A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). I. Vocal repertoire and call emission

Vocal communication in wild long-tailed macaques (Macaca fascicularis) is described in terms of (1) a preliminary vocal repertoire and the situations in which calls occur in the natural habitat of this species and (2) quantitative measurement of the natural occurrence of calls in the field. Although a number of calls are relatively discrete (e.g., a male loud call), gradation is pronounced for both wide-spectrum (“harsh”) and narrow-spectrum (“clear”) vocal signals. Thirteen general types of harsh calls are identified provisionally as elements of the vocal repertoire. The exact number of discrete clear calls contributing to the vocal repertoire could not be ascertained precisely, but these calls were classified operationally into six broadly acoustically different classes in order to measure natural vocal behavior. Vocalizations tended to occur in temporal “clusters” during sample, periods. Narrow-band clear or “coo” calls were more frequently performed by macaques than wide-band harsh calls. The possible functional implications of the correlated occurrence of multiple vocal signals are discussed.     

Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis)

Summary The seeds in fruits consumed by primates may be chewed and digested, swallowed and defecated intact, or separated from the flesh and spat out. We show by a combination of close field observations and experiments with caged animals, that long-tailed macaques (Macaca fascicularis) have a remarkably low threshold of 3–4 mm for swallowing seeds and also that wild macaques rarely break them. The seeds of 69% of the ripe fruit species eaten are spat out intact or cleaned outside the mouth and dropped. Seed-spitting significantly reduces the swallowed food bulk and may lessen the risk of releasing seed toxins during mastication. However, it requires that even small fruits are processed in the mouth one or a few at a time. We suggest that fruit storage in the cheek pouches of cercopithecine monkeys allows them to spit seeds individually without excessively slowing fruit intake while feeding on patchily distributed fruit. In contrast, Apes and New World monkeys apparently swallow and defecate most ripe seeds in their diet and colobine monkeys break and digest them, detoxifying seed defenses by bacterial fermentation.     

Genetic characterization of long-tailed macaques (Macaca fascicularis) on Tabuan Island Indonesia

Protein and mitochondrial DNA variations (D-loop region PCR-RFLP) were analyzed for 7 serum and 40 clot samples collected from long-tailed macaques (Macaca fascicularis) living on Tabuan Island, Indonesia. Protein polymorphisms were examined electrophoretically for 5 and 12 kinds of protein in serum and erythrocytes, respectively. Each of the protein loci tested showed a monomorphic pattern. Polymorphisms were detected in the analysis of the D-loop-containing region of mtDNA (PCR-RFLP) using 32 restriction endonucleases. Two haplotypes, differing 1.03% in sequence divergence were observed, and both were previously undetected in other local populations. Based on genetic features and differences in pelage color as outlined inFooden's (1995) morphological analysis, the present results suggest that long-tailed macaques on Tabuan Island are a unique population. From the genetic analyses performed here, Tabuan monkeys are considered to be the same species group as those populations of Sumatra and Java (Fooden, 1995).     

Breeding seasonality among long-tailed macaques,Macaca fascicularis,in Peninsular Malaysia

The females among more than 7000 long-tailed macaques, Macaca fascicularis,that had recently been trapped for biomedical research were examined for pregnancy. The animals were taken from the wild in the north of Peninsular Malaysia during the period 1978 to 1979 and in the south from 1978 to 1982. Both samples showed some pregnancies in all months of the year and a peak during the months of May to July. Additional peaks in other months in some years showed that, while the midyear pregnancy peak was significant, it was not as marked a phenomenon as is the breeding peak in many other species. This might be due to the complexity and unpredictability of both the climate and the macaques’ food supply in Peninsular Malaysia. The additional peaks also illustrated the pitfalls of generalizing about breeding seasonality on the basis of small samples.     

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.     

