Int J Primatol DOI 10.

1007/s10764-011-9514-y

Of Least Concern? Range Extension by Rhesus Macaques (Macaca mulatta) Threatens Long-Term Survival of Bonnet Macaques (M. radiata) in Peninsular India
Rishi Kumar & Sindhu Radhakrishna & Anindya Sinha

Received: 28 May 2010 / Accepted: 17 January 2011 # Springer Science+Business Media, LLC 2011

Abstract Rhesus and bonnet macaques are the 2 most common and widely distributed of the 8 macaque species of India. Rhesus macaques are widely distributed across southern and southeastern Asia, whereas bonnet macaques are restricted to peninsular India. We studied the current distributional limits of the 2 species, examined patterns of their coexistence in the interspecific border zones, and evaluated losses in the distributional range of bonnet macaques over the last 3 decades. Our results indicate that whereas rhesus macaques have extended their geographical range into the southern peninsula, bonnet macaques have been displaced from many areas within their former distributional range. The southern and the northern distributional limits for rhesus and bonnet macaques, respectively, currently run parallel to each other in the western part of the country, are separated by a large gap in central India, and converge on the eastern coast of the peninsula to form a distribution overlap zone. This overlap region is characterized by the presence of mixed-species troops, with pure troops of both species sometimes occurring even in close proximity to one another. The range extension of rhesus macaquea natural process in some areas and a direct consequence of introduction by humans in other regionsposes grave implications for the endemic and declining populations of bonnet macaques in southern India. Keywords Conservation . Anthropogenic impacts . Distribution . Macaca mulatta . Macaca radiata . Mixed-species troops

R. Kumar : S. Radhakrishna : A. Sinha (*) Ecology, Behaviour and Conservation Programme and School of Natural Sciences and Engineering, National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560012, India e-mail: asinha@nias.iisc.ernet.in A. Sinha The Primate Programme, Nature Conservation Foundation, Gokulam Park, Mysore 570002, India

R. Kumar et al.

Introduction Primates that live in close association with other primate species in a community affect one another in terms of density, distribution, diet, and behavior (Waser 1987). Interspecific competition between primate species may occur through interference or by exploitation; studies documenting the effects of competition report that niche partitioning, decrease in population densities, and reduction in distribution range or even local extinction are some of the typical species responses to the continued presence or association of other species (Cowlishaw and Dunbar 2000; Waser 1987). Fooden (1982), for example, suggests that interspecific competition may have been an important determinant in the evolution of ecogeographic segregation among the south Asian macaques and provides evidence in support of this hypothesis by invoking the current ecological separation between sympatric Macaca radiata and M. silenus in peninsular India, and between M. nemestrina and M. fascicularis in Sumatra. Such ecogeographic separation is also evident in a number of macaque species that display marginal sympatry with <1% overlap in their distribution, particularly at the boundaries of their ranges (Fooden 1982). This is observed, e.g., between Macaca radiata and M. mulatta in India, M. leonina and M. assamensis in the Indo-Chinese peninsula (Fooden 1982), and between M. tonkeana and M. maura in Sulawesi (Froehlich and Suprianta 1996). Human intervention, in contrast, has brought together many primate species that were historically separated by relatively great distances. For example, in Hongkong, Macaca mulatta now commonly occurs with introduced M. fuscata, M. fascicularis, M. thibetana, and M. nemestrina (Burton and Chan 1996; Southwick and Southwick 1983), whereas in certain parts of Japan, M. fuscata shares its habitat with introduced feral populations of M. cyclopis (Fooden and Wu 2001). Such sympatry, both natural and anthropogenic, may result in polyspecific associations in the form of mixedspecies troops and hybrids, as has been reported for Macaca mulatta M. fascicularis and M. fascicularis M. nemestrina in Malaysia; for M. tonkeana M. hecki, M. maura M. tonkeana, M. tonkeana M. ochreata; and for M. nigra M. hecki and M. nigrescens M. hecki in Sulawesi (Bernstein 1966, 1968; Bynum 2002; Fooden 2006; Supriatna et al. 1992; Watanabe et al. 1991a; b; Watanabe and Matsumura 1991). Mixed troops of Macaca mulatta and M. radiata have also been reported along their common distribution boundary in central and southern India (Fooden 2000; Fooden et al. 1981; Koyama and Shekar 1981). Rhesus macaques (Macaca mulatta) and bonnet macaques (M. radiata) are the most common of the 8 species of Macaca occurring in India (Fooden 2000). Rhesus macaques have perhaps the largest distributional range within the genus: 7 illdefined subspecies of the taxa are broadly distributed across Afghanistan, Bangladesh, Bhutan, India, Nepal, Pakistan, China, Burma, Laos, Thailand, and Vietnam (Brandon-Jones et al. 2004; Fooden 2000). Bonnet macaques, in contrast, are believed to consist of 2 subspecies, both of which are endemic to India (Brandon-Jones et al. 2004; Fooden 1981; Saha 1984). Within India, the range of rhesus macaques extends over the entire northern and central parts of the country except northern Kashmir, high altitudes of the Western Himalaya, Great Indian Desert, and west-central India (Fooden 1989, 2000; Roonwal and Mohnot 1977). Bonnet macaques have been reported to range over the entire southern part of the

