BiologicalJournal of the Linnean Society (1996), 59: 327-350. With 4 figures
The Asian Colobinae (Manunalia:
Cercopithecidae) as indicators of Quaternary
clim.atic change
DOUGLASBRANDON~ONES
Department
if Palaeontology, Natural History Museum, Cromwell Road, London, SW7 SBD
Received 21 March 1995, acceptedfor publication 22 March 1996
A reappraisal of the zoogeography and systematics of Asian colobines demonstrates marked
discontinuities in their distribution. The Bornean proboscis monkey is separated by Sumatra from its sole
congener on the Mentawai Islands. /}gathrix species have a discontinuous distribution at the range limit
of the Asian Colobinae. The existence in the Himalayas of some disjunct relatives of the south Indian
fauna, has obscured a wider disjunction in which for example, the hooded black leaf monkey,
Semnopithecusjohnii, has one subspecies in southern India and another in north Vietnam. A closely related
Vietnamese leaf monkey is a subspecies of the otherwise Indonesian S. auratus. Presbytis comata is disjunct
between westJava, northern Sumatra and northern Borneo. The Mentawai Islands P. potenziani is closely
related. Biogeographic parallels imply a common cause and previous continuity across the intervening
areas. The only wholly compatible explanation is that the disjunct areas alone retained adequate
moisture and temperature to support their endemic biota during a cool drought. That not only genera,
but species are disjunct, indicates such conditions prevailed recently, and are probably attributable to the
Pleistocene glaciations. The supposition that its maritime climate shielded Asian rainforest from the
glacial drought known to have partially deforested Africa and South America, is inapplicable to the
Indian subcontinent, and ignores the climatic effects of the emergence of the Sunda and the Sahul
shelves. Such known influences, the distribution of drought indicator plants, fossil plants and fossil
mammals, grassland birds and freshwater fish, and the anatomical specializations of Nasalis confirm the
instability of the Asian environment. The absence of endemic representatives of certain primates in
north Sumatra implies the occurrence of two cold droughts. Available evidence appears to correlate the
deforestations with the abrupt curtailment of glacial Stages 7 and 5, at about 190000 years BP and about
80000 years BP. The greater significance of climatic than topographical barriers in delineating the
Oriental zoogeographic region, and a rapid speciation rate, is implied. Morphological change is
evidently generated by geographic dispersal, rather than geographic isolation.
© 1996 The Linnean Society of London
ADDITIONAL KEY WORDS: - biogeography - dispersal - glaciation - Pleistocene - rainforest speciation - Sunda shelf
CONTENTS
Introduction .
Taxonomic arrangement
The zoogeography of the Asian colobines
Parallels in Oriental biogeography .
Relic populations
An explanation for the existence of relic populations
Corroborative evidence for climatic change
Evidence indicating a second deforestation
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© 1996 The Linnean Society of London
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D. BRANDON:JONES
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Chronology . .
Conclusion
Acknowledgements
References .
Appendix . . .
INTRODUCTION
Primates are probably zoogeographically the best documented of all animals,
alongside birds and butterflies. One of the dominant mammalian groups in tropical
environments, their conspicuousness and relative ease of identification often enable
reports unsubstantiated by scientific specimens to be included in investigations of
their geographic distribution. The specialized cellulose dietary requirement of the
Old World monkey subfamily Colobinae subjugates the constituent genera to
fluctuations in the geographic distribution of their respective food plants. Evidence of
alterations in colobine distributions is therefore a potential indicator of alterations in
vegetational distributions. The Asian Colobinae range from 90S in the Malay
archipelago to 35°N in Pakistan, a geographic distribution approximating that of the
Oriental zoogeographic region. Within this area the distributions of the principal
colobine taxa are associated with those of at least three distinct vegetational zones.
A reappraisal of their zoogeography and systematics demonstrates marked
discontinuities in the distribution of closely related Asian colobines. These
disjunctions are shared with other fauna and flora, but cannot be explained by
existing physical constraints on dispersal. Climatic change appears to supply a
consistent explanation for the disjunctions. They can be identified as relics of
formerly continuous populations whose partial elimination is attributable to
increased aridity during successive Pleistocene glaciations.
TAXONOMIC ARRANGEMENT
The Asian colobine classification outlined by Brandon-jones (1984), and
elaborated by Brandon-jones (1993, 1995, 1996a), is here employed (see Table 1).