A pilot study of the social correlates of levels of urinary cortisol,prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis)

Urine samples were collected from individuals in a wild population of Sumatran long-tailed macaques (Macaca fascicularis), and the levels of cortisol, immunoreactive prolactin, and (for males) testosterone were determined. The amount of foraging during the 2 hr preceding urine collection were found to affect the levels of urinary cortisol, but not those of the other hormones. Immigration into a new group and having one's infant kidnapped led to increased levels of cortisol. Levels of cortisol and testosterone were correlated both within and between individuals, whereas prolactin varied independently. The effects of age, reproductive status, and social rank on the mean values of individuals were also examined. Lactating females had higher prolactin levels than non-lactating ones; reproductive state interacted with the age effect on prolactin and possibly cortisol. No effects of social status were found in spite of a small, but consistent effect of rank on birth rate in this population. Among males, age and rank are strongly linked. The low ranking old males had increased levels of cortisol, even though the younger high-ranking males were involved in the fiercest conflicts.     

The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis

Demographic changes were recorded throughout a 12-year period for three social groups ofMacaca fascicularis in a natural population at Ketambe (Sumatra, Indonesia). We examined the prediction that females' lifetime reproductive success depended on dominance rank and group size. Average birth rate was 0.53 (184 infants born during 349 female years). For mature females (aged 8–20 yr) birth rate reflected physical condition, being higher in years with high food availability and lower in the year following the production of a surviving infant. High-ranking females were significantly more likely than low-ranking ones to give birth again when they did have a surviving offspring born the year before (0.50 vs 0.26), especially in years with relatively low food availability (0.37 vs 0.10). Controlled comparisons of groups at different sizes indicate a decline in birth rate with rroup size only once a group has exceeded a certain size. The dominance effect on birth rate tended to be strongest in large groups. Survival of infants was rank-dependent, but the survival of juveniles was not. There was a trend for offspring survival to be lower in large groups than in mid-sized or small groups. However, rank and group size interacted, in that rank effects on offspring survival were strongest in large groups. High-ranking females were less likely to die themselves during their top-reproductive years, and thus on average had longer reproductive careers. We estimated female lifetime reproductive success based on calculated age-specific birth rates and survival rates. The effects of rank and group size (contest and scramble) on birth rate, offspring survival, age of first reproduction for daughters, and length of reproductive career, while not each consistently statistically significant, added up to substantial effects on estimated lifetime reproductive success. The group size effects explain why large groups tend to split permanently. Since females are philopatric in this species, and daughters achieve dominance rank positions similar to their mother, a close correlation is suggested between the lifetime reproductive success of mothers and daughters. For sons, too, maternal dominance affected their reproductive success: high-born males were more likely to become top-dominant (in another group). These data support the idea that natural selection has favored the evolution of a nepotistic rank system in this species, even if the annual benefits of dominance are small.     

Determining genetic background in captive stocks of cynomolgus macaques (Macaca fascicularis)

Background As in other model organisms, genetic background in the non‐human primates Macaca mulatta and Macaca fascicularis is an experimental variable that affects the response of other study variables. Genetic background in model organisms is manipulated by breeding schemes but is generally pre‐determined by the source population used to found captive stocks. In M. fascicularis three such sources have been distinguished, however, these are not routinely taken into consideration when designing research. Methods We exemplify a mitochondrial DNA (mtDNA)‐based strategy to trace the maternal geographic origins of M. fascicularis animals of unspecified origins. Results Macaca fascicularis of unspecified origins kept at primate research centers carry mtDNA haplotypes representing all three major genetic subdivisions. Conclusions We suggest that the genetic background of study animals could be better specified in the future using an mtDNA‐based approach, which would enable informed selection of study animals and help reduce variation within and among studies.     

Effects of excess selenomethionine on selenium status indicators in pregnant long-tailed macaques (Macaca fascicularis)

Forty pregnant long-tailed macaques were treated daily for 30 d with 0, 25, 150 or 300 μg selenium as L-selenomethionine/kg body weight. Erythrocyte and plasma selenium and glutathione peroxidase specific activities, hair and fecal selenium, and urinary selenium excretion were increased by and were linearly related to L-selenomethionine dose. Hair selenium was most sensitive to L-selenomethionine dose, with an 84-fold increase in the 300 μg selenium/(kg-d) group relative to controls (r=0.917). Daily urinary selenium excretion (80-fold,r=0.958), plasma selenium (22-fold,r=0.885), erythrocyte selenium (24-fold,r=0.920), and fecal selenium (18-fold,r=0.911) also responded strongly to L-selenomethionine. Erythrocyte and plasma glutathione peroxidase specific activities increased 154% and 69% over controls, respectively. Toxicity was associated with erythrocyte selenium >2.3 μg/mL, plasma selenium >2.8 μg/mL, and hair selenium >27 μg/g. Plasma, erythrocyte, and hair selenium concentrations may be useful for monitoring and preventing the toxicity of L-selenomethionine administered to humans in cancer chemoprevention trials.     

