Age-specific functions of stone handling, a solitary-object play behavior, in Japanese macaques (Macaca fuscata)

Stone handling (SH) in Japanese macaques, a form of solitary-object play, is newly acquired only by young individuals, and is the first example of a directly nonadaptive behavior that is maintained as a behavioral tradition within free-ranging provisioned social troops. We report here the first systematic investigation of this behavior in a stable captive social troop, the Takahama troop, which is housed in an outdoor enclosure of the Primate Research Institute (PRI), Kyoto University, Japan. This study was conducted to evaluate relevant competing hypotheses regarding the function of object play (e.g., misdirected foraging behavior and motor training) to explain the proximal causes and ultimate function(s) of SH. The "misdirected foraging behavior" hypothesis can be ruled out because of the lack of a clear temporal relationship between feeding and the occurrence of SH in any age class. Age-related differences in SH performance and behavioral patterns were observed, suggesting possible differences in the immediate cause and ultimate function between young and adults. Young individuals engaged in frequent bouts of short duration, involving locomotion and vigorous body actions throughout the day, which is typical for play by young in general. This pattern of behavior is consistent with the motor training hypothesis, which states that play occurs during the development of motor and perceptual skills and is thus potentially critical for neural and cognitive development. This practice is continued by those who acquire it at an early age, with adults engaging in significantly fewer but longer bouts that involve more stationary, complex manipulative patterns, almost exclusively in the late afternoon. We propose that for adults, at the proximate level SH is psychologically relaxing, but ultimately functions to maintain and regenerate neural pathways, and potentially helps to slow down the deterioration of cognitive function associated with advanced age in long-lived provisioned and captive macaques.     

Comparison of stone handling behavior in two macaque species: implications for the role of phylogeny and environment in primate cultural variation

This study describes the stone handling (SH) behavior of captive rhesus macaques and compares it with that of a captive troop of Japanese macaques with reference to the relative contributions of phylogeny-driven behavioral propensities, environmental differences and socially facilitated learning to the formation of culture. These systematically collected data demonstrate for the first time that two closely related macaque species might share a common cultural behavior, SH. The rhesus troop displayed SH behavioral patterns that was already described in Japanese macaque troops. The one exception was a new pattern not yet seen in any Japanese macaque troop. Differences in the physical environment of the two study enclosures may be responsible for some of the variation in observed SH behavioral patterns in these two troops. These data support the idea that environmental factors can be important for the formation of cultural variation, when the key materials needed to perform the behavior are present in both habitats (stones). Our results are consistent with the prediction made by Huffman and Hirata [The biology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 267-296] that an interactive triad of phylogenetic, environmental and social factors can be responsible for the formation of cultural variation in primates.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

Reproductive biology of rhesus and Japanese macaques

This paper offers a comparison of the reproductive biology of the Japanese macaques of Arashiyama, Japan and the free-ranging rhesus macaques of Silver Springs, Florida, U.S.A. The data indicate that rhesus macaques of Silver Springs have a higher reproductive rate than the Japanese macaques of Arashiyama. The reproducive rate of the rhesus monkeys over three birth seasons is 82% and that for the Japanese macaque is 53%. The higher reproductive rate of rhesus monkeys is accomplished through an earlier onset of sexual maturation (4 and 5 years for the rhesus and 5 and 6 years for the Japanese monkeys) and a shorter interbirth interval (14.27±5.54 months for rhesus and 18.00±6.57 months for Japanese monkeys). It is suggested that, because of the relatively harsh winters experienced by Japanese macaques, the slower reproductive rate of the Japanese monkeys has been selected for in order to enable females to lengthen the time in which maternal care is extended to their offspring.     

Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Niche separation of sympatric macaques, Macaca assamensis and M. mulatta, in limestone habitats of Nonggang, China

Comparative studies of sympatric species are essential in understanding those species’ behavioral and ecological adaptations as well as the mechanisms that can reduce resource competition enough to allow coexistence. We collected data on diet, activity budget and habitat use from two sympatric macaque species, the Assamese macaque (Macaca assamensis) and the rhesus macaque (M. mulatta), in a limestone seasonal rainforest of Nonggang Nature Reserve, southwestern Guangxi, China. Our results show that the two sympatric macaques differ in diet, activity budget, and habitat use: (1) out of the 131 plant species that were used by both macaque species as food over the year, only 15 plant species (11 %) were shared. Rhesus macaques used more plant species as major foods, and had higher dietary diversity and evenness indexes than Assamese macaques. (2) Assamese macaques fed predominantly on leaves, whereas rhesus macaques fed more selectively on fruits. The rhesus macaques’ diet varied according to season, and was significantly correlated to season fluctuation in fruit availability. (3) Assamese macaques devoted more time to resting, and less time to feeding than rhesus macaques (4) Assamese macaques were present mostly on the cliff, and tended to stay on the ground, whereas rhesus macaques were present mostly on the hillside, and showed preference to lower and middle canopy. The observed differences in diet and habitat use between the two macaque species represent behavioral patterns enabling their coexistence.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata)

We conducted behavioral observations simultaneously with fecal sample collection on eight nonlactating females 2-3 times per week, October 1997-March 1998, to examine the relationship between ovarian hormones and the sexual behavior of female Japanese macaques (Macaca fuscata) during the mating season. We analyzed samples by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone-glucuronide (E1) and pregnanediol-glucuronide (PdG) were used to separate ovarian cycles into three phases (follicular, periovulatory, and luteal). Hormonal profiles indicate average cycle lengths of 27.6 +/- 4.2 days (+/- SD; n = 26). Average lengths of the luteal and follicular phases were 12.3 +/- 3.8 days (+/- SD) and 8.3 +/- 3.4 days (+/- SD), respectively. We observed female Japanese macaques engaging in sexual activity throughout the ovarian cycle, with the highest rates occurring during the follicular and periovulatory phases as compared to the luteal phase. The attractivity of female Japanese macaques increased significantly during the follicular and periovulatory phases of the ovarian cycle, when E1 levels are peaking and PdG levels drop to baseline. In addition, females displayed a significant increase in proceptive behavior during the follicular and periovulatory phases. Grooming bouts, as well as proximity between female and male macaques, also increased significantly during the follicular and periovulatory phases. We conclude that fluctuating levels of ovarian hormones in different phases of the cycle are significantly associated with variable rates of copulatory and pericopulatory behaviors in these Japanese macaque females.     

Age-related differences in the performance, diffusion, and maintenance of stone handling, a behavioral tradition in Japanese macaques

Identifying the sources of behavioral diversity in non-human primates is vital to understanding the evolution of human behavior. Stone handling (SH, hereafter) is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. This behavior is socially transmitted from generation to generation in Japanese macaques (Macaca fuscata), as a behavioral tradition. SH behavior in particular may reflect on the origin and evolution of stone-tool material culture. The objective of this study was to assess how group size, age structure, and age- and sex-related differences may account for the substantial intra- and inter-troop variations in SH reported in ten troops of Japanese macaques. Our results supported the hypothesis that patterns of variation in SH across troops reflected variability in group size and composition in age classes. We found that troop size was correlated with the proportion of troop members exhibiting SH simultaneously. The effect of troop size on the synchronized performance of SH may reveal the contagious nature of play. Our results suggest that the age structure of the group may affect the diffusion of SH. As predicted by the surplus energy hypothesis, a major functional hypothesis about play, intra-group variation in SH reflected more age- than sex-related differences. SH mainly occurred and was more frequent in younger than in older individuals, whereas no significant sex differences were found. SH episodes were shorter, more vigorous, and SH patterns were more diverse and less complex in immature than in mature individuals. The present findings reveal that age-related factors and group size may constrain the performance, diffusion, and maintenance of SH within a troop. Contrary to most other socially transmitted stone-tool using behaviors in non-human primates and early hominids, there is no optimal SH pattern. Provided some form of social learning, the non-adaptive nature of SH may allow particular SH pattern preferences to emerge at the group level. Our findings urge the use of an inter-populational comparative approach based on multivariate analyses when addressing the question of the evolution of behavioral traditions in primate and human populations.     