Of Least Concern? Range Extension by Rhesus Macaques

country, from Cape Comorin northward to the northern end of the Western Ghats mountains, Manjara Plateau, and the northern end of Velikonda range in the Eastern Ghats mountains (Fooden et al. 1981). The distributional ranges of bonnet and rhesus macaques traditionally have been considered to be separated by the Godavari River in east-central India and by the Tapti River in the western part of the country (Fooden 2000; Pocock 1939; Prater 1971; Roonwal and Mohnot 1977). Koyama and Shekar (1981) similarly concluded that the 2 rivers, along with the semi-arid zone of the Deccan Plateau of central India, acted as a barrier to the spread of both species. The last surveys of their distribution indicated that the northernmost limit of bonnet macaques was variously at 20.78N and 73.92E (Fooden et al. 1981) or at 20.08N and 73.58E (Koyama and Shekar 1981), whereas the southern limit of rhesus macaques was reported at 21.33N and 73.50E in western India (Koyama and Shekar 1981) and 15.77N and 79.68E in eastern India (Fooden et al. 1981). However, there have been occasional reports of the presence of rhesus macaques south of these 2 rivers (Krishnan 1972; Pocock 1939; Southwick et al. 1961; Spillett 1966). Fooden et al. (1981) suggested that this could be due to the natural extension of the geographical boundary of the species, while Koyama and Shekar (1981) opined that humans had introduced rhesus macaques artificially in these areas. In the present scenario of rapid urbanization, loss of forest habitats, and extensive forest fragmentation, it is critical to reassess species distribution ranges, particularly for species such as bonnet and rhesus macaques, which are neglected because of their ubiquitous urban presence. There has been recent concern, in fact, about the threatened status of many commensal populations of both species (Kumara et al. 2010; Singh and Rao 2004), although their status in the IUCN 2008 Red List is Least Concern. Bonnet macaques, being rather restricted in distribution, will be more vulnerable to changes in or the shrinkage of their habitat than would the more extensively distributed rhesus macaques. Rhesus macaques are believed to be among the most aggressive macaques in their species-typical temperament (Clarke et al. 1988; Clarke and Boinski 1995; Thierry 1985, 2007). The expansion of the distribution range of rhesus macaques in southern India at the expense of the more ecologically and behaviorally sensitive bonnet macaques could thus pose serious threats to the latter species. We here aim to reassess the northern and southern distribution boundaries of bonnet and rhesus macaques, respectively, in India. More specifically, our objectives were to establish current distribution boundaries of the species, identify the patterns of coexistence of the 2 species in the interspecific border zones, and evaluate the loss in the distributional range of bonnet macaques.

Methods We surveyed a total of 40 districts, comprising 564 locations, in the central and southern Indian states of Maharashtra, Andhra Pradesh, Gujarat, Goa, and Karnataka (Table I). We investigated 33 locations mentioned by Fooden et al. (1981) and all the macaque localities described by Koyama and Shekar (1981) in their respective surveys of the species. In addition, we selected survey areas on the basis of the following criteria: 1) reports of rhesus macaque presence within the geographical range of bonnet macaques; 2) areas adjacent to the previously defined boundaries of the 2 species; and 3) new,

R. Kumar et al. Table I Troops of rhesus macaques, bonnet macaques and of mixed-species directly sighted and reported by secondary sources in different Indian states Serial no. State/district Number of troops Rhesus macaque Bonnet macaque Mixed-species

Direct Secondary Direct Secondary Direct Secondary sighting sources sighting sources sighting sources Andhra Pradesh State 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. Goa State 13. 14. Gujarat State 15. 16. 17. 18. 19. Karnataka State 20. Maharashtra State 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. Mumbai Raigadh Thane Nandurbar Amravati Nagpur Akola Gondia Gadchiroli Sindhudurg Osmanabad Nanded 1 2 2 4 1 2 2 3 4 1 1 1 1 1 2 2 9 14 3 3 2 2b 1b Bidar 1 Dang Navsari Surat Bharuch Valsad 1 1 1 4 2 1 1 1c 4 North Goa South Goa 1 2 1b Guntur Warangal Kurnool Prakasam Nalgonda East Godavari Hyderabad Krishna Medak Anantpur 7 7 2 6 2 5 7 3 3 3 1 2 7 2 3
a

