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.     

Social interactions of juvenile female bonnet monkeys,Macaca radiata

This study reports observations on juvenile female bonnet macaques (Macaca radiata) in a field cage environment. Interaction and proximity data collected on different age classes of juvenile females indicate distinct changes in social behavior from the time a female is weaned until her first pregnancy. Behavioral development includes an increase in solitary behavior, an early disinterest in younger animals, and a surprisingly low interaction rate with relatives. Important aspects of ontogeny are lost in analyses that treat all juvenile females as a single age-class. This research was supported partially by US PHS Grant No. RR00169.     

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.     

Sources of variation in interbirth intervals among captive bonnet macaques (Macaca radiata)

Female fitness is a function of variation in the length of females' reproductive careers, the viability of their offspring, and the frequency with which they give birth. Infant loss shortens interbirth intervals in most primate species, but we know considerably less about other factors that contribute to variation in the length of interbirth intervals within groups. In one large captive group of bonnet macaques, maternal parity, age, experience, family size, and recent reproductive history are all associated with variation in the length of intervals that follow the birth of surviving infants. Primiparous females have the longest interbirth intervals, while multiparous females who have produced surviving infants in the past and have raised their last infant successfully have the shortest interbirth intervals. Infant sex and maternal rank have no direct effect upon the length of interbirth intervals. One of the underlying causes of variation in the length of interbirth intervals after surviving births seems to be variation in the timing of conceptions among females. Females who conceive early in the mating season tend to have shorter interbirth intervals than other females. However, females who are multiparous, experienced, and have recently raised infants have late conceptions and short interbirth intervals.     

Dominance and the social behavior of adult female bonnet macaques (Macaca radiata)

Female bonnet macaques are ranked according to naturally occurring dyadic aggressive interactions. Several possible correlates of these ranks are examined. Maternal rank and early life history are found to be highly correlated with rank. In addition, a number of social relationships (female/female presentations, female/female mounts, contact among females and aggression) are found to be related to rank. The meaning of rank outside of head to head encounters is discussed. This research was supported in part by the California Primate Research Center, University of California, Davis, Davis, California 95616.     

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.     

Social mechanisms of population regulation in a captive group of bonnet macaques (Macaca radiata)

The purpose of the present paper is to evaluate the factors that contributed to annual variation in fertility and infant survival in a relatively undisturbed captive group of bonnet macaques (Macaca radiata) over a 16-year period. The size and composition of this population fluctuated over time, and these changes were consistently associated with changes in female fertility and infant survival. Female fertility was highest when there were relatively few adult females in the group and when there were relatively few adult females per adult male. Similarly, infant survival was highest in years when there were relatively few adult females present and when cohorts of infants were small. Since environmental factors, such as availability of food and vulnerability to predation, were unlikely to constrain population growth in captivity, the data suggest that other mechanisms may have affected demographic processes in this captive group.     

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.     

Normal hematological indices, blood chemistry and histology and ultrastructure of pancreatic islets in the wild Indian bonnet monkeys (Macaca radiata radiata)

The present study is aimed at determining some haematological and biochemical parameters in the wild Indian bonnet monkeys as also the microscopic and ultrastructural characteristics of their pancreatic islets. Adult wild Indian bonnet monkeys (Macaca radiata radiata) of both sexes weighing between 2.5 and 4 kg were used in these experiments. Their platelet, reticulocyte and total leukocyte counts and the blood concentrations of hemoglobin and plasma proteins and the serum concentrations of aspartate amino transferase, alanine amino transferase and calcium are similar to the values reported for M. mulatta. Plasma glucose is lower when compared with reported values of M. mulatta and M. fascicularis. Insulin levels are comparable with those of M. mulatta and M. nigra. Histology of islets is similar to that of humans. Ovoid cell collections of islet cells are scattered throughout the pancreas. Ultrastructure of A, B and D cells is similar to humans. These findings suggest that this relatively underutilized macaques may be a suitable model for biomedical research.     

Dyadic and triadic reconciliation in pigtail macaques (Macaca nemestrina)

The tendency in primates for former antagonists to approach and affiliate following aggression has been termed reconciliation because the response is thought to resolve social conflicts produced by aggression. In primate societies, however, an aggressive interaction between two individuals often spreads to include other group members, especially the kin of the combatants. If post conflict affiliation resolves aggressive conflicts in a group, then affiliative increases might occur between combatants and the kin of their opponents following aggression as well as between former opponents. This hypothesis was tested in a captive group of 39 pigtail macaques (Macaca nemestrina) by comparing affiliative response frequencies of combatants during the 5 minute period following aggression to affiliative response frequencies during 5 minute baseline periods not preceded by aggressive activity. Following aggression, affiliation rates increased between combatants and their opponents, aggressors and the kin of their opponents, and aggressors and their own kin. Additional analyses showed that aggression among kin was reconciled more often than aggression among nonkin. Recipients of aggression reconciled with their attackers more often than aggressors reconciled with their victims. Animals with similar dominance ranks reconciled proportionately more often than those with large rank disparities and aggressive infractions of a calculated dominance hierarchy were reconciled more often than attacks consistent with the hierarchy. Results suggest that both dyadic and triadic reconciliations occur in M. nemestrina and that compared to other primate species M. nemestrina exhibit a moderate-to-high conciliatory tendency.     

