Wild Long-tailed Macaques Research Articles

The prevalence of simian malaria in wild long-tailed macaques throughout Peninsular Malaysia

The parasite Plasmodium knowlesi has been the sole cause of malaria in Malaysia from 2018 to 2022. The persistence of this zoonotic species has hampered Malaysia’s progress towards achieving the malaria-free status awarded by the World Health Organisation (WHO). Due to the zoonotic nature of P. knowlesi infections, it is important to study the prevalence of the parasite in the macaque host, the long-tailed macaque (Macaca fascicularis). Apart from P. knowlesi, the long-tailed macaque is also able to harbour Plasmodium cynomolgi, Plasmodium inui, Plasmodium caotneyi and Plasmodium fieldi. Here we report the prevalence of the 5 simian malaria parasites in the wild long-tailed macaque population in 12 out of the 13 states in Peninsular Malaysia using a nested PCR approach targeting the 18s ribosomal RNA (18s rRNA) gene. It was found that all five Plasmodium species were widely distributed throughout Peninsular Malaysia except for states with major cities such as Kuala Lumpur and Putrajaya. Of note, Pahang reported a malaria prevalence of 100% in the long-tailed macaque population, identifying it as a potential hotspot for zoonotic transmission. Overall, this study shows the distribution of the 5 simian malaria parasite species throughout Peninsular Malaysia, the data of which could be used to guide future malaria control interventions to target zoonotic malaria.

Leptospira Seroprevalence in Free-Ranging Long-Tailed Macaques (Macaca fascicularis) at Kosumpee Forest Park, Maha Sarakham, Thailand.

Leptospirosis is a zoonotic disease that is ubiquitously distributed and is classified as a re-emerging infectious disease in humans and animals. Many serovars are carried by wildlife; all of them are capable of causing illness in humans. The purpose of this study was to investigate the prevalence of Leptospirosis in wild long-tailed macaques (Macaca fascicularis) at Kosumpee Forest Park, Mahasarakham, Thailand. A cross-sectional study was conducted at the park. Blood samples were collected via saphenous vein from 30 free-ranging long-tailed macaques. All samples were tested by the microscopic agglutination test. The LipL32 gene was used to detect pathogenic Leptospira in blood samples by conventional polymerase chain reaction. Screening of the 30 wild macaques showed an overall Leptospira seroreactivity of 13.33%. Three of 30 macaques reacted against Leptospira serovar Shermani and one macaque was infected with Leptospira serovar Sejroe. None of the macaques presented clinical signs of leptospirosis. None of the blood samples showed the detection of the LipL32 gene. The results indicate that the long-tailed macaques at Kosumpee Forest Park may act as natural reservoirs for Leptospirosis. Further, the results provide evidence-based information indicating that several pathogenic Leptospira serovars are circulating in the wild macaques in the study area.

The Distribution of Intestinal Amoebae in Wild Long-Tailed Macaques (Macaca fascicularis) in Sabang City, Aceh Province, Indonesia

Amoeba that infects primates can also be found in humans and can be zoonotic. This study aims to identify the distribution of intestinal amoeba in the wild Long-Tailed Macaque (LTM) group located at Cot Murong, Kebun Mangga, and Tugu Zero Kilometer Monument (IZKM) in Sabang City, Aceh Province, Indonesia. A total of 177 stool samples from 59 tails from the three LTM groups were examined microscopically. The results of the examination confirmed seven species of intestinal amoeba, three of which belonged to the genus Entamoeba, namely the Entamoeba histolytica/dispar/moshkovskii complex, Entamoeba coli, Entamoeba pölecki, and four other species from different genera, namely Iodamoeba butschlii, Blastocystis sp., Endolimax nana and Dientamoeba fragilis. The prevalence of intestinal amoeba in wild LTM in Sabang City was 57.6% (102/177). Dientamoeba fragilis was only found in the LTM group of Kebun Mangga. Entamoeba coli dominated the highest prevalence in all LTM groups. The LTM group located around Cot Murong and IZKM had a higher concentration of infection with intestinal amoeba than the Kebun Mangga location. The statistical tests showed a significant difference between the proportions of Iodamoeba butschlii, Endolimax nana and Dientamoeba fragilis, both found in the LTM Cot Murong, Kebun Mangga, or IZKM groups. This study is the first to report amoebic infection prevalence in the wild LTM group in Sabang City, Aceh Province. The pathogenic amoeba that cannot be distinguished microscopically from morphologically identical amoebae needs to be identified molecularly to identify variants and their potential as zoonotic agents.
 HIGHLIGHTS
 
