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:
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 species were detected to T. obscurus and
1 shows characteristics of the T. - Figure pelage study p. phayrei (4.4 4.5%) and are even higher than
other animal and of species of the genus Trachy- those observed between the three members of the pithecus. T. cristatus group (T. cristatus, T. germaini and T. 274 T. Geissmann et al. - The Tenasserim Lutung
an
and
17 0.237 0.241 0.245 0.235 0.233 0.220 0.220 0.226 0.243 0.239 0.255 0.235 0.249 0.260 0.241 0.242 - model HKY 16 0.227 0.2160.216 0.217 0.230 0.235 0.196 0.211 0.207 0.225 0.220 0.220 0.218 0.222 0.222 0.033 - 0.188 the
15 - with 15 0.2250.225 0.2250.225 0.2310.231 0.234 0.250 0.210 0.226 0.221 0.240 0.235 0.235 0.222 0.232 0.237 0.031 0.188
14 0.210 0.1990.199 0.203 0.209 0.227 0.197 0.202 0.198 0.089 0.089 0.087 0.108 0.108 - 0.188 0.178 0.2020.202 corrected
- 13 0.192 0.184 0.192 0.230 0.235 0.202 0.204 0.194 0.0710.071 0.067 0.098 0.033 0.098 0.183 0.176 0.194 distances
12 0.201 0.198 0.196 0.216 0.220 0,2030.203 0.208 0.206 0.075 0.071 0.102 - 0.031 0.098 0.178 0.175 0.185 ML
are
11 0.200 0.194 0.202 0.230 0.235 0.205 0.220 0.200 0.065 0.065 - 0.093 0.089 0.080 0.187 0.176 0.199 diagonal 10 0.183 0.185 0.183 0.231 0.217 0.182 0.187 0.183 0.007 - 0.061 0.066 0.063 0.082 0.1870.187 0.176 0.188 the
9 0.182 0.189 0.182 0.230 0.216 0.182 0.187 0.177 - 0.007 0.061 0.070 0.066 0.082 0.190 0.180 0.192 above
8 - 8 0.083 0.077 0.087 0.106 0.097 0.032 0.044 0.148 0.152 0.164 0.168 0.159 0.162 0.178 0.168 0.180 differences,
7 - 7 0.079 0.087 0.083 0.110 0.101 0.036 0.042 0.155 0.155 0.178 0.169 0.166 0.1660.166 0.182 0.171 0.176 observed 6 0.071 0.077 0.079 0.106 0.101 - 0.035 0.031 0.152 0.152 0.167 0.166 0.164 0.1620.162 0.171 0.161 0.176 are
5 0.114 0.106 0.097 0.089 0.093 0.093 0.0890.089 0.176 0.176 0.188 0.178 0.187 0.183 0.1970.197 0.187 0.185 0.114 0.106 0.097 diagonal
4 - 0.114 0.106 0.097 0.082 0.096 0.099 0.096 0.185 0.185 0.185 0.175 0.183 0.171 0.187 0.183 0.187 the * - 0.102 taxa. 3 - Below 0.045 0.038 -0.089 0.089 0.089 0.073 0.077 0.080 0.152 0.152 0.166 0.161 0.157 0.163 0.185 0.175 0.192 - 0.097 - 0.177 - 0.033 - 0.242 1. - 0.108 -0.237 9.1 monkey - 2 0.047 0.037 0.0960.096 0.096 0.072 0.080 0.072 0.157 0.154 0.162 0.152 0.164 0.182 0.175 0.190 - 0.047 - 0.038 - 0.036 - 0.044 - 0.007 0.161 - 0.033 position. of leaf - 0.065 per ratio I1 - 0.045 0.044 0.103 0.103 0.066 0.073 0.077 0.152 0.152 0.164 0.164 0.157 0.I7I0.171 0.182 0.182 0.187 analysed (4) (16) (5) 8) substitutions (3) (8) (15) among ( (13) (14) mitratamitrata (2) crepusculus francoisifrancoisi (7) phayrei (6) auratus (9) 12) priam hector comata (17)(17) 1) transitiomtransversion ( ( (11) Distances (10)10) a represent barbei obscurus phayrei phayrei chstatuscristatus germaini entellus entellus comatcomata melalophos guereza barbel phayrei phayrei francoisifrancoisi germaini auratus pileatus geei T. johniijohnii vetulus 2. T. geeil T. T. T. T. T.T T. T. T. T. T. T. T. S.5. S. P. P. C. Values Table estimated > Contributions to Zoology, 73 (4) - 2004 275
- in the a. auratus) (3.1 4.2%). The two analyzed subspe- of Ye”, the collection of Asiatic Society of
cies of T. and T. Calcutta. He it to “Pr. phayrei ( T. p. phayrei p. cre- Bengal, compared Phayrei” pusculus) differ in 8.9% which is as unexpected as and “Pr. obscurus”, distinguishing it by having
the extremely high difference detected between four
of T. “no in species Trachypithecus (T. geei, pileatus, T. vertical crest, as the former; nor is the oc- johnii and T. vetulus) and all the other species of cipital hair lengthened and conspicuously paler, as
the - the latter group (14.8 18.8%). Interestingly, invariably in the latter species: the shoulders and
3.1 - 9.8% from the four species differ only in two outside of the arm are silvered in both specimens;
the hector members of genus Semnopithecus (S. e. and underparts resemble thoseof Pr. obscurus. The
