Evolution and Diversity of Macaques: Research Progress and Prospects
Current situation and status of long-tailed macaques (Macaca fascicularis)
Suchinda Malaivijitnond1*, Yuzuru Hamada2
1Primate Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand
2Section of Morphology, Primate Research Institute, Kyoto University, Inuyama, Japan
Long-tailed macaques (Macaca fascicularis) are the most frequently encountered primate in Thailand. They are currently considered at low risk for extinction, however, they are threatened by habitat fragmentation or loss, inbreeding or outbreeding depression and hybridization. At present, no management measures have been taken and updated information on their situation and status are urgently needed. We sent questionnaires throughout Thailand to a total of 7,410 sub-districts, and received 1,425 (or 19.23%) replies. We traveled to the sub-districts from which the positive replies to questionnaires on long-tailed macaques were obtained, from December 2002 to December 2007 and found long-tailed macaques in 74 locations which ranged from the lower northern and northeastern (ca. 16 30f N) to the southernmost part (ca. 6 30f N) of Thailand. The distribution of long-tailed macaques at present is similar to that reported 30 years ago, however, their habitats have changed from natural forests to temples or recreation parks. Moreover, the troops tend to be over-populated. On average, 200 monkeys per location were counted and some populations had more than 1,000 individuals. In some locations, they were regarded as pests. In many places, local authorities took short-term management measures, such as translocation and contraception,. Pros and cons need to be considered in the maintenance of macaque populations. Although many troops of Thai long-tailed macaques have inflated population densities, some local troops exhibited morphological, genetic and behavioural uniqueness that may be important to conserve. Therefore, management plans and conservation strategies should be established for Thailandfs long-tailed macaque population.
Key words: hybridization, Indochina, Isthmus of Kra, long-tailed macaques, over-concentration, Sunda, translocation, Thailand
*Corresponding author and request for reprint: Dr. Suchinda Malaivijitnond
Primate Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, THAILAND
Tel: 66-2-2185275 Fax: 66-2-2185256 E-mail: email@example.com
Present Distribution and status of Macaques in Vietnam
Vo Dinh Son1, Suchinda Malaivijitnond2, Shunji Goto3, Cao Quoc Tri1, Nguyen Van Hung4, Le Van Hoang4, Tran Cong Trang5, Tran Huy Vu5, & Yuzuru Hamada6
1Department of Conservation Education, Saigon Zoo & Botanical Gardens,Vietnam
2Primate Research Unit, Faculty of Science,Chulalongkorn University, Thailand.,3JAmami Wild Animal Research, Inc., Japan, 4Highland University, Vietnam, 5 University of Agriculture and Forestry, Vietnam. 6Morphology Section, Primate Research Institute, Kyoto University, Japan
In a cooperative macaque research project (2004-2008), the members from Saigon Zoo and Primate Research Institute, Kyoto University have conducted a survey on distribution and status of Vietnam macaques in Central highland and its vicinity (ca. 16o16 N. to ca. 9o11fN.). The study was implemented by field survey and questionnaire survey for province level. A part of the study was carried out by 5 students of University as their graduate researches. As for pet monkeys, samples for DNA, morphological measurements and photos were obtained. Additional GPS information was used for macaque distribution. Capture and release survey was carried out in Ca Mau.
The study covered 150 sites. Among five macaque species occurring in Vietnam, Macaca fascicularis is the most successful species having a wide range, from Son Tra (16o 6f N) to Ca Mau southwards. In Central Highland, locating around 12oN. -15oN., we found this species at 40 localities, while Macaca arctoides and Macaca nemestrina at 67 localities and at 65 localities, respectively.
Whilst, only 5 localities for Macaca mulatta were found concentrating in the area ca.15oN to ca.16oN. Rhesus macaques having intermediate tailed- length between rhesus and long tailed macaque were found. These ghybridh macaques occurred in Son Tra, A Luoi and Central Highland areas. The populations in the Cu Lao Cham island, which situates 30 km east from Hoi An, also showed intermediate morphology between the two species, indicating the hybridization. Based on our analysis, we can conclude that gyellowh monkey reported by village people is probably Rhesus macaque and the contacting or co-occurrence zone of these two species is estimated at the area locating at ca.12o N. to ca.15o N, locating east to the Truongson mountain chains. No Macaca assamensis was found during the survey.
Non–indigenous macaques (confiscated or pet) have been released into the wild troops. At recreation areas or pagodas (e.g., Nui Ba Den where hybrids with M. nemestrina, M. mulatta, and M. fascicularis were found) from two to three macaque species coexist in the same group that consequently lead to be hybrid. Field study revealed that forest habitat fragmentation have led macaque population to become isolated each other, meanwhile persistent hunting have made them very timid. Deforestation for resettlement, illegal hunting and trading of primates have reduced wild macaques populations.