Semnopithecus is commonly treated as congeneric with Presby tis, chiefly owing to the
supposed intermediate position of Presbytis potenriani. Recent research (BrandonJones, 1993) has shown that its principal 'intermediate' characters were the result of
misallocation and misrepresentation of key diagnostic features. The reality is that the
distinctions between the two genera are certainly of a greater magnitude than, for
example, those that separate the Eygathrix subgenera, Eygathrix and Rhinopithecus. This
has been appreciated in a recent primate classification (Groves, 1993), which
advocated further subdivision, elevating the Semnopithecus subgenus, Trachypithecus to
generic status.
THE ZOOGEOGRAPHY OF THE ASIAN COLOBINES
The proboscis monkey, Nasalis larvatus is restricted to Borneo (Fig. 1). The only
other extant species of the genus, Nasalis concolor, is endemic to the Mentawai Islands,
Indonesia (Fig. 1) with no generic representative on the intervening island of
ASIAN COLOBINES AS CUMATIC INDICATORS
329
Sumatra. This restricted and disjunct distribution exists despite, at any rate by
colobine standards, the exceptional aquatic ability of Nasalis larvatus. The proboscis
monkey swims well, using a powerful dog paddle, with the head held well above the
water. An adult male was captured swimming across the mouth of the Sapagaya
river in Sabah, Malaysia, where the river is a quarter of a mile or more wide. When
a boat came alongside, the animal dived and remained submerged so long that the
occupants of the boat began to fear for its welfare (Davis, 1962). Harrisson (in Napier
& Napier, 1967) reported underwater swimming in this species for a recorded
distance of 9-12 metres. Kern (1964) reported an account of an adult male which
had been found 'floundering' in the South China Sea.
Pygathrix species inhabit subtropical and temperate forests in eastern Indochina
and southern China, but only at the periphery of colobine range (Fig. 1). The species
TABLE 1. The species of Asian Colobinae (Brandon-jones, 1984, 1993, 1995, 1996a,b)
Species
Distribution
Nasalis (Nasalis) laroatus
Nasalis (Simias) concolor
Pygathrix(Rhinopithecus) roxellana
Pygathrix (Rhinopithecus) bieti
Pygathrix(Rhinopithecus) brelichi
Pygathrix(Rhinopithecus) avunculus
Pygathrix(Pygathrix) nemaeus
Pygathrix(Pygathrix) nigripes
Presbytis potenziani
Presbytis comata
Presbytisfredericae
Pesbytis frontata
Presbytisjemoralis
Borneo, except central Sarawak
Mentawai Islands
Sichuan, Gansu, Shaanxi and Hubei, China
Hengduan mountains, Yunnan, China
Fanjing mountain, Guizhou, China
Central north Vietnam
Central Vietnam and east central Laos
South Vietnam, south Laos and east Cambodia
Mentawai Islands
WestJava, north Sumatra, north and east Borneo
Central Java
Central, east and southeast Borneo
Malay peninsula, central Sumatra, Batu Islands, northwest
Borneo
Riau archipelago, south Malay peninsula, east central
Sumatra, Great Natuna Island
Southwest Sumatra
Karimata Islands, and Borneo, except central Sarawak and
lowland northwest Borneo
Southwest India between Western Ghats and coast to 14°N
South Himalayas from Afghanistan border to Tibet between
Sikkim and Bhutan; India northwest of range of S. hypoleucos
to Aravalli Hills and Kathiawar, and northeast to Khulna
province, Bangladesh; north, east and southeast Sri Lanka
Southwest, central and north Sri Lanka
Western Ghats of India and Cat Ba Island, north Vietnam
North central Vietnam
Central Laos
Central Vietnam
Northeast Vietnam; Guangxi, Guizhou and Sichuan, China
Northwest Vietnam; Java, Bali and Lombok
Sumatra, Riau-Lingga archipelago, Bangka, Belitung, Borneo
Serasan, west coastal peninsular Malaysia, south central
Thailand, Cambodia and south Vietnam
Yunnan, China; north Indochina into Burma
Tripura and southern Assam, India; adjacent Bangladesh;
north Shan and lowland southwest and south Burma; Malay
Peninsular and neighbouring small islands (not Singapore)
Bangladesh and Assam east ofJamuna and Manas rivers;
north and highland west Burma; Yunnan, China
Bhutan and Assam west of Manas river
Presbytis siamensis
Presbytis melalophos
Presbytis rubicunda
Semnopithecus (Semnopithecus) hypoleucos
Semnopithecus (Semnopithecus) entellus
Semnopithecus
Semnopithecus
Semnopithecus
Semnopithecus
Semnopithecus
Semnopithecus
Semnopithecus
Semnopithecus
(Trachypithecus) vetulus
(Trachypithecus) johnii
(Trachypithecus) delacouri
(Trachypithecus) laotum
(Trachypithecus) hatinhensis
(Trachypithecus) francoisi
(Trachypithecus) auratus
(Trachypithecus) cristatus
Semnopithecus (Trachypithecus) barbei
Semnopithecus (Trachypithecus) obscurus
Semnopithecus (Trachypithecus) pileatus
Semnopithecus (Trachypithecus) geei
D. BRANDON:JONES
330
r-
~Pyga'hrlX
*-
NassJis /sNsfus
V
Pygathrixnema8US
o
Pygsthrix. avuncuJus
o
Pygalhrixbrelichl
II Pygathrix roxsllana
o
blot!