 Intestinal amoeba species found in fecal samples of the wild long-tailed macaques group of Sabang City, Aceh Province, Indonesia, can also be found in human stool samples
 As many as three of the seven identified amoeba species, namely Entamoeba histolytica, Dientamoeba fragilis, and Blastocystis sp. is a pathogen that can cause diarrhea and colitis in humans and non-human primates
 The prevalence of amoeba infection in wild macaques in Sabang City is in the high category and tends to increase the incidence of infection in the macaque group, which has more susceptible individuals, namely infants, children, and females
 
 GRAPHICAL ABSTRACT

Prevalence of simian malaria parasites in macaques of Singapore.

Plasmodium knowlesi is a simian malaria parasite currently recognized as the fifth causative agent of human malaria. Recently, naturally acquired P. cynomolgi infection in humans was also detected in Southeast Asia. The main reservoir of both parasites is the long-tailed and pig-tailed macaques, which are indigenous in this region. Due to increased urbanization and changes in land use, there has been greater proximity and interaction between the long-tailed macaques and the general population in Singapore. As such, this study aims to determine the prevalence of simian malaria parasites in local macaques to assess the risk of zoonosis to the general human population. Screening for the presence of malaria parasites was conducted on blood samples from 660 peridomestic macaques collected between Jan 2008 and Mar 2017, and 379 wild macaques collected between Mar 2009 and Mar 2017, using a Pan-Plasmodium-genus specific PCR. Positive samples were then screened using a simian Plasmodium species-specific nested PCR assay to identify the species of parasites (P. knowlesi, P. coatneyi, P. fieldi, P. cynomolgi, and P. inui) present. All the peridomestic macaques sampled were tested negative for malaria, while 80.5% of the 379 wild macaques were infected. All five simian Plasmodium species were detected; P. cynomolgi being the most prevalent (71.5%), followed by P. knowlesi (47.5%), P. inui (42.0%), P. fieldi (32.5%), and P. coatneyi (28.5%). Co-infection with multiple species of Plasmodium parasites was also observed. The study revealed that Singapore’s wild long-tailed macaques are natural hosts of the five simian malaria parasite species, while no malaria was detected in all peridomestic macaques tested. Therefore, the risk of simian malaria transmission to the general human population is concluded to be low. However, this can be better demonstrated with the incrimination of the vectors of simian malaria parasites in Singapore.

Do males bond? A study of male-male relationships in Nicobar long-tailed macaques Macaca fascicularis umbrosus

In primates, males compete for a mate, which is a non-sharable resource. This makes the conditions less conducive for males to have stable relationships. One such special kind of relationship is a bond where the interactions are reciprocated, equitable and differentiated. Bonds in macaque societies are based on the degree of within-group contest competition for mates which is dependent on the synchronization of female fertile phase and reliability of fertility signals. Species of the Fascicularis group, including Nicobar subspecies, show intermediate reliability in the signals with mild peaks, and studies have shown reciprocity but no differentiation. We conducted a study on a group of wild Nicobar long-tailed macaques Macaca fascicularis umbrosus to understand the existing patterns of male-male relationships. We examined whether there is reciprocity in affiliation among the individuals and whether the rate of affiliation is balanced. We also measured the dominance linearity and steepness in the group to understand the monopolizability of females. We used social network analysis to understand whether the relations are differentiated based on hierarchical position and whether the high-ranking individuals are the most central individuals in the distribution of grooming in the group. We found that there is reciprocity among the males although that is not equitable. There was no rankrelated differentiation of affiliation among the males of the group. Instead, the identities of individuals influenced affiliation patterns. Our results correspond to the existent strong relationships but lack of social bond otherwise found in the Fascicularis group of macaques.

Plasmodium knowlesi and other malaria parasites in long-tailed macaques from the Philippines