Key word: Distribution, Present Status, Macaca, Hybrid monkey, Yellow monkey, Central highland.
Distribution of macaques and observed pet primates in Laos
Hiroyuki Kurita1, Suchinda Malaivijitnond2, Bounnam Pathoumthong3,
Fong Samouth3, Chanda Vongsombath3, Phouthone Kingsada3, Yuzuru Hamada4
1Division of Cultural Property, Board of Education, Oita City
2Primate Research Unit, Department of Biology, Faculty of Science, Chulalongkorn University 3Department of Biology, Faculty of Science, National University of Laos
4Morphology Section, Primate Research Institute, Kyoto University
Lao Peoplefs Democratic Republic (Laos) situates adjacent to China, Vietnam, Thailand, Cambodia, and Myanmar. In Laos, primate fauna is rich, and 2 or 3 species of slow lorises, 5 species of macaques, 4 or more species of langurs, and 4 or more species of gibbons are known to be distributed, but the exact distribution and taxonomy have not been determined. We, therefore, try to determine the distribution of primates in northern and southern regions of Laos by round-trip and interview methods. We conducted round-trip survey three times between 2005 and 2007.
Subject areas in the southern Laos were Khammouane, Savannakhet, Saravan, Xekong, Champasak and Attapeu Provinces, and those in the northern regions were Phongsali, Luang Nam Tha, Oudom Xay, Luang Prabang and Houa Phanh Provinces. Using visual materials (brochures and posters), we asked village peoples and rangers of National Biodiversity Conservation Areas about primate species inhabiting the village area. When we got information about pet primates from residents, we also observed pet individuals and collected samples (hairs, oral epithelium, or feces) for DNA analysis under their ownersf permission.
In the northern regions, we interviewed at 46 sites. Slow lorises (big and small, Nycticebus bengalensis and N. pygmaeus), rhesus (Macaca mulatta), pig-tailed (M. nemestrina leonina), stump-tailed (M. arctoides) and Assamese macaques (M. assamensis), and Phayerfs (Trachypithecus phayrei) and Francois langurs (T. francoisi), and two species of gibbons (Nomascus concolor and N. leucogenys). In the southern regions, we interviewed at 42 sites from two surveys. Two species of slow lorises, five species of macaques, including long-tailed macaques (M. fascicularis), and four species of langurs, including red-shanked douc (Pygathrix nemaeus) and silvered langurs (T. cristatus) were reported. Concerning gibbons, N. leucogenys was confirmed by the observation of pet individuals, but distribution of other gibbon species was indefinite. Although residents of multiple villages suggested distribution of long-tailed macaques, we could collect no real evidence for the distribution. On this symposium, we will present details of distribution of macaque species.
We observed 60 pet primates from the following species in the northern and southern regions: Macaca nemestrina leonina, M. mulatta, M. assamensis, M. arctoides, Trachypithecus phayrei, Pygathrix nemaeus and Nomascus leucogenys. We will show their sex-age composition, keeping forms and difference in frequency of observed species between the northern and southern regions.
Primatology in Myanmar
Maung Maung Gyi
Department of Zoology, University of Yangon, University Campus, University P.O., MYANMAR
Myanmar possesses a diverse forest types with different climates that provide a favourable condition for various fauna. Among these, diversified types of primates as well as monkeys are inhabits. According to Tun Yin (1967), one species of prosimian, five species of macaques, five species of leaf monkeys and three species of gibbons are distributed throughout the Myanmar. Forest Ministry of Myanmar and Wildlife Conservation Society of Myanmar have worked in co-operation to study the ecology and conservation of Hoolock gibbon in Ma-ha-myine Wildlife Sanctuary in Central Myanmar. Collaboration project between Yangon University and Kyoto University to study macaque about their current distribution status and evolutionary process had been started in 2004 based on MoU. Primate researchers from both countries have been conducting research survey in different places of Myanmar and so far, quite a number of information have been collected. As the future development of primatology in Myanmar, studies on the monkeys about their ecology, morphology, behaviour and population genetics had been emphasized to promote the conservation of primates and their natural environments.