Development of the brain in staged embryos of the long-tailed monkey (Macaca fascicularis)

The external characteristics and successive morphological changes of the brain and its derivatives were studied in 69 long-tailed monkey embryos representing developmental stages 8 through 16. This morphogenesis follows a similar pattern to those of the rhesus, baboon, and human. Minor differences in the temporal sequence of specific developmental events include: 1) otic disc, adenohypophyseal pouch, and hippocampal internal sulcus formation in the long-tailed macaque occur at stage 10, stage 11, and after stage 16 respectively, which is comparable to human stages 9, 10, and 16; 2) formation of the trigeminal primordium and the motor root of the trigeminal nerve and evagination of the neurohypophysis occur at stage 12, stage 14, and stage 15, while in the human embryo these features are observed at stage 14, stage 15, and stage 16, respectively; and 3) closure of the lens pore, like in the rhesus monkey, occurs during stage 15, while in the baboon and human it takes place during stage 14. These temporal differences in the embryonic period are important factors to be taken into consideration in any embryological and teratological studies when usingM. fascicularis as a primate model.     

Testing kin altruism in long-tailed macaques (Macaca fascicularis) in a food-sharing experiment

Social grooming and coalition formation have been main foci in studies concerning altruism in monkeys. Results have been inconclusive because the altruistic nature of these behaviors remains unclear. I investigated altruism in a more transparent context via an apparatus in which captive long-tailed macaque females had the choice to exploit a food source themselves or to yield the food to a test partner. I hypothesized that if potential donors behaved altruistically toward kin, they would yield the food sources longer to kin than to nonkin. Of 11 tested potential donors, 8 did not discriminate between daughters or sisters and nonkin. Thus, the experiments do not support the kin altruism hypothesis. Three females let their youngest offspring have more food than matched juvenile nonrelatives. Behavioral observations strongly suggested,however, that it was primarily spiteful behavior toward juvenile nonrelatives that caused the differences between kin and nonkin in these three cases.     

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.     

Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques

An 835 base pair (bp) fragment of mitochondrial DNA (mtDNA) was sequenced to characterize genetic variation within and among 1,053 samples comprising five regional populations each of longtail macaques (Macaca fascicularis) and rhesus macaques (Macaca mulatta), and one sample each of Japanese (M. fuscata) and Taiwanese (M. cyclopis) macaques. The mtDNA haplotypes of longtail macaques clustered in two large highly structured clades (Fas1 and Fas2) of a neighbor-joining tree that were reciprocally monophyletic with respect to those representing rhesus macaques, Japanese macaques, and Taiwanese macaques. Both clades exhibited haplotypes of Indonesian and Malaysian longtail macaques widely dispersed throughout them; however, longtail macaques from Indochina, Philippines, and Mauritius each clustered in a separate well-defined clade together with one or a few Malaysian and/or Indonesian longtail macaques, suggesting origins on the Sunda shelf. Longtail macaques from Malaysia and Indonesia were far more genetically diverse, and those from Mauritius were far less diverse than any other population studied. Nucleotide diversity between mtDNA sequences of longtail macaques from different geographic regions is, in some cases, greater than that between Indian and Chinese rhesus macaques. Approximately equal amounts of genetic diversity are due to differences among animals in the same regional population, different regional populations, and different species. A greater proportion of genetic variance was explained by interspecies differences when Japanese and Taiwanese macaques were regarded as regional populations of rhesus macaques than when they were treated as separate species. Rhesus macaques from China were more closely related to both Taiwanese and Japanese macaques than to their own conspecifics from India.     