and S. e. priam). The two analyzed species of Pres- tail is very slightly paler than the body; whereas in
andP. differ in 3.1%. twelve adults of bytis (P. c. comata m. mitrata) Pr. obscurus... the tail is in every
All three tree reconstruction methods revealed one much paler than the body. The size of the full
the same topology and differed only by bootstrap grown animal is also considerably inferior to that
or puzzling support values (Figure 2). The analyzed of Pr. obscurus, and perhaps a little exceeds that
langur species are divided in three significantly of Pr. Phayrei. In the female specimen, there is a
clades with the Pres- white the interior base supported one containing two space at of the thigh, more
the Semno- the bytis species, one two representatives ofi developed on one side than on other. The pale
T. T. T. the pithecus as well as geei, pileatus, johnii markings of face resemble those of Pr.
and T. vetulus (in the following named Indian clade) obscurus....”
Tra- and finally, a clade with all the remaining
animal. The Yet all chypithecus species including the study was not quite clear, because in a footnote
the three clades however are he added that the taxidermist who relationships among prepared the skins
not significantly supported (57 - 89%), although a was positive that they had“a thin raised crest” when
is indicated. fresh. Then sixteen Trachypithecus clade grouping years later he (Blyth, 1863)
Within the Indian clade, the relationships among changed the type locality to the interior of Tippera
the species are not well resolved. There is strong Hills (now Tripura, northeastern India), and altered
T. support, however, for a S. e. priam/ vetulus and the description, stating that the face is totally black.
T. T. of a geei/ pileatus clade. The Trachypithecus clade Thus began a century and a half confusion.
consists for three significantly supported major Apart from brief descriptions by Anderson(1881)
them. and Blanford both of groups with unresolved relationships among (1888), whomaccepted Blyth’s
of T. cristatus altered the next One comprises all members the group (1863) account, important mention
who ( T. cristatus, T. germaini and T. a. auratus), a sec- was by Wroughton (1917), figured the head
ond and and a of “the and stated that “the evidence one T. p. crepusculus T. f.francoisi, type”, seems
third T. and to me conclusive that barbel to the section one including T. obscurus, p. phayrei belongs of which have the hair T. barbei. The reconstructed trees allow no clear langurs laid straight back
from the forehead the resolution of the relationships among the latter three over crown” (p.47). The photo-
of species, however, although NJ and ML algorithms graph (which is the male syntype, as verified by
of T. and who examined in the indicate a sister grouping obscurus T.p. CPG, lutung types Zoologi-
phayrei. cal Survey of India in 1978) shows an animal with
a totally black face.
Pocock (1928) accepted Blyth’s alterations of
Discussion 1863, apparently mainly because “the Rev. J.
Barbe... is known to have collected in Chittagong
and the Hills” Taxonomic history Tipperah (p.668), and consequently
used the barbei senior for name as a synonym mela-
“ the northernmost of what he Blyth (1847:34) described “Pr. Barbei nobis, merus, subspecies called
Pithecus a in which he n.s.?” from an adult male and female presented by pyrrhus, species placed
the Rev. J. Barbe, from “the Tenasserim Province almost all mainland Southeast Asian lutungs (in- 276 T. Geissmann et al. - The Tenasserim Lulling
Fig. 2. 50%-majority rule consensus trees for a) the maximum-
parsimony, b) the neighbor-joiningand c) the maximum-like-
lihood algorithms. Numbers on nodes indicate bootstrap or
quartet-puzzling support values. In the maximum-likelihoodtree,
branch substitutions lengthsare drawn according to the number of
per position, with the bar indicating 0.1 substitutions per site.
