Macaque Species Research Articles

Seroprevalence of Dengue, Zika, and Chikungunya Viruses in Wild Monkeys in Thailand.

Zoonotic pathogens such as arboviruses have comprised a significant proportion of emerging infectious diseases in humans. The role of wildlife species as reservoirs for arboviruses is poorly understood, especially in endemic areas such as Southeast Asia. This study aims to determine the exposure history of different macaque species from national parks in Thailand to mosquito-borne flaviviruses and alphavirus by testing the serum samples collected from 25 northern pigtailed macaques, 33 stump-tailed macaques, and 4 long-tailed macaques for the presence of antibodies against dengue, Zika, and chikungunya viruses by plaque reduction neutralization assay. Specific neutralizing antibodies against Dengue virus (DENV1-4) and Zika virus (ZIKV) were mainly found in stump-tailed macaques, whereas neutralizing antibody titers were not detected in long-tailed macaques and pigtailed macaques as determined by 90% plaque reduction neutralization assay (PRNT90). One long-tailed macaque captured from the south of Thailand exhibited antibody titers against chikungunya virus (CHIKV), suggesting enzootic of this virus to nonhuman primates (NHPs) in Thailand. Encroachment of human settlements into the forest has increased the interface that exposes humans to zoonotic pathogens such as arboviruses found in monkeys. Nonhuman primates living in different regions of Thailand showed different patterns of arboviral infections. The presence of neutralizing antibodies among wild monkeys in Thailand strongly suggests the existence of sylvatic cycles for DENV, ZIKV, and CHIKV in Thailand. The transmission of dengue, Zika, and chikungunya viruses among wild macaques may have important public health implications.

Mitogenomics of macaques (Macaca) across Wallace's Line in the context of modern human dispersals

Wallace's Line demarcates a biogeographical boundary between the Indomalaya and Australasian ecoregions. Most placental mammalian genera, for example, occur to the west of this line, whereas most marsupial genera occur to the east. However, macaque monkeys are unusual because they naturally occur on both western and eastern sides. To further explore this anomalous distribution, we analyzed 222 mitochondrial genomes from ∼20 macaque species, including new genomes from 60 specimens. These comprise a population sampling of most Sulawesi macaques, Macaca fascicularis (long-tailed macaques) specimens that were collected by Alfred R. Wallace and specimens that were recovered during archaeological excavations at Liang Bua, a cave on the Indonesian island of Flores. In M. fascicularis, three mitochondrial lineages span the southernmost portion of Wallace's Line between Bali and Lombok, and divergences within these lineages are contemporaneous with, and possibly mediated by, past dispersals of modern human populations. Near the central portion of Wallace's Line between Borneo and Sulawesi, a more ancient dispersal of macaques from mainland Asia to Sulawesi preceded modern human colonization, which was followed by rapid dispersal of matrilines and was subsequently influenced by recent interspecies hybridization. In contrast to previous studies, we find no strong signal of recombination in most macaque mitochondrial genomes. These findings further characterize macaque evolution before and after modern human dispersal throughout Southeast Asia and point to possible effects on biodiversity of ancient human cultural diasporas.

Ancient Pets. The health, diet and diversity of cats, dogs and monkeys from the Red Sea port of Berenice (Egypt) in the 1st-2nd centuries AD

ABSTRACT Exploration of the ancient transcontinental port of Berenice has enabled us to reveal some of the cultural roots of today’s societal bond with ‘commensals’; this bond included emotional ties with domesticated animals. The ‘pet cemetery’ at the port functioned from the mid-1st to mid-2nd century AD. The 585 unearthed burials were dominated by cats, dogs and two species of macaques. At least some of these animals came from outside the African continent. The sex and age profiles of the cats corresponded to those recorded in contemporary urban populations. Among the animals buried at Berenice there featured numerous pathological lesions and diseases that would have prevented unaccompanied survival. Although dogs were mainly of a light, Spitz-type, there was also a taller variant, as well as toy-dogs. The type of burial and furnishings point to the transposition of funerary customs also to pets.