0
.......
1---1
Figure 1. Distribution of the genera Nasalis and JYgathrix.
of the subgenus Rhinopithecus have a discontinuous distribution. JYgathrix bieti, for
example, exists only on the steep flanks and gorges of the Hengduan mountains,
Yunnan, south west China, and P. brelichi on a single mountain top refugium (Fanjing
mountain) in Guizhou, central south China (Jablonski, 1993).
The Semnopithecus subgenus, Trachypuhecus is represented by Semnopithecus vetulus in
south-west and north Sri Lanka, and by S. johnii in the Western Ghats of southern
India (Fig. 2). Otherwise it is absent from the Indian subcontinent, but reappears to
the east of the Bay of Bengal. S. auratus occurs inJava, Bali and Lombok (Indonesia).
S. cristatus inhabits the peripheral areas of Presbytis distribution in the Malay
archipelago and western Malay peninsula; and S. (Trachypithecus) distribution
stretches northwards through Indochina to Bhutan where it is represented by S. geei;
to southern Assam and Tripura (India), and east Bangladesh where both S. obscurus
and S. pileatus occur; to north-eastern Assam and north Burma as S. pileatus, and to
southern China as S. francoisi, S. barbei and S. pileatus. Semnopithecus (Semnopithecus)
entellus is partially sympatric with S. vetulus and S. johnii, but its distribution also
embraces the whole of the Indian subcontinent (apart from the small south-western
area occupied by S. lrypoleucos) as far as Kathiawar (India), the fringes of the Great
Indian Desert, south-west Bangladesh, and the Himalayan foothills from Sikkim
(India) to the Afghanistan border (Fig. 2). Comparative field studies (see Bennett &
Davies, 1994) in Sri Lanka indicate that Semnopithecus entellus, the colobine most
successful in contemporary times at divorcing itself from the rainforest environment,
is more omnivorous than S. vetulus.
Presbytis distribution (Fig. 3) corresponds to the 'everwet' rainforest (van Steenis,
1961) of the Malay peninsula to l3°50'N (Gairdner, 1915) and the Malay
ASIAN COLOBINES AS CUMATIC INDICATORS
331
I
.....
~
,
\
IIIJ Semn.,.-us (8BnmcpHhecus)
"
~ SemnopJthecUS vetulus,S.joIInH. $. d8Iacouri, S. &sotum. S.hatinhensls. S. franco/$land $. auratus
~
5emnopftlltK;u$crfstalu$, $. barb6i, $. obscufU8, S. plleatus and S. geeJ
o
500km
f------l
Figure 2. Distribution of the genus Semnopithecus.
archipelago. The endemism of this genus, (denoted in this paper by the vernacular
name 'sureli') to the everwet rainforest indicates a dietary dependence on its produce.
Surelis diverge from the leaf monkeys and langurs in apparently being incapable of
subsisting solely on mature leaves. The sureli diet probably contains a staple element
(perhaps seeds, see Davies, Bennett & Waterman, 1988) whose availability is
vulnerable to seasonal climatic variation. S. (Trachypithecus) extends its distribution
out of the everwet rainforest into the seasonal rainforests ofIndochina and east Java.
