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A New Species of Dwarf Lemur (Cheirogaleidae: Cheirogaleus Medius Group) from the Ankarana and Andrafiamena-Andavakoera Massifs, Madagascar

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A New Species of Dwarf Lemur (Cheirogaleidae: Cheirogaleus Medius Group) from the Ankarana and Andrafiamena-Andavakoera Massifs, Madagascar Primate Conservation 2016 (30): 59–72 A New Species of Dwarf Lemur (Cheirogaleidae: Cheirogaleus medius Group) from the Ankarana and Andrafiamena-Andavakoera Massifs, Madagascar Cynthia L. Frasier1, Runhua Lei1, Adam T. McLain2, Justin M. Taylor1, Carolyn A. Bailey1, Azure L. Ginter1, Stephen D. Nash3,4, Richard Randriamampionona5, Colin P. Groves6, Russell A. Mittermeier4 and Edward E. Louis Jr.1,5 1Grewcock Center for Conservation and Research, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE, USA 2Department of Mathematics and Sciences, State University of New York Polytechnic Institute, Utica, NY, USA 3Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA 4Conservation International, Arlington, VA, USA 5Madagascar Biodiversity Partnership, Manakambahiny, Antananarivo, Madagascar 6School of Archaeology and Anthropology, Australian National University, Canberra, ACT, Australia Abstract: A new species of dwarf lemur, Cheirogaleus shethi sp. nov., of the C. medius group is described from the dry and transitional forests of northern Madagascar. This species can be found along the forest corridor from Ankarana Special Reserve east to the Analamerana Special Reserve down to the Bekaraoka forest in the Loky-Manambato Protected Area. This species is genetically distinct from other members of the C. medius species group and is sister to a poorly known lineage in Sambava. The identification of this new species highlights the importance of northern Madagascar as a reservoir of biodiversity. Key Words: Dwarf lemurs, primate, Strepsirrhini, taxonomy Introduction the scientific literature, both supportively by those who view it as justified and critically by those who do not (Thalmann Dwarf lemurs (Cheirogaleidae: Cheirogaleus) are small, 2007; Tattersall 2007, 2013). A combination of factors has led arboreal, nocturnal strepsirrhine primates endemic to the to controversy about species status in dwarf lemurs. The arbo- island of Madagascar (Groves 2000; Lei et al. 2014). The real and nocturnal habits of Cheirogaleus make them difficult genus Cheirogaleus has recently been the focus of in-depth to study in the wild. Additionally, the small number of avail- field research combined with genetic analyses that revealed able museum specimens and their spottily documented collec- greater species diversity within this genus than previously tion localities often limit their utility. Based on morphology, suspected (Groves 2000; Hapke et al. 2005; Groeneveld et al. Groves (2000) recognized seven species of Cheirogaleus: C. 2009, 2010; Thiele et al. 2013; Lei et al. 2014, 2015). Field major É. Geoffroy Saint-Hilaire, 1812; C. medius É. Geoffroy expeditions undertaken from the Ankarana Special Reserve Saint-Hilaire, 1812; C. crossleyi Grandidier, 1870; C. adipi- (SR) east to the Analamerana SR have resulted in the iden- caudatus Grandidier, 1868; C. sibreei (Forsyth Major, 1896); tification of a distinct dwarf lemur in this region (Lei et al. C. ravus Groves, 2000; and C. minusculus Groves, 2000. 2014). This lineage was recognized previously (Hapke et al. Groeneveld et al. (2009) subsequently synonymized C. ravus 2005; Thiele et al. 2013) and is described here as a new spe- into C. major, and C. adipicaudatus into C. medius. Groves’ cies, although with a slightly different circumscription than (2000) specific delimitation can, however, now be seen as initially suggested (Thiele et al. 2013). overly conservative based on recent fieldwork and genetic Taxonomic expansion has occurred in other lemur genera, research (Hapke et al. 2005; Groeneveld et al. 2009, 2010; in particular Microcebus and Lepilemur (Louis et al. 2006a, Thiele et al. 2013; Lei et al. 2014, 2015). Lei et al. (2014, 2006b, 2008; Rasoloarison et al. 2013; Hotaling et al. 2016). 2015) proposed four new species, including the recently The proliferation of new lemur species has been addressed in described Cheirogaleus andysabini Lei et al., 2015, and 59 Frasier et al. resurrected C. thomasi (Forsyth Major, 1894) (corresponding Madagascar, Sambava and Bekaraoka. The individuals from in large part to C. adipicaudatus). Thiele et al. (2013) also Sambava were placed as sister to those from Ankarana and described a new species, C. lavasoensis, bringing the current Bekaraoka, and all were identified as C. medius. Thiele et al. number of accepted species to eight. It is likely that other spe- (2013) also expanded the dataset with the inclusion of genetic cies remain to be described, with an ever-growing enumera- data from dwarf lemurs in southern Madagascar. Although tion presented in the “Species