Vocal communication of wild bonnet macaques (Macaca radiata)

Field observations and spectrographic analyses of sound recordings of South Indian bonnet macaques revealed a vocal repertoire of at least 25 basic patterns. The repertoire consists of well separated sound classes and acoustic categories connected by structural intergradation. Besides structural variations within and between different elements of the repertoire, the vocal system ofMacaca radiata is characterized by regular combinations of particular basic patterns. These combinations occurred not only between calls of similar structure and function but also between calls usually emitted in entirely different social contexts. According to the qualitative analysis, sex-specific asymmetries of the vocal behaviour were less pronounced than age-dependent characteristics. The comparison of clear call vocalizations ofMacaca radiata andM. fuscata revealed significant species-specific differences on the structural and the behavioural level. Evaluations of the structural features of alarm calls of various macaque species imply marked differences between members of thefascicularis group andsinica group on one hand and thesilenus group andarctoides group on the other.     

Strategies used by bonnet macaques (Macaca radiata) to reduce predation risk while sleeping

Sleep results in a decrease in alertness, which increases an animal’s vulnerability to predation. Therefore, choice of sleeping sites would be predicted to incorporate predator-avoidance strategies. The current study, conducted in two national parks in southern India, examined the behaviors adopted by bonnet macaques (Macaca radiata) to reduce the risk of being preyed upon while sleeping. Bonnet macaques from an urban setting with a low predatory risk were included for comparison. The physical characteristics of the sleeping sites in the forest corresponded with features that were most difficult for predators to access; bonnet macaques selected emergent trees with high boles near human settlements. These trees typically overhung water. Within the canopy, individuals slept in huddled subgroups near the terminal ends of branches, preferentially selecting branches over water. Subgroups were generally composed of members of the same age and sex, which likely promoted social bonding. Adult males and females with infants selected branches higher than members of other age and sex categories. The lateral distances of individuals along branches from the main trunk were similar across demographic categories. The size of a subgroup appeared to be limited by the weight a branch could support; lateral distances were maintained by regulation of mean subgroup weight, with heavier individuals forming smaller subgroups. The urban troop slept on the top of a building. Subgroup compositions at the urban site were similar to those at the forest sites. However, subgroup size, not restricted by branch fragility, resulted in larger subgroups than those found in the forest. Our results indicate that bonnet macaques adopted a suite of behaviors that reduced their risk of being preyed upon at night by selecting sleeping sites that minimized predator encounters and by selecting the safest locations within the canopy.     

Early environment shapes the development of gaze aversion by wild bonnet macaques (<Emphasis Type="Italic">Macaca radiata</Emphasis>)

Among many species of primates, staring is perceived as a sign of aggression and averting the gaze usually serves to reduce such conflict. The current study conducted in southern India documented developmental differences among wild bonnet macaques (Macaca radiata) in their latency to gaze avert after establishing eye contact with other individuals. Feeding stations were used to gather macaques within a small area to facilitate the video recording of group dynamics and eye contact between subordinate and dominant individuals. Individuals were grouped into three age classes: juveniles, subadult males, and adult males. Comparisons were also made between urban and forest dwelling troops. In the forest, juveniles established eye contact with older males for significantly longer periods of time than did adults. A linear trend was observed in which the latency to gaze avert after establishing eye contact decreased with age. This trend was not evident in the urban troops, for which the latency to gaze avert did not change significantly with age. Urban juveniles were also more likely to be chased when they established eye contact with adults compared with their forest counterparts. These differences could be the result of increased predatory risk in the forest setting — the necessity for heightened predator vigilance in forests may reduce the frequency with which juveniles are monitored and chased or attacked as a result of their eye contact. Conversely, the rarity of predators in the city may engender more intense aggressive behavior between monkeys, accelerating the rate of learning to signal appeasement to dominant males.     

Mother-infant relationships in bonnet macaques: Sources of variation in proximity

Family composition is an important predictor of variation in proximity among captive bonnet macaque (Macaca radiata) mothers and their infants. Infants that have several immature sisters in the group are initially more independent that infants with fewer sisters, but as they reach 6 months of age infants with several sisters become less independent than their peers. The effects of the presence of juvenile females on the relative independence of their infant siblings seem to be related to the fact that the members of families with several immature females are the targets of more aggression than are the members of other families.     