KEY WORDS : Myanmar, primates, macaques, primatology, conservation
A Research Report on the Distribution of Macaques in Myanmar
Toru Oi1, Aye Mi San2, Nang Wah Wah Min2**, Tin Nwe2, Yuzuru Hamada3
1Kansai Research Center, Forestry and Forest Products Research Institute
2Department of Zoology, University of Yangon, **Present Affiliation: Nippon University
4Primate Research Institute, Kyoto University
Myanmar is one of the areas which might have worked as corridors for macaques to deploy their distribution in Asia from Miocene to Pleistocene. In order to elucidate the history of speciation of macaques and provide the strategy to conserve them, we should clarify the geographical distribution of them in this country. To correct the deficit of knowledge about the current distribution of macaques in Myanmar, we conducted interviews with local people at 149 sites and visual roadside survey. We drove 8,530km along the main road in Rakhine Mountains, Central Plain, Shan Plateau, the northern part of Malay Peninsular to conduct this research during the period from November 2004 to January 2007. The results were (1) our information extended their distribution of long-tailed macaques (Macaca fascicularis) northwards along the coastal forests to be connected with the information in Bangladesh, and found that long-tailed macaques inhabited mainly coastal area below 50m in altitude; (2) rhesus macaques (Macaca mulatta) had the widest distribution both in vertically and horizontally among five species of macaques, and new information of this species were obtained in Rakhine Mountains; (3) we obtained new information of pig-tailed macaques (Macaca nemestrina leonine or Macaca leonine) in Rakhine Mountains, Chin Plateau and Bago Mountains, and found that they also had the wide distribution, but tended to inhabit the area of more than 700 m in altitude; (4) we obtained new information of stump-tailed (Macaca arctoides) and Assamese macaques (Macaca assamensis) in Rakhine Mountains, but at a quite fewer sites than other macaque species.
Key words: Macaques, distribution, Myanmar, roadside survey, interview
Corresponding Author, E-mail: firstname.lastname@example.org
Feeding Ecology and Reproductive Seasonality of Myanmar Long-tailed Macaque (Macaca fascicularis aurea) inhabiting the Bayin Nyi Naung Mountain, Myanmar
AYE MI SAN
Department of Zoology, University of Yangon, University P.O., MYANMAR
The Myanmar long-tailed macaques (Macaca fascicularis aurea) are distributed to coastal regions in Myanmar (Oi et al. in this symposium). A troop of long-tailed macaque inhabits the isolated steep limestone-rock Bayin Nyi Naung Mountain (BNNM), Kayin State. Their ecology was studied from September, 2004 to May, 2007. BNNM troop is isolated from other populations by the Thanlwin River and its flood plain, and human settlements, and the immigrants from other population were not found. They have the multi-male and multi-female type of troop with members ranging from 30 to 50 individuals during the study period. In the troop, the higher ranking individuals tend to have the higher priority to access the food resources and mating partners which is reflected by the reproductive outcome. The adult sex ratio was 1:1.2 males to females.
The animals were found to change food items seasonally from the total of 23 species of plants and 21 items of provisioned food from the pilgrimages by focal animal and ad libitum sampling methods. From the month June to October is the most natural plant abundant period, because of the coincided with the rainy season. The BNNM troop shows the reproductive seasonality which appears to be related with the natural food availability. The frequency of mating behaviour reached the maximum from November to February that coincided with maximum swelling of sexual skins in females. The birth season was found from March to July or August during three year study period, thus, the lactation period coincides with the season of higher natural plant food availability in the study area. The nominotypical subspecies of long-tailed macaques, which is distributed lower latitude than the Myanmar subspecies, does not show the reproductive seasonality. Thus, the seasonality in climate and food availability would have influenced on the Myanmar subspecies (BNNM population at least). The geographical range of Myanmar long-tailed macaques is latitudinally wide, from 10 to 21 degree, and there may be variation in the reproductive seasonality, which is the future subject.
KEY WORDS: Myanmar long-tailed macaques, Macaca fascicularis aurea, Bayin Nyi Naung Mountain, reproductive seasonality, food availability, birth season
Corresponding author: Aye Mi San
A Socio-ecological Study on Rhesus Macaque (Macaca mulatta): Comparison of Behavioral Activity between Urban and Village Groups.
Mohammed Firoz Jaman & Michael A. Huffman
Primate Research Institute, Kyoto University,Inuyama, Japan
We are investigating socio-ecological aspects of two different free ranging rhesus macaque troops, one living in an urban setting (} 80 individuals) and the other in a rural setting (} 42 individuals) in Bangladesh. The urban site is located in Gendaria area in and around the property of Shadona Traditional Pharmaceutical Co. in Dhaka, the capital city. The rural site is located in and around Bormi village, about 65 km north of Dhaka.
This research project, to be conducted over a 3 -year span, was started in April 2007. The main objectives of the project are to compare and quantify the activity budgets of two populations of rhesus living in different environments and to understand how activity patterns correlate with seasonal and other environmental factors under these two different conditions. Also, the nutritional intake accounted for by the consumption of natural vegetation by monkeys of different age-sex classes in the rural site will be analyzed in order to evaluate the nutritional condition of the troop for conservation purposes.