Deforestation on the Indonesian island of Sulawesi and the loss of primate habitat

Sulawesi is an important island for primates. All 17 species that are found there are endemics. The island also includes contact zones between species of macaques (genus Macaca) where hybrids may arise. Sulawesi continues to be deforested, especially in the lowlands most suitable for estate crops and other agricultural products. We carried out an island-wide review of the current extent and rates of deforestation, and the impact this is having on the habitat available to all primates and within macaque hybrid zones. The provinces of West Sulawesi and Southeast Sulawesi suffered the highest rate of deforestation. Macaca ochreata in Southeast Sulawesi and Tarsius pelengensis on Peleng island in Central Sulawesi have lost the most habitat at 14%, followed by M. hecki and M. tonkeana. Forest loss also occurred in all macaque contact zones. The greatest losses occurred at contact zones between the western population of M. tonkeana and M. ochreata. Corn, coffee, cocoa, and oil palm are commodities that are spreading throughout the island. The extent of deforestation in the hybrid zones is alarming, particularly as none of them are represented in protected areas. To help address these problems, a careful integration of conservation and development is suggested, including making trade-offs explicit, and conducting transdisciplinary research on social-ecological systems at the interface of policy and management at local scales.

Variability in the number of infraorbital foramina in rhesus macaques (Macaca mulatta) and cynomolgus macaques (Macaca fascicularis).

This study aimed to determine the number of infraorbital foramina in monkeys of the Papionini tribe. The authors performed a μCT analysis of the morphology of the infraorbital foramina. A total number of 52 simian skulls belonged to two macaque species: Macaca mulatta and Macaca fascicularis were used in the study. The number of infraorbital foramina was counted macroscopically and with the use of a magnifying glass. Next, the skull representing the most common morphological type was selected and scanned by micro-computed tomography (μCT). The Shapiro-Wilk normality test was used in the study. To compare the differences in the number of infraorbital foramen between species, sex and sides, the Mann-Whitney U test was applied. Three infraorbital foramina were present in most individuals from the test group. The Mann-Whitney test revealed no statistically significant difference between the number of foramina on the right- and left-hand side. Likewise, no statistically significant differences between the numbers of infraorbital foramina across sexes were observed. Volumetric reconstructions revealed the presence of separate infraorbital canals for each infraorbital foramen. Craniofacial innervation in macaques is formed by complex branching patterns of cranial nerves. Variability in the number of infraorbital foramina suggests a variable maxillary innervation pattern in these animals. Based on the analysis of volumetric projections, the presence of two labial branches and a single nasal branch of the infraorbital nerve is suggested. Detailed descriptions are supported by quantitative data and μCT evidence.

Chromosome-level de novo assembly of the pig-tailed macaque genome using linked-read sequencing and HiC proximity scaffolding.

BackgroundMacaque species share >93% genome homology with humans and develop many disease phenotypes similar to those of humans, making them valuable animal models for the study of human diseases (e.g., HIV and neurodegenerative diseases). However, the quality of genome assembly and annotation for several macaque species lags behind the human genome effort.ResultsTo close this gap and enhance functional genomics approaches, we used a combination of de novo linked-read assembly and scaffolding using proximity ligation assay (HiC) to assemble the pig-tailed macaque (Macaca nemestrina) genome. This combinatorial method yielded large scaffolds at chromosome level with a scaffold N50 of 127.5 Mb; the 23 largest scaffolds covered 90% of the entire genome. This assembly revealed large-scale rearrangements between pig-tailed macaque chromosomes 7, 12, and 13 and human chromosomes 2, 14, and 15. We subsequently annotated the genome using transcriptome and proteomics data from personalized induced pluripotent stem cells derived from the same animal. Reconstruction of the evolutionary tree using whole-genome annotation and orthologous comparisons among 3 macaque species, human, and mouse genomes revealed extensive homology between human and pig-tailed macaques with regards to both pluripotent stem cell genes and innate immune gene pathways. Our results confirm that rhesus and cynomolgus macaques exhibit a closer evolutionary distance to each other than either species exhibits to humans or pig-tailed macaques.ConclusionsThese findings demonstrate that pig-tailed macaques can serve as an excellent animal model for the study of many human diseases particularly with regards to pluripotency and innate immune pathways.