Intergroup interactions in wild Barbary macaques (Macaca sylvanus), Ghomaran Rif mountains,Morocco

Data are presented on intergroup interactions between six groups of Macaca sylvanus in the Ghomaran region of the Moroccan Rif mountains. Intergroup encounters (0.026/observation hour) were defined as two groups being near each other (< 150 m). Encounters were further classified into: 1) neutral (indeterminate) encounters, in which very little intergroup interaction took place, with the exception of male monitoring (N = 7); 2) approach-retreat encounters with intergroup displacement, in which, without any overt agonism, members of one group slowly approached another and caused it to retreat (N = 3); and 3) agonistic encounters with intergroup displacement (N = 3). These results are compared to the only other study of intergroup interactions in wild Barbary macaques, and it is concluded that 1) observations of intergroup unification and/or coordination of movement in Barbary macaques (“herding”) probably resulted from observer error, or if these phenomena do occur, they are rare throughout the range of this species; 2) approximately half of all intergroup encounters in both studies resulted in intergroup displacement and/or intergroup agonism, evidence of intergroup competition; and 3) current data on intergroup interactions in Barbary macaques conform to the predictions of Wrangham's model of mutually competitive female-bonded, multimale groups.     

Ultrastructural specialization of intestinal epithelium over Peyer's patches in the bonnet monkey, Macaca radiata.

The follicle associated epithelium (FAE) which separates the lymphoid follicle of Peyer's patch from the gut lumen is known to have specialized cells called M cells or "microfold" cells in man and certain animals. These cells are considered to be involved in antigen uptake and transport. Our light microscopic study of the small intestine of bonnet monkeys suggested the presence of such specialised cells in FAE. We have confirmed the presence of M cells in bonnet monkey FAE having ultrastructural features very similar to those of human M cells.     

Triadic interactions among Macaca radiata: Passports and buffers

Male members of a group of captive Macaca radiata at the California Primate Research Center held and carried infants as they approached or were approached by higher-ranking males and as they were threatened by other males. Male infants between the ages of 25 and 84 weeks were involved in triadic interactions more frequently than were female infants of any age or male infants of other ages. That males were less likely to be harassed while huddling with or embracing infants suggested that infants provided an effective buffer against aggression.     

Role of prolactin on Leydig, Sertoli and germ cellular neutral lipids in bonnet monkeys, Macaca radiata.

To elucidate the specific influence of prolactin on neutral lipids in Leydig, Sertoli and germ cell compartments of the testis in immature and mature monkeys, the present study was carried out by injecting ovine prolactin (oPRL) (1 mg/kg body weight/twice daily for 10 days ip), to both age groups. Similarly, bromocryptine (an ergot alkaloid which inhibits prolactin secretion) was given to other sets of immature and mature monkeys (1 mg/kg body weight/twice daily for 10 days ip) to induce hypoprolactinemia. It was observed that after oPRL administration the total lipid accumulated in the germ cells of immature and mature monkeys. Total lipid was markedly decreased in the Leydig cells of mature monkeys only. But no such influence of PRL was evident in the Leydig cells of immature monkeys, suggesting an age-dependent effect of PRL on the Leydig cells. The increase in total lipid in the germ cells following PRL treatment was contributed by mono, di- and triacyl glycerols and free cholesterol. However, an opposite effect of PRL was evident in the Leydig cells of mature monkeys, where the cholesterols and glyceride fractions registered a decrease. The reduced cholesterol fractions in the Leydig cells following PRL treatment suggests the utilization of cholesterol for steroidogenesis. Sertoli cells were found to be comparatively resistant to change in PRL status. Bromocryptine treatment brought about the opposite effect of PRL in almost all parameters studied in both immature and mature monkeys. In general, these findings with prolactin suggests that PRL has a specific and definite influence on testicular neutral lipids and the response of different cellular compartments was found to vary.     

Relationship between testosterone and hepatic lipids in mature male bonnet monkeys, Macaca radiata (Geoffroy).

Administration of testosterone propionate (TP; 1 mg/kg body weight/day; im, for 30 days) to mature male bonnet monkeys, decreased total lipids, glyceride glycerol and cholesterol concentrations in hepatic tissue. The decrease in glyceride glycerol was due to decrease in monoacyl and triacyl glycerol. Both, free and esterified cholesterol were decreased after testosterone administration. Eventhough, total phospholipid was not significantly altered, phosphatidylserine and cardiolipin were increased, due to testosterone administration. Testosterone inhibited NADP-isocitrate dehydrogenase activity in liver. The findings suggest that testosterone acts as a lipolytic hormone and its action may be direct through its specific receptors in liver.     

Not in their genes: Phenotypic flexibility, behavioural traditions and cultural evolution in wild bonnet macaques

Phenotypic flexibility, or the within-genotype, context-dependent, variation in behaviour expressed by single reproductively mature individuals during their lifetimes, often impart a selective advantage to organisms and profoundly influence their survival and reproduction. Another phenomenon apparently not under direct genetic control is behavioural inheritance whereby higher animals are able to acquire information from the behaviour of others by social learning, and, through their own modified behaviour, transmit such information between individuals and across generations. Behavioural information transfer of this nature thus represents another form of inheritance that operates in many animals in tandem with the more basic genetic system. This paper examines the impact that phenotypic flexibility, behavioural inheritance and socially transmitted cultural traditions may have in shaping the structure and dynamics of a primate society — that of the bonnet macaque (Macaca radiata), a primate species endemic to peninsular India. Three principal issues are considered: the role of phenotypic flexibility in shaping social behaviour, the occurrence of individual behavioural traits leading to the establishment of social traditions, and the appearance of cultural evolution amidst such social traditions. Although more prolonged observations are required, these initial findings suggest that phenotypic plasticity, behavioural inheritance and cultural traditions may be much more widespread among primates than have previously been assumed but may have escaped attention due to a preoccupation with genetic inheritance in zoological thinking. This paper is dedicated with admiration and gratitude to the late Dr Raja Ramanna, a man who held all primates in great esteem.