The city troop subsists mainly on provisioned foods (chick peas, bread and bananas) provided by Shadona authorities, as it is traditionally believed that the monkeysf presence bestow them with good fortune. The rural troop subsists on natural vegetation and food items obtained from frequent crop raiding of agricultural vegetable and fruits from the fields and market place.
Here we present a preliminary analysis of the data collected between September and October, 2007 from the first field season (rainy season). Troop and age-sex class differences in activity budgets will be presented. Behavioral data was collected mainly by focal animal sampling, each session lasting for 10-min. A total of 370 hours of observation was made (2220 focal samples), distributed equally across each age/sex class in both troops. To date we have also recorded and collected 15 preferred plant food items, processed and awaiting nutritional analysis. A brief outline of the research on Bangladeshi macaques will also be presented.
Mitochondrial DNA Diversity in Rhesus Macaques of Bangladesh
Yoshi Kawamoto1, Mohammed M. Feeroz2 & Md. Kamrul Hasan2
1Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
2Department of Zoology, Jahangirnagar University, Savar, Dhaka, Bangladesh
Rhesus macaques (Macaca mulatta) are found both in the natural habitat and inside human settlements in Bangladesh. Six populations are found in urban areas within human settlements of the country by 50 to 300km from each other and the number of groups in these populations varies from one to four. A total of 176 groups are recorded in the natural forested areas of the country. The southeastern region supports the highest number of groups while central part supports the lowest. Overall group size of rhesus macaques in natural habitat varies from 10 to 78 (mean=30.9}10.8, n=176). The sex ratio of adult males and females is higher and that between adults and immature is lower in groups in their natural habitats than those of groups found in urban areas.
Molecular variation of mitochondrial DNA (mtDNA) was investigated for rhesus macaques (Macaca mulatta) of Bangladesh using DNA samples obtained from feces. Partial sequence (583-599 bps) of mtDNA containing the second variable region of the D-loop was compared for 39 individuals from five localities in the country. A total of seven haplotypes were detected with substitutional or insertion/deletion mutations. They contained a unique polymorphism of pentanucleotide short tandem repeats (STRs). There were at least four different length types from two to five repeats of the unit nucleotide. One site of substitution and one site of single nucleotide insertion/deletion were also involved in the polymorphism. The mutation hot spots of the STR polymorphism were located between the first and second conserved sequence blocks (CSB1 and CSB2) as observed previously in some other mammals.
Geographical distribution of the STR polymorphism revealed local differences where the northeastern population was polymorphic with three STR haplotypes but other local populations were simply monomorphic with a single STR haplotype. Molecular phylogenetic analysis with reported sequences outside Bangladesh indicated low substitution diversity of mtDNA in Bangladesh. Clustering results suggested close relationship to India and divergence from Laos and China.
Current trends in macaque research in Taiwan
Institute of Wildlife Conservation
National Pingtung University of Science and Technology
ABSTRACT@Macaque research in Taiwan was launched since the 70s to examine their physiology for medical purposes. As an endemic species, the Taiwanese macaque (Macaca cyclopis) drew tremendous attention when researchers in Taiwan started to make effort on understanding wildlife in their natural habitats in the 80s. It is important to investigate the behavioral and ecological patterns of the Taiwanese macaque in order to understand how this wide-spread non-human primate interacts with its environment and what ecological role they play in natural ecosystems in Taiwan. In addition, increasing incidents of human-macaque conflict make primate research essential to achieve the coexistence of humans and macaques.
Behavioral and ecological patterns have been widely investigated in different groups inhabited at different sites. Food items of the macaque were collected, and their ranging pattern was suggested to be related the distribution of food trees in space. Fruits are the primary food resource of the macaques. It has been suggested that the macaque is the principle seed disperser of three Lauraceae trees which predominate in the low-altitude forest. Thus, the macaque is considered to play an important ecological role in the forest ecosystem. The social interactions and social relationship were investigated in a long-term study on a wild group, on which the association between kinship and social dominance, feeding activities, and social interactions were examined. This long-term study enables us to assess how various ecological factors and social factors affect female reproductive success in the Taiwanese macaque.
The increased spatial proximity of humans and macaques in recent years accelerates the level of conflict between humans and macaques. Crop raiding by macaques and the cost of crop raiding to farmers have been estimated in the central part of Taiwan. Specific study has been conducted to investigate the ranging pattern and utilization on orchards by macaque groups living in a particular region where the crop raiding was severe. It is found that unregulated provisioning influences behavior, ecology and health of the macaques. These studies might contribute to resolving the increasing conflict between humans and macaques.
We are on the process of revealing the ecological role that the Taiwanese macaque play in the forest ecosystem. However, more long-term studies on different groups inhibited at sites varied in altitudes, latitudes and/or habitat types are needed to comprehend our understanding of this species.