Efficient Surveillance of Plasmodium knowlesi Genetic Subpopulations, Malaysian Borneo, 2000-2018.

Population genetic analysis revealed that Plasmodium knowlesi infections in Malaysian Borneo are caused by 2 divergent parasites associated with long-tailed (cluster 1) and pig-tailed (cluster 2) macaques. Because the transmission ecology is likely to differ for each macaque species, we developed a simple genotyping PCR to efficiently distinguish between and survey the 2 parasite subpopulations. This assay confirmed differences in the relative proportions in areas of Kapit division of Sarawak state, consistent with multilocus microsatellite analyses. Analyses of 1,204 human infections at Kapit Hospital showed that cluster 1 caused approximately two thirds of cases with no significant temporal changes from 2000 to 2018. We observed an apparent increase in overall numbers in the most recent 2 years studied, driven mainly by increased cluster 1 parasite infections. Continued monitoring of the frequency of different parasite subpopulations and correlation with environmental alterations are necessary to determine whether the epidemiology will change substantially.

The relative efficacy of the cranium and os coxa for taxonomic assessment in macaques.

The cranium is generally considered more reliable than the postcranium for assessing primate taxonomy, although recent research suggests that pelvic shape may be equally reliable. However, little research has focused on intrageneric taxonomic discrimination. Here, we test the relative taxonomic efficacy of the cranium and os coxa for differentiating two macaque species, with and without considering sexual dimorphism. Geometric morphometric analyses were performed on cranial and os coxa landmarks for 119 adult Macaca fascicularis, M. mulatta, and Chlorocebus pygerythrus. Among-group shape variation was examined using canonical variates analyses. Cross-validated discriminant function analysis provided rates of correct group classification. Additionally, average morphological distances were compared with neutral genetic distances. Macaque species were clearly differentiated, both cranially and pelvically, when sex was not considered. Males were more often correctly classified based on the os coxa, while female classification rates were high for both morphologies. Female crania and male os coxa were differentiated approximately the same as genetic distance, while male crania were more similar (convergent), and female os coxa were more divergent than expected based on genetic distance. The hypothesis that cranial and os coxal shape can be used to discriminate among macaque species was supported. The cranium was better at differentiating females, while the os coxa was better at differentiating male macaques. Hence, there is no a priori reason for preferring the cranium when assessing intragenetic taxonomic relationships, but the effects of high levels of sexual dimorphism must be corrected for to accurately assess taxonomic signatures.

Lipidome analysis of milk composition in humans, monkeys, bovids, and pigs

BackgroundLipids contained in milk are an essential source of energy and structural materials for a growing neonate. Furthermore, lipids’ long-chain unsaturated fatty acid residues can directly participate in neonatal tissue formation. Here, we used untargeted mass spectrometric measurements to assess milk lipid composition in seven mammalian species: humans, two macaque species, cows, goats, yaks, and pigs.ResultsAnalysis of the main milk lipid class, triacylglycerides (TAGs), revealed species-specific quantitative differences in the composition of fatty acid residues for each of seven species. Overall, differences in milk lipid composition reflect evolutionary distances among species, with each species group demonstrating specific lipidome features. Among them, human milk contained more medium and long-chain unsaturated fatty acids compared to other species, while pig milk was the most distinct, featuring the highest proportion of long-chain polyunsaturated fatty acids.ConclusionsWe show that milk lipidome composition is dynamic across mammalian species, changed extensively in pigs, and contains features particular to humans.

Prevalence and subtype diversity of Blastocystis in human and nonhuman primates in North China.