2 4

5 3 43 6

Mahabubnagar 12

1b 5 1 1c 1c 1c

West Godavari 1 2b

Of Least Concern? Range Extension by Rhesus Macaques Table I (continued) Serial no. State/district Number of troops Rhesus macaque Bonnet macaque Mixed-species

Direct Secondary Direct Secondary Direct Secondary sighting sources sighting sources sighting sources 33. 34. 35. 36. 37. 38. 39. Total troops Species and mixedspecies troops
a b c d

Aurangabad Pune Ahmadnagar Satara Kolhapur Sangli Nashik 64 39 103 1 111 6 6 3 1 2 1 1 1 2 29 140

1d

11

1 12

Solitary bonnet macaque individuals Bonnet macaque-dominated troops Rhesus macaque-dominated troops Rhesus macaque-Hanuman langur mixed-species troop

previously unlisted, areas in which either rhesus or bonnet macaque presence was reported by the local people. We conducted our survey from October 2004 to April 2008 (488 field days), on foot along roads and trails, and in vehicles along major roads, and covered ca. 7000 km. We dedicated comparable effort to the survey of areas north and south of the previously defined boundaries of the 2 species (north of the distribution boundaries: 1646 km, 132 locations, 137 days; south of the distribution boundaries: 1550 km, 125 locations, 122 days; the region between the distribution boundaries: 3804 km, 307 locations and 229 days). We surveyed forest areas as well as rural and urban areas in accordance with the criteria that we had used for the selection of our study sites. The vegetation of the surveyed forest sites could be classified into 6 major vegetation types: evergreen forest, semi-evergreen forest, moist deciduous, dry deciduous, thorn forest, and littoral forest (Champion and Seth 1968). We surveyed most of the study areas (544 of the 564 locations) twice and the 20 locations within the 8 protected areas (state-protected wildlife sanctuaries and national parks) 3 times. We confirmed species presence based on direct sightings of macaque troops as well as on secondary information from reliable sources. Whenever we sighted a troop, we recorded its location (with a hand-held GPS), size, agesex composition of the individuals, and its natural history, including history of introduction by translocation, wherever relevant. We conducted both surveys and interviews at all our study sites, as appropriate, including areas where macaques were earlier reported but could not be located during our study. We obtained secondary information on the locations of macaque troops from the local people, state forest department personnel, and researchers, all through informal

R. Kumar et al.

Fig. 1 Distribution boundaries of the bonnet and rhesus macaque in central India, indicating the overlapping-distribution zone of the two species. All 259 of the 564 surveyed locations where macaque presence was recorded have been indicated in the map but may not all be distinguishable due to their near-coincident distribution.

interview sessions, and from records maintained by the state forest departments. People living near the study areas were well informed about the location of macaque troops and provided good pointers on the presence of the respective species in different areas. Visibility was usually excellent in the study areas and ca. 90% of our surveyed areas contained human habitations. The macaque troops were relatively easy to detect in these areas, as most of them were habituated to human presence. We observed most of the directly sighted troops (92.5%) during the first surveys themselves; the second surveys yielded sightings of only 12 additional troops, and we sighted only 2 new troops during the third round of surveys.

Results We recorded macaque presence at 259 of the 564 locations surveyed. We obtained information on a total of 255 macaque groups, including 140 bonnet macaque troops, 103 rhesus macaque troops, 12 bonnet macaquerhesus macaque mixedspecies troops, 3 solitary bonnet macaque individuals, and a common langurrhesus macaque mixed-species troop (Table I, Fig. 1). Of these, we located a total of 186

