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Taxonomy of the Bornean Slow Loris, with New Species Nycticebus Kayan (Primates, Lorisidae) ∗ RACHEL A

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Taxonomy of the Bornean Slow Loris, with New Species Nycticebus Kayan (Primates, Lorisidae) ∗ RACHEL A American Journal of Primatology 75:46–56 (2013) RESEARCH ARTICLE Taxonomy of the Bornean Slow Loris, With New Species Nycticebus kayan (Primates, Lorisidae) ∗ RACHEL A. MUNDS1 ,K.A.I.NEKARIS2, AND SUSAN M. FORD3 1Department of Anthropology, University of Missouri Columbia, Columbia, Missouri 2Department of Anthropology and Geography, Oxford Brookes University, Oxford, Great Britain 3Department of Anthropology, Southern Illinois University, Carbondale, Illinois More species of nocturnal primates are now recognized than in the past, because many are cryptic species. Subtle morphological disparities, such as pelage pattern and color variation, vocal cues, and genetics have aided in elucidating the number of diagnosable species in a genus. The slow lorises (genus Nycticebus) once included only two species, but recent taxonomic studies resulted in the description of three additional species; further incompletely explored variability characterizes each of the currently described species. The Bornean loris in particular is characterized by pelage and body size variation. In this study, we explored facemask variation in the Bornean loris (N. menagensis). Differing facemask patterns, particularly influenced by the amount of white on the face, significantly clustered together by geographic regions, separated by notable geographic boundaries. Our results support the recognition of four species of Bornean lorises: N. menagensis, N. bancanus, N. borneanus, and N. kayan. Genetic studies are required to support these findings and to refine further our understanding of the marked variability within the Bornean loris populations. Am. J. Primatol. 75:46–56, 2013. C 2012 Wiley Periodicals, Inc. Key words: Nycticebus menagensis; Nycticebus bancanus; Nycticebus borneanus; cryptic species; morphology; sympatric, allopatric INTRODUCTION tissue, highly subtle morphological cues, and dis- Technological advances have improved our agreements on what defines a species [Bradley and knowledge about the diversity of several nocturnal Mundy, 2008; Isaac et al., 2004; Tattersall, 2007]. mammals; many of these nocturnal mammals in- Here we examine morphological and geographic vari- clude cryptic species that were falsely lumped to- ation in the Bornean slow loris [Nycticebus mena- gether as one species [Bickford et al., 2006]. With gensis, Lydekker, 1893]. A small taxonomic study on a better understanding of what differentiates these species-level differences in N. menagensis done pre- cryptic mammals, new species have been recognized viously found diversity within this species [Nekaris [Bearder, 1999; Jacobs et al., 2006; Munshi-South, and Munds, 2010], but no thorough investigation of 2006; Yoder et al., 2000]. Additional species have intraspecific variation has been conducted to date. been distinguished by their unique calls [Bearder, Contract grant sponsor: Systematics Research Fund of the Lin- 1999; Jacobs et al., 2006; Niemitz, 1984], others by naean Society; Contract grant sponsor: Primate Conservation variation in sexual anatomy [Anderson, 2000], or Inc.; Contract grant sponsor: International Animal Rescue In- subtle and obvious pelage variations [Bearder, 1999; donesia; Contract grant sponsor: Royal Society; Contract grant sponsor: Primate Society of Great Britain; Contract grant spon- Bradley and Mundy, 2008; Carraway and Verts, sor: Primate Conservation Inc.; Contract grant sponsor: Primate 2002; Ford, 1994], and the increased use of genetics Action Fund; Contract grant sponsor: Margot Marsh Biodiver- has resulted in the exponential recognition of new sity Foundation; Contract grant sponsor: SYNTHESYS Project (European Community Research Infrastructure Action, FP6 species [Chen et al., 2006; Merker et al., 2010; Yo- “Structuring the European Research Area” Programme); Con- der et al., 2000]. Although the number of recognized tract grant number: NL-TAF-3491. ∗ species of primates has more than doubled in the Correspondence to: Rachel A. Munds, Department of Anthro- past 25 years and our understanding of what defines pology, 107 Swallow Hall, University of Missouri, Columbia, MO a species has improved, some species, particularly 65203, USA. E-mail: [email protected] the nocturnal ones, remain hidden to science. Many Received 09 April 2012; revised 13 July 2012; revision accepted 19 July 2012 compounding variables contribute to the poor under- standing of these species: difficulty of distinguishing DOI 10.1002/ajp.22071 Published online in Wiley Online Library (wileyonlinelibrary. between allopatric species, inability to collect genetic com). C 2012 Wiley Periodicals, Inc. Bornean Loris Taxonomy / 47 Until recently, the