eluding cristatus, germaini, ohscurus and phayrei). He specified that the skin of the lips and chin is
he At the same time, described a new subspecies, black. Four other specimens were identified with
with Ye the from the Mt. Nwa- atrior, type locality Forest, “in island the new subspecies; one foot of
of Moulmein in Ataran tail and the Division of Tenasserim”, labo, Tavoy (a little grayer on the under-
as follows (p.673): side than the type), one from 14°25’N, 98°45’E,
east of Tavoy but in Thailand (slightly grizzled on
“A very dark form nearly uniformly coloured deep, the head, tail and elsewhere), one from “Maw to
brown all the Lai” and of unknown dusky over upper parts and the out- Maw (sic), Thailand, one
side of the legs, with less sheen on the hairs; but locality.
the outer side of the about the el- A few the author reconsidered arms, especially years later, same
is bows, paler than the shoulders and back. The some of his taxonomic lumping, dividing South-
under side is dark, dusky grayish brown. The tail east Asian langurs into Presbytis and Trachypithecus is at most only slightly paler than the body.” and, within the latter, recognizing obscurus and Contributions to Zoology, 73 (4) - 2004 111
distinct from He noted that phayrei as species pyrrhus (Pocock, the eyelids are in fact pale in the
He 1935). referred atrior to T. as a sub- female but that dirt and pyrrhus skin, exposure may have species, and corrected its type locality from “the altered their color in the male; and suggested that
island of Moulmein” “100 miles S. ofMoulmein” white hairs to may have fallen off the lips of both it the (making apparently exact same locality as skins. He also revealed that the skulls of both speci-
Some of the other localities also the barbei). were mens were present in collection, though unmen-
in different to tioned given slightly form; according Napier by Blyth. Relegating barbei to the status of
(1985), the correct localities, with approximate coor- subspecies under Presbytis cristatus, he diagnosed dinates, are as follows: foot of Mt. Nwalabo, it as follows: ca,14°0rN, 98°25’E; H. Maw Tee Maw (= Huai
Menam Mothimo), I4°31’N, 98°38’E; Noi, “... distinguished from all other races the ... by
I4°25’N, and 98°45’E the absence 98°51’E; 14°25’N, (in general of silvering of the pelage which at
Sai Yoke The coordinates of Ye are the most is area). approx. very faintly visible towards the foreparts
15°15’N, 98°E. Mt. are in of Ye and Nwalabo Burma, the dorsal surface in some skins, by the tail (es- the other three in Thailand. are pecially towards the tip) being appreciably paler
Hill (1936) described the types of barbei in de- than the dorsal surface, and also by the general colour tail. The body hairs are buff at the base and black being somewhat paler.”
in the distal half; the shoulders and arms are lighter,
and the fore- He Pocock’s atrior “probably grey originally” (p.107), placed as a junior synonym, darken the the and it arms again; legs, especially shanks, gjive a range “from Tippera, East Pakistan, are also paler. The hands and feet are black. A few to Tenasserim and adjoining parts of Siam” (Kha- white hairs were present near the lips and round juria, 1955:98). the confirm whether nares, but he was unable to In 1967, Foodcn (1971) collected what he called
im- there were pale areas on the facial skin: “It is Presbytis cristatus at three localities in Kancha-
in possible these old skins to find the exact amount naburi, including Pocock’s locality of Menam Noi of skin pigmentation present. As far as the face is (correctly Ban Huai MaenamNoi), describing them
the concerned, however, there is no indication that as “dark brownish-gray to blackish” (p.41), lack-
round the mouth was than the defined whitish area eyes or any paler ing “large sharply mouth patch” the of both rest of the face” (Hill, 1936:108). He recom- P. phayrei and P. obscurus (but, by impli- mended keeping barbei as a distinct species within cation, having the white eye-rings?). the restricted to the and genus Trachypithecus, probably In 1974 1977 Eudey (1979) observed two
type locality which he seemed to accept as being different species of lutung in Huay Kha Khaeng the Tippera Hills. Game Sanctuary, about I5°27’-30’N, 99°15’-19’E.