Blastocystis is of public health concern due to its global distribution in diverse animals including humans. Here, fecal specimens sampled from human and nonhuman primates were examined for Blastocystis by PCR and sequence analysis of the small subunit ribosomal RNA gene. Among age cohorts, the parasite was positive only for three of 126 (2.4%) adults admitted to a hospital in Harbin, Heilongjiang province, with a less common human subtype (ST), ST5, determined. Blastocystis was identified in 7.0% of nonhuman primates (NHPs), giving an infection rate of 6.8% (4/59) to zoo NHPs in Harbin and 7.1% (9/126) to lab NHPs in Beijing. No significant prevalence differences by macaque species, age, gender, and sample source were observed. Among the subtypes found in NHPs, seven belonged to ST1, three to ST2, one to ST3, and the remaining two to mixed ST1/ST3 and ST2/ST3. Although the data here showed no direct evidence linking human infections to Blastocystis of NHP origin, individuals might acquire colonization of ST5 from livestock sources judged by occurrence of this subtype also in cattle in Harbin and pigs and sheep in unspecified cities of Heilongjiang as noted in previous reports. In addition, given the nonrigid (but sometimes, perhaps cryptic) host specificity of ST1, ST2, and ST3 and their dominant role in human affections globally as discussed in a previous NHP report by Alfellani et al. (Parasitology 140:966-971, 2013a), precautions should be taken to minimize the possible transmission of those subtypes from NHPs to humans in North China.

Toward a Macaque Model of HIV-1 Infection: Roadblocks, Progress, and Future Strategies.

The human-specific tropism of Human Immunodeficiency Virus Type 1 (HIV-1) has complicated the development of a macaque model of HIV-1 infection/AIDS that is suitable for preclinical evaluation of vaccines and novel treatment strategies. Several innate retroviral restriction factors, such as APOBEC3 family of proteins, TRIM5α, BST2, and SAMHD1, that prevent HIV-1 replication have been identified in macaque cells. Accessory proteins expressed by Simian Immunodeficiency virus (SIV) such as viral infectivity factor (Vif), viral protein X (Vpx), viral protein R (Vpr), and negative factor (Nef) have been shown to play key roles in overcoming these restriction factors in macaque cells. Thus, substituting HIV-1 accessory genes with those from SIV may enable HIV-1 replication in macaques. We and others have constructed macaque-tropic HIV-1 derivatives [also called simian-tropic HIV-1 (stHIV-1) or Human-Simian Immunodeficiency Virus (HSIV)] carrying SIV vif to overcome APOBEC3 family proteins. Additional modifications to HIV-1 gag in some of the macaque-tropic HIV-1 have also been done to overcome TRIM5α restriction in rhesus and cynomolgus macaques. Although these viruses replicate persistently in macaque species, they do not result in CD4 depletion. Thus, these studies suggest that additional blocks to HIV-1 replication exist in macaques that prevent high-level viral replication. Furthermore, serial animal-to-animal passaging of macaque-tropic HIV-1 in vivo has not resulted in pathogenic variants that cause AIDS in immunocompetent macaques. In this review, we discuss recent developments made toward developing macaque model of HIV-1 infection.

Avoidant social style among wild crested macaque males (Macaca nigra) in Tangkoko Nature Reserve, Sulawesi, Indonesia

Abstract Although it is well established that female crested macaques (Macaca nigra) display very tolerant social styles, less is known about the extent to which crested macaque males can be characterized by the social style concept. We examined core social style traits and other measures of social interactions in three groups of wild crested macaque males in Tangkoko Reserve, Indonesia. Comparisons with males of other macaque species suggest that they display a mixture of tolerant and despotic indicators, a pattern inconsistent with tolerant, despotic or uniformly intermediate designations. Their apparent avoidance of affiliative interactions and reconciliation involving contact suggest that their relationships also contrast with the typically affiliative and relaxed social style of female crested macaques. Rather than labeling them as distinctly tolerant or despotic, we describe the social style of crested males as ‘avoidant’, which may reflect tense relationships due to high levels of risky reproductive competition.