Molecular Evidence for Distinct Genotypes of Monkey B Virus (Herpesvirus Simiae) Which Are Related to the Macaque Host Species

Although monkey B virus (herpesvirus simiae; BV) is common in all macaque species, fatal human infections appear to be associated with exposure to rhesus macaques (Macaca mulatta), suggesting that BV isolates from rhesus monkeys may be more lethal to nonmacaques than are BV strains indigenous to other macaque species. To determine if significant differences that would support this supposition exist among BV isolates, we compared multiple BV strains isolated from rhesus, cynomolgus, pigtail, and Japanese macaques. Antigenic analyses indicated that while the isolates were very closely related to one another, there are some antigenic determinants that are specific to BV isolates from different macaque species. Restriction enzyme digest patterns of viral DNA revealed marked similarities between rhesus and Japanese macaque isolates, while pigtail and cynomolgus macaque isolates had distinctive cleavage patterns. To further compare genetic diversity among BV isolates, DNA sequences from two regions of the viral genome containing genes that are conserved (UL27 and US6) and variable (US4 and US5) among primate alphaherpesviruses, as well as from two noncoding intergenic regions, were determined. From these sequence data and a phylogenetic analysis of them it was evident that while all isolates were closely related strains of BV, there were three distinct genotypes. The three BV genotypes were directly related to the macaque species of origin and were composed of (i) isolates from rhesus and Japanese macaques, (ii) cynomolgus monkey isolates, and (iii) isolates from pigtail macaques. This study demonstrates the existence of different BV genotypes which are related to the macaque host species and thus provides a molecular basis for the possible existence of BV isolates which vary in their levels of pathogenicity for nonmacaque species.     

Molecular phylogeny of macaques: implications of nucleotide sequences from an 896-base pair region of mitochondrial DNA

We determined the nucleotide sequences of an 896-base pair region of mitochondrial DNA (mtDNA) from 20 primates representing 13 species of macaques, a baboon, and a patas. We compared these sequences and the homologous sequences from four macaques and a human against each other and deduced the phylogenetic relationships of macaques. The results from the phylogenetic analyses revealed five groups among the macaques: (1) Barbary macaque, (2) two species of Sulawesi macaques, (3) Japanese, rhesus, Taiwanese, crab-eating, and stump-tailed macaques, (4) toque, pig-tailed, and lion-tailed macaques, and (5) Assamese and bonnet macaques. The phylogenetic position of Tibetan macaque remains ambiguous as to whether it belongs to the fourth or fifth group. Phylogenetic trees revealed that Barbary macaque diverged first from the other Asian macaques. Subsequently, the four groups of Asian macaques diverged from one another in a relatively short period of time. Within each group, most of the species diverged in a relatively short period of time following the divergence of the groups. Assuming that the Asian macaques diverged from the outgroup Barbary macaque three million years ago (MYA), the divergence times among groups of Asian macaques were estimated at 2.1-2.5 MYA and within groups at 1.4- 2.2 MYA. The intraspecific nucleotide diversity observed among three rhesus macaques was so large that they did not form a monophyletic cluster in the phylogenetic trees. Instead, one of them formed a cluster with Japanese and Taiwanese macaques, whereas the other two formed a separate cluster. This implies that either polymorphisms of mtDNA sequences that existed before the divergence of these three species (ca. 700,000 years ago) have been retained in rhesus macaques or introgression has occurred among the three species.      

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.     

Consortships and conceptions in captive rhesus macaques (Macaca mulatta)

A captive group of rhesus macaques (Macaca mulatta) was observed during the breeding season to determine if consortship behavior, rather than promiscuous matings, resulted in higher reproductive success for either partner. The 38 adult females in this group were observed “in consort” with the 5 adult or 4 subadult males on 179 occasions. Most of these consortships were short-term, lasting less than one day. Six females engaged in consortships with one male that spanned more than three days, but the majority of these long-term associations did not result in a pregnancy with that male. The term “consortship” has been traditionally accepted as a specific nonhuman primate mating pattern, but the exact nature of this behavioral pattern and its evolutionary importance have been less clearly understood. Consort behavior could be considered a precursor to a monogamous mating system if long-term exclusive sexual associations resulted in higher reproductive success for the participants. But this study demonstrates that for rhesus macaques, who exhibit both consort behavior and more promiscuous matings, there is no clear reproductive advantage to long-term consortships. In light of the inconsistent use of the term consortship, the possible adaptive significance of an exclusive male-female sexual association for the evolution of human mating patterns needs to be reevaluated.     