The considered third time Pocock with matter was a by One, “brown, reddish-brown, gray or black”
and (1939), whonow relegated both barbei Blyth, 1847 dorsal pelage lacking facial patches, she iden-
the tified cristata. (with type locality Tipperah) and melamerus to as Presbytis The other, more com-
and had olivaceous synonymy of Trachypithecus phayrei phayrei, mon, “pale gray, gray or grayish- continued to use the name T. pyrrhus atrior (syn- black” color, with “gray faces with distinctive white
Tenas- mouth the onym probably barbei Blyth, 1863) for the patches, although mouth patch appeared
serim This he that in the be in one the lutung. time, specified to pale (gray) group”; degree of ex-
of the but in the of white type atrior eyelids are cut away, pression eye patches was variable, mainly
other “have a livid, between as was the of BM(NH) specimens they yel- groups, presence a crown
lowish crest. She hue” (p. 143). provisionally identified this langur as
Khajuria (1955) considered the matter in detail. Presbytis phayrei. He examined Blyth’s syntypes, now in the Indian Agrawal (1974) was the first to notice that Blyth’s
with 1863 corrections based information Museum, Calcutta, and noted that they agree were on not
.1. Hlyth’s 1847 description except that the faces are- from the Rev. Barbe but from a Mr. M. Barbe,
1863 black, and thus concur with his description. but he made nothing of this fact. Instead, he trav- 278 T. Geissmann et al. - The Tenasserim Lulling
eled and collected four ofwhat and has little around the to Tripura specimens patch very paling eyes (see
lie P. the correctly identified as phayrei, apparently Groves, 2001). We should add that eye-patches
which he found there. He that to include white only lutung argued appear pigment or possibly a re-
his with new specimens agreed Blyth’s original flective layer (usually, at any rate), whereas the
with (1847) description, but not the specimens la- mouth patch seems to be a simple depigmentation
beled as syntypes (now in the Zoological Survey of variable extent and intensity. But whether T.
of so that these latter be labeled barbei has facial is unclear: of India), must wrongly any markings the
and that, being from Tcnasserim, they represent P. Calcutta syntypes the male has a jet-black face, while
cristatus atrior Pocock, while P. barbei is the female has a synonym only pale eyelids (Khajuria, 1955).
of P. phayrei. Hill (1936) and Khajuria (1955) both warned against
Given their disagreement, Khajuria and Agrawal deducing original skin pigmentation from preserved
combined forces and reexamined the material of dirt and presumed syn- museum (because exposure,
in the of three types together presence colleagues according to Khajuria), and Khajuria and Agrawal
(Khajuria and Agrawal, 1979). They concluded that (1979) noted the influence of preservative chemi-
the the they were indeed syntypes, clincher being cals. Wroughton (1917) was informed by the di-
the asymmetrical white patch on the inside of the rector of the Indian Museum that the male syntype
thigh of the female skin. As for the color of the had been “mounted and exhibited for the last 70
the white have been lost because face, parts may years”, and during this time it is not unlikely that
of preservative chemicals (they had been lost in the facial skin had not only faded but been repainted.
of P. We remark that similarly preserved specimens obscurus). They may repainting was apparently
noted 1847 again that Blyth’s locality was based routinely done to faded or otherwise “unsatisfac-
on information supplied by Rev. J. Barbe, and had tory” specimens. For instance, the type of Eriodes
been in 1863 the evidence of informa- the changed on hemidactylus (in Paris Museum; a synonym of
tion supplied by Mr. M. Barbe, and “as such, we the northern woolly spider monkey Brachyteles
in are not sure whether this change the locality was hypoxanthus, a species characterized by its mottled
based and on factual information”, recommended face) was repainted black, and the type of Gorilla search in a thorough Tenasserim as well as in Tripura castaneiceps (a plaster bust in the Academy of
(in case it did occur there, hav- Natural of really despite not Sciences, Philadelphia; a synonym the
ing been found by Agrawal (1974)). They recom- western gorilla. Gorilla gorilla gorilla, but purported
P. mended provisionally accepting barbei as a full to be distinguished by its red topknot) was like-
species, and noted that except for the color of the wise repainted completely black.
which is doubtful “it lips, anyway, approximates None of the type series of Pocock’s atrior seems
cristatus atrior from Presbytis Tenasserim”. ever to have been mounted on public display, so
From all it evident this, seems that a black lutung facial repainting can probably be ruled out although lives in a small area of far western Thailand and and discoloration fading by preservatives presum-
Burma. The adjoining parts of earliest name for ably cannot. CPG paid particular attention to evi- this is taxon barbei Blyth, 1847 (synonym atrior dence of facial colouring during his examination
Pocock, 1928); pelage characters alone distinguish of the skins in 2003; the mouth in all of them is it from its T. obscurus and T. and the but both absolutely neighbors tightly sewn up lips are shriveled, phayrei, which arc strikingly particolored, and T. the Sai Yoke and Mt. Nawlabo skins have clear germaini, which has a spangled pelage with long indications of depigmentation around the mouth but
and it be be pale cheek-whiskers, can recognized as a not a sharply demarcated patch such as can made distinct species of isolated affinities. out in preserved skins of T. obscurus and Tphayrei, There remains the question of facial depigmen- while all of them definitely did have depigmented tation. obscurus Trachypithecus and T. phayrei have eyelids.
conspicuous white a eye-patches and large white Fooden’s (1971) descriptions are unclear: his patch around the mouth, extending up to the base specimens lacked a “large sharply defined whitish ofthe while T. lacks the white nose, germaini mouth mouth patch”, but perhaps had the white eye-rings. - Contributions to Zoology, 73 (4) 2004 279
of four in and central Fig- 3- Distribution range Trachypithecus species the southern parts of Burma Thailand.