This vegetational divergence from Presby tis, which echoes that between Procolobus
(Piliocolobus) and Colobus in east Africa (see Oates, Davies & Delson, 1994), may reflect
a comparable dietary separation. (For comparative dietary information on sympatric
Presby tis siamensis and Semnopithecus obscurus, see Curtin, 1977 and Bennett & Davies,
1994; for that of their African counterparts, see Oates, 1994.)
PARALLELS IN ORIENTAL BIOGEOGRAPHY
The disjunct geographic distributions of the Asian co1obines conform to a
recurring pattern. Other vertebrates (probably including man), invertebrates and
plants, which occur in the eastern part of the Oriental Region, have outlying
populations in the southern part of the Indian subcontinent. (See Fig. 2, Appendix
and Blanford & Blanford, 1861; Annandale, 1911; Smith, 1931, 1935; Ali, 1935,
1949; Champion, 1936; Pocock, 1939; Hora, 1944, 1948; Abdu1ali, 1949; Biswas &
Sampatkumaran, 1949; Hora & Jayaram, 1949; Jayaram, 1949; Roonwa1, 1949;
Silas, 1951, 1953; Coon, 1966; Holloway, 1974; Subramanyam & Nayar, 1974.)
332
D. BRANDON:JONES
That partial recolonization has masked the real extent of these disjunctions is
indicated by the tripartite geographic distribution inJava (Indonesia), north-eastern
Indochina (including southern China), and southern India, of the superspecies
Semnopithecus (Tracl!Jpithecus) auratus (Fig. 2). One of the constituent species, the
hooded leaf monkey, Semnopithecus johnii, has a subspecies in southern India, and a
second, S. j. poliocephalus, in Vietnam. A second species, the ebony leaf monkey, S.
auratus, is similarly split between Vietnam andJava. The remaining member species,
S. francoisi, S. hatinhensis, S. laotum and S. delacouri are all restricted to north-eastern
Indochina and southern China (Brandon-jones, 1995, 1996b).l)gathrix (Fig. 1) and
the Indochinese representatives of the superspecies S. auratus (Fig. 2), share a western
perimeter with the loris, Nycticebus pygmaeus (see Groves, 1971); the macaque, Macaca
thibetana (see Tan, 1985; Fooden, 1988; Fooden et al., 1994); the gibbon species,
Hylobates concolor, H. gabriellae and H. leucogenys (see Groves, 1972; Geissmann, 1990;
Groves & Wang, 1990); and a disproportionately rich fauna and flora (Voous, 1947;
de Beaufort, 1951; Florin, 1963).
The grey-backed sureli, Presbytis comata, also has a disjunct tripartite distribution at
its generic range limit in westJava, northwestern Sumatra and northeastern Borneo
(Brandon-jones, 1996a). Its eastern limit in Java corresponds with that of
Semnopithecus auratus mauritius (see Brandon-jones, 1995). In Sumatra its distribution is
P. potenziani
P. comata
P. femoralis
P. fredericae
P. frontata
P. siamensis
P. me/a/ophos
P. rubicunda
*
0
•
•
....
0
*
'V
Figure 3. Distribution of the species of the genus Presbytis.
500km
I
ASIAN COLOBINES AS CUMATIC INDICATORS
333
identical to that of the gibbon subspecies, Hylobates lar vestitus (see Fooden, 1969;
Wilson & Wilson, 1977; Gittins, 1978) and closely approximates that for the orangutan (Pongo pygmaeus) which, although widespread in Borneo, is restricted to the
northwestern end of Sumatra (Miller, 1903; Schneider, 1905; Carpenter, 1964). The
distribution of P. comata in both Sumatra and Borneo, coincides with that of the
black-and-red populations of the squirrel, Callosciurus prevostii which is represented in
the intermediate areas by populations of different colour pattern (Chasen & Kloss,
1925). The range of Presbytis comata everetti in northern Borneo (see Brandon-jones,
1993, 1996a) circumscribes the entire Sunda Island distribution of the fish genera,
Gastromyron and Neagastromyzon (see de Beaufort, 1951); and most of that of the
smooth-tailed tree-shrew, Dendrogale (see Napier & Napier, 1967), the mountain
ground squirrel, Dremomys (see Moore & Tate, 1965) and the limbless lizard,
Ophisaurus (see Inger, 1958), all of which have their closest relatives in mainland
southeast Asia. Some local plant species also have remarkably disjunct phytogeographic affinities (Stapf, 1896; Holttum, 1964; van Steenis, 1964). Notable examples
are Artocarpus melinoxylus which is represented by one subspecies in north Borneo and
a second in eastern Indochina arrett, 1959), and Potentilla mooniana whose
distribution is Sri Lanka, Java, the eastern Himalayas and Mt. Kinabalu (Sabah,
Malaysia) (Croizat, 1968).