Key words: primate research, Macaca cyclopis, ecological role, social interaction, conflict
Distribution and sub-species morphological differences in three primate species of Sri Lanka (Macaca sinica, Semnopithecus priam, Trachypithecus vetulus).
Charmalie AD Nahallage & Michael A. Huffman
Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
Sri Lanka has four primate species, the toque macaque (Ms), gray langur (Sp), purple-faced langur (Tv) and slender loris. Little detailed information on the current distribution and conservation status of these species is known. Furthermore, the relationship between geographical distribution and sub-speciation of these species remains to be studied in detailed.
The main objective of our on-going study, conducted since 2003, is to up-date the approximate distribution of each of these species to the sub-species level. The census is being conducted using multi-lingual / picture questionnaires distributed throughout the country by students of the University of Sri Jayawardenepura, and University of Uva. In addition, questionnaires were distributed to all the National Parks in the country and extensive surveys have been conducted by the authors, interviewing local inhabitants and directly observing populations at selected sites across the country.
Three extensive surveys were conducted so far in 5 provinces covering the lowland, central, highland dry and wet zones. Ms have the widest distribution both in the dry and wet zones. Sp are distributed mainly in the northern and southern dry zones while Tv are distributed in the lowland wet and dry zone and the highlands. Mixed species grouping were noted for Ms and Sp in the southern dry zones.
To determine the morphological differences between the sub-species of these three species, photographic records are being collected. Thus far, during three field visits to Sri Lanka between 2004 and 2007 this work has revealed that Ms in lowland dry zones have lighter body and tail color with relatively short head crown hair compared to Ms in the central regions where fur is dark brown to red and tails are black. Highland Ms are lighter in body and tail color than the central ones and have the largest body size and longest head crown hair. Tv in the lowland wet and dry zones have a white rump patch and are smaller in size compared to highland Tv, who without a rump patch have both longer body fur and cheek hairs. For Sp, no clear-cut morphological differences could be found other than that of more whitish body fur color of those in the southern lowland dry zone.
In addition to morphological descriptions of sub-species level variation, we have begun collecting fecal samples to evaluate these morphological differences at the genetic level to verify or refute their presumed sub-species status. However, currently due to the difficulties of taking fecal samples out of the country, this work is still at the collection stage. We have plans to build on the infrastructure and faculty skills at the University of Sri Jayawardenepura so that this work can be done in-situ in the future.
Demography, Ecology, Behaviour and Conservation of Indian Macaques
National Institute of Advanced Studies, Indian Institute of
Science Campus, Bangalore, India
Nature Conservation Foundation, Mysore, India
Located strategically at the junction of the Palearctic and the Indomalayan biogeographic realms, India harbours sixteen primate species, including two lorises, eight macaques, five langurs and a gibbon. There have, however, been very few long-term studies on these species and the current status of most of their populations largely remains unknown. We have been involved, over the last fourteen years, in investigating the demography, ecology, behaviour, genetics and conservation of seven of the eight Indian macaque species, namely the bonnet macaque M. radiata, liontailed macaque M. silenus, rhesus macaque M. mulatta, Assamese macaque M. assamensis, pigtailed macaque M. leonina, stumptailed macaque M. arctoides and the Arunachal macaque M. munzala. We were, in fact, responsible for the discovery of the Arunachal macaque, a new species from northeastern India, in 2005. Some of our current research has been investigating the demography, social behaviour, cognition and culture in bonnet macaques of southern India; the ecology and conservation of liontailed macaques in southwestern India; the community ecology and conservation of five primate species in northeastern India and the population genetics of the sinica group of macaques. The social structure and behavioural ecology of several of these macaques appear to have been influenced by their close proximity to human populations over the last centuries. Although our studies demonstrate the behavioural and social plasticity of many of these species that face rapid changes in their environment, they also highlight the socioecological problems that their populations are forced to confront as they increasingly interact with burgeoning human populations.
Significance of Demonstrating the Intra- and/or Inter-species Differences in Biomedical Research Using Macaques as Experimental Models
Tsukuba Primate Research Center, National Institute of Biomedical Innovation,
Tsukuba, Ibaraki, Japan
The fundamental process of animal experimentation involves the demonstration of biological response of laboratory animals induced by various experimental treatments. The history of establishing modern laboratory animals is the process of minimizing the genetic variation in a population because host reaction to experimental treatment must be affected by genetic factor(s) of an individual animal. The efforts of inbreeding or maintaining a closed colony of laboratory rodents resulted in the establishment of various strains with different genetic backgrounds. Once various strains are established, searching for the most susceptible or resistant strain to a particular experimental treatment becomes important and is an effective step in clarifying the factor(s) that causes a difference in biological response. That is the use of inter-species difference.