Perception of stimuli presented as photographic slides in cynomolgus macaques (Macaca fascicularis)

The present study was designed to assess a monkey's perception of specific visual stimuli by measuring both the behavioral responses and duration of attention to the presentation of photographic slides. Five adult male cynomolgus macaques (Macaca fascicularis) were placed individually in an open field apparatus and presented a series of slides consisting of apples, a gorilla mask, a collage of colors, a human being, and a plain field. The slide of the gorilla mask followed by that of the human being received the most attention while the plain field received the least. In addition, the gorilla mask and human being elicited a range of behavioral responses with the higher ranking animals displaying a greater number of aggressive responses and the lower ranking animals displaying a greater number of submissive gestures. Taken together, these data would suggest that the slides of the gorilla mask and the human being were perceived by the monkeys as threatening. These results are consistent with a continuing theme observed among a number of studies of primate social perception — namely, that potentially threatening stimuli are a significant determinant of visual observing.     

Feeding ecology of the long-tailed macaque(Macaca fascicularis) in Kalimantan Tengah,Indonesia

I studied long- tailed macaque (Macaca fascicularis)feeding behavior and ecology as part of a larger behavioral ecological study at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. I collected data on feeding behavior via scan sampling of all visible individuals in the focal group (approximately 800 observation hours). I established vegetational plots and monitored them monthly to determine food availability and abundance. I found long- tailed macaques to be primarily frugivorous;leaves, flowers, insects and bark provided the remainder of the diet. They used at least 33 plant species as food sources, but >60% of the diet was provided by only 5 species. Based on previous vegetational analyses, these tree species were among the highest in relative density. However, selection ratios for 19 food species indicate that 13 of them were selected more often than expected. Long- tailed macaques appear to be selective feeders but can exploit a variety of food sources during periods of food scarcity.     

A case of simple tool use in wild liontailed macaques (Macaca silenus)

Three members of a group of liontailed macaques (Macaca silenus) were seen to use leaves for food preparation. Other examples of prey-selection and hunting behaviour in liontailed macaques reflect individual- and group-specific skills. The absence of similar patterns in bonnet macaques (Macaca radiata) living in the same habitat might be related to differences in the social design and indicate the high significance of social aspects for the occurrence and manifestation of innovative behaviour.     

Responses to urinary stimuli in pigtailed (Macaca nemestrina) and stumptailed (Macaca arctoides) macaques

Responses to different urine samples were studied in pigtailed (M. nemestrina) and stumptailed (M. arctoides) macaques. Both species exhibited more interest towards urine samples from their own species than neutral stimuli. Responses towards urine samples from other macaque species did not significantly differ from those towards neutral stimuli. In stumptailed macaques, no differential interest was observed between urine samples from a known (the adult male of the group) and an unknown adult male conspecific.     

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.     

Presence of antibody to Cyno-EBV in domestically bred cynomolgus monkeys (Macaca fascicularis).

The presence of an antibody to the Cyno-EBV was studied with Cyno-EBV bearing cell line (Ts-B-9) as antigen in 186 domestically bred cynomolgus monkeys (Macaca fascicularis) ranging in age from birth to 18 yr as well as in 20 adult (older than 10 yr) cynomolgus monkeys of wild origin. The maternal antibody to Cyno-EBV persisted for less than four mo after birth in infant monkeys. After one yr of age, all the domestically bred monkeys were consistently positive for Cyno-EBV. In the monkeys of wild origin also, the anti-Cyno-EBV antibody was detected without exception. Antibody titers in adult monkeys varied from 1:80 to 1:640.     

Disproportionate participation by age/sex classes in aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal monkey forest, Bali, Indonesia

We observed 420 aggressive interactions between tourists and Macaca fascicularis at the Padangtegal Wanara Wana Temple forest site in Bali, Indonesia, during the months of June and July 2001. The data collected included patterns of aggression, presence or absence of food, and demographic information on resident macaques and human visitors. Analyses of the interactions suggest that macaques respond differentially to humans according to the age/sex classes involved. Additionally, adult and subadult male macaques participated in more aggressive behaviors than expected, while adult female macaques and immatures participated in such behaviors less than expected. These variations in interaction patterns between macaques and tourists may have substantial implications for management issues and the potential for pathogen transmission.