations. In the present study, we report seven such complex manipulative behaviors that include six extractive foraging behaviors, and teeth flossing, in a population of Nicobar long-tailed macaques. The apparent purpose of these behaviors was an extraction of encased food, processing food, foraging hidden invertebrates, and dental flossing. Among these behaviors, three behaviors viz. wrapping, wiping, and teeth-flossing were tool-aided behaviors, where macaques used both natural and synthetic materials as tools. Occasionally macaques also modified those tools prior to their use. The substrate use patterns of leaf rubbing and teeth flossing were similar to that observed in other macaques. The spontaneous tool modification to perform wrapping was a first time observation. These observations suggest that Nicobar long-tailed macaques have a high level of sensorimotor intelligence which helps to evolve such innovative foraging solutions.     

Social communication among captive stump-tailed macaques (Macaca arctoides)

I compared the frequency of occurrence, contextual usage, and meaning of some of the most prominent gestural signals in stump-tailed macaques. I recorded the occurrence of 15 visual and tactile behavior patterns in a multimale multifemale captive group of stump-tailed macaques with the behavior sampling method in 100 hr of observation and analyzed the data via factor analysis and analyis of variance. The hindquarter presentation was the most frequent gesture. It was displayed by subordinates to appease dominants even in the absence of impending risk of aggression. Bared-teeth, lip-smack, teeth-chatter, and present-arm are submissive signals as well, but they differ from the presentation and from one another in their contextual usage. Nonthrusting mount, hip-touch, hip-clasp, and genital manipulation are directed down the hierarchy and appear to reflect dominance, reassurance, protection, or bonding. Mock-bite is a ritualized aggressive behavior pattern, often used to resolve uncertain dominance relationships. Ventroventral embrace occurs as a female bonding pattern. Overall, most gestural signals in stump-tailed macaques relate to dominance and submission and, to a lesser extent, social bonding.     

Fatty acid supplements improve hair coat condition in rhesus macaques

As captive rhesus macaques often exhibit hair loss, alopecia was quantified and behavior was recorded before, during, and after fatty acid supplementation in six macaques. Fatty acid treatment was associated with a decrease in alopecia and in self‐grooming behavior. Therefore, fatty acids may be a viable treatment for alopecia in some captive primates.     

Coat condition, housing condition and measurement of faecal cortisol metabolites--a non-invasive study about alopecia in captive rhesus macaques (Macaca mulatta)

BACKGROUND: Previous studies have characterized alopecia in captive rhesus macaques (Macaca mulatta) by a mixed partial to complete alopecia in a bilateral symmetric pattern. METHODS: In this study, coat condition assessments were related to exogenous and endogenous factors in captive rhesus macaques under different housing conditions in order to identify disturbances in environmental factors controlling or influencing hair growth. Additionally, the degree of alopecia was investigated in relation to adrenal endocrine function as an indicator of social stress using faecal glucocorticoid measurements. RESULTS: Hair loss was found to vary with season and sex, was most pronounced in adult females during the winter and spring months. Generally, infants were not affected, but alopecia developed during adolescence. However, the housing system, available enclosure space and variations in group size and composition also appeared to influence coat condition. Levels of immunoreactive cortisol metabolites (11-oxoetiocholanolone) in faeces were significantly negatively correlated with alopecia, suggesting a relationship between hypothalamic-pituitary-adrenal (HPA) axis activity and hair loss in captive rhesus macaques. CONCLUSIONS: Although the present study demonstrates the influence of the HPA axis on coat condition, it is not known if hair loss is caused by abnormal behaviour or hormonal imbalances of the HPA axis itself. Our data suggest that alopecia in rhesus macaques is a highly complex multicausal disorder.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

Social behavior in stump-tailed macaques (Macaca speciosa) after lesions of the dorsolateral frontal cortex

This experiment observed the effects of dorsolateral frontal cortex ablations on quantified social interactions of stump-tail macaques within the context of the social behavior of a larger group. A caged group of 11 stump-tail macaques, six females and five males, was observed for 100 hours pre-operatively. Post-operatively, five operates and five sham operates matched for sex, age, and rank were observed for 110 hours. Aggression increased following surgery. The female operates ranked No. 3 and No. 5 were seen to fall to the bottom of the dominance hierarchy two months after surgery. The fall in dominance as measured by displacement behavior was found to permeate several behavioral categories including presenting, threatening, and aggression. The female operates appeared to fall in inverse relationship to their ranks. The male operates showed minimal disruptions after surgery. The length of the time between surgery and the outbreak of violence might represent the length of time required for subordinates to notice and confirm the behaviors resulting from attentional defects in the high-ranking female operates.     