Since the first breeding station of laboratory primates was established in Sukumi, Soviet Union, in 1927, more than 100 breeding colonies were established and they maintained hundreds of thousands of laboratory primates belonging to more than 40 different species by the end of 20th century. Among them, macaque monkey species have become the most commonly used laboratory primate and form the largest population in breeding colonies. Well-organized and large-scale breeding stations have maintained these colonies through successive generations (without introduction of feral individuals) by paying attention to the genetic management of populations to avoid inbreeding and to maintain genetic variation within breeding populations. These efforts make it possible to establish glaboratory primate STRAINSh with different genetic backgrounds under the same environmental condition. However, there are few trials to demonstrate the intra- and/or inter-species differences among macaque species. Here, I would like to show the following intra- and inter-species difference among macaque species that gave us important information about pathogenesis as well as host defense mechanism for the development of novel vaccines against infectious diseases.
1) The intra- and inter-species difference in the susceptibility to Human Immunodeficiency Virus (HIV) and Simian Immunodeficiency Virus (SIV):
It is a well-known inter-species difference that pig-tailed macaques are the most susceptible macaque species to both HIV and SIV. Rhesus macaques are more susceptible to SIV than cynomolgus monkeys. Indian rhesus are more susceptible to SIV than Chinese rhesus (intra-species difference).
2) The inter-species difference in the susceptibility to the monkey malaria parasite (Plasmodium coatneyi):
Both Japanese macaques and rhesus macaques are susceptible, but cynomolgus macaques are resistant to monkey malaria parasite infection. The pathology is more severe in Japanese macaques than rhesus macaques.
Genetic Diversity of Macaque Colonies at Primate Research Institute, Kyoto University and the Prospects for Laboratory Use
Primate Research Institute, Kyoto University, Japan
Primate research Institute, Kyoto University (KUPRI) maintains breeding colonies of Japanese (Macaca fuscata) and rhesus (M. mulatta) macaques for various biological and behavioral research. Four groups of M. fuscata (Takahama, Wakasa A and B, and Arashiyama) and two groups of M. mulatta (India and China) are kept in enclosure as separate colonies to maintain genetic characteristics of their localities of origin. Each colony has multi-male and multi-female social organization consisting of 30 to 50 individuals. More than 30 years have passed since these colonies were established.@I perform a population genetic study for these macaque colonies, with the goal to answer three questions: 1) How has genetic diversity changed from the time of establishment to present? 2) How is an increase of inbreeding? 3) Consequently, is there any effect of inbreeding on the health or reproduction capacity of these colonies? For that purpose, I conducted microsatellite genotyping for all the members of each colony to quantify genetic diversity of each group, to test their paternity, and to confirm all mother-infant records. In addition, microsatellite genotyping of individuals that were removed from the group because of use in the laboratory or for health reason are in progress to construct the pedigrees over 30 years history of the colonies.
In this presentation, I will show preliminary results of the study on macaque colonies at KUPRI, with special reference to genetic structure of the groups of M. fuscata and M. mulatta by analyzing 15 loci of autosomal microsatellite DNA. Mean heterozygosity (H), one of the indices of genetic diversity, was estimated to be 0.598 to 0.657 and 0.606 to 0.706 for the groups of M. fuscata and M. mulatta, respectively. Comparing this to previous studies using similar set of markers, the level of H for the group of M. fuscata at KUPRI was comparable to the wild troops of this species, such as Nikko, Hagachi, Tsubaki, Katsuyama and Koshima (0.559-0.646; Shotake and Yamane 2002). The amount of genetic differentiation among these colony groups and other population genetic parameters will be also shown. Finally, I will discuss importance of the macaques with known pedigree and comparative experiment using individuals with different origin in biological study using nonhuman primates.
History and Current Condition of Hybridization between Taiwanese
and Japanese Macaques in Wakayama, Japan
Wildlife Management Office Inc., Japan
A hybrid population of Japanese and Taiwanese macaques lives near a large native population of Japanese macaques in Wakayama Prefecture. The origin of this population is from a group of Taiwanese macaques that escaped from small private zoo in 1955. We heard that the number of monkeys at the zoo was 10-30 before they escaped.
There is an abundance of food such as acorns, bamboo, Unshu oranges, and the area is warm. Taiwanese macaques were able to settle there and their numbers increased in these favorable conditions.
The Wakayama Prefecture Government and Wakayama Taiwanese macaque Working Group carried out a census six times and conducted a population transition simulation. Two social groups of approximately 200 animals in total were observed in 1999. Four social groups of nearly 270 animals in total were estimated in 2003.
The Wakayama Prefecture Government has begun a program to prevent hybridization in native populations of Japanese macaques, and captured and removed approximately 90% of the hybrid animals from 2002 to the present.