Black circles: localities for Trachypithecus barbei.
- - - BURMA: I Ye Forest, Ataran Division; 2 Nwalabo Taring (= Mt. Nwalaboo). THAILAND: 3 Khao Yai, Huay Kha Khaeng
Game Reserve; 4 - Ban Kerng Chada; 5 - Ban Tamrong Phato; 6 - Phlu, Khao; 7 - Ban Huai Maenam Noi, and Huai Mothimo (= H. Maw Tee Maw).
Open circles: localities for T. phayrei.
- - BURMA: 1 - Lampha; 2 Mulayi Taung. THAILAND: 3 - Mae Sot; 4 - Ban Mae Lamao; 5 - Tha Chang Tai; 6 Ban Pong Nam - - Rong; 7 Khlung, Khlong; 8 - Ko Keow; 9 - Wong, Nam Mae, 40 mi E ofUm Pang; 10 Wong, Nam Mae, 53 mi E ofUrn Pang; 11
- - Ban Pak Nam Pho; 12 - Phetchabun; 13 - Kata Taek; 14 Ban Muang Baw Ngam; 15 - Chongkrong; 16 - Khao Kamphaeng; 17
- Lat Bua Khao.
Squares: localities for T. germaini. THAILAND; - - - 1 Khao Yai, Huay Kha Khaeng Game Reserve; 2 Lat Bua Khao; 3 Pak Chong, Sathani; 4-“Siam”, 13°45', 99°25';
5 - “Siam”, 13°40', 99°25'; 6 - Phachi, Mae Nam; 7 - Nakhon Pathom; 8 - Tahkamen, BangPakong R.
Triangles: localities for T. obscurus.
BURMA: 1 - Tavoy. THAILAND: 2 - Phet Buri. 280 T. Geissmann et al. - The Tenasserim Lulling
the in Eudey (1979), however, described animals which data were available various previous reports.
both mouth- and From this becomes that the distribution usually had eye-patches, but some- it clear range times the or is indeed somewhere between eye rings were missing poorly expressed; extremely restricted,
2 if the considering the variability of their pelage, as well 10,000 and 12,000 km (possibly larger spe-
it is cies’ extends north- and/or This as the easterly locality (see next section), pos- range southwards).
distribution of sible that the population is affected by gene-flow may be the smallest range any Tra- from T. phayrei, but even so the constant occur- chypithecus species. Because species with small
Di- rence of the white mouth patch is noteworthy. distribution areas are more vulnerable than species rect observations of live animals represent the most with large distribution areas, and because the range
of of the Indo- reliable information on the presence or absence of T. barbel is located in the centre the light mouth patch. Because the mouth patch is Burmese region - a biodiversity hotspot which has
in lost 95.1% consistently present, but not “sharply defined”, already of its primary vegetation (Mitter- all observations made of live T. barbei so far, it is meier et ah, 1999; Myers et ah, 2000) - an evalu- equally possible that this characteristic is typical ation of the species’ conservation status should of the species. urgently be carried out.
Trachypithecus barbei is evidently a species
has white and which, usually at any rate, eye-rings
ill-defined a somewhat white mouth patch. The Affinities
Bangkok animal has both these features extremely
Tra- well developed. Because it was previously unknown whether
chypithecus barbei has pale face markings around
the the eyes and around mouth, the affinities of the
rela- Distribution of Trachypithecus barbei species remained controversial, and a close
obscurus and the tionship to both the T. group T.
barbei The type locality of both Presbytis Blyth, cristatus group were suggested (e.g. Groves, 2001).
1928 1863 and Pithecus pyrrhus atrior Pocock, is The examination of our study animal reveals that
the Ye, Tenasserim. The distribution is limited to a small white facial markings are present though the
of area far western Thailandand adjoining parts of mouth patch is not sharply demarcated, suggesting
obscurus Burma, between about 14° and 15°30’N and from a closer affinity with the T. group than
in the with the T. the Bay of Bengal as far east as 98°30’E cristatus group. northern of the and 99°E in the southern data show that the ani- end range Our genetic clearly study
To T. T. obscurus end. the north occurs T. phayrei, to the south mal belongs to the group (represented obscurus. to the southeast T. germaini. Fooden by T. obscurus and T. p. phayrei) and not to the T.
cristatus T. T. (1976, Fig. 4) mapped these species’ ranges (in- group (represented by cristatus, ger- cluding them all in Presbytis), but included both T. mainiand T. a. auratus). The molecular differences barbei under between T. barbei and T. obscurus/T. and T. germaini Presbytis cristatus. p. phayrei
In Fooden’s the three localities - are in the same those between map, westernmost (4.4 4.5%) range as
in T. of “cristatus” (localities 13, 14 and 18 his ear- other closely related species such as vetulus and lier publication (Fooden, 1971)) represent T. barbei. S. e. priam (3.1%), T. cristatus, T. germaini and T.
