Macaca Silenus Research Articles

Occurrence and distribution of Indian primates

Global and regional species conservation efforts are hindered by poor distribution data and range maps. Many Indian primates face extinction, but assessments of population status are hindered by lack of reliable distribution data. We estimated the current occurrence and distribution of 15 Indian primates by applying occupancy models to field data from a country-wide survey of local experts. We modeled species occurrence in relation to ecological and social covariates (protected areas, landscape characteristics, and human influences), which we believe are critical to determining species occurrence in India. We found evidence that protected areas positively influence occurrence of seven species and for some species are their only refuge. We found evergreen forests to be more critical for some primates along with temperate and deciduous forests. Elevation negatively influenced occurrence of three species. Lower human population density was positively associated with occurrence of five species, and higher cultural tolerance was positively associated with occurrence of three species. We find that 11 primates occupy less than 15% of the total land area of India. Vulnerable primates with restricted ranges are Golden langur, Arunachal macaque, Pig-tailed macaque, stump-tailed macaque, Phayre’s leaf monkey, Nilgiri langur and Lion-tailed macaque. Only Hanuman langur and rhesus macaque are widely distributed. We find occupancy modeling to be useful in determining species ranges, and in agreement with current species ranking and IUCN status. In landscapes where monitoring efforts require optimizing cost, effort and time, we used ecological and social covariates to reliably estimate species occurrence and focus species conservation efforts.

Decline of the Endangered lion-tailed macaque Macaca silenus in the Western Ghats, India

The Endangered lion-tailed macaque Macaca silenus is endemic to rainforest patches of the Western Ghats mountains in south-western India. Most populations of this primate are severely fragmented and declining and the species is locally extinct in some areas. This study evaluates the status of this macaque in the Talakaveri, Pushpagiri and Sharavathi Valley Wildlife Sanctuaries and adjacent areas in the state of Karnataka. We sighted four, two and three groups, consisting of five, nine and 14 individuals, in these three sanctuaries, respectively. The recently discovered population in the Sirsi-Honnavara area of Karnataka state is possibly the only viable population, with .750 individuals, but is confined to unprotected reserve forests with extensive human habitation, agricultural land and livestock reserves. We make recommendations for the long-term conservation of the species, and for the Sirsi-Honnavara population in particular.

The Lion-tailed Macaque Macaca silenus (Primates: Cercopithecidae): conservation history and status of a flagship species of the tropical rainforests of the Western Ghats, India

The lion-tailed Macaque (Macaca silenus) is a threatened species inhabiting the rainforests of the Western Ghats mountain range in southern India. Once assessed to be less than a thousand individuals remaining in the wild habitats, the population is now estimated to be between 3000 and 3500 individuals. However, the rainforest habitats of the species are highly fragmented. During the past three decades or less, the population of this species has severely declined due to habitat degradation and illegal hunting in several areas of its occurrence. In situ conservation programs included notification of certain areas as Lion-tailed Macaque conservation regions. Several captive breeding programs have been initiated in order to have a viable captive population of the species. However, the analysis reveals that both in situ and ex situ conservation programs have not achieved the desired success and the species is even more endangered than it was a few decades ago. In this article, we discuss these conservation programs and suggest further measures for effective conservation of lion-tailed Macaques.

The Lion-tailed Macaque Macaca silenus (Primates: Cercopithecidae): conservation history and status of a flagship species of the tropical rainforests of the Western Ghats, India

The Lion-tailed Macaque Macaca silenus (Primates: Cercopithecidae): conservation history and status of a flagship species of the tropical rainforests of the Western Ghats, India

Glycan stem-cell markers are specifically expressed by spermatogonia in the adult non-human primate testis