Is the scapula a good indicator of taxonomy?: A geometric morphometric analysis using macaque monkeys

In primates, scapular shape is often thought to correlate to locomotor patterns with distinct morphologies observed in arboreal versus terrestrial species. However, the extent to which intra‐generic morphological differences might be related to taxonomic differences as opposed to convergent locomotor behaviors remains to be tested. Thus, we tested the hypothesis that closely related, but behaviorally distinct, species may exhibit variation in their scapular morphology that match known phylogenetic relationships among the specious macaque monkey. Our sample (n=230) represented nine species; M. fascicularis, M. mulatta, M. fuscata, M. arctoides, M. radiata, M. nigra, M. nemestrina, and M. sylvanus and a Colobine outgroup (Trachypithecus cristatus). 3D scans of the left scapula were taken using an HDI structured light scanner and 5 landmarks and 61 sliding semilandmarks were applied to the scans to capture overall form. Following Procrustes superimposition, Canonical Variates Analysis (CVA) was performed and Procrustes coordinates were extracted and used for a Discriminant Function Analysis (DFA). The results of the CVA showed clear differences between Trachypithecus and macaques, as well as between M. fuscata and M. radiata and all other macaques. In the cross‐validated DFA, only 34.1% of individuals were correctly classified. The outgroup Trachypithecus showed a correct classification rate of 70%, as did M. nigra consistent with relatively distinct morphology in this taxon. Overall, patterns of morphological variation observed in the CVA do not match phylogenetic history, therefore suggesting environmental factors might influence the pattern of morphological variation among macaque species in novel ways, though this remains to be tested.Support or Funding InformationThis research is supported by a National Science Foundation Grant (NSF BCS‐1830745), Field Museum Visiting Researcher Fellowship, Primate Research Institute Cooperative Research Grant, University at Buffalo Asian Studies Grant, and the Mark Diamond Research Fund (SP‐18‐13).

Unparalleled Rapid Evolution of KIR Genes in Rhesus and Cynomolgus Macaque Populations.

The killer cell Ig-like receptors (KIR) modulate immune responses through interactions with MHC class I molecules. The KIR region in large cohorts of rhesus and cynomolgus macaque populations were characterized, and the experimental design enabled the definition of a considerable number of alleles (n = 576) and haplotypes, which are highly variable with regard to architecture. Although high levels of polymorphism were recorded, only a few alleles are shared between species and populations. The rapid evolution of allelic polymorphism, accumulated by point mutations, was further confirmed by the emergence of a novel KIR allele in a rhesus macaque family. In addition to allelic variation, abundant orthologous and species-specific KIR genes were identified, the latter of which are frequently generated by fusion events. The concerted action of both genetic mechanisms, in combination with differential selective pressures at the population level, resulted in the unparalleled rapid evolution of the KIR gene region in two closely related macaque species. The variation of the KIR gene repertoire at the species and population level might have an impact on the outcome of preclinical studies with macaque models.

Comparative ecological and behavioral study of Macaca assamensis and M. mulatta in Shivapuri Nagarjun National Park, Nepal