They have been depicted as such in our Fig. 3. a. auratus (3.1 - 4.2%) or P. c. comata and P. m.
The Huay Kha Khaeng Reserve, where T. barbei mitrata (3.1%). Hence, our findings support rec-
be affected from is of the Tenasserim may by gene-flow T. phayrei, ognition lutung ( T. barbei) as a well to the east of Ye, and not far southwest of distinct species (Khajuria and Agrawal, 1979;
Kata Taek, one of Fooden’s (1976) localities for T. Groves, 2001). phayrei, and not far northeast of Fooden’s locali- Besides the clarification of the phylogenetic po- ties 15 and 16 for the same species. sition of T. barbei, the molecular genetic study re-
This for first time study the accurately assesses vealed further interesting insights into the evolu-
T. T. the geographical distribution of barbei, although tion of Asian colobines such as the parapyhly of Contributions to 73 - 2004 Zoology, (4) 281
phayrei or the close of T. T. Minimal relationship geei, change for a specific tree topology. Syst. Zool.
20: 406-416. pileatus, T. johnii and T. vetulus to members of the
Foodcn J. 1971. Report on primates collected in western genus Semnopithecus. Although the results are Thailand January-April, 1967. Fieldiana. Zool. 59: 1-62. contrary to general reflect morphology, they very Fooden J. 1976. Primates obtained in peninsular Thailand well the distribution pattern of the species. Maybe with notes June-July, 1973, on the distribution of conti- the paraphyly of T. and of phayrei Trachypithecus nental Southeast Asian leaf-monkeys (Presbytis). Primates
in genera] can be explained by ancient hybridiza- 17: 95-118.
Groves C. 2001. Primate tion events between of T. taxonomy. Washington, DC: Smith- ancestors p. phayrei and sonian Institution Press. the T. francoisi group and between Trachypithecus Hill WCO. 1936. Note on Barbe’s leaf-monkey {Trachy- and Semnopithecus, respectively. This hypothesis pithecus barbei Blyth). Proc. Zool. Soc., London 1936: still remains be tested. to 105-109.
H. Khajuria 1955, incorrectly dated as 1954. Notes on the
of systematics three leaf-monkeys in the collection of the
Indian Museum (Zool. Surv.), Rec. Indian Mus. 52: 95- Acknowledgements 99.
Khajuria H, VC. Agrawal 1979. On the types of Presbytis We thank the following people for providing samples for the barbei Blyth. Primates 20: 317-319. genetic part of this study: Tilo Nadler (EPRC, Cue Phuong MittermeierRA, Myers N, Gil PR, Mittcrmcier CG. 1999. National Ernie Thetford (Howletts Alexander Sliwa Park), Zoo), Hotspots: earth's biologically richest and most endan- (Wuppertal Zoo), Chai Manfred Ade Yong (Bangkok Zoo), (ZMB terrestrial gered ecoregions. Cemex, Conservation Inter-
Julia von Maltzan Dressen Berlin), (Munich Zoo), Wolfgang national & Agrupacion Sierra Madre, Mexico. (Krefeld Zoo), Bryan Caroll (Bristol Zoo), Monika Melcher Myers- N, Mittermeier RA, Mittermeier CG, da Fonseca (Erfurt Zoo), Thomas Ziegler Primate and (German Center) GAB, Kent J. 2000. Biodiversity hotspots for conserva- Guha Biswajit We are to Hans Zischler (Singapore Zoo). grateful tion priorities. Nature 403: 853-858.
for discussions and and Vincent for helpful support, to Nijman PH. 1985. Napier Catalogueofprimates in the British Museum reading and commenting upon our manuscript. and (Natural History) elsewhere in the British Isles. Part
HI: family Cercopithecidae, subfamily Colobinae. Lon-
don: British Museum (Natural History).
Pocock RI. 1928. The References langurs, or leaf monkeys, of British
India. Part II. J. Bombay Nat. Hist. Soc. 32: 660-677.