The genera, Nasalis and Presbytis are both represented by endemic species on the
Mentawai Islands. Some authors have regarded P. patenziani as a close relative of
Semnopithecus francoisi, but a morphological reassessment and its adult male
vocalization, clearly ally P. potenziani with Presbytis comata, and especially with P.c.
everetti (Brandon-]ones, 1993). The fauna of the Mentawai Islands also includes an
endemic gibbon and an endemic macaque (Whitten & Whitten, 1982), and Kloss
(1928) recorded a "remarkably distinct subspecies of Paradoxurus hermaphroditus; a
representative of Hemigale derbyanus, [an] animal not known from small islands; a local
race of Cervus unicolor, three members of' Sciuropterus' allied to Sumatran animals, but
a genus (s[ub]g[enus]) not known in any form from the rest of the [West Sumatran]
chain; a race of Lariscus niobe; an endemic squirrel (Sciurus melanogaster) and Manis
javanica. None of these have been found in the Batu Islands which represent any
bridge that may have led from Sumatra". Musser & Carleton (1993: 604) listed ten
rodent species endemic to the Mentawai Islands. The discovery by Kloss (in Chasen
& Kloss, 1926) of Egretta eulophotes on one of them (Sipura), was "the first time" he had
"met with this bird in Malaysia during twenty-five years of collecting". Siberut (the
northernmost of the four Mentawai islands) and Sipura specimens of Halcyon
coromanda which, predicted by locality, would be attributable to subspecies from the
Pagai (the two southernmost Mentawai Islands), Batu islands (adjacent to Siberut) or
western Sumatra, were inseparable from a series from Borneo, Singapore andJohor,
Malaysia (Chasen & Kloss, 1926). The frog, Kalophrynus punctatus occurs only in
Borneo and the Mentawai Islands (Inger, 1966). There is evidence that the
phytogeographic affinities of the archipelago may be similarly anomalous. Ridley
(1926) drew particular attention to the following examples. His new species,
Zuccarinia cordata, a "curious plant (probably a tree)" pertained to a previously
monotypic genus, known only fromJava. Another new species, Staurogyne citrina was
the only yellow-flowered member of its genus, the other species having white or
brown flowers. The "curious new genus Polycycliska" belonged "to the small Malayan
group of Coptophyllum and Pomazota", The occurrence of Xanthophytum villarii,
a
334
D. BRANDONJONES
ASIAN COLOBINES AS CUMATIC INDICATORS
c
~
Ssmnopithecus (Trachypithecus)
•
Sealevel
o
~
SemnopithBcus (Trachypithecus)
•
Sealevel
Figure 4. A, the estimated distribution of Presbytis and Semnopithecus (Trachypithecus) before the earlier
deforestation. B, the presumed distribution of Presbytis and Semnopithecus (Trachypithecus) after earlier
deforestation. The 120-metre sea depth is used as an indication of the area of the Sunda shelf exposed
at this time. C, the presumed distribution of Presbytis and Semnopithecus (Trachypithecus) between periods of
deforestation. D, the presumed distribution of Presby tisand Semnopithecus (Trachypithecus) during the second
deforestation.
335
336
Do BRANDONJONES
"previously known only from the Philippines", was "a remarkable extension of
distribution".
REUC POPULATIONS
The disjunct elements in the flora and fauna of the Oriental Region share
common geographic limits and therefore presumably a common cause. Theories
such as convergent evolution or dispersal by raft, wind, volant animals or by human
agency, are inapplicable or inadequate as explanations for the discontinuous
distribution of many of these species (see below). They are therefore superfluous for
those of the remaining species.