Of Least Concern? Range Extension by Rhesus Macaques

troops and the 3 solitary bonnet macaque individuals via direct observation, and assigned locations to 69 troops through secondary information. Distribution Limits of the 2 Species The southern distributional limit of rhesus macaques in India is marked by the moist deciduous forests of Dang district (Gujarat) on the northern spur of the Western Ghats mountain range in western India, the dry deciduous forests of Amravati district (Maharashtra) in central India, the dry deciduous forests of Prakasam district (Andhra Pradesh) in eastern India, and having extended south of the Krishna River, ends just north of it in the Eastern Ghats mountains (Fig. 1). However, the species is absent from the coastal plains east of the Ghats on the eastern coast of the peninsula. The northern distributional limits of endemic bonnet macaques in peninsular India extend up to the moist deciduous forests in Dang district in western India, the dry deciduous forest in Osmanabad district (Maharashtra) in central India, and the agricultural lands of Mahabubnagar (Andhra Pradesh) in eastern India and end south of the Krishna River in Guntur district (Andhra Pradesh) on the eastern coast of the country (Fig. 1). We could not locate bonnet macaques in many site localities in eastern India, earlier reported as part of the distribution range of the species; these include Hyderabad City and its neighboring areas, particularly the northern parts of Mahabubnagar district in the state of Andhra Pradesh (Saha 1984; Srinivasulu and Nagulu 2001). We encountered only rhesus macaque troops in these areas but recorded the presence of 3 isolated troops of bonnet macaques within the rhesus macaque distributional range, 2 in the Vijayawada Hills and 1 in Rajahmundry, on the banks of the Godavari River, again in the state of Andhra Pradesh (Fig. 2). A comparison of our results with the earlier rhesus and bonnet macaque distributional limits in peninsular India (Fooden et al. 1981; Koyama and Shekar 1981) indicates that the former species has extended its southern distributional limits further southward, in eastern India by an area of ca. 3500 km2 (Fig. 1). This overlap region, extending to a maximum width of ca. 45 km, is now virtually devoid of bonnet macaque troops, although many of these locations had earlier reported the species (Fig. 1). The presence of rhesus macaques in areas formerly inhabited only by bonnet macaques is particularly pronounced south of the dry deciduous Srisailam forests in Andhra Pradesh, where the distribution boundary of rhesus macaques reaches its southernmost point in the town of Giddalur in the Prakasam district of the state. The mean ( SD) bonnet macaque troop size was 17.66.8, ranging from 9 to 40 individuals (n=47), while the rhesus macaque troop size ranged from 8 to 76 individuals, with a mean of 24.514.9 (n=38). Introduced Macaque Populations Our secondary data on the history of the populations in the distribution overlap zone of the 2 species revealed that a large number of rhesus macaque groups had been introduced into the eastern and the western flanks of the bonnet macaque distribution range during the last 3 decades (Table II, Fig. 3). Virtually all these groups, including a single, isolated troop in south-central Maharashtra (Fig. 1), had been translocated either into protected forest areas or into villages on the fringes of forests from other,

R. Kumar et al.

Fig. 2 Introduced troops of the rhesus macaque, isolated troops of rhesus and bonnet macaques, and mixed-species troops of both the species in central India.

more urban, parts of the state severely affected by humanmacaque conflict. It is noteworthy that the introductions of rhesus macaque groups in the western flank of the bonnet macaque distribution range, which occurred on a smaller scale and involved only a few individuals or troops, have largely remained restricted to the areas where they were originally introduced (Table II). In contrast, the large-scale introduction of the species that occurred near Kotulapenta, a site north of the Srisailam forests, in the eastern flank of the peninsula, has resulted in its southward migration leading to a virtually complete replacement of bonnet macaques by rhesus macaques in this part of the species-overlap region. Overlap in the Distribution of the 2 Species The species distribution patterns within the overlap region vary across the peninsula. For example, in the moist deciduous forests of the Western Ghats, rhesus and bonnet macaques occur very close to each other, separated occasionally by only a few kilometers (Fig. 1). However, in central India, the large, arid Desh and Marathvada regions exclude both species, with the bonnet macaque distribution following the Western Ghats to the south while the rhesus macaque distribution moves northward, creating a large gap between them. In the dry deciduous forests of the Eastern Ghats, in contrast, the rhesus macaque population has extended southward and this infiltration has created a significant distribution overlap zone. This overlap zone

Of Least Concern? Range Extension by Rhesus Macaques Table II Macaque troops introduced by translocation across our study areas Serial no. State/district Species and number of individuals Year of introduction Source of information

Andhra Pradesh State 1. 2. 3. 4. Goa State 5. Gujarat State 6. 7. 8. 9. 10. 11. 12. Surat Thane Mumbai Raigadh Sindhudurg Aurangabad Osmanabad Bonnet macaque* Rhesus macaque*** Rhesus macaque*** Rhesus macaque*** Rhesus macaque** Rhesus macaque** Rhesus macaque** 1998-2000 1972-73 1972-1973, 2000-2007 2000 Local peoplec Forest Departmentd, Pande 2005 Forest Departmentd, Pande 2005 Forest Departmentd Local peoplec Local people Local peoplec Maharashtra State North Goa Rhesus macaque** Local people Hyderabad Mahabubnagar Kurnool Nalgonda Bonnet macaque* Rhesus macaque*** Rhesus macaque**** Bonnet macaque* 2000-2002 1998-2000 1970-2005 Local people Local peoplea Forest Department, Local peopleb Local peoplec