Pocock RI. 1935. The of the Pithecus monkeys generae (or VC. 1974. Agrawal Taxonomic status of Barbe’s leaf mon- Pres t is) and by Pygathrix found to the east of the Bay of key, Presbytis barbei Blyth. Primates 15: 235-239. Proc. Zool. Bengal. Soc., London 1934: 895-961. Anderson J. 1881. Catalogue of Mammalia in the Indian Pocock Rl. 1939. The Fauna of British India, including Museum, Calcutta. Parti. Primates, Prosimiae, Chiroptera, and Burma: Ceylon Mammalia. Vol. I. Primates and and Insectivora. Calcutta: Trustees of the Indian Museum. Carnivora (in part), families Felidae and Viverridae. Blanford WT. 1888. The fauna of British India, including London: Taylor and Francis. Ceylon and Burma: Mammalia. Part I: Introduction, Rowe N. 1996. The pictorial guide to the living primates. Primates, Carnivora and Insectivora. London: and Taylor East Hampton, New York: Pogonias Press. Francis. Saiki RK, Gelfand Stoffel DH, S, Scharf SJ, Higuchi R. Blyth E. 1847. Supplementary of the curator of the report Horn Mullis GT, KB, Erlich HA. 1988. Primer-directed Zoological Department of the Asiatic of Society Bengal. ofDNA enzymatic amplification with a thermostable DNA J. Asia!. Soc. Bengal. Calcutta 16: 728-737. polymerase. Science 239: 487-491. Blyth E. 1863. Catalogue of the mammalia in the Museum Saitou N, Nei M. 1987. The neighbor-joining method: A of the Asiatic Society of Calcutta: Asiatic Bengal. Society new method of reconstructing phylogenetic trees. Mol. of Bengal. Biol. Evol. 4: 406-425. Corbet GB, Hill JE. 1992. The mammals of the Indomalayan Sambrook Friteh Maniatis J, EF, T. 1989. Molecular clon- region: A systematic review. Oxford: Oxford University ing: A laboratory manual. Cold Spring Harbor, NY: Cold Press. Spring Harbor Laboratory Press. Davies AG, Oates JF. (cds.) 1994. Colobine monkeys: Their Strimmer K, Von Haeseler A. 1996. Quartet puzzling: A ecology, behaviour and evolution. Cambridge : Cambridge maximum likelihood method for reconstructing tree to- University Press.
pologies. Mol. Biol. Evol. 13: 964 - 969. A. 1979. and Eudey Differentiation dispersal of macaques Swofford DL. 1999. PAUP*: phylogenetic analysis using (Macaca spp.) in Asia. Davis, CA: University of Califor-* and other parsimony (* methods), Version 4. (Sinauer nia, PhD thesis. Associates, Sunderland). I'itch WM. 1971. Toward the course of evolution: defining Walsh PS, DA, R. 1991. Chelex Metzger Higuchi 100 as 282 T. Geissmann et al. - The Tenasserim Lutung
a medium for simple extractipon of DNA for PCR-based 1971, and 1, p,42 Fig. locality 15; Fooden, 1976, p. 112).
typing from forenscic material. BioTechniques 10: 506- Ban Pak Nam Pho, Nakhon Sawan, 15°43', 100°09' (Fooden,
513. 1976, p. 112).
RC. Scientific results from Wroughton 1917. the mammal Ban Pong Nam Rong, Kamphaengphet, 16°20', 99° 15' (Fooden,
No. XV. J. Nat. Hist. Soc. 25; 40-51. and survey. Bombay 1971, p.42 Fig. 1, locality 5; Fooden, 1976, p. 112).
Chongkrong, Kanchanaburi, 14°41', 98°52' (Fooden, 1971, Received: 5 February 2003 p.42 and Fig. I, locality 16; Fooden, 1976, p.112).
Accepted: 11 March 2004 Kata Taek, Uthai Thani, 15°28', 99°23' (Fooden, 1971, p.42
and Fig. 1, locality 10; Fooden, 1976, p. 112).
Khao Kamphaeng,Seeswad = Si Sawat, Kanchanaburi, 14°37',
99° 18' (Pocock, 1935, p.959; Napier, 1985, p.67). Appendix: Gazetteer Khlung, Khlong, Kamphaengphet, 16°05', 99°20' (Fooden,
1976, p. 112; Napier, 1985, p.67). Coordinates and references for localities shown in the distri- Ko Keow, Kamphaengphet, 15°57', 99°26' (Fooden, 1971,
bution 2, map, Fig. and p.42 Fig. 1, locality 8; Fooden, 1976, p. 112).