Geophagy by the bonnet macaques (Macaca radiata) of southern India: A preliminary analysis

Bonnet macaques (Macaca radiata) in the Marakkanam Reserved Forest of southern India consume termitaria soils. Samples from the ingested termite mounds are compared with samples taken from the surrounding uneaten soils in an attempt to determine why the termitaria soils are eaten. Particle size, clay and primary mineral composition, geochemistry, and scanning electron microscopic analyses are used to search for a possible explanation for geophagy among the bonnet macaques. Kaolin minerals abound throughout the Marakkanam soil sample suite. But the termitaria soils are distinguished by the presence of small amounts of smectite. An abundance of kaolin minerals in combination with small amounts of smectite strongly resembles the mineralogy ofeko, a traditional African remedy for stomach ailments, and Kaopectate™, a western anti-diarrhoeal preparation. The percentage of mature leaves and fruits ofAzadirachta indica consumed by the bonnet macaques is relatively high. Plant feeding deterrents, such as, acid detergent fibre (ADF) and the inherent nature of the fruits ofAzadirachta indica, when consumed in large quantities to act as a purgative, could cause gastrointestinal upsets and diarrhoea. At Marakkanam, bonnet macaques ingest termitaria earth that would act as a pharmaceutical agent to alleviate gastrointestinal upsets and control diarrhoea.     

Behavioral changes across the menstrual cycle in isosexual groups of bonnet macaques (Macaca radiata)

Behavioral changes were systematically recorded across menstrual cycles over a six-month period in two laboratory-housed isosexual triads ofMacaca radiata (bonnet macaque). The purpose of this study was to determine whether females of this species demonstrate premenstrual behavioral changes as reported for humans, or heightened levels of aggression during the first half of their cycle as reported in some species of Old World monkeys. A total of 34 menstrual cycles were divided into five segments including two follicular, one periovulatory, and two luteal phases. The mean frequencies of behaviors were analyzed according to phase, rank, and time since triad formation, for a total of 34 menstrual cycles. There was no evidence of an increase in spatial separation during the premenstrual phase or during any other phase of the menstrual cycle. Although contact aggression did not show an increase during the early follicular half of the cycle (phases 1 and 2) or during the phase of the cycle immediately preceding menses (phase 5), contact aggression did show two peaks: one in the early-mid luteal half of the cycle (phase 4) and a peak in the mid-late follicular (phase 2). The non-aggressive hierarchical behaviors did not follow the same pattern as contact aggression. Instead the distribution of these behaviors showed a pattern similar to that of estrogen levels across the cycle. Subjects’ location in pen also varied significantly according to cycle phase: subjects spent more time on perches during the premenstrual phase and more time on the pen floor during the periovulatory phase. The increase in contact aggressive behaviors during the early-mid follicular phase and the mid-late luteal phase does not suggest a simple hormonal correlate as these two phases are characterized by high levels of estrogen and progesterone, respectively. However, the distribution of non-aggressive hierarchical behaviors suggest that this category of agonistic interaction may be related to mating competition among females of this species. Results are discussed with reference to the social behavior and promiscuous mating strategy ofM. radiata. The findings in this present study are compared with previous studies utilizing other species of Old World monkeys. Differences in study design and group composition are considered as factors effecting discrepant results both within and between species.     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Infectious disease,behavioural flexibility and the evolution of culture in primates

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.     

Japanese macaques form a cross-modal representation of their own species in their first year of life

We tested whether infant Japanese macaques (Macaca fuscata) have a cross-modal representation of their own species. We presented monkeys with a photograph of either a monkey or a human face on an LCD monitor after playing back a vocalization of one of those two species. The subjects looked at the monitor longer when a human face was presented after the monkey vocalization than when the same face was presented after human vocalization. This suggests that monkeys recall and expect a monkey’s face upon hearing a monkey’s voice.     

Reconciliation in three groups of lion-tailed macaques

We studied postconflict behavior in three captive groups of lion-tailed macaques (Macaca silenus). After a conflict, we monitored the aggressee as the focal individual during a 10-min postconflict period and made control observations the following day on the same individual. Selective attraction between former opponents occurred in the first minutes of the postconflict period. The conciliatory tendency was relatively high, about 40%. Although no specific behavior was used to reconcile, postconflict contacts were especially intense and a rich repertoire of affiliative patterns was exihibited. With regard to the rate and form of reconciliation, lion-tailed macaques resemble Sulawesi macaques, which belong to the same phyletic lineage. We also discuss the possible interrelations between conciliatory patterns and other characteristics of social organization.     