Resource partitioning reduces the competition between different species within the same habitat, promoting their coexistence. To understand how such species co-adapt to reduce conflicts, we examined the behavior of two primates, Assamese macaque (Macaca assamensis) and rhesus macaque (Macaca mulatta), from April 2017 to March 2018 in Sivapuri Nagarjun National Park (SNNP), Kathmandu Valley, Nepal. We performed 1580 and 1261 scan sessions on wild multi-male/multi-female groups of Assamese and rhesus macaques, respectively, at 15-min sampling intervals. Assamese macaques consumed fewer plant species (38 species) than rhesus macaques (88 species). Overlapping food sources between the macaque species resulted in a Pianka index of 0.5. Assamese macaques consumed more items of tree, climber, and vine species, whereas rhesus macaques fed on more shrub, herb, and grass species. The proportions of plant parts consumed by the two species differed—more leaves, fruits and cones were used by Assamese macaques than rhesus macaques, whereas more flowers, seeds, and pods were consumed by rhesus macaques than Assamese macaques. Assamese macaques had a smaller home range (0.55 km2) than rhesus macaques (4.23 km2), and Assamese macaques had a shorter daily moving distance (1.6 km) than rhesus macaques (4.0 km). Although feeding time did not differ between the two macaque species, less time was devoted to social activities by Assamese macaques (16.0%) than by rhesus macaques (33.7%). Assamese macaques were generally arboreal, with 94.0% of their activities in trees, whereas rhesus macaques were largely terrestrial, with 58.5% of their activities on the ground. These differences in food selection, home-range size, ranging and activity patterns, and habitat use suggest that Assamese and rhesus macaques reduce resource competition through resource partitioning to coexist in a landscape matrix.

Triadic grooming among adult females in a free-ranging group of Japanese macaques.

This study aimed to quantitatively describe triadic grooming bouts in a free-ranging group of Japanese macaques (Macaca fuscata). Two types of triadic grooming bouts occurred less frequently and for a shorter duration than dyadic grooming bouts: straight-line type (SL), where individual A grooms B, who then grooms C; and two-to-one type (TO), where individuals X1 and X2 groom Y. TO-type grooming was recorded more often than SL-type grooming. As in the dyadic grooming bouts, two females who had direct grooming interactions in both SL-type (i.e., between A and B or between B and C) and TO-type groomings (i.e., between X1 and Y and between X2 and Y) and two groomers who did not have direct grooming interactions in TO-type grooming were closely related to each other in more than the half of the pairs recorded. Groomers were more likely to be subordinate to groomees in triadic grooming. Almost all of the observed pairs in SL- and TO-type groomings were also recorded in dyadic grooming bouts. These findings indicate that like dyadic grooming, triadic grooming bouts are largely influenced by blood relatedness through maternal lines and dominance relationships between participants. Based on affiliative relationships maintained through dyadic grooming, triadic grooming could be influenced by such affiliative relationships and then function to strengthen bonds between participants. Possible relationships between triadic grooming and the level of social tolerance among individuals are discussed from the viewpoints of interspecies differences among macaque species and regional differences in Japanese macaques.

Macaca leonina has a wider niche breadth than sympatric M. mulatta in a fragmented tropical forest in southwest China.

Niche differentiation has long been identified as an essential stabilizing mechanism for the coexistence of sympatric species. Using camera trapping data obtained during 2012-2016, we identified Macaca leonina and M. mulatta as the dominant macaque species in the Naban River Watershed National Nature Reserve (NRW-NNR), a tropical forest in southwestern China. In general, M. leonina exhibited a wider distribution and greater niche breadth than co-occurring M. mulatta. According to a fitted maximum entropy model (MaxEnt), M. leonina was predicted to predominantly occur in forest at higher elevation, whereas M. mulatta was predicted at lower elevation; the broadleaved evergreen forest was predicted as the most suitable vegetation for both species to inhabit, while the unsuitable area was bordered by rubber plantation, in which both food scarcity and human disturbance restricted the movement of macaques. Although the niches of these two species highly overlapped across space and time, we also found evidence for their spatiotemporal niche differentiation. When the two species inhabited independent areas with different elevations and vegetation, they maintained a similar activity pattern; however, in the zones of overlap, their activity patterns differed significantly. Further comparative field studies of these two macaques, considering other niche dimensions, are required to ensure their coexistence and long-term conservation.