BackgroundMacaca fascicularis (long-tailed macaque) is the most widespread species of macaque in Southeast Asia and the only species of monkey found naturally in the Philippines. The species is the natural host for the zoonotic malaria species, Plasmodium knowlesi and Plasmodium cynomolgi and for the potentially zoonotic species, Plasmodium inui. Moreover, other Plasmodium species such as Plasmodium coatneyi and Plasmodium fieldi are also natural parasites of M. fascicularis. The aims of this study were to identify and determine the prevalence of Plasmodium species infecting wild and captive long-tailed macaques from the Philippines.MethodsA total of 95 blood samples from long-tailed macaques in the Philippines were collected from three locations; 30 were from captive macaques at the National Wildlife Rescue and Rehabilitation Center (NWRRC) in Luzon, 25 were from captive macaques at the Palawan Wildlife Rescue and Conservation Center (PWRCC) in Palawan and 40 were from wild macaques from Puerto Princesa Subterranean River National Park (PPSRNP) in Palawan. The Plasmodium spp. infecting the macaques were identified using nested PCR assays on DNA extracted from these blood samples.ResultsAll 40 of the wild macaques from PPSRNP in Palawan and 5 of 25 captive macaques from PWRCC in Palawan were Plasmodium-positive; while none of the 30 captive macaques from the NWRRC in Luzon had any malaria parasites. Overall, P. inui was the most prevalent malaria parasite (44.2%), followed by P. fieldi (41.1%), P. cynomolgi (23.2%), P. coatneyi (21.1%), and P. knowlesi (19%). Mixed species infections were also observed in 39 of the 45 Plasmodium-positive macaques. There was a significant difference in the prevalence of P. knowlesi among the troops of wild macaques from PPSRNP.ConclusionWild long-tailed macaques from the island of Palawan, the Philippines are infected with P. knowlesi, P. inui, P. coatneyi, P. fieldi and P. cynomolgi. The prevalence of these Plasmodium spp. varied among the sites of collection and among troops of wild macaques at one site. The presence of these simian Plasmodium parasites, especially P. knowlesi and P. cynomolgi in the long-tailed macaques in Palawan presents risks for zoonotic transmission in the area.

Correlation between genotypes and geographic distribution of Entamoeba nuttalli isolates from wild long-tailed macaques in Central Thailand

Entamoeba nuttalli found in non-human primates is the phylogenetically closest species to Entamoeba histolytica and is potentially pathogenic. However, infection of wild long-tailed macaques (Macaca fascicularis) with E. nuttalli has not been found. In this study, the prevalence of Entamoeba infections in wild long-tailed macaques was examined in seven locations in six provinces of Thailand. The positive rate for E. nuttalli in 214 fecal samples was 43.9% using PCR, but no infection with E. histolytica or Entamoeba dispar was found, demonstrating that long-tailed macaque is one of the natural hosts for E. nuttalli. Twenty-four E. nuttalli isolates were successfully cultured and four of them were axenized. The sequences of the 18S ribosomal RNA genes of E. nuttalli from long-tailed macaques differed from those of E. nuttalli isolates from other species of wild macaques. Eleven types of sequences in serine-rich protein genes were identified in the 24 isolates and these were specific for each location in Thailand. By analysis of six tRNA-linked short tandem repeat loci, these isolates were divided into 14 types, and each type was also location-specific. Phylogenetic analysis revealed correlation between genotypes of the parasite and the geographic distribution of the host macaques. Genetic distance and geographic distance correlated significantly in a Mantel test, with r values of 0.888 based on the tRNA-linked short tandem repeat loci and 0.815 based on the serine-rich protein genes. These results suggest that genetic divergence and co-evolution of the parasite occurred during dispersion and colonization of the host macaque, and that genotypic analysis of the parasite may enable identification of the geographic localization of the host.

Analysis of wild macaque stone tools used to crack oil palm nuts.

The discovery of oil palm (Elaeis guineensis) nut-cracking by wild long-tailed macaques (Macaca fascicularis) is significant for the study of non-human primate and hominin percussive behaviour. Up until now, only West African chimpanzees (Pan troglodytes verus) and modern human populations were known to use stone hammers to crack open this particular hard-shelled palm nut. The addition of non-habituated, wild macaques increases our comparative dataset of primate lithic percussive behaviour focused on this one plant species. Here, we present an initial description of hammerstones used by macaques to crack oil palm nuts, recovered from active nut-cracking locations on Yao Noi Island, Ao Phang Nga National Park, Thailand. We combine a techno-typological approach with microscopic and macroscopic use-wear analysis of percussive damage to characterize the percussive signature of macaque palm oil nut-cracking tools. These artefacts are characterized by a high degree of battering and crushing on most surfaces, which is visible at both macro and microscopic levels. The degree and extent of this damage is a consequence of a dynamic interplay between a number of factors, including anvil morphology and macaque percussive techniques. Beyond the behavioural importance of these artefacts, macaque nut-cracking represents a new target for primate archaeological investigations, and opens new opportunities for comparisons between tool using primate species and with early hominin percussive behaviour, for which nut-cracking has been frequently inferred.