Number of individuals: * 1 individual, ** 210 individuals, *** 10100 individuals, **** more than 1000 individuals
a

These macaques appear to have been translocated illegally from Hyderabad city but this could not be confirmed definitively by the local people

The local people attested to the large-scale, organised translocations of these macaques by several non-governmental, human welfare organisations Although the local people could not provide any detailed information on the history of these individuals, they were possibly abandoned after they had outgrown their use as pets or released by monkey trappers in the area Records maintained by the Forest Department offices in Thane, Mumbai and Raigadh

continues eastward until the Krishna River, where the distribution ranges of both the species again separate (Fig. 1). Mixed-Species Troops We recorded the presence of several mixed-species macaque troops across the peninsula (Table II, Fig. 2). We typically encountered these troops in areas where rhesus macaques had been introduced or where bonnet macaque enclaves exist within rhesus macaquedominated regions. We classified the mixed troops as rhesus macaquedominated or bonnet macaquedominated on the basis of the relative number of individuals of the 2 species in each troop. The former were more common in the eastern peninsula while the latter were encountered much more frequently in

R. Kumar et al.

Fig. 3 Extension of the range of the rhesus macaque into the distribution zone of the bonnet macaque over the last three decades in central India. The earlier southern distribution boundary of the rhesus macaque has been drawn from Fooden et al. (1981). Note that no bonnet macaque troops could be found in the sites marked as erstwhile locations of the species.

the western region, particularly within the distribution region of bonnet macaque (Table II). In the distribution overlap zone, rhesus and bonnet macaque troops often occurred in close proximity to one another, although direct interactions between the 2 species were rare and typically occurred only competitively over food resources. The pure species groups were never observed to associate during foraging or group movement. Finally, we did not detect any obvious hybrid individuals within the observed mixed-species troops. However, we observed certain rhesus macaque individuals that differed in their tail length and morphology from typical members of their species in Andhra Pradesh, particularly within the distribution overlap region.

Discussion Our study clearly indicates that rhesus macaques have extended the boundaries of their geographical range in southeastern India by ca. 3500 km2 since the last macaque distribution surveys in this part of the subcontinent (Fooden et al. 1981). The southward descent of this typically aggressive species has now led to the

Of Least Concern? Range Extension by Rhesus Macaques

displacement of endemic bonnet macaques from many areas within their original distribution range in peninsular India. When Fooden et al. (1981) examined the interspecific boundary of these 2 species in 19791980, they briefly discussed the invasion of rhesus macaques into the formerly bonnet macaqueoccupied Vijayawada Hills in the state of Andhra Pradesh as a minor oscillation in the otherwise stable and separate geographic distributions of these 2 species. The scenario has certainly changed today. The pace of irrigation development in the basin of the Krishna River has accelerated significantly during the last 30 yr, and several dams and bridges have been constructed across the river (Venot et al. 2008). This has resulted in the development of large swathes of agricultural lands in the Krishna Basin (Guntur district of Andhra Pradesh) that has possibly aided the movement of rhesus macaques south of the river into the Guntur and Prakasam districts of the state. It should be noted that such land-use changes could also facilitate the northward movement of bonnet macaques, which are comparable to rhesus macaques in their ecological adaptability. However, the largescale translocations of rhesus macaques from humanmacaque conflict-prone areas into the dry deciduous forests of Srisailam, coupled with the aggressive temperament of the species, have resulted in the preferential movement of rhesus macaques southward through the Srisailam forests into neighboring areas. We suggest that the movement of rhesus macaques into the formerly bonnet macaquedominated areas in southeastern India has been largely effected by human-induced factors and could constitute a permanent and continuous movement, even today. The contrast in the distribution boundaries of the 2 species in the western and central parts of India further supports this hypothesis. In the moist deciduous forests of western India, the interspecific boundaries run parallel to each other and become separated by a large gap further eastward in the arid regions of central India. It is only in the eastern part of peninsular India that the boundaries converge and form a distinct distribution overlap area. At several locations, we did not locate macaques (ca. 10% of bonnet macaque and 25% of rhesus macaque troops; Table I) that had been definitively reported by our secondary sources. We believe this is not due to any inherent visibility problem with either species because most of these sites were located on plains close to human habitations. Instead, given the extreme crop-raiding propensity of rhesus macaques and that of bonnet macaques to a lesser extent, it is likely that some troops may have remained undetected while foraging in croplands. This could explain why we could not directly sight a greater proportion of rhesus macaque troops. We may have thus underestimated the total number of rhesus macaque troops during our surveys. However, this does not affect our conclusion regarding the displacement of bonnet macaques by rhesus macaques in the distribution overlap region; in fact, in this particular context, it serves to support our hypothesis. The intrusion of rhesus macaques into the bonnet macaque distributional range is significant, both for the reasons behind its occurrence and the consequences of this incursion. Large-bodied primate species typically dominate smaller-bodied species and displace or exclude them from food resources (Strier 2007). This has been clearly documented, e.g., in the interspecific interactions of the Neotropical howlers, capuchins, and muriquis (Dias and Strier 2000). The larger rhesus macaques are more dominant to the comparatively smaller bonnet macaques and typically displace

