Lutung, Trachypithecus Barbei (Blyth, 1847)
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Contributions to Zoology, 73 (4) 271-282 (2004) SPB Academic Publishing hv, The Hague The Tenasserim Lutung, Trachypithecus barbei (Blyth, 1847) (Primates: Cercopithecidae): Description of a live specimen, and a reassessment of phylogenetic affinities, taxonomic history, and distribution ³ Thomas Geissmann Colin+P. Groves²Christian Roos ¹, 'Anthropological Institute, Universitdt Zurich-Irchel, Winterthurerstrasse 190, CH-8057 Zurich, Switzer- 2 land, e-mail: [email protected]; School of Archaeology and Anthropology, Australian Na- 3 tional University, Canberra, ACT 0200 Australia, e-mail: [email protected]; Gene Bank of Pri- mates, Primate Genetics, German Primate Center, Kellnerweg 4, 37077 Gottingen, Germany, e-mail: [email protected] Keywords: Trachypithecus barbei; taxonomy; systematics; evolution; genetics Abstract Introduction The Tenasserim lutung Trachypithecus barbei was previously The Tenasserim Lutung, Trachypithecus barbei field known from museum and observations only. specimens (Blyth, 1847) is the least known of all of Asia’s We discovered a zoo specimen and present the first confirmed primates. For instance, the only synthesis ofcolobine evidence for the continuedexistence of the species since 1967. research (Davies and Oates, 1994) mentions T. We describe the cranial pelage and colorationcharacteristics of which We first barbei once and does not infor- this species were previously unknown. present only provide any molecular evidence for recognizing T. barbei as a distinct spe- mation on the species. Likewise, Corbet and Hill cies and forassessing its phylogenetic affinities relative to other (1992) include the species as Semnopithecus incertae members of the We document the taxo- genus Trachypithecus. sedis, and Rowe (1996) does not mention it at all. based nomic history of T. barbei and present a distribution map The is restricted species to a tiny range around on a compilation of all known locality records. o 14°00’-15°15’N, 98 00’-98°25’E on the Burma- Thailand border. It was described by Blyth (1847), him in 1863 in but redescribed a which has Contents by way muddied the waters ever since. On 21 March 2001, TG encountered a leaf mon- Introduction 271 the Materials and methods 272 key at Bangkok Zoo which, to judge by facial Results 273 characteristics, appeared to be a member of the T. Pelage characteristics 273 obscurus group (sensu Groves, 2001, i.e. includ- 273 DNA sequences ing T. obscurus and T. phayrei) but did not fit the Discussion 275 T. description of either T. obscurus or phayrei. The Taxonomic history 275 mammal curator of the Dr. Distribution of Trachypithecus barbei 280 Bangkok Zoo, Yong Affinities 280 Chai, suggested it might be a hybrid between the 281 Acknowledgements two The species. provenance of the animal is un- References 281 it in known; was bought an animal market. Because Appendix: Gazetteer 282 captive leaf monkeys have rarely bred in Asia (TG, Trachypithecus barbei 282 T. 282 pers. observation in numerous zoos), the study ani- phayrei mal is This T. germaini 282 unlikely to be captive bred. leaf mon- T. obscurus 282 key will be referred to as simply “study animal” in the following text. CPG examined the syntypes of Pr(esbytis) barbei Blyth in the Zoological Survey of India, Calcutta, in the early 1980s, and specimens ofThai and Bur- 272 T. Geissmann et al. - The Tenasserim Lulling Lon- the indicated above mese lutungs in the Natural History Museum, performed with same primers as Kit don, in the 1980s and 1990s and in October, 2003. with the Big Dye Terminator Cycle Sequencing (Perkin-Elmer) following the manufacturer’s rec- reactions ommendations. All sequence were run on Materials and methods automated A81377 an sequencer (Perkin-Elmer). Sequences were deposited at Genßankand are avail- To test the phylogenetic relationship of the study able under the accession numbers AYS 19449 - animal to other langurs, CR sequenced a fragment AYS 19463 (see also Table 1). h DNA of the mitochondrial cytochrome gene. was To get a more complete overview on Trachypi- T. data extracted from hair samples i( T. barbei, phayrei thecus evolution, the set was expanded with T. and crepusculus, T. auratus auratus, T. cristatus, homologous sequences from T. pileatus T. geei, germaini, T. francoisifrancoisi, T. vetulus, T. johnii, both deposited at GenBank. Sequence differences mitrata P. comata comata, P. melalophos and S. and distances in the 573 bp long alignment were entellus blood of hector), peripheral lymphocytes (T. estimated by two measures sequence divergence. and obscurus, S. entellus priam and C. guereza) First, the observed proportion of base differences museum skin ( T. phayrei phayrei) by standard me- between taxa was