An ethological study on chimpanzees at the artificial feeding place in the Mahale mountains,Tanzania—with special reference to the booming situation

A provisioned chimpanzee group in the Mahale Mountains was observed. The characteristic feature of chimpanzee behavior is that many types of behavior occur at one time as a bout of interactions. This can be seen in the booming situation in the wild. Similar situations were observed at the artificial feeding place. The behavior of the initiators of the interactions differed according to age, sex and social status. The chimpanzees' behavior was studied as a system. The relationships between each behavior pattern were investigated by analysis of the sequential behaviors of the same individual, and that of chains of signal-response behaviors, as well as that of behaviors which appeared when a third individual joined the initial interaction. Appeasement behaviors were more flexible, while others were more stereotyped. Part of the appeasement behavior resembled begging behavior. Appeasement behavior is thought to have a rather new phylogenetic origin. It is suggested that the various chimpanzee behaviors have evolved as a harmonious system which can be observed in the booming situation. The origin of chimpanzee society based on the evolution of their behavior system is discussed. Analysis of triplet interactions indicated that the types of triplet interaction in chimpanzees are quite different from those of multiple male group species such as macaques and baboons.     

中国熊猴的分类整理

本文通过查看国内收藏的标本对M.assamensis进行了分类整理,认为M.a.coolidgei的亚种地位应予恢复,滇西地区熊猴可能代表一个新类群。通过t检验,滇南和越南等地与滇西北和西藏东南部等地熊猴头骨的某些特征表现出显著或极显著差异。作为区分coolidgei与assamensis的指标:coolidgei体型较小,肩背毛较短,35—75mm,背毛环纹略显或不明显,0—2环,体色更为灰暗;assamensis体型较大,肩背毛较长,85—110mm,背毛环纹明显,3—4环。     

Stable isotope ratios in hair and teeth reflect biologic rhythms

Biologic rhythms give insight into normal physiology and disease. They can be used as biomarkers for neuronal degenerations. We present a diverse data set to show that hair and teeth contain an extended record of biologic rhythms, and that analysis of these tissues could yield signals of neurodegenerations. We examined hair from mummified humans from South America, extinct mammals and modern animals and people, both healthy and diseased, and teeth of hominins. We also monitored heart-rate variability, a measure of a biologic rhythm, in some living subjects and analyzed it using power spectra. The samples were examined to determine variations in stable isotope ratios along the length of the hair and across growth-lines of the enamel in teeth. We found recurring circa-annual periods of slow and fast rhythms in hydrogen isotope ratios in hair and carbon and oxygen isotope ratios in teeth. The power spectra contained slow and fast frequency power, matching, in terms of normalized frequency, the spectra of heart rate variability found in our living subjects. Analysis of the power spectra of hydrogen isotope ratios in hair from a patient with neurodegeneration revealed the same spectral features seen in the patient's heart-rate variability. Our study shows that spectral analysis of stable isotope ratios in readily available tissues such as hair could become a powerful diagnostic tool when effective treatments and neuroprotective drugs for neurodegenerative diseases become available. It also suggests that similar analyses of archaeological specimens could give insight into the physiology of ancient people and animals.     

Recognition of social relationships in bridging behavior among Tibetan macaques (Macaca thibetana)

Bridging behavior among male Tibetan macaques (Macaca thibetana) was studied in a free-ranging group at Mt. Huangshan, China. This behavior was defined as a type of affiliative behavior in which two individuals simultaneously lifted up one infant. Bridging behavior occurred after an adult male carried an infant to another male or approached another male who was holding an infant. Each male frequently held and groomed a particular infant in the group, which was named an “affiliated” infant of the male. Males were more frequently provided with their affiliated infant by other males than with other non-affiliated infants. This finding suggests that male Tibetan macaques recognized the affiliative relationship between a male and his affiliated infant, and chose that infant for bridging behavior on the basis of this knowledge. Such choice might be important for effective bridging behavior or other affiliative interactions between males. © 1995 Wiley-Liss, Inc.     