External characteristics and associated developmental changes in two species of Sulawesi macaques,Macaca tonkeana andM. hecki,with special reference to hybrids and the borderland between the species

The degree of intergradation between two species of Sulawesi macaques,Macaca tonkeana andM. hecki, was studied by examining the diagnostic external characteristics of more than 100 monkeys kept as pets by natives. Two possible hybrid monkeys were found and both originated from the borderland between the two species, located in the most proximal region of the northern peninsula of Sulawesi. The previously postulated wide area of integradation between the two species at the possible contact zone was, however, not recognized, and typical examples oftonkeana orhecki were found to be present on the two sides of a narrow “hybrid” zone which was defined by direct observations. Furthermore, despite considerable individual variations, we were able to allocate most monkeys to one or other of the species. Each of ten external characteristics of the members of both species more or less encompassed the individual variations, but may undergo changes with the development of the monkeys. The mechanisms of reproduction of hybrid monkeys and the maintenance of differences between the species are discussed.     

NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan

A macaque population produced by the hybridization of native Japanese macaques (Macaca fuscata) and introduced Taiwanese macaques (M. cyclopis) in Wakayama Prefecture was shown to possess three DNA haplotypes of the natural resistance-associated macrophage protein 1 (NRAMP1). Based on genotyping and comparison with M. fuscata populations, it was revealed that the introduced M. cyclopis population was polymorphic for the NRAMP1 locus. Extensive crossbreeding of the introduced species with the native species was confirmed using this genetic marker and the proportion of M. cyclopis genes was 57.4%. Results of statistical tests suggested non-random mating in the hybrid population.     

Identifying innovation in laboratory studies of cultural evolution: rates of retention and measures of adaptation

In recent years, laboratory studies of cultural evolution have become increasingly prevalent as a means of identifying and understanding the effects of cultural transmission on the form and functionality of transmitted material. The datasets generated by these studies may provide insights into the conditions encouraging, or inhibiting, high rates of innovation, as well as the effect that this has on measures of adaptive cultural change. Here we review recent experimental studies of cultural evolution with a view to elucidating the role of innovation in generating observed trends. We first consider how tasks are presented to participants, and how the corresponding conceptualization of task success is likely to influence the degree of intent underlying any deviations from perfect reproduction. We then consider the measures of interest used by the researchers to track the changes that occur as a result of transmission, and how these are likely to be affected by differing rates of retention. We conclude that considering studies of cultural evolution from the perspective of innovation provides us with valuable insights that help to clarify important differences in research designs, which have implications for the likely effects of variation in retention rates on measures of cultural adaptation.     

Affiliative function of the silent bared-teeth display in moor macaques (Macaca maurus): Further evidence for the particular status of sulawesi macaques

The silent bared-teeth display is described in a captive group of Moor macaques (Macaca maurus). It occurs with either closed or open mouth and is observed in both affinitive and playful interactions. It does not appear to convey specific information about the social status of partners and should be viewed as a signal advertising the emitter's peaceful intentions. This is consistent with what is known for other species of macaques on Sulawesi island.     

Cladistic analyses of behavioural variation in wild Pan troglodytes: exploring the chimpanzee culture hypothesis

Long-term field studies have revealed considerable behavioural differences among groups of wild Pan troglodytes. Here, we report three sets of cladistic analyses that were designed to shed light on issues relating to this interpopulation variation that are of particular relevance to palaeoanthropology.In the first set of analyses, we focused on the proximate cause of the variation. Some researchers have argued that it is cultural, while others have suggested that it is the result of genetic differences. Because the eastern and western subspecies of P. troglodytes are well differentiated genetically while groups within the subspecies are not, we reasoned that if the genetic hypothesis is correct, the phylogenetic signal should be stronger when data from the eastern and western subspecies are analysed together compared to when data from only the eastern subspecies are analysed. Using randomisation procedures, we found that the phylogenetic signal was substantially stronger with in a single subspecies rather than with two. The results of the first sets of analyses, therefore, were inconsistent with the predictions of the genetic hypothesis.The other two sets of analyses built on the results of the first and assumed that the intergroup behavioural variation is cultural in nature. Recent work has shown that, contrary to what anthropologists and archaeologists have long believed, vertical intergroup transmission is often more important than horizontal intergroup transmission in human cultural evolution. In the second set of analyses, we sought to determine how important vertical transmission has been in the evolution of chimpanzee cultural diversity. The first analysis we carried out indicated that the intergroup similarities and differences in behaviour are consistent with the divergence of the western and eastern subspecies, which is what would be expected if vertical intergroup transmission has been the dominant process. In the second analysis, we found that the chimpanzee cultural data are not only comparable to a series of modern human cultural data sets in terms of how tree-like they are, but are also comparable to a series of genetic, anatomical, and behavioural data sets that can be assumed to have been produced by a branching process. Again, this is what would be expected if vertical inter-group transmission has been the dominant process in chimpanzee cultural evolution.Human culture has long been considered to be adaptive, but recent studies have suggested that this needs to be demonstrated rather than assumed. With this in mind, in the third set of analyses we investigated whether chimpanzee culture is adaptive. We found the hypothesis that chimpanzee culture is adaptive was supported by an analysis of data from the Eastern African subspecies, but not by an analysis of data from the eastern and western subspecies.The results of our analyses have implications for the number of subspecies in Pan troglodytes, the relationship between hominin taxa and Palaeolithic industries, and the evolution of hominin cognition and behaviour.     

