domingo, 12 de abril de 2015



[Mammalogy • 2015] Macaca leucogenys | White-cheeked Macaque • A New Macaque Species from Modog, southeastern Tibet

A hairy-necked Macaca leucogenys youngster
Image: Mr. Cheng Li/Tibet Forestry

We describe a newly discovered Macaca species from the Modog, in southeastern Tibet, China, Macaca leucogenys sp. nov or the “White-cheeked Macaque”. Based on 738 photos taken during direct observations and captured by camera traps this new species appears to be distinct from the Macaca sinica species group. Moreover, the species is distinguished from all potential sympatric macaque species (M. mulatta, M. thibetana, M. assamensis, and M. munzala) in exhibiting a suite of pelage characteristics including relatively uniform dorsal hair pattern, hairy ventral pelage, relative hairless short tail, prominent pale to white side- and chin-whiskers creating a white cheek and round facial appearance, dark facial skin on the muzzle, long and thick hairs on its neck, and a round rather than arrow-shaped male genitalia. This new macaque species was found to exploit a diverse set of habitat types from tropical forest at 1395 m, to primary and secondary evergreen broad-leaved forest at 2000 m, as well as mixed broadleaf-conifer forest at 2700 m. Its range may extend to neighboring counties in Tibet and the part of southeastern Tibet controlled by India. The white-cheeked macaque is threatened by illegal hunting and the construction of hydropower stations. Discovery of this new primate species further highlights the high value for biodiversity conservation of southeastern Tibet and calls for more intensive surveys, studies, and environmental protection in this area. 
Keywords: new species; Macaca leucogenysM. thibetanaM. assamensisM. munzala; Southeastern Tibet
Southeastern Tibet (a part of this area is controlled by India called Arunachal) is a biodiversity-rich area located at the junction of the Eastern Himalaya and Indo-Burma region, a global biodiversity hotspot [Myers et al., 2000]. The area consists of a diverse series of ecosystems from alluvial grasslands and subtropical broadleaf forests to alpine meadows above the tree line at an altitudinal range of 150–6000 m above sea level. In China, the two macaque species present in this area have long been referred to as Macaca assamensis assamensis and M. mulatta [Mammals in Tibet, 1986]. Recently, Indian primatologists reported the existence of M. thibetana in this area [Kumar et al., 2005] and in 2005 described a new macaque species (M. munzala) in the Tawang and Kameng districts (Cuona County in China) [Chakraborty et al., 2007; Mishra & Sinha, 2008; Sinha et al., 2005]. In 2005, a dark macaque skin collected by R. Suresh Kumar was identified as M. thibetana [Kumar et al., 2005] despite the fact that the known range of M. thibetana is located more than 1000 km to the east (Fig. 1). The specimen was described as exhibiting fur that was “dark chocolate brown dorsally with a long thick pelage that extended over all the limbs, while the peripheral hairs, indicative of the ventral region of the body, were pale and whitish” [Kumar et al., 2005: 1387].
Figure 1. Map showing the rough distribution range of each species or subspecies of Macaca in southeast Tibet.

M. munzala is reported to be sympatric with M. assamensis pelops in Tawang and Kameng but usually lives in high altitude forests between 2000 and 3500 m above sea level [Sinha et al., 2005; Fig. 1]. Molecular analyses support M. munzala as a distinct species and indicate its close phylogenetic relationship with M. assamensis, M. thibetana, and M. radiata [Chakraborty et al., 2007]. Therefore, southeastern Tibet appears to represent a region of high macaque diversity, with possibly four species present [Kumar et al., 2005; Fig. 1]. However, recently Biswas et al. [2011] questioned the species status of M. munzala. These authors argued that macaques in this area show great diversity in tail length, pelage color, facial skin color, and facial and hair patterns, and therefore M. munzala could represent a subspecies of M. assamensis. Thus, the taxonomy of macaques in this region remains unclear.
In order to clarify the species status and diversity of macaques in Southeastern Tibet, in 2013 and 2014 we combined direct field observations and photographs obtained from camera traps to survey the macaque population in this region. Camera traps represent a time- and labor-efficient method of data collection that has been used widely to survey mammalian diversity and behavior. Camera traps are increasingly used in primate field studies, especially in the case of unhabituated elusive terrestrial primates [Boyer-Ontl & Pruetz, 2014; Pebsworth & LaFleur, 2014]. In southeastern Tibet, macaques live in dense tropical or subtropical evergreen forests, travel across mountainous terrain, and spend a considerable amount of time foraging on ground. Given the difficulties of following unhabituated groups, we used photographs obtained from camera traps, to compare pelage characteristics of the local macaque populations. When we encountered a macaque group, we attempted to take additional photographs or videos of all individuals.
In total, we obtained 738 photos of macaques from Modog (Fig. 1). However, the population we observed and photographed exhibited pelage and body characteristics unlike any other known macaque species. Here, we describe the morphological characteristics of this macaque population and propose that it represents a new species, Macaca leucogenys or the white-cheeked macaque. In our analysis, we compare M. leucogenys with potentially sympatric macaque species (M. thibetana, M. a. assamensis, M. a. pelops, and M. mulatta). Due to ethical concerns regarding killing wild primates, we did not obtain a voucher specimen for the proposed new species. Rather, we describe M. leucogenys based on hundreds of photographs, similar to the method used by Sinha et al. [2005] in describing M. munzala and Jones et al. [2005] did for Lophocebus kipunji. Article 73.1.4 of the International Code of Zoological Nomenclature allows for the designation of photographs as type specimens [Polaszek et al., 2006]. We also provided first-hand, but preliminary, information about its ecology.
Order Primates Linnaeus, 1758
Superfamily Cercopithecoidea Gray, 1821
Family Cercopithecidae Gray, 1821
Genus Macaca Lacépède, 1799