Androgen correlates of male reproductive effort in wild male long-tailed macaques (Macaca fascicularis): A multi-level test of the challenge hypothesis

The challenge hypothesis (Wingfield et al., 1990) has been broadly utilised as a conceptual framework to study male androgen correlates of reproductive challenges in mammals. These studies mainly assessed male androgen responsiveness to a general degree of challenge over extended periods of time. Short term co-variation between the socio-sexual challenging context and androgen levels remains, however, largely understudied. We thus aim at providing a multi-level test of the challenge hypothesis by investigating the inter- and intra-individual variations in faecal androgen excretion associated to 1) breeding seasonality, 2) dominance rank, 3) mate-guarding activity and 4) value of the guarded female. We studied long-tailed macaques, a species in which males engage in highly challenging monopolisation of females over discreet periods of time. This particularity allows testing specifically the predicted increase from level B to level C in the challenge hypothesis. The study was carried out during two reproductive seasons on three groups of wild long-tailed macaques. We combined behavioural observations and non-invasive measurements of faecal androgen metabolite (fAM) levels. We found that, as predicted by the challenge hypothesis, male long-tailed macaques respond not only to seasonal but also to short term reproductive challenges by adapting their androgen levels. First, males exhibited a seasonal rise in fAM levels during the mating period which may be triggered by fruit availability as shown by our phenological data. Second, males had increased androgen levels when mate-guarding females and, across mate-guarding periods, males had higher fAM levels when monopolising high-ranking parous females than when monopolising low-ranking ones. Finally, high-ranking males had higher fAM levels than low-ranking males year round. Our study confirms that, in species with a high degree of female monopolisability, androgen may be an important physiological fitness enhancing tool for males by increasing female monopolisation efficiency (in particular with highly valuable females) and helping males to respond to rank take-over challenges.

Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): Physiological stress and aggression

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the male’s ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities.

Costs of and Investment in Mate-Guarding in Wild Long-Tailed Macaques (Macaca fascicularis): Influences of Female Characteristics and Male-Female Social Bonds.

Male primates living in multimale groups tend to direct mate and mate-guarding choices toward females of high reproductive value, i.e., high-ranking, parous females, or females with which they share strong bonds. Little is known, however, about the constraints that may limit male mate-guarding choices (the costs of this behavior) and the influence of the females’ quality on male investment in mate-guarding. We aimed to study the effects of female rank, parity status, and male–female social bond strength on the costs of and investment in mate-guarding by males. We carried out our study during two reproductive seasons on three groups of wild long-tailed macaques in Indonesia. We combined behavioral observations on male locomotion and activity with noninvasive measurements of fecal glucocorticoids (fGC). Males spent less time feeding when mate-guarding nulliparous females than when mate-guarding parous females and tended to have higher fGC levels when mate-guarding low-ranking nulliparous females than when mate-guarding high-ranking nulliparous ones. Evolution should thus favor male choice for high-ranking parous females because such a decision brings benefits at proximate (reduced costs of mate-guarding) and ultimate (higher reproductive value) levels. Further, male investment in mate-guarding was flexible and contingent on female reproductive and social value. Males were more vigilant and more aggressive toward other males when mate-guarding females to which they were strongly bonded and/or high-ranking ones than when mate-guarding other females. Our findings bring a new dimension to the study of mate choice by showing that males not only mate preferentially with high-quality females but may also aim to secure paternity with these females through optimized monopolization.

Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.

Microsatellite DNA polymorphisms for colony management of longtailed macaques (Macaca fascicularis) population on the Tinjil Island

Perwitasari-Farajallah D, Kyes RC, Iskandar E (2010) Microsatellite DNA polymorphisms for colony management of long-tailed macaques (Macaca fascicularis) population on the Tinjil Island. Biodiversitas 11: 55-58. Polymorphic genetic markers are the basic requirement for studies on population and conservation genetics of non-human primates. In this paper, we screened microsatellites for their polymorphism and gene typing of DNA samples from blood of wild long-tailed macaques (Macaca fascicularis) from Tinjil Island population. Among the three primer sets tested, two are polymorphic. They were D1S548 and D3S1768. Average observed heterozygosity (Ĥ) within populations ranged between 0.264-0.555. D1S1768 locus was highly polymorphic and 24 alleles were detected among two loci. Estimation of genetic variability for the Tinjil population (Ĥ) was 0.485. The results obtained provide furtherinsight into the long-term viability of the population and help in creating genetic management of both captive and natural habitat breeding colonies of primates.Key words: microsatellite, variations, social groups, long-tailed macaques, Macaca fascicularis

Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques ( Macaca fascicularis)

Whereas it is well known that in strictly seasonal breeding primates (income breeders), alike other vertebrates, males show pronounced changes in testicular and adrenal hormone levels concurrent with reproductive activity, hormonal patterns in males of non-strictly seasonal breeding primate species (capital breeders) and their relation to seasonal and social correlates remain largely unknown. In the present study, we examined the annual pattern of fecal androgen and glucocorticoid excretion and their relationship to environmental (rainfall, temperature) and social factors (number of cycling females, male aggression and copulation rates, male dominance rank) in a group of wild long-tailed macaques ( Macaca fascicularis), a species with a moderate degree of reproductive seasonality and classified as capital breeder. The study was carried out in the Gunung Leuser National Park, North Sumatra, Indonesia over a period of ten months encompassing the conception and the birth season. Our results show that male long-tailed macaques exhibit a distinct annual variation in both androgen and glucocorticoid levels. Androgen (but not glucocorticoid) levels were significantly elevated during the conception period in association with elevated rates of male–male aggression and copulatory activity, both strongly related to the number of cycling females in the group. Neither glucocorticoid nor androgen levels were related to male dominance rank or to the environmental parameters investigated. Interestingly, levels of both hormones started to increase in the late birth season and thus 1–2 months prior to the mating season, suggesting that male long-tailed macaques go through pre-breeding hormonal changes in preparation for prospective challenges. Our data thus provide the first evidence that males of a non-strictly seasonal breeding species/capital breeder show endocrine patterns generally similar to those found in strictly seasonal/income breeders.

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.

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.

Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques ( Macaca fascicularis)

The extent to which catharrine primate males are able to discern the fertile phase during the female ovarian cycle under natural conditions is still debated. In a recent study, we showed that wild male long-tailed macaques are able to detect the fertile phase, but the cues males used to assess female reproductive status remained unclear. In the present study, we tested female sex skin swelling and specific female behaviors for their reliability in signaling the fertile phase, as determined by measurement of fecal estrogens (E) and progestogens (P) during nine ovulatory cycles in seven free-ranging females. We found that changes in sex skin swellings showed a significant positive correlation to the E/P ratio, but swelling size did not significantly differ between cycle phases. In contrast, the frequency of two of the tested female behaviors, namely initiation of sexual interactions and reaching back for the male during copulation, was not only correlated with female reproductive hormones, but was significantly elevated during the fertile phase compared to nonfertile phases of the cycle. We thus conclude that female sex skin swelling does not reliably indicate the timing of the fertile phase in long-tailed macaques, whereas certain female behaviors do. Since cycles differed considerably in the number of males with which females had sexual interactions as well as in the number of sexual interactions with dominant males, the signaling character of these specific female behaviors appears to be robust against inconsistencies in these social variables. Female behavior might therefore play an important role in the recognition of the fertile phase by male macaques under natural conditions.

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.