The glycan cell surface molecules, stage-specific embryonic antigen (SSEA)-1, -3 and -4 and tumor-rejection antigen (TRA)-1-60 and -1-81, are expressed in specific combinations by undifferentiated pluripotent cells, i.e. embryonic stem cells, induced pluripotent stem cells, embryonal carcinoma cells, primordial germ cells and embryonic germ cells. Upon differentiation of the cells, these markers vanish. Recently, it has been shown that also neonatal and adult mouse testes contain pluripotent cells. Here, we aimed at identifying in situ possibly pluripotent cells in the adult primate testis. Monoclonal antibodies raised against the glyco-epitopes SSEA-1, -3 and -4 and TRA-1-60 and -1-81, respectively, were tested to detect cells expressing the antigens, by immunohistochemistry on Bouin's-fixed and paraffin-embedded adult primate testes. Man, the new-world monkey, Callithrix jacchus (common marmoset), and the old-world monkey species, Macaca mulatta (Rhesus macaque) and Macaca silenus (Lion-tailed macaque), were included. The percentage of SSEA-4-positive cells in three adult marmoset testes was determined using flow cytometry. Spermatogonia in the testes of C. jacchus were labeled by SSEA-4, TRA-1-60 and -1-81-antibodies. In the macaques, spermatogonia were detected by SSEA-4 and TRA-1-81-antibodies. TRA-1-61 did not bind to macaque spermatogonia. Also, SSEA-1 and -3 did not bind to spermatogonia in any species. In human testes, we never obtained any clear staining. The total percentage of SSEA-4-positive cells in marmoset testes was 8.6 +/- 1.61%. SSEA-4 and TRA-1-81-antibodies may be very well suited for the identification and isolation of spermatogonia, and possibly also germline stem cells, in the non-human primate testis.

Thoracolumbar Hemilaminectomy and Spinal Cord Decompression in a Lion-tailed Macaque (Macaca silenus)

A 16-yr-old, castrated male lion-tailed macaque (Macaca silenus) presented with acute bilateral pelvic limb paralysis. Cisternal and lumbar myelograms demonstrated right-sided spinal cord compression at T13-L1. During an extradural hemilaminectomy, chronically ruptured disk material was removed at T13-L1, with moderate venous dilatation observed cranially. The macaque fully recovered from clinical signs within 2 mo.

Status of Macaca silenus in the Kudremukh Forest Complex, Karnataka, India

We assessed the population status of endangered lion-tailed macaques (Macaca silenus) in the rain forests of Kudremukh Forest complex (Kudremukh National Park, Someshwara Wildlife Sanctuary and Mookambika Wildlife Sanctuary), Western Ghats, Karnataka in January 2007. We performed a census of 20 groups in Kudremukh NP, 4 groups in Someshwara WS, and 6 groups in Mookambika WS. We estimated the population size as ca. 451 individuals in the 3 parks. The forests of Kudremukh NP and Someshwara WS are continuous, and the present finding of 24 groups in a single continuous forest confirms the existence of another significant population of lion-tailed macaques.

Variation of the melanocortin 1 receptor gene in the macaques

Melanocortin 1 receptor (MC1R), a G-coupled seven-transmembrane receptor protein, plays a key role in the regulation of melanin synthesis in mammals. Sequence variation of the MC1R gene (MC1R) has been associated with pigmentation phenotypes in humans and in several animal species. The macaques (genus Macaca) are known to show a marked inter-specific variation in coat color although the causative genetic variation remains unclear. We investigated nucleotide sequences of the MC1R in 67 individuals of 18 macaque species with different coat color phenotypes including black and agouti. Twenty-eight amino acid replacements were identified in the macaques, but none of these amino acid replacements could explain the black coat color of Macaca silenus and the Sulawesi macaque species. Our molecular evolutionary analysis has revealed that nonsynonymous substitution/synonymous substitution (dN/dS) ratio of the MC1R has not been uniform in the macaque groups and, moreover, their coat color and dN/dS ratio were not related. These results suggest that the MC1R is unlikely to be responsible for the coat color variation of the macaques and functions of MC1R other than pigmentation might be associated with the different selective pressures on the MC1R in macaques.