Three social groups of 30(-50) in total were observed in 2006. The remnants of the hybrid population include 7 females who have been sterilized by surgery.
Now, we have two grave matters:
(1) Decline of capture efficiency, and
(2) Difference of census (counting the remnants).
Genetic Monitoring for Preventing Hybridization between
Native and Exotic Macaque Species in Japan
@@ Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
Adverse effects on the ecosystem caused by exotic species have evoked controversy in Japan. Prevention and removal of those effects on the ecosystem caused by introduced exotic species through human activity were declared in the gInvasive Alien Species Acth enacted by the government in 2004. The Japanese macaque (Macaca fuscata), an endemic primate species, has drawn special attention because of its hybridization with closely related species brought and released by humans in the country.
Invasion by exotic macaque species has been monitored by genetic assessment with molecular markers as well as direct observation and radio tracking. Application of sex-specific markers such as maternally inherited mitochondrial DNA (mtDNA) and paternally inherited Y-chromosomal DNA have significant roles in analyzing the causes and effects of the man-made change. Species specific nuclear DNA markers are also important to evaluate the degree of hybridization.
There are at least three sites in Japan where hybridization of feral groups of exotic macaques with Japanese macaques were confirmed. All cases seem to be initiated by adult male transfer from Japanese macaques to the exotic species group. For Taiwanese and rhesus macaques, admixture of gene pools with Japanese macaques progresses without significant deleterious affects on reproduction, suggesting the lack of a postzygotic isolation mechanism between those species. However, the degrees of hybridization vary among study sites and transfer of exotic genes to Japanese macaques is rarely known except a case between rhesus and Japanese macaques in Chiba prefecture.
Based on government policy, genetic monitoring is used to prevent the introduction of exotic genes into the native population. However, phylogenetic proximity between related species obscures their difference, mainly due to the scarcity of diagnostic markers and diversity within species. I will introduce how the monitoring is designed and used in management programs in Japan.
Morphological Assessment of Taiwanese-Japanese Macaque Hybrids in Wakayama Prefecture, Japan
Yuzuru HAMADA, Ayumi YAMAMOTO, Yutaka KUNIMATSU, & Toshio MOURI
Morphology Section, Primate Research Institute, Kyoto University
One troop of Taiwanese macaques (Macaca cyclopis) was released from a menagerie, and hybridized with native Japanese macaques (Macaca fuscata) in Wakayama Prefecture. There are already hybrids of F1, F2 and possibly more, with various combinations of mating. The Prefectural Government carried out elimination of Taiwanese and hybrid macaques. The working group was set up in 2003 to assess and describe the state of hybridization. We assessed their morphology at the time of autopsy and on skeletal specimens. Since Taiwanese and Japanese macaques are phylogenetically close to one another, their morphologies are also similar, making assessment of hybridization from morphology difficult. However, the species difference should be found in the head, teeth, and tail. The capturing was started in March 2003, and 338 Taiwanese and supposed hybrid individuals including fetuses, have been caught and autopsied. The skeletal specimens were then prepared. Firstly, we will summarize the morphological differences in the skull and mandible found between pure Taiwanese (Mc) and Japanese macaques (Mf). Mc tends to have smaller skulls, as shown by the average maximum head length; 114.6 (5.39 mm, SD; males) and 110.4 (2.40; females) in Mc and 133.1 (5.89; males) and 119.4 (4.93; females) in Mf (data from Fooden, 2006). As for shape differences, canonical discriminant analysis using 17 craniometric traits showed that Mc and Mf could be separated by the orbital width (Mc < Mf). Frequencies of cranial non-metric traits also showed species differences, but not necessarily decisively; e.g., the average numbers of canalis hypoglossalis were 1.30 (0.46) in Mc and 1.72 (0.60) in Mf, those of canalis suborbitalis were 3.80 (0.81) in Mc and 3.33 (0.93) in Mf, etc. Secondly, dental sizes were compared between the two species. Mc has smaller teeth in general. However, Mc has proportionally larger canines (upper and lower) and mesial lower premolars, and on the other hand, smaller molars, especially M2 and M3. Thirdly, tail length and caudal vertebrae were inspected in hybrids. The two measurements of tail length at autopsy and by X-ray photos were almost identical (R2=0.98). The range of relative tail length (standardized by the crown rump length, %) was as wide as 18.3– 95.5 % (average 49.3%), covering the averages of pure Mc and Mf, 95% and 15%, respectively. The average number of caudal vertebrae was 16.2 (range: 8 – 24), which correlates well with relative tail length (R2=0.82). Thus, a diverse degree of hybridization has already occurred. A preliminary analysis showed that the relative tail length strongly correlates with the degree of hybridization evaluated from genetics (Kawamoto in the present symposium). Therefore, the tail length is a good indicator of the degree of hybridization between Mc and Mf.