R. Kumar et al.

them by aggressively driving them away from food sources or preferred habitats (Kumar et al. submitted). The artificial introduction of large numbers of rhesus macaques into bonnet macaque habitats has thus resulted in the latter species being pushed out of its distributional range at a much faster rate than would have occurred naturally, with grave implications for its future survival. In their continuing study on the population dynamics of commensal bonnet macaques, Singh and his co-workers have cautioned about the survival prospects of an apparently hardy, commensal species such as the bonnet macaque, populations of which are decreasing, particularly in the face of conflict with humans (Kumara et al. 2010; Singh and Rao 2004). We suggest that even the habitats of this species are under threat, particularly from invasion by the typically aggressive rhesus macaques. Although the presence of seemingly large populations of bonnet macaques in human-inhabited areas has caused them to be categorized as a Least Concern species (Molur et al. 2003), the species is now virtually locally extinct from many locations earlier reported by Molur et al. (2003), particularly in the state of Andhra Pradesh (Fig. 1), and should perhaps be considered for elevation to the Near Threatened Species category. The rhesus macaquebonnet macaque distribution overlap zone in southeastern India appears to be characterized by the presence of several mixed-species troops. Southwick and Southwick (1983) suggested that anthropogenic factors such as release of captive individuals, provisioning of food, and environmental disturbances as a result of human activities may lead to polyspecific associations among primates. Burton and Chan (1996) opined that although human intervention via the development of agriculture and clearing of primary forests may initiate interspecific interactions among primates, the sustained association between taxa depends on the nature of the interactions between the species involved. Our observations on the interspecific interactions between rhesus and bonnet macaques in the states of Maharashtra and Andhra Pradesh, respectively in the western and eastern parts of the Indian peninsula, support this view (Kumar et al. submitted). All the observed mixed-species troops consisted of a single, or rarely 2, adult individual(s) of one species integrated into a troop of the other species (Kumar et al. submitted). However, in general, we never observed pure troops of the 2 species to associate or display any affiliative behavior toward one another for any significant length of time despite the close proximity of the 2 species in the distribution overlap zone. Given the presence of mixed-species troops across their distribution boundaries, hybridization of rhesus and bonnet macaques appears to be a very real possibility. Researchers have recorded the incidence of interspecific hybrids in many cercopithecine species including macaques (Burton and Chan 1996; Southwick and Southwick 1983). Detwiler et al. (2005) suggested that parapatric hybridization among closely related allotaxa in African cercopithecines, usually a natural process, could be altered by human-induced factors. Hybridization between an introduced species and a native, endemic one could pose a severe threat to the genetic integrity of the latter, as has already been documented for introduced Macaca cyclopis endemic M. fuscata in Japan (Kawamoto 2005) or introduced M. nemestrina native M. mulatta in northern Thailand (Malaivijitnond et al. 2007). However, Fooden (1980) has argued that hybridization between rhesus and bonnet macaques is highly improbable because of the differences in the male and

Of Least Concern? Range Extension by Rhesus Macaques

female reproductive anatomy of the 2 species. Yet, recent studies indicate a possible hybrid origin of Macaca arctoides from proto-M. thibetana/assamensis and proto-M. fascicularis (Tosi et al. 2000, 2003), species that belong to completely different species-groups and differ significantly in their penile morphology (Fooden 1980). Although we did observe certain individuals that could represent morphological hybrids between the 2 species in the overlap region, more detailed morphometric and genetic investigations are required to ascertain whether such individuals merely represent natural variants of the species or are true hybrids. If, however, these individuals do represent interspecific hybrids, this could raise the specter of yet another way in which the existence of an already threatened species could be endangered even further.
Acknowledgments This study was made possible by a fellowship granted to R. Kumar by the Central Scientific and Industrial Research Organisation, Government of India, and the fieldwork was partially supported by a research grant awarded to A. Sinha by the Department of Science and Technology, Government of India, New Delhi. We thank the Forest Departments of the states of Andhra Pradesh and Maharashtra for research permits and their logistic help in the field. We thank M. K. Ganguly, A. K. Ganguly, C. Srinivasulu, M. S. Chaitra, T. R. Shankar Raman, D. Mudappa, D. Chakraborty, and U. Ramakrishnan for their help during the course of this study and R. Raghunath for his help in preparing the figures. Finally, we thank Oliver Schlke and 2 anonymous reviewers for their insightful comments on earlier versions of this article.