The captive audience: the educative influence of zoos on their visitors in India

A questionnaire survey was conducted to assess the educative influence of zoo visits on their visitors at three Indian zoos. Although 300 questionnaires were completed at each site, 150 questionnaires each for ‘zoo visitors’ and the ‘general public’, only 863 (96%) were used in the analysis because the others were incomplete. A significantly higher number of ‘zoo visitors’ (n=111/150, 74%) were found to be aware of the appearance and biology of the Lion‐tailed macaque Macaca silenus in comparison with the ‘general public’ (n=67/150, 45%) at Thiruvananthapuram Zoo (TZ). When asked about the goals of a zoo, a relatively greater percentage of the ‘zoo visitors’ at Arignar Anna Zoological Park (20%) and TZ (29%) stated that the goal of the zoo was to protect endangered species, while 69% of the ‘zoo visitors’ at Shri Chamarajendra Zoological Garden said they did not know. As high as 64% of the ‘zoo visitors’ across the three zoos said that a zoo could definitely help protect wild animals. Overall, the ‘zoo visitors’ correctly answered a greater number of questions on the biology, behaviour and habitat of Lion‐tailed macaques in comparison with the ‘general public’. Our study suggests that zoos are an excellent learning environment to convey the ‘conservation and education’ messages but currently they are an underutilized resource. Zoos could initiate the process of educating their public by providing them with ‘pocket’ guides and brochures on wildlife at the entrance and also by conducting 15 minute‐long talks at the animal exhibits about crucial conservation and wildlife issues.

Echinococcus multilocularis Infection of Several Old World Monkey Species in a Breeding Enclosure

Echinococcus multilocularis, the causative agent of alveolar echinococcosis, is spreading geographically in Europe, and prevalence rates in foxes, the final host, are increasing. Concomitantly, the rate of newly diagnosed human infections has already doubled in Germany. We report a cluster of alveolar echinococcosis in 24 animals of different Old World monkey species (15 cynomolgus monkeys, 5 rhesus monkeys, and 4 lion-tailed macaques) in northern Germany. The cluster described is the largest ever recorded in a single center. Cynomolgus monkeys were very susceptible and constituted the monkey species at highest risk, indicating that this species could act as a sentinel animal for the transmission of alveolar echinococcosis in zoological gardens or similar institutions.

A world survey of husbandry practices for Lion‐tailed macaques Macaca silenus in captivity

A questionnaire survey was conducted to compare husbandry and management protocols for Lion‐tailed macaques Macaca silenus in 42 zoos in various parts of the world. A relatively higher number of zoos outside India compared with those in India reported foraging behaviour in their individuals, whereas abnormal behaviour was rare. The reproductive success of macaques in these zoos was also significantly higher than that in Indian zoos. The results of this study suggest that group composition, enclosure design, dietary preparation and nutrition, as well as visitor–animal interaction influence the welfare and breeding success of Lion‐tailed macaques in Indian zoos. Also, poor management is a problem in the Indian‐zoo scenario. Hence, we emphasize the need for good zoo management through proper record‐keeping, regularized behaviour monitoring and administration of environmental enrichment, and a well‐established marking/tagging method to identify individual animals.

A note on enrichment for captive lion-tailed macaques (Macaca silenus)

Two enrichment techniques were devised with the aim of reducing stress and improving welfare for captive lion-tailed macaques in an Indian zoo. In Study A, a log, cotton ropes and a feeding basket were added to the enclosures in different combinations to provide structural and feeding enrichment and were subsequently removed, while in Study B, singly-housed individuals were transferred to a large open-moated enclosure in which they were group-housed. The effects of these two enrichment techniques (social and physical) appeared to significantly improve the welfare of the study individuals by stimulating them to exhibit higher levels of natural behaviours along with the suppression of several abnormal behaviours.

Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group

The 12 presently recognized taxa forming the Macaca silenus group represent the most diverse lineage within the genus Macaca. The present study was set up to clarify the phylogenetic relationships of the extant members of the M. silenus group and to explain their geographical distribution patterns seen today. A combined approach involving the analysis of one paternal (TSPY) and two maternal (cyt b and 12S–16S rRNA) molecular markers enabled us to resolve the phylogenetic relationships within this lineage. Our Y chromosomal marker is not informative enough to allow detailed conclusion. Based on our mitochondrial data, however, M. pagensis, endemic to the three southern Mentawai islands (Sipora, North- and South Pagai), split off early (2.4–2.6 mya) and represents a sister clade to the macaques from the northern Mentawai island of Siberut and from those of the Southeast Asian mainland, which diverged in a radiation-like splitting event about 1.5–1.7 mya. By combining our new results with available data on behavioural as well as climate and sea level changes in Southeast Asia during the Plio- and Pleistocene, we have developed two scenarios for the evolutionary history of this primate group, which may help explain the current geographical distribution of its members.

Birth Patterns in Wild and Captive Lion-Tailed Macaques (Macaca silenus)

During a 5-yr study of lion-tailed macaques in their natural habitat, we found that: 1) most births occurred from January to April (70%) and from September to December (19%), showing a bimodal pattern with a major and a minor birth peak; 2) the period of peaks remained the same over 5 yr; and 3) a similar pattern of birth peaks occurred both in groups in large forest complexes that had overlapping home ranges with other groups and in single groups that were isolated in forest fragments in the same region but with similar ecological conditions. The results suggest more of a birth seasonality than mere breeding synchronization in the wild lion-tailed macaques. We also analyzed data on births in captivity in European Zoos for 10 yr. We observed no seasonality or peaks in births, and the pattern was the same over the years. Data on rainfall suggest that resource availability in the wild habitat may not be uniform throughout the year; hence, ecological factors may play an important role in determination of birth patterns in the natural habitats of lion-tailed macaques.

Dominance hierarchy and social grooming in female lion- tailed macaques (Macaca silenus) in the Western Ghats, India

This article reports the structure of dominance and its relationship with social grooming in wild lion-tailed macaque females. The strength of dominance hierarchy was 0.79 on a scale of 0 to 1 indicating a moderate linearity in the ranking system. Dominance scores were converted into an ordinal as well as an interval scale. Grooming scores were also converted into interval scales using standard scores. Grooming received and grooming given correlated positively and negatively respectively with dominance ranks indicating that high ranking females received more and gave less grooming. Grooming was also positively related to encounter rates for dyads of females. More grooming among adjacent ranks, and grooming being more reciprocal, occurred only in the case of dominant females. The grooming patterns, therefore, appeared to be more of despotic than egalitarian nature. While ranking macaques into different Grades of social systems ranging from despotic to egalitarian, Thierry (2004) has placed lion-tailed macaques in Grade 3 corresponding to the 'relaxed' social system. Our results indicate that the grooming and dominance relationships in this species are more despotic, and hence, the Grade for this species requires to be shifted toward 2 or 1.

Population Dynamics of a Group of Lion-Tailed Macaques (Macaca silenus) Inhabiting a Rainforest Fragment in the Western Ghats, India

We observed the overall population dynamics and number of births and deaths in identified individuals between January 2002 and October 2005, in a large group of lion-tailed macaques in the Anaimalai Hills of the Western Ghats in the south Indian state of Tamilnadu. The group inhabited an isolated rainforest fragment located inside a private tea/coffee garden. The group size increased from 56 in January 2002 to 84 in October 2005. All females reproduced, and the interbirth interval was 23.18 months. Of the 37 infants born between 2002 and 2005, only 1 died providing an infant survivorship rate of about 97.3%. Although births occurred in all months, most of the infants were born between February and March, and this pattern of births was consistent over the years, indicating a major birth peak in this species. The population growth rate in this unusually large group was found to be higher than even in those groups of lion-tailed macaques that inhabit large and relatively undisturbed rainforest complexes. This high growth rate could be attributed to the availability of abundant cultivated fruit plants including commercial crops such as coffee seeds. The observations provide a perspective for the management of other groups of this endangered species inhabiting rainforest fragments.

Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India

Resource partitioning in a community of diurnal arboreal mammals consisting of the lion-tailed macaque Macaca silenus, bonnet macaque (BM) Macaca radiata, Nilgiri langur Semnopithecus johnii, and the Indian giant squirrel Ratufa indica of the Western Ghats, southern India, was studied. Differences in their diet, vertical stratification, food resource niche breadth, niche overlap, and behavioral interactions were examined. Resource partitioning was through differential habitat use, resource use, and vertical stratification. Of the four species, the BM was not a resident species and made frequent forays into evergreen forest from the adjacent deciduous forest during the flowering season of Cullenia exarillata and fruiting season of Ficus microcarpa. The macaques had narrower niches, and the langur and the squirrel had wider niches. Niche overlap was highest between the two macaques. Overlap among the study species was particularly pronounced during the flowering of C. exarillata. There was significant correlation between niche overlap and intolerance among the study species. Certain species pairs showed little or no mutual intolerance despite high overlap. Cooperative interactions such as alarm calls occurred more frequently among the resident species. Interaction matrices revealed an underlying pattern of interspecific dominance hierarchy, with the BM dominating over the other three species. Our study suggests that the BM do not coexist with the other three because of high overlap with its congener and low occurrence of cooperative interactions.

Preliminary observations on the differences in reproductive behaviour between breeding and non-breeding captive lion-tailed macaques ( Macaca silenus) housed in Indian zoos

Rearing history and levels of abnormal behaviour exhibited by lion-tailed macaques housed in Indian zoos was found to influence their ability to breed. Proven breeders were born in zoos while the non-breeding individuals were confiscated from private owners. Proven breeders also exhibited significantly lower percentages of abnormal behaviour and higher levels of social interactions and autogrooming when compared to the non-breeding macaques. These differences may have been due to non-breeders being housed in isolation and in contact of humans. This could have had an influence on the development of reproductive and social behaviours during the early stages in their lives.

Use of Enclosure Space by Captive Lion-Tailed Macaques (Macaca silenus) Housed in Indian Zoos

Captive nonhuman animals use enclosure space differentially. Enclosure features strongly influence this. This study recorded both the enclosure space used by 47 captive lion-tailed macaques housed in 13 zoos across India and the behavior of the macaques. The exhibition of abnormal behaviors, food-related behaviors, and social interactions correlated significantly with the use of the edge zone (the part of the enclosure closest to the visitor area). Animals housed in barren enclosures used the edge zone to a significantly greater percentage than did those housed in complex exhibits. Percentages of autogrooming, social interactions, and food-related behaviors significantly correlated with the use of the enrich zone. Space use studies assist in recognizing areas within the enclosure, which captive animals actively use. Conversely, the studies can identify areas infrequently used and show how to make maximum use of these enclosure areas. Further studies targeting both the increase in percentages of natural behaviors exhibited and use of the enrich zone used the current study on captive lion-tailed macaques for their design.

Influence of visitor presence on the behaviour of captive lion-tailed macaques ( Macaca silenus) housed in Indian zoos

To study the influence of ‘visitor presence’ on captive lion-tailed macaques, a behavioural study (Short Term Effects) was conducted on 30 individuals housed in 8 zoos across India. The study animals were observed on ‘visitor presence’ days and on ‘visitor absence’ days, which were zoo holidays. To record the long-term impact of ‘visitor presence’ on captive primate behaviour, a study on the Long Term Effects was also conducted. In this study, the behaviour of seven singly-housed individuals was recorded independently when ‘on-exhibit’ and ‘off-exhibit’ in enclosures of similar sizes. In the Short Term Effects, visitors influenced 20% more abnormal behaviour and 3% more social, mating and aggressive behaviours. In the study on Long Term Effects, visitors were found to influence a 30% increase in abnormal behaviour. In addition, in this study on Long Term Effects, use of space in the enclosure varied with individuals using the areas of the enclosure with trees, shrubs and water bodies (enriched zone) more when ‘off-exhibit’ than when ‘on-exhibit’. ‘Visitor presence’ was thus found to influence the behaviour of captive lion-tailed macaques in a negative way suggesting that ‘visitor presence’ might adversely affect their welfare.