Lat Bua Khao, Nakhon Ratchasima, 14°52', 101 °36' (Fooden, Trachypithecus barbei 1976, p. 112; Napier, 1985, p,67). BURMA: Mae 98°34’ Sot, Tak, 16°43’, (Fooden, 1976, p. 112). Nwalabo (= Ml. Nwalaboo), Disk, Taung Tavoy Tenasserim, Phetchabun, Phetchabun, 16°25', 101 °08' (Elliot, 1909, cited 98°25' ca. 14°01', (Pocock, 1928, p.673; Fooden, 1976, in Fooden, 1976, p. 112; Napier, 1985, p.67).
p. 113; Napier, 1985, p.55). Tha Tai, Tak, 99°03' Chang 16°51', (Fooden, 1976, p. 112). Ye Forest, Ataran Division, Tenasserim, 15° 15', 98°00' (type Wong, Nam Mae, 40 mi (=65 km) E of Um Pang, Nakhon of barbei and atrior locality ; Blyth, 1847, p.734; Pocock, 99°10' Sawan, ca. I5°55', (Fooden, 1976, p. 112; Napier, 1928, Fooden, p.673; 1976, p. 113; Napier, 1985, p.55). 1985, p.68).
THAILAND: Wong, Nam Mae, 53 mi (=85 km) E of Um Pang, Nakhon Ban Huai Maenam Noi Yoke (Menam Noi), Sai area, 99°25' Sawan, ca. 15°55', (Fooden, 1976, p. 112; Napier, Kanchanaburi, 14°25’, 98°51’ (Fooden, 1971, and p.39 1985, p.68).
Fig. I, locality 18; Fooden, 1976, p. 113; Napier, 1985,
p.55). T. germaini
Ban 98°3T Kerng Chada, Kanchanaburi, 15°08', (Fooden, THAILAND:
1971, p.39 and Fig. 1, locality 13; Fooden, 1976, 13). p.l Khao Yai, Huay Kha Khaeng Game Reserve, 15°28', 99°I9' Ban Tamrong Phato, Kanchanaburi, 14°54', 98°31' (Fooden, (Eudey, 1979, p.l04). 1971, p.39 and Fig. 1, locality 14; Fooden, 1976, p.l 13). Lat Bua Khao, Nakhon Ratchasima, 14°52', 101 °36' (Kloss, Huai Mothimo H. Maw Tee Sai Yoke ca. (= Maw), area, 1919, cited in Fooden, 1976, p.l 13). 0 14°25', 98 51' (Napier, 1985, p.55). Nakhon Pathom, Nakhon Pathom, 13°49', 100°03' (Pocock, Khao Yai, Huay Kha Khaeng Game Reserve, 15°28', 99°19' 1935, p.935; Fooden, 1976, p.l 13). (Eudey, 1979, 104). p. Pak Chong, Sathani, Nakhon Ratchasima, 14°42', 101 °25' Maw Tee Maw, see Huai Mothimo. (Fooden, 1976, p.l 13). Menam Noi, Sai Yoke area, ca. 14°25’N, 98°51’E (Napier, Phachi, Mae Nam, Rat Buri, ca. 13°25', 99°25' (Gairdner, 1985, p.55). 1914, cit. in Fooden, 1976, p.l 13).
Moulmein, 100 miles S. of, see S.W. Siam, Sai Yoke area. “Siam”, 13°40', 99°25' (Gairdner, 1914, cit. in Napier, 1985, Phlu, Khao, vicinity, headquarters Sai Yoke camp, area, P-56).
Kanchanaburi, ca. I4°25', 98°45' (Pocock, 1928, p.6V3; “Siam”, 13°45', 99°25' (Gairdner, 1914, cit. in Napier, 1985, 1976, 13; 1985, Fooden, p.l Napier, p.67). P-56). Siam, S. Sai Yoke area, I4°25’N, 98°45’E (Napier, 1985, Tahkamen, Bang Pakong R., between Pachim and Kabin, p.55). Chachoengsao, 13°33', 100°58' (Pocock, 1935, p.936;
Fooden, 1976, p.l 13; Napier, 1985, p.56). T. phayrei
BURMA: T. obscurus
Tenasserim, 16°18', 98° 19' Lampha, (Napier, 1985, p.67). BURMA:
16° Mulayi Taung (Dawna Range), Tenasserim, 1198°32' of Tavoy (mouth Tavoy R.), Tavoy Disk, Tenasserim, ca. (Napier, 1985, p.67). 13°45', 98° 17' (Pocock, 1939, p.I4l; Fooden, 1976, p.l 13; THAILAND: Napier, 1985, p,64). Ban Mae Lamao, Tak, I6°48‘, 98°45' (Fooden, 1971, p.42 THAILAND:
and Fig. 1, locality 4; Fooden, 1976, p.l 12). Phet Buri, vicinity, Phet Buri, ca. 13° I O', 100°00' (Gardner, Ban Muang Baw Ngam, Kanchanaburi, 14°55', 98°55' (Fooden, 1914, cit. in Fooden, 1976, p.l 14, Pocock, 1935, p.945).