Evolution and ecology of macaque societies

Preface J. E. Fa and D. G. Lindburg Part I. Biogeography and Evolution: 1. Evolutionary relationships of the Macaques G. A. Hoelzer and D. J. Melnick 2. Genetic relatedness between populations of Macaca fascicularis on Sumatra W. Scheffrahn and J. R. de Ruiter 3. Secondary intergradation between Macaca maurus and M. tonkeana, and the species status of M. togeanus J.W. Froelich and J. Supriatna Part II. Population Biology, Ecology and Conservation: 4. A comparison of ecological strategies of Pig-tailed Macaques, Mandrills and Drills J. O. Caldecott, A. Feistner and L. Gadsby 5. A comparison of Rhesus Macaques in temperate and tropical environments J. O. Caldecott, A. Feistner and L. Gadsby 6. Demography and dynamics of Barbary Macaque troops in different habitats N. Menard and D. Vallet 7. Grouping patterns and group composition in Macaca nigrescens A. Kohlhaas and C. H. Southwick 8. Socioecological dynamics of Japanese Macaque troop ranging T. Maruhashi, Y. Takahata and H. Takasaki 9. Riverine refuging by wild Sumatran Long-tailed Macaques (Macaca fascicularis) C. P.van Shaik, A. van Amerongen and M. van Noordwijk 10. Comparison of provisioned and wild Long-tailed Macaques B. Wheatley, M. Gonder and D. K. Harya Putra 11. Inter-regional and inter-seasonal variations of food quality in Japanese Macaques N. Nakagawa, T. Iwamoto, N. Yokota and G. Soumah 12. Population management and viability of the Gibraltar Barbary Macaques J. E. Fa and R. Lind 13. Eco-ethology of Tibetan Macaques at Mt. Emei, China Q. Zhao Part III. Mating and Social Systems: 14. Differential reproduction in male and female Barbary Macaques A. Paul and J. Kuester 15. Reproductive behaviour of captive Lion-tailed Macaques D. J. Lindburg 16. Sexual behaviour and mating system in wild Pig-tailed Macaques in West Sumatra T. Oi 17. Determinants of reproductive seasonality in Japanese Macaques L. Fedigan and L. Griffin 18. Behaviour of mixed species groups of macaques F. D. Burton and L. Chan 19. The population genetic consequences of Macaque social organisation and behaviour D. J. Melnick and G. A. Hoelzer 20. Variation in social mechanisms by which males attain the alpha rank among Japanese Macaques D. S. Sprague, S. Suzuki and T. Tsukahara 21. Life history of females in a wild population of Yaku Macaques D. A. Hill and N. Okaysu 22. Twenty year social history of a dominant Stumptail Macaque matriline R. Rhine and A. Maryanski 23. Branch shaking and related displays in wild Barbary Macaques P. T. Mehlman 24. The interplay of kinship organisation and facial communication in the Macaques A. Zeller 25. Vocal communication in Macaques M. D. Hauser.

Evolution and Ecology of Macaque Societies

Preface J. E. Fa and D. G. Lindburg Part I. Biogeography and Evolution: 1. Evolutionary relationships of the Macaques G. A. Hoelzer and D. J. Melnick 2. Genetic relatedness between populations of Macaca fascicularis on Sumatra W. Scheffrahn and J. R. de Ruiter 3. Secondary intergradation between Macaca maurus and M. tonkeana, and the species status of M. togeanus J.W. Froelich and J. Supriatna Part II. Population Biology, Ecology and Conservation: 4. A comparison of ecological strategies of Pig-tailed Macaques, Mandrills and Drills J. O. Caldecott, A. Feistner and L. Gadsby 5. A comparison of Rhesus Macaques in temperate and tropical environments J. O. Caldecott, A. Feistner and L. Gadsby 6. Demography and dynamics of Barbary Macaque troops in different habitats N. Menard and D. Vallet 7. Grouping patterns and group composition in Macaca nigrescens A. Kohlhaas and C. H. Southwick 8. Socioecological dynamics of Japanese Macaque troop ranging T. Maruhashi, Y. Takahata and H. Takasaki 9. Riverine refuging by wild Sumatran Long-tailed Macaques (Macaca fascicularis) C. P.van Shaik, A. van Amerongen and M. van Noordwijk 10. Comparison of provisioned and wild Long-tailed Macaques B. Wheatley, M. Gonder and D. K. Harya Putra 11. Inter-regional and inter-seasonal variations of food quality in Japanese Macaques N. Nakagawa, T. Iwamoto, N. Yokota and G. Soumah 12. Population management and viability of the Gibraltar Barbary Macaques J. E. Fa and R. Lind 13. Eco-ethology of Tibetan Macaques at Mt. Emei, China Q. Zhao Part III. Mating and Social Systems: 14. Differential reproduction in male and female Barbary Macaques A. Paul and J. Kuester 15. Reproductive behaviour of captive Lion-tailed Macaques D. J. Lindburg 16. Sexual behaviour and mating system in wild Pig-tailed Macaques in West Sumatra T. Oi 17. Determinants of reproductive seasonality in Japanese Macaques L. Fedigan and L. Griffin 18. Behaviour of mixed species groups of macaques F. D. Burton and L. Chan 19. The population genetic consequences of Macaque social organisation and behaviour D. J. Melnick and G. A. Hoelzer 20. Variation in social mechanisms by which males attain the alpha rank among Japanese Macaques D. S. Sprague, S. Suzuki and T. Tsukahara 21. Life history of females in a wild population of Yaku Macaques D. A. Hill and N. Okaysu 22. Twenty year social history of a dominant Stumptail Macaque matriline R. Rhine and A. Maryanski 23. Branch shaking and related displays in wild Barbary Macaques P. T. Mehlman 24. The interplay of kinship organisation and facial communication in the Macaques A. Zeller 25. Vocal communication in Macaques M. D. Hauser.