References
Bernstein, I. S. (1966). Naturally occurring primate hybrid. Science, 154, 15591560. Bernstein, I. S. (1968). Social status of two hybrids in a wild troop of Macaca irus. Folia Primatologica, 8, 121131. Brandon-Jones, D., Eudey, A. A., Geissmann, T., Groves, C. P., Melnick, D. J., Morales, J. C., et al. (2004). Asian primate classification. International Journal of Primatology, 25, 97164. Burton, F. D., & Chan, L. (1996). Behavior of mixed species groups of macaques. In J. E. Fa & D. G. Lindburg (Eds.), Evolution and ecology of macaque societies (pp. 389412). New York: Van Nostrand Reinhold. Bynum, E. L. (2002). Morphological variation within a macaque hybrid zone. American Journal of Physical Anthropology, 118, 4549. Champion, H. G., & Seth, S. K. (1968). The forest types of India. New Delhi: Government of India Press. Clarke, A. S., & Boinski, S. (1995). Temperament in nonhuman primates. American Journal of Primatology, 37, 103125. Clarke, A. S., Mason, W. A., & Moberg, G. P. (1988). Differential behavioral and adrenocortical responses to stress among three macaque species. American Journal of Primatology, 14, 3752. Cowlishaw, G., & Dunbar, R. I. M. (2000). Primate conservation biology. Chicago: University of Chicago Press. Detwiler, K. M., Burrell, A. S., & Jolly, C. J. (2005). Conservation implications of hybridization in African cercopithecine monkeys. International Journal of Primatology, 26, 661684. Dias, L. G., & Strier, K. B. (2000). Agonistic encounters between muriquis, Brachyteles arachnoids hypoxanthus (Primates, Cebidae), and other animals at the Estaco Biolgica de Caratinga, Minas Gerais, Brazil. Neotropical Primates, 8, 138141. Fooden, J. (1980). Classification and distribution of living macaques. In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 19). New York: Van Nostrand Reinhold. Fooden, J. (1981). Taxonomy and evolution of the sinica group of macaques: 2. Species and subspecies accounts of the Indian bonnet macaque, Macaca radiata. Fieldiana Zoologica, 9, 152. Fooden, J. (1982). Ecogeographic segregation of macaque species. Primates, 23, 574579.