Species differences of male loud calls and their perception in sulawesi macaques

Playback experiments were conducted to investigate interspecific discrimination of male loud calls in Sulawesi macaques. Loud calls of four macaque species living in Sulawesi (Macaca tonkeana, M. maurus, M. hecki, andM. nigrescens) and a control stimulus (an 8-sec frequency modulated sound) were played back to semi-free-ranging Tonkean macaques (M. tonkeana). A preliminary acoustic analysis indicated that the calls of these four species differ in some spectral and temporal features. In the playback experiments, Tonkean macaques responded in a similar manner to conspecific calls and calls of two other species,M. maurus andM. hecki. In contrast, animals responded more weakly to the call ofM. nigrescens and the control stimulus. Males responded more strongly than females to all stimuli, while females appeared to be more discriminating for species differences than males. Analyses on the acoustic features of loud calls suggested that high frequency, wide frequency range, and repetition of sound units at a high rate elicit quick responses from animals.     

Vertical distribution of wild Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island, Japan: Preliminary report

A census of wild Yakushima macaques (Macaca fuscata yakui) was carried out in a 23-km² area of the western coast of Yakushima Island, Japan. We analyzed the census data to investigate changes in monkey distribution associated with the vertical distribution of vegetation. In the lowland coastal zone of 0–300 m above sea level (a.s.l.), 4.8 troops and 62.4–99.8 monkeys are estimated to have existed per km². In the mountainside zones of 300–900 m a.s.l., the troop density decreased to 1.3–1.6 troops/km². Since there was no difference in size between the coastal and mountainside troops, population density should decrease with altitude to about 30–36 monkeys per km². On the other hand, 2.4 troops and about 36 monkeys were estimated to have inhabited per km² in the mountain summit zone of 900–1,323 m a.s.l. Nature Conservation College     

Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance

In many anthropoid primates, mating activity is not restricted to the ovarian cycle but also occurs during pregnancy. Although it has been suggested that the main function of this post-conception mating is to confuse paternity, studies showing whether or not male primates can distinguish between the fertile phase of the conception cycle (FPCC) and the period of peak post-conception mating (peak PCM) are almost non-existent. Here, we examine whether the pattern of female sexual traits (specific sexual behaviors, sexual swelling) and female attractiveness to males differ between FPCC and peak PCM in 6 wild female long-tailed macaques. We also use fecal hormone analysis to investigate whether female traits during peak PCM are related to changes in female sex hormones. All females exhibited a distinct period of heightened mating activity around days 45-60 of gestation. During peak PCM, swelling size and frequency of female solicitations (but not reaching back) were significantly correlated with changes in the estrogen to progestogen ratio. Swelling size, frequency of female sexual behaviors and copulations and proportion of male-initiated copulations and ejaculations were not significantly different between FPCC and peak PCM. Although males spent significantly less time consorting females during peak PCM, all (particularly low-ranking and non-resident males) invested heavily in terms of reproductive costs associated with mate-guarding and mating during pregnancy. We conclude that post-conception mating in wild long-tailed macaques is not merely a by-product of endocrine changes and devoid of adaptive function. Our results more strongly support the hypothesis that it may form part of a female reproductive strategy to confuse paternity, which appears to apply particularly to low-ranking and extra-group males.