Intergroup variation in stable isotope ratios reflects anthropogenic impact on the Barbary macaques (Macaca sylvanus) of Gibraltar

Interactions with humans impact many aspects of behavior and ecology in nonhuman primates. Because of the complexities of the human–nonhuman primate interface, methods are needed to quantify the effects of anthropogenic interactions, including their intensity and differential impacts between nonhuman primate groups. Stable isotopes can be used to quickly and economically assess intergroup dietary variation, and provide a framework for the development of specific hypotheses about anthropogenic impact. This study uses stable carbon and nitrogen isotope analysis to examine intraspecific variation in diet between five groups of Barbary macaques, Macaca sylvanus, in the Upper Rock Nature Reserve, Gibraltar. Analysis of hair from 135 macaques showed significant differences in δ¹³C and δ¹⁵N values between a group with minimal tourist contact and groups that were main tourist attractions. Because we observed no overt physiological or substantial behavioral differences between the groups, feeding ecology is the most likely cause of any differences in stable isotope ratios. Haphazard provisioning by tourists and Gibraltarians is a likely source of dietary variation between groups. Stable isotope analysis and observational data facilitate a deeper understanding of the feeding ecology of the Barbary macaques relevant to the role of an anthropogenic ecology for the species.     

Fishing in Macaca fascicularis: A Rarely Observed Innovative Behavior

Observations of fishing behavior in nonhuman primates are rare and isolated, and there is no prior published observation on the behavior in long-tailed macaques (Macaca fascicularis). We observed fishing behavior in 3 groups of long-tailed macaques from 2 separate study sites in North Sumatra and East Kalimantan, Indonesia. We propose that the behavior is rare and fulfills the requirements for classification as innovation. Further, all of the fishing individuals were watched by other members of their group, with their actions inciting attempts at fishing by them. We consider the possibility that the behavior has the potential to become cultural within the populations.     

Mechanisms of social reciprocity in three primate species: Symmetrical relationship characteristics or cognition?

Agonistic intervention behavior was observed in captive groups of chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), and stumptail monkeys (M. arctoides). Reciprocity correlations of interventions were determined while removing from the data the effects of several symmetrical relationship characteristics, that is, matrillineal kinship, proximity relations, and same-sex combination. It was considered likely that if significant reciprocity persisted after controlling for these characteristics, the reciprocity was based on cognitive mechanisms. Statistical significance was tested by means of recently developed matrix permutation procedures. All three species exhibited significant reciprocity with regard to beneficial interventions, even after controlling for symmetrical traits. Harmful interventions were, however, reciprocal among chimpanzees only. This species showed a “revenge system”, that is, if A often intervened against B, B did the same to A. In contrast, both macaque species showed significantly inversed reciprocity in their harmful interventions: if A often intervened against B, B rarely intervened against A. Further analysis indicates that the strict hierarchy of macaques prevents them from achieving complete reciprocity. Compared to chimpanzees, macaques rarely intervene against higher ranking group members. The observed contrast can be partially explained on the basis of differences in available space, as indicated by a comparison of indoor and outdoor living conditions for the chimpanzee colony. Yet, even when such spatial factors are taken into account, substantial behavior differences between chimpanzees and macaques remain.     

个体亲近程度对藏酋猴攻击行为的影响

友好和冲突行为决定了群居动物的社会结构及其表现形式,表现为个体间近距差异。但目前尚不清楚藏酋猴个体间亲近关系的差异性是否会影响冲突和攻击的强度。本研究于2020年9月至2021年5月对栖息于安徽黄山的藏酋猴鱼鳞坑YA1群进行跟踪观察,采用目标动物取样法采集行为数据,全事件记录法用于攻击行为数据的补充,分析个体间近距、理毛和攻击行为矩阵的关系,并采用GLMM模型探讨攻击行为的影响因素。结果显示：藏酋猴个体间近距指数越大,理毛时间越长;个体间近距指数矩阵与攻击总次数、轻度攻击和重度攻击次数矩阵均呈显著正相关;个体间亲近关系越紧密,攻击次数和强度越大,但相较雄性间和异性间,雌性间攻击次数和强度最小。这些结果表明,个体间近距持续时间会增加理毛和攻击行为的可能性,雌性个体间社会关系更稳定,但并未发现藏酋猴根据个体间亲近关系调整攻击强度。本研究为进一步了解多雌多雄的藏酋猴群体的社会关系和社会结构提供了数据支持。