calculated by PAUP 4.0b10 (Swof- al. and Sam- thods as outlined in Walsh et (1991) ford, 1999). Second, a maximum-likelihood (ML) DNA Mini brook et al. (1989) and the QlAamp estimate was obtained with the PUZZLEsoftware, Kit, respectively. A 620 bp long fragment of the version 5.0(Strimmerand Von Haeseler, 1996) with et al., 30.2% 11.7% gene was PCR-amplified (Saiki 1988) using base frequencies (28.9% A, C, G, GA the oligonucleotide primers s’-CTCCTCATT 29.1% T) and a transitiomtransversion ratio (9.11) AACATGAAATAT-3’ and s’-CTTTGTTGTTTG estimated from the data set. The PCR GATTTGTG-3’. resulting products were Phylogenetic tree reconstructions were carried separated on 1% agarose gels and visualized by out using three algorithms: maximum-parsimony ethidium staining. The fragments were excised from (MP) (Fitch, 1971) and neighbor-joining (NJ) (Saitou the gel and the DNA extracted using the Qiagen and Nei, 1987) as implemented in PAUP and maxi- Gel Extraction Kit. Direct sequencing reactions were mum-likelihood, included in PUZZLE. Support of Table I. Origin of samples for the genetic study “a Accession-Nr. Species Origin Institution/Sponsor Accession-Nr. Trachypithecus barbelbarbei - Bangkok Zoo, Thailand AY519462 T. obscurus - Wuppertal Zoo, Germany AYS 19459 T. phayrei phayrei SW-Burma ( ZMB, Germany AYS 19460 T. Vietnam \ Vietnam AY519461AYS 19461 p. crepusculus Vietnam EPRC, Vietnam T. francoisifrancoisi francoisifruncoisi - Bristol Zoo, Great Britain AYS 19458 T. cristatus - Singapore Zoo, Singapore AYS 19456 T. germaini - Bangkok Zoo, Thailand AY519457AYS 19457 T. auratus auratus - Bristol Zoo, Great Britain AYSAY51945519455 - AF294626 T. pileatus - GenBank T. geei - GenBank AF294618AF2946I8 T. johnii - Erfurt Zoo, Germany AYS 19453 T. vetulus - Bristol Zoo, Great Britain AY519454AYS 19454 AYS 19452 Semnopithecus entellus priam - Krefeld Zoo, Germany AYS 19452 S. entellus hector Nepal DPZ, Germany AYS 19451 Presbytis comatacomata comata - Howletts Zoo, Great Britain AYS 1944919449 P. melalophos mitrata - Howletts Zoo, Great Britain AY519450AYS 19450 - Colobus - Munich AYS 19463 guereza Zoo, Germany "Abbreviations: ZMB; Zoologisches Museum der Humboldt Universitat Berlin; EPRC; Endangered Primate Rescue Center, Cue Phuong National Park; DPZ; Deutsches Primatenzentrum. - 2004 Contributions to Zoology, 73 (4) 273 The general color of the study animal is grayish black with no silvering, and only slightly lighter ventrally (Fig. la). The tail is dark gray, slightly paler than the body. The root of the tail and the area around the ischial callosities are whitish. The long, upright crown hair forms a distinct crest. The face is with violet gray a tinge. The animal has the whitish eye-rings fully encircling the eyes and a mouth depigmented area on the typical ofleaf mon- of the T. obscurus keys group. With the possible exception of some aspects of facial pigmentation, the study animal closely fits the original description of T. barbei (Blyth, 1847) and the coloration of the syntypes of T. barbei (as summarized in Groves, 2001). It differs from T. obscurus in that (Fig. lb) the legs and the crown are not contrastingly paler than the body. It differs from T. in the absence of phayrei any brownish or It further differs from buffy pelage. T. p. phayrei in the absence of contrastingly light underparts, from T. p. crepusculus (Fig. 1c) in the presence of large white and from both eyerings, T. p. crepusculus and T. shanicus p. in its much darker overall col- oration. It differs from members of the T. cristatus group in exhibiting light face markings (although there can be a area round the mouthand lighter gray eyes in T. one species, germaini). and from T. germaini Id), the (Fig. only species of the group occurring Fig. I. characteristics of the Photographs showing pelage (A) in Thailand, in the much darker overall coloration study animal, i.e. Trachypithecus barbei (Bangkok Zoo, Thai- and the absence of long, light circumfacial hair. land); (B) T. obscurus (Zurich Zoo, Switzerland); (C) T. phayrei crepusculus (EndangeredPrimate Rescue Center, Cue Phuong, Vietnam) and (D) T. germaini (Bangkok Zoo). Photographs by TO. DNA sequences In order to elucidate the of internal branch lengths was either determined by phylogenetic position the study a 573 bootstrap analyses (MP and NJ) performed with animal, bp long fragment of the mitochondrial b 1000 replications or indicated by the ML quartet cytochrome gene was sequenced from a number of langur and puzzling support values (1000 puzzling steps). species phylogeneti- cally analyzed. Pairwise difference analyses within Trachypithe- Results cus revealed that T. barbei is different in 4.4 - 16.4% other to species of the genus (Table 2). The lowest characteristics differences of the Pelage study animal to other Trachy- pithecus