The distinctive flora and fauna of southern India, southern China, eastern
Indochina, northern Borneo, west Java, northwestern Sumatra and the Mentawai
Islands must therefore constitute relics of populations with former continuity
between these areas. It is inferred that the distribution of Nasalis formerly
incorporated Sumatra at least; that Semnopithecus (Trachypithecus), represented by pied
populations, ranged from Java to most oflndia, taking in south-eastern China, and
probably parts of the Middle East (Fig. 4A); and that Presby tis comata extended at least
through Sumatra, Borneo andJava (Fig. 4C). Part of the area vacated by this biota
has evidently been reclaimed by its descendants. In Semnopithecus species, this
reclamation is accompanied by a unidirectional alteration in pelage colour,
commencing from the predominantly black relic species, S. auratus and S. johnii, and
passing through grey to brown. In some cases this is succeeded by a red stage, which
less often dilutes to albinotic at the furthest extent of the associated dispersal route.
The same sequence emanating from the predominantly grey relic species, Presbytis
comata appears bereft of the preceding black stage (Brandon-jones, 1995, 1996a).
Similar chromatic successions (susceptible to the same interpretation) have been
identified by Hershkovitz (1968, 1977) in South American primates. It is probable
that Semnopithecus entellus originated from S. johnii by way of S. vetulus in southern Sri
Lanka.
AN EXPLANATION FOR THE EXISTENCE OF REUC POPULATIONS
The picture that emerges is one of recolonization by descendants of the very
localized peripheral remnants which escaped a period of predominant deforestation.
The relic populations therefore are not peculiarly adapted to their present climate,
terrain or altitude, but persist in areas which escaped complete deforestation. The
deforestation apparently so profoundly affected some of these relic populations,
notably most of those in China and Indochina, that they have evidently ceased
dispersal. Indochinese relic primates remain confined by a physically indetectable
geographic perimeter which has no discernible influence on the dispersal of their
non-endemic recolonizing congeners, Semnopithecus barbei, S. cristatus, Nycticebus coucang,
Macaca arctoides, M. assamensis, M. jascicularis, M. mulatta and M. nemestnna. The flora
and fauna in these isolated zones are so diverse and the relic zones themselves so
clearly delineated and so widely separated that it is inconceivable that factors such as
epidemic disease, interspecific competition or predation could have been responsible.
ASIAN COLOBINES AS CLIMATIC INDICATORS
337
Numerous other explanations have been offered, as the following brief survey
reveals, ranging from land submergence to polyphyletic evolution.
In order principally to account for prosimian distribution, Wallace (1876) inferred
that during much of the Tertiary era, Sri Lanka and south India were isolated from
the rest of the subcontinent "by a considerable extent of sea, and probably formed
part of an extensive southern continent or great island" which included Madagascar,
central and southern Africa. "The very numerous and remarkable cases of affinity
with Malaya, require however some close approximation to these islands, which
probably occurred at a later period". After the still later land connection with the
"Himalo-Chinese fauna, a rapid immigration of new types took place, and many of
the less specialised forms of mammalia and birds (particularly those of ancient
Ethiopian type) became extinct". Needless to say, there is no geological evidence for
"a now submerged southern continent", although continental drift can explain some
of the faunal similarity between Madagascar and the southern Indian
subcontinent.
Blanford (1879, 1901), Hill (1934) and Mani (1974a) believed that glacial low
temperatures drove Himalayan plants and animals "towards the equator, and
subsequently, as the temperature increased, to the higher parts of the hills". Blanford
(1879) suggested that "the ancient Indo-African fauna", such as the prosimians,
anthropoid apes and mouse deer, may have been isolated by the Pliocene dispersal
of the Pakistan Siwalik fauna which was then itself almost exterminated by the low
temperatures of the glaciation. The flaw in this argument is that certain elements of
the disjunct flora and fauna, such as macaques and leaf monkeys, are not endemic
to cool high altitude regions. Blasco's (1971) implication that the ability of the Nilgiri
marten and tahr to descend to 900 m and even lower, would enable them to disperse
from the Himalayas to southern India, does not explain their absence from the areas
in between.
Sarasin (1910) attributed the disjunction to the central Indian Deccan lava flows.