Assessment of the subtypes and the zoonotic risk of Blastocystis sp. of experimental macaques in Yunnan province, southwestern China

Blastocystis is an enteral eukaryote with an omnipresent existence in animals and humans globally. Animals have been proposed to be a major reservoir for the transmission of Blastocystis to individuals due to their high prevalence and large amount of zoonotic subtypes. However, limited data on Blastocystis infection in experimental macaques in China exists. The objective of the current study was to investigate the frequency and subtypes of Blastocystis infection in macaques in southwestern China. A total of 505 fecal samples were collected from experimental macaques in Yunnan province and were analyzed by nested PCR and phylogenetic analyses on the basis of small subunit rRNA (SSU rRNA) gene fragments. A total of 235 specimens were positive for Blastocystis sp., and the prevalence of Blastocystis sp. was 46.5% (235/505). Significant differences in prevalence were also observed among the various species of macaques (P <0.0133, df = 2, χ2 = 8.64) and the different feed types (P <0.0093, df = 1, χ2 = 6.77). Moreover, three zoonotic subtypes, ST1, ST3, and ST5, were identified by DNA sequence analysis. There were mainly single subtype infections with some mixed subtype infections, and the predominant subtype was ST3. The results suggested a high prevalence and diversified subtypes in macaques in Yunnan province, southwestern China. Macaques are likely to be potential reservoirs capable of zoonotic transmission of Blastocystis sp. to humans. To our knowledge, this study is the first large-scale systematic analysis of Blastocystis sp. colonization in Yunnan province in the subtropics of China; these results contribute to the in-depth study of genetic characteristics and the prevention, control, and treatment of Blastocystis sp. in macaques in Yunnan province and other regions.

Rhesus and Cynomolgus IGH Genotyping Yields Comprehensive Databases of Germline VDJ Alleles for In-Depth Immunological Studies

Rhesus and cynomolgus macaques are important animal models for the pre-clinical assessment of candidate drugs and vaccines. Four main sub-groups are used: Indian and Chinese origin rhesus macaques and Mauritian and Indonesian cynomolgus macaques. Here, we applied the IG gene inference tool IgDiscover and extensive Sanger sequencing-based genomic validation to define germline VDJ alleles in these 4 sub-groups, comprising 45 macaques in total. We observed a significant allelic overlap between Chinese and Indian origin rhesus macaques and, surprisingly, also between the two macaque species, consistent with significant levels of admixture. The island-restricted Mauritian cynomolgus population displayed the lowest number of alleles of the sub-groups, yet they maintained high individual allelic diversity. Our analysis resulted in comprehensive DBs of germline IGH alleles for rhesus and cynomolgus macaques, of which 64% and 79% of alleles respectively were not previously described, thereby facilitating high-quality B cell response studies in these species.

Management of Forest-Dwelling and Urban Species: Case Studies of the Lion-Tailed Macaque (Macaca silenus) and the Bonnet Macaque (M. radiata)

Species conservation depends on the needs of the species concerned. For example, obligatory forest-dwelling and typically urban primate species require different conservation approaches. Here, I compare the ecology, life history, and behavior of two species of macaques in southern India; review what we know about the conservation challenges for each; and propose conservation measures. Lion-tailed macaques (Macaca silenus) are endemic to the rainforests of the Western Ghats and are endangered as a result of fragmentation of their habitats and low population growth. I recommend identification of contiguous forest habitats for viable lion-tailed macaque populations, improving the quality of their degraded habitats, and the linking of forest fragments with native vegetation as management measures for their conservation. In contrast, the bonnet macaque (M. radiata) is a habitat generalist endemic to southern India, but is losing its range to the relatively larger bodied and more aggressive rhesus macaque (M. mulatta). It is not a typically forest-dwelling species, and its populations are declining drastically in its traditional habitats that include Hindu temples, tourist spots, and roadsides with fruit-bearing trees and agricultural crops. The population has remained stable only where the habitat allows the macaques to forage in scrub jungle and includes a temple where the monkeys can obtain food from visitors. India is dotted with small hillocks with natural scrub or deciduous forest vegetation with one or two Hindu temples, and it appears that such habitats are the most suitable places for the long-term conservation of this species. These two case studies serve as examples of the different approaches needed to conserve forest-dwelling and urban primates, and with appropriate modifications, may inform the conservation of many other species.