Vocal communication of tonkean macaques in confined environments

Vocal recordings of one semi-free-ranging group and one captive group of Tonkean macaques (Macaca tonkeana) were used to establish the vocal repertoire of the species. Only the alpha male of the groups uttered a very distinctive loud call. Localization variants of coo calls were found. Alarm calls given by this species were acoustically similar to those by Japanese, rhesus, and long-tailed macaques (M. fuscata, M. mulatta, andM. fascicularis). Adult females uttered a specific variant of vocalizations during sexual morphological changes. The repertoire of agonistic vocalizations was more variable than that of any other macaque species investigated. These characteristics were discussed with reference to previous studies on vocalizations of macaque species.     

Copulatory behavior in relation to anatomical characteristics of three macaques

Anatomy of copulatory organs and patterns of copulatory behavior were studied in three species of Macaca. The copulatory behavior of the rhesus monkey (M. mulatta) and crab-eating macaque (M. fascicularis) were similar. Mounting time was longer in stump-tailed macaque (M. arctoides) (48 seconds) than in the rhesus monkey or crab-eating macaque (8.5 seconds). Species differences were correlated with anatomical differences in the female and male reproductive organs. In the stump-tailed macaque the male has a relatively long penis, and the female has an elaborate vestibular colliculus in the vestibule. Both rhesus and crab-eating macaques have a short penis, and the female has no vestibular colliculus. Under scanning electron microscope, cone-like projections (3–4 mm) were observed on the surface of the glans and corpus penis of M. arctoides. In M. fascicularis shorter projections (0.05–0.1 mm) were observed on the glans penis but not the corpus penis.     

Bioacoustic monitoring of aggression in group-housed rhesus macaques

Many captive primate facilities house rhesus macaques in multimale-multifemale social groups in large enclosures that simulate the natural social and environmental features characteristic of the species, enhancing their reproductive performance as well as their psychological well-being, yet one of the most difficult management problems in socially housed macaques is their propensity for exhibiting spontaneous bouts of deleterious aggression. To address this management problem, an automated bioacoustic monitoring system might be developed that is capable of detecting and forecasting problematic patterns of contact aggression. To evaluate the utility of this approach, this study examined the magnitude of aggression and the co-occurrence of certain vocalization types and aggression in 10 groups of rhesus macaques. The data confirmed aggression as a significant problem in rhesus groups and indicated that certain patterns of vocalizations are indicative of the type or level of aggression. The detection and classification of these vocalization types need further research to eventually design and implement an efficacious bioacoustic system for monitoring aggression in rhesus macaques.     

Congenital limb malformations in the free-ranging macaques of Kowloon

This paper describes the instances of gross hand and limb malformations in the free-ranging macaques in the forested region of the Kowloon peninsula of Hong Kong. The incidence in this location is compared to that of other macaque groups, most notably the Japanese and rhesus macaques in free-ranging and captive conditions. Etiology is linked to what is known about suspected local teratogenic agents, particularly in pesticides and fuel emissions.     

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.     

Food provisioning and stone handling tradition in Japanese macaques: a comparative study of ten troops

By addressing the influence of food provisioning on stone handling (SH), a behavioral tradition in Japanese macaques, this study contributes to the ongoing debate in cultural primatology by asking whether human intervention influences the emergence or propagation of behavioral traditions. SH is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. We tested the hypothesis that the frequency of food provisioning affects the daily performance, form, and context of occurrence of SH by influencing a troop's feeding-related activity budget. We used a standardized observation procedure to investigate SH in ten troops of Japanese macaques. In troops provisioned several times a day, SH was more frequent, longer, and more prevalent during provisioning than nonprovisioning periods. These effects of provisioning were not significant in troops provisioned less frequently. SH was more frequently integrated with food-related activities in troops supplied with food several times a day than in the other troops. Food provisioning may be a key factor in the innovation and transformation phases of the SH tradition in Japanese macaques.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.