R. Kumar et al. Fooden, J. (1989). Classification, distribution and ecology of Indian macaques. In P. K. Seth & S. Seth (Eds.), Perspective in primate biology (Vol. 2, pp. 3346). New Delhi: Today and Tomorrows Printers and Publishers. Fooden, J. (2000). Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana Zoologica., 96, 1180. Fooden, J. (2006). Comparative review of the fascicularis-group species of macaques (Primates: Macaca). Fieldiana Zoologica., 107, 143. Fooden, J., Mahabal, A., & Saha, S. S. (1981). Redefinition of rhesus macaque-bonnet macaque boundary in peninsular India. Journal of the Bombay Natural History Society, 78, 463474. Fooden, J., & Wu, H. Y. (2001). Systematic review of the Taiwanese macaque, Macaca cyclopis Swinhoe, 1863. Fieldiana Zoologica., 98, 170. Froehlich, J. W., & Suprianta, J. (1996). Secondary intergradation between Macaca maurus and M. tonkeana in South Sulawesi, and the species status of M. togeanus. In J. E. Fa & D. G. Lindburg (Eds.), Evolution and ecology of macaque societies (pp. 4370). New York: Van Nostrand Reinhold. IUCN. (2008). 2008 IUCN red list of threatened species. www.iucnredlist.org (Accessed April 1, 2010). Kawamoto, Y. (2005). NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan. Primates, 46, 203206. Kumar, R., Radhakrishna, S., & Sinha, A. (submitted). Species-specific traits or ecological design? Demography and behaviour of rhesus macaque and bonnet macaque troops in central and southern India. Koyama, N., & Shekar, P. B. (1981). Geographic distribution of the rhesus and bonnet monkeys in westcentral India. Journal of the Bombay Natural History Society, 78, 240255. Krishnan, M. (1972). An ecological survey of the larger mammals of peninsular India. Journal of the Bombay Natural History Society, 69, 469501. Kumara, H. N., Kumar, S., & Singh, M. (2010). Of how much concern are the least concern species? Distribution and conservation status of bonnet macaques, rhesus macaques and Hanuman langurs in Karnataka, India. Primates, 51, 3742. Malaivijitnond, S., Takenaka, O., Kawamoto, Y., Urasopon, N., Hadi, I., & Hamada, Y. (2007). Anthropogenic macaque hybridization and genetic pollution of a threatened population. Natural History, 7, 1123. Molur, S., Brandon-Jones, D., Dittus, W., Eudey, A., Kumar, A., Singh, M., et al. (Eds.). (2003). Status of South Asian primates: Conservation assessment and management plan (C.A.M.P.) workshop report 2003. Coimbatore, India: Zoo Outreach Organization/CBSG-South Asia. Pande, P. (2005). National parks and sanctuaries in Maharashtra (Vol. I and II). Mumbai: Bombay Natural History Society. Pocock, R. I. (1939). Fauna of British India, mammals (vol. I): Primates and carnivora (2nd ed.). London: Taylor and Francis. Prater, S. H. (1971). The book of Indian animals (3rd ed.). Mumbai: Bombay Natural History Society and Oxford University Press. Roonwal, M. L., & Mohnot, S. M. (1977). Primates of south Asia Ecology, sociobiology, and behavior. Cambridge, MA: Harvard University Press. Saha, S. S. (1984). The present southern limit of the rhesus macaque (Macaca mulatta) in peninsular India, specially in the Godavari and the Krishna river basins. In M. L. Roonwal, S. M. Mohnot, & N. S. Rathore (Eds.), Current primate researches (pp. 153165). Jodhpur, India: Zoology Department, Jodhpur University. Singh, M., & Rao, N. (2004). Population dynamics and conservation of commensal bonnet macaques. International Journal of Primatology, 25, 847859. Southwick, C. H., Beg, M. A., & Siddiqi, M. R. (1961). A population survey of rhesus monkeys in villages, towns and temples of north India. Ecology, 42, 538547. Southwick, C., & Southwick, K. (1983). Polyspecific groups of macaques on the Kowloon Peninsula, New Territories, Hong Kong. American Journal of Primatology, 5, 1724. Spillett, J. J. (1966). A report on wild life surveys in south and west India. Journal of the Bombay Natural History Society, 65, 146. Srinivasulu, C., & Nagulu, V. (2001). Status of primates in Andhra Pradesh. ENVIS Bulletin: Wildlife and Protected Areas, 1, 109112. Strier, K. B. (2007). Primate behavioral ecology (3rd ed.). Needham Heights, MA: Allyn and Bacon. Supriatna, J., Froehlich, J. W., Erwin, J. M., & Southwick, C. H. (1992). Population, habitat and conservation status of Macaca maurus, Macaca tonkeana and their putative hybrids. Tropical Biodiversity, 1, 3148.

Of Least Concern? Range Extension by Rhesus Macaques Thierry, B. (1985). Patterns of agonistic interactions in three species of macaque (Macaca mulatta, M. fascicularis, M. tonkeana). Aggressive Behavior, 11, 223233. Thierry, B. (2007). Unity in diversity: lessons from macaque societies. Evolutionary Anthropology, 16, 224238. Tosi, A. J., Morales, J. C., & Melnick, D. J. (2000). Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution, 17, 133144. Tosi, A. J., Morales, J. C., & Melnick, D. J. (2003). Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution, 57, 14191435. Venot, J. P., Sharma, B. R., & Rao, K. V. G. K. (2008). The Lower Krishna Basin trajectory: Relationships between basin development and downstream environmental degradation, IWMI Research Report 125. Colombo, Sri Lanka: International Water Management Institute. Waser, P. M. (1987). Interactions among primate species. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 210226). Chicago: Chicago University Press. Watanabe, K., Lapasere, H., & Tantu, R. (1991). External characteristics and associated developmental changes in two species of Sulawesi macaques, Macaca tonkeana and M. hecki, with special reference to hybrids and the borderland between the species. Primates, 32, 6176. Watanabe, K., & Matsumura, S. (1991). The borderland of possible hybrids between three species of macaques, M. nigra, M. nigrescens, and M. hecki, in the northern peninsula of Sulawesi. Primates, 32, 365369. Watanabe, K., Matsumura, S., Watanabe, T., & Hamada, Y. (1991). Distribution and possible intergradations between Macaca tonkeana and M. ochreata in the borderland of the species in Sulawesi. Primates, 32, 385389.