Two Cases of Hybridization between Macaca nemestrina and Macaca fascicularis in the Temple Sites, Thailand
Faculty of Human and Cultural Sciences, Musashi University, Tokyo
In this report I show the two cases of hybridization between Macaca nemestrina and Macaca fascicularis in the temple sites. I had a chance to visit nine primates sites for one month from 20 Aril to 20 May, 2007 by the arrangements by Drs. Suchinda Malaivijitnond and Yuzuru Hamada. I found the hybridization in What Tham Kham, Sakon Nakhon where I stayed from 3 May to 7 May and in Wattham Purtakhion, Chumphon from 13 May to 17 May.
In What Tham Kham, one troop was fed artificially. In the parking area the shop persons sell the food for monkeys and the children of the shops controlled and protected the tourists against the monkeys. The troop size was over 150 animals and it is difficult to detect its detailed age-sex composition for few days. The maximum number counted in one march was 142 individuals and 22 babies, totally, 164 animals. In the case of the maximum, the composition was 52 females, 8 adult males, 20 young adult males, 53 juveniles, 22 babies, and 9 unidentified animals.
Some estimated hybrid monkeys were found between Macaca nemestrina and Maraca fascicularis by the tail-length and some mixed morphological features in the age-sex class of juvenile, young males, and adult females. I could not find the hybrid individuals among the eight full adult males.
In Wat Tham Purtakhion, Chumphon, one troop of Macaca nemestrina and one troop of dusky langurs Trachypithecus obscurus were found in this small area. For the pig-tailed macaques, three records of identifying the animalsf age-sex classes in march were got; 46 animals on 13 May, 57 animals 0n 14 May, and 42 animals on 17 May, 2007. The composition of the case of the maximum number was 21 young adult and adult females, 1 adult male and 8 young adult males, and 21 juveniles, and one baby.
Only one adult male estimated over 13 years old were found and this male was the first ranking male which is really the hybrid individual, estimated between Macaca nemestrina and M. fascicularis. Among the juveniles some animals had longer tail than the usual of the normal pig-tailed monkeys. But we need more information about the growth data of the tail length during the juvenile period.
This first ranking male is a very interesting material to study the genetically based sexual behaviors of the two species in comparison with these non-hybrid alpha malesf sexual behaviors. The other males were all younger than the first ranking male. The second ranking male seemed to be a non-hybrid individual. The hybrid alpha male attracted the four estrous females around this male. The females presented to the male and some females got the copulation and ejaculation of the male. In the video, I show such estimated hybrid animals and sexual behaviors.
Between the genus Macaca species, rare hybridization incidences were reported in the natural situation, however, in the artificial situations some incidences were found. The dispersion of the hybrid animals toward the natural populations will result in deep impacts for the conservation. I propose some minimum rules should be designed to such areas where the monkeys are inhabiting.
Special lecture at the Primate Research Institute on 18th February 2008
The Role of Grooming in Macaque Social Markets
Michael D. Gumert
Division of Psychology,
School of Humanities and Social Sciences,
Nanyang Technological University,
Nanyang Avenue, Singapore, 639798
Ph: (65) 6514-1094
ABSTRACT: Macaque society is characterized by frequent grooming and other forms of social interaction. Grooming patterns are closely associated with kinship and dominance, but not all grooming is accounted for by these factors. Grooming is known to serve hygienic functions, but it is also widely documented for its role in social relationships, such as maintenance and formation of social bonds, reconciliation, and social exchange. Social markets, where macaques use grooming to gain access to social resources, may explain some grooming. Grooming may allow a macaque to be tolerated, access an infant, engage in sexual activity, or coordinate other forms of social trade with their partner. A market perspective postulates that grooming coordinates trades for social resources and that such trades are influenced by the current economic conditions in a social market. Research on a group of long-tailed macaques (Macaca fascicularis) in Kalimantan Tengah, Indonesia yielded support that some grooming is related to social trades and that these trades are influenced by social markets. Data was collected on grooming reciprocity and interchange with tolerance across age-sex classes. In addition, data from grooming interchanges with infant handling in female-female pairs and grooming interchanges with sexual activity in male-female pairs was obtained. Grooming was found to coordinate social trade through several mechanisms. First, grooming increased the tolerance a grooming receiver exhibited towards their partner. Second, grooming increased the likelihood that a receiver would preferentially engage in social activity with their groomer. Finally, the duration of grooming invested by the initial groomer during interchanges with sexual activity and infant handling was related to partner supply and competitor demand. These results support a biological market interpretation of social exchange. Grooming coordinates social trades and it appears to be an investment in a partner because the amount of grooming given is related to the economic conditions in which the trade occurred.