genus N. ycticebus Boddaert tographs and museum specimens of N. menagensis, 1785 comprised two species, the pygmy loris (N. pyg- we hope to reveal a greater diversity within this maeus) and the polytypic slow loris (N. coucang), species than originally presumed. We propose that, which consisted of four subspecies [Groves, 1971]. as in other Bornean mammals and nocturnal pri- Only in 1998 was one of the subspecies of N. cou- mates, morphological disparities differentiate mul- cang recognized as a distinct species (N. bengalensis) tiple taxa within the N. menagensis group. [Groves, 1998]. More than a decade after the first split in the original N. coucang, the three remain- ing subspecies of N. coucang (N. javanicus, N. mena- METHODS gensis, N. coucang) have been elevated to species Twenty-three photographs and twenty-seven level, based on genetic and morphological research museum specimens of N. menagensis were examined [Nekaris et al., 2008; see also Chen et al., 2006; for facemask differences. This sample included the Ravosa, 1998; Roos, 2003]. More taxonomic research type specimens for the subspecies N. coucang ban- is required, as there is clear variation within each of canus (= N. menagensis bancanus) and N. coucang the currently recognized slow loris taxa [Groves and borneanus (= N. m. borneanus), as well as specimens Maryanto, 2008; Nekaris and Jaffe, 2007; Nekaris that have been designated as topotypes of N. cou- and Munds, 2010]. cang menagensis (= N. m. menagensis, whose type Nycticebus menagensis is found on the island of skin is missing; [Timm and Birney, 1992]). Unfortu- Borneo, some of the small Philippine islands to the nately,wehavebeenunabletolocatethetypeofN. northeast of Borneo, and some small islands to the m. philippinus. Requirements for using images and southwest of Borneo. Historically, four subspecies specimens were: a color image (photographs); gen- have been recognized across this region: N. m. ban- eral locale is known either by museum tag or per- canus, N. m. borneanus, N. m. menagensis, and N. m. sonal communication from photographer or source philippinus. These distinctions were not only based stating where image was photographed; a clear view on distinct pelage characteristics, but also body size of the facemask; and a clear view of the top of differences with adult body weights (in the same sea- the head (crown). Features analyzed included those son) ranging from 265–610 g (based on museum spec- shown elsewhere to provide meaningful discrimina- imens), with reports of up to 800 g from animals tion between slow lorises [Nekaris and Jaffe, 2007; rescued from trade. Across Borneo and on the small Nekaris and Munds, 2010]. These included 13 fea- islands, slow lorises are actually scarce, with what tures clustered into four groups based on cranial re- may be a disjunct distribution; as field studies are gion: (1) Circumocular patch traits (patch top, pres- still lacking, no overlap between subspecies is known ence of eye rim, eye rim color, patch middle, patch [Nijman and Nekaris, 2010; Wells et al., 2004]. bottom); (2) Interocular stripe traits (width, shape); Slow lorises are found in a multitude of habitats (3) Crown traits (crown and fork shape, ear fur cov- from heavily degraded to pristine rainforests, plan- erage, preauricular hair width); and (4) Miscella- tations, and lowland and montane forests [Nekaris neous traits (mask color, nose color, black and white et al., 2008; Thorn et al., 2008; Wiens and Zitzmann, “shade” in a black and white image) [Nekaris and 2003]. Although they are most common at an alti- Jaffe, 2007; Nekaris and Munds, 2010]. A guide was tudinal limit of approximately 1000 m asl [Thorn created for future researchers to replicate or expand et al., 2008, some Bornean specimens in museum col- upon this study easily (see Appendix A). A complete lections come from about 1300 m, and in Java, they list of the 27 museum specimens examined is in- are found at nearly 1500 m]. The Bornean slow loris cluded in Appendix B. We were granted permission is listed as vulnerable by the IUCN. Habitat loss and from the listed museums to study their collections the illegal wildlife trade are affecting their survival for this project. We adhered to the American Society = [IUCN 2010; Nekaris and Nijman 2007]. In addi- of Primatologists principles for the ethical treatment tion, Borneo has lost a third of its forest in less than of primates. 25 years [Rautner and Hardino, 2005]. Much pheno- Of the original 13 features, only eight showed typic variation has been detected within N. mena- variation across the sample of Bornean lorises. Thus gensis [Nekaris and Munds, 2010], and studies are we used the following features in further analyses: needed to determine if this variation differentiates two Circumocular patch traits (patch top, patch bot- additional discrete taxa, as such research would as- tom); two Interocular
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