groups of Cheirogaleus” sec- they did not supplement the northern dataset, additional ana- tion of Lei et al. (2014; pp.17−22). Gardner and Jasper (2015) lytical tools were applied in Thiele et al.’s work (2013) that reported a possible new Cheirogaleus lineage from the island also supported the sister relationship of Sambava to Beka- of Nosy Hara in northern Madagascar. raoka within the C. medius group. The Ankarana individual Hawkins et al. (1990) mentioned a dwarf lemur in Anka- (Hapke et al. 2005; Groeneveld et al. 2009, 2010) was not rana Special Reserve in northern Madagascar and referred to included, possibly due to missing data. Thiele et al. (2013) it as “Cheirogaleus ? medius.” They suggested trapping to recognized that dwarf lemurs in the Sambava (subgroup clarify the species' identification, as it could also have been CmeA) and Bekaraoka (CmeB) area of Madagascar repre- C. major. Hapke et al. (2005) incorporated a genetic sample sented a separate lineage and gave it the interim designation from Ankarana that was taken from the Collection des speci- of Cheirogaleus sp. Bekaraoka Sambava (CmeA+CmeB). mens morts, Parc Botanique et Zoologique Tsimbazaza in Multiple field expeditions from the Ankarana SR east Antananarivo. The Ankarana species was confirmed to be a to the Analamerana SR, crossing through the Andrafiamena- member of the C. medius group (designated CmeB in that Andavakoera Protected Area augmented the Cheirogaleus study, GenBank accession number AY605904), but Hapke et dataset (Lei et al. 2014). In this study, genetic data grouped al. (2005) hinted that this individual may be a member of an individuals from Ankarana and Bekaraoka into one clade; independent lineage based on genetic distance, but did not the lineage was identified as a probable new species of dwarf propose designating it as such. Groeneveld et al. (2009, 2010) lemur (C. sp. nov. 4, Fig. 1). Individuals from Sambava were expanded the dataset with additional samples from northern excluded from C. sp. nov. 4, and were referred to as Confirmed Figure 1. Subtree of the phylogenetic relationships between taxa within the Cheirogaleus medius group based on cytb sequence data as presented in Lei et al. (2014; Fig. 2). Numbers on branches represent maximum likelihood values followed by posterior probability support. Tip labels include locality, followed by number of individuals carrying the haplotype in brackets, then the locality numbers. 60 New species of dwarf lemur Candidate Species (CCS) 7, but more information is required Loky-Manambato region and the Andrafiamena Classified to confidently describe the CCS7 lineage (Leiet al. 2014). Forest (Mittermeier et al. 2010; Salmona et al. 2014). The Ankarana SR covers more than 18,000 ha in north- Genetic samples, measurements and photographs of sev- ern Madagascar and is about 108 km southwest of the large eral Cheirogaleus individuals captured along the Ankarana- port city of Antsiranana. Ankarana was established in 1956, Andrafiamena-Analamerana corridor were obtained prior to and first explored widely in the 1960s (Wilson et al. 1988). their release (Fig. 2). The genetic samples were analyzed as A plateau of limestone dating to the Jurassic Period, caves part of a larger phylogenetic study of the genus Cheirogaleus and underground rivers, and deciduous tropical forests are the conducted by Lei et al. (2014) including pre-existing data most notable geographic features of the reserve (Rossi 1974a; from Bekaraoka (Groeneveld et al. 2009). Together, they were Fowler 1989). The cave systems of Ankarana have been fea- determined to be consistently distinct from all other samples tured in popular writings and documentaries as a wonder of of the C. medius group and designated as C. sp. nov. 4 (Lei et the natural world (Wilson 1990). Ankarana displays great al. 2014). Here, we describe this new species of dwarf lemur diversity in birds (Fowler et al. 1989) and cave-dwelling endemic to the Ankarana-Andrafiamena-Analamerana corri- marine life (Gurney 1984; Palacios-Vargas and Wilson 1990; dor and the Loky-Manambato region in northern Madagascar. Banister 1994; Wilson 1996), as well as primates (Wilson et al. 1995). In addition to Cheirogaleus, Ankarana SR is home Methods to populations of the lemur genera Avahi, Daubentonia, Eul- emur, Hapalemur, Lepilemur, Microcebus, Phaner, and Pro- Sampling and morphology pithecus (Wilson et al. 1988, 1989, 1995). Subfossil remains See Lei et al. (2014) for a comprehensive list of locali- of several extinct lemur species (Archaeolemur, Babakotia, ties and numbers of individuals that were represented in the Megaladapis, Mesopropithecus, Pachylemur, Paleopropithe- most recent genus-wide study of Cheirogaleus. Here, we enu- cus), as well as two genera still extant elsewhere in Mada- merate only those belonging to the C. medius group along gascar but now extinct locally (Indri indri, Prolemur simus), with individuals
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