Macaca leucogenys Species Novum || WHITE-CHEEKED MACAQUE

Figure 5. Facial skin becomes darker and darker, and pale side-whiskers become more prominent with age (A, B: infants; C: juveniles with different age; D: adult female; E: adult male in the right, adult female in the left and two small juveniles). There are virtually no dark hairs on the face of adults. These photos also show light ventral coloration and long and thick hairs on the neck.

Holotype: An adult male, photographed by camera traps (Figs. 4A, 5E, 6A and B). This male was photographed and videoed resting during an undisturbed grooming bout in which more than three group members groomed him.
Paratypes: Two adult females photographed by the same camera trap captured the holotype. One is the female in Fig. 4B (photographed on January 24, 2014). The other female is present in Fig. 5D and E (photographed on January 28, 2014). The holotype and two paratypes are likely members of the same group because they were photographed by the same camera trap. Members of this group included one adult male (holotype), three adult females (two paratypes and one other female), at least eight subadults or juveniles, and one infant. Subdults and juveniles were distinguished by less prominent side-whiskers. We are trying to obtain live specimens so that they can be observed and studied in an appropriate facility and when they die, their skins, skulls, and skeletons will be deposited at Dali University.
Type locality: Gangrigebu (29°28′19.73″N, 95°49′25.00″E, 2410 m above sea level), Modog County, Tibet, China.
Diagnosis: The white-cheeked macaque is robust, heavyset with a relatively short tail. The species can be morphologically distinguished from all other known Macaca species, especially potential sympatric species by a suite of characteristics including relatively uniform dorsal pelage, hairy ventral pelage, relative hairless short tail, prominent pale to white side- and chin-whiskers creating a white cheek and round facial appearance, dark facial skin on the muzzle, and long and thick hairs on neck (Table II). Adults emit high-pitched alarm calls in the presence of humans (Fig. 2). Moreover, there is no inflection between the glans penis and shaft and the glans looks like a ring (based on three photos from only one adult male) rather than exhibiting a sagittate shape which is characteristic of the sinica species group of macaque.
Figure 9. Photos showing differences between Macaca leucogenys and three potential sympatric macaque specie. Macaca mulatta is not shown because it can be easily differentiated from M. leucogenys by the different color of dorsal pelage. M. a. pelops is not shown because it has a generally similar pelage pattern with M. a. assamensis but has a longer tail.
A and B [cited from Sinha et al., 2005]: M. munzala lacks side- and chin-whiskers. C (female) and D (male): Macaca assamensis assamensis has prominent chin whiskers but side whiskers are less prominent creating a triangular face. Hairs on its ventral part and neck are thin and short. E (female) and F (male): Macaca thibetana has prominent side- and chin-whiskers creating a round facial appearance, but it has thin and short hair on neck and has a shorter tail.
 Cheng Li, Chao Zhao and Peng-Fei Fan. 2015. White-cheeked Macaque (Macaca leucogenys): A New Macaque Species from Modog, southeastern Tibet. American Journal of Primatology. (Am. J. Primatol.) DOI: 10.1002/ajp.22394
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