Mani (1974c) countered that these Cretaceous-Eocene flows cannot be responsible
for the discontinuity in a Tertiary Assam fauna which, largely during the Pliocene,
colonized the southern Indian hills.
Prompted mainly by the disjunct distribution of certain hill-stream fish, Hora
(1944, 1953) formulated the 'Satpura Hypothesis', named by him from the range of
mountains which in conjunction with a series of hills was postulated to have formed
a migratory route from Assam to Southern India when the hills were uplifted. The
Garo-Rajmahal Gap (northwest Bangladesh; see Fig. 1) however, forms a
conspicuous hiatus in this conjectured route, and the evidence indicates the absence
of a bridging uplift belt "since the earliest Gondwana times" (Mani, 1974c). The
hypothesis is also refuted by the absence of a Western versus Eastern Ghats bias in
the southern Indian hill range representation of Assamese mammalian genera
(Kurup, 1974).
The 'Brij Hypothesis' proposed by Dilger (1952) was based on evidence from
Sanskrit literature and unearthed examples of ancient sculpture, of a wet tropical belt
which traversed India from the eastern Himalayas to the west coast north of the
Vindhya-Satpura Trend about 2000 years ago. Dilger acknowledged that hill-stream
fish could not have availed themselves of this potential migratory route.
All the above explanations are irrelevant to the biogeography of the Sunda
subregion and Indochina. Their inadequacies have encouraged the almost mystical
speculations by Croizat (1968) and Mani (1974c) that the "available biogeographical
338
D. BRANDON:JONES
evidence points ... to the inescapable conclusion that the same genera and species do
indeed arise polyphyletically in widely separated areas".
Chasen (1940) postulated that Presby tis cornata was part of an "eastern drift"
entering the Sunda subregion from Indochina by way of Borneo. His interpretation
neither identifies its progenitor, nor explains its absence in southwestern Borneo and
southern Sumatra. Medway's (1970) conclusion that the grey-backed populations are
the product of convergent evolution is even less convincing, since their habitats have
no distinctive unifying character which might have induced the pelage colour
convergence; and in Borneo these habitats are sympatrically occupied by brown or
red surelis which inexplicably remain unaffected by the elusive convergence factor.
The distinctiveness of the Mentawai Islands fauna has been attributed to the depth
of the strait between the archipelago and Sumatra maintaining geographic isolation
during the last million years when sea levels have fluctuated by over 200 metres
(Dring, McCarthy & Whitten, 1990). This interpretation does not account for the
closer affinities of both Nasalis concolor and Presby tis potenriani with Bornean, rather
than with Sumatran colobines.
Volcanic activity (e.g. Ninkovich & Donn, 1976), changes in sea-level or land
subsidence with widespread submergence, or land elevation leading to increased
availability of montane environments (e.g. Mattauer et al., 1985) have occurred in
parts of the region and must have had local effects. Nevertheless there appears to
have been no single or series of geological events sufficiently all-encompassing to
have sculpted, from the Indian subcontinent through to the Malay archipelago, the
intricate distributional patterns detailed above. There was no tectonic activity in
Southeast Asia during the Pleistocene (Heaney, 1991). In the absence of geological
events major and recent enough to have created the observed biogeographic
configuration, and with the inaccuracy or inadequacy of the above-cited explanations, the only remaining explanation seems to be climate change.
Consistent temperature differences, independent of seasonal variation, occur
between certain Asian colobine relic areas, notably those of Pygathrix in Sichuan
Province (China) and Vietnam. Therefore an alteration of temperature alone could
not account for the localized elimination of flora and fauna in the intervening and
thermally intermediate areas. A climatic explanation for the montane biogeographic
disjunctions in Africa (e.g. Moreau, 1963, 1969; Carcasson, 1964) is that they
represent floras and faunas adapted to cool and wet conditions which spread
between mountains when such a climate prevailed, only to be eliminated from the
invaded lowland areas during a subsequent warmer and drier climate. The warm,
moist climatic conditions of the Mentawai Islands and the lowland relic areas of
Vietnam and southeast China do not accord with such a hypothesis. The topography
of the two last mentioned relic areas would also provide no refuge for flora and fauna
from a hot and dry climate. The only explanation wholly consistent with the
evidence is that the relic areas alone retained adequate moisture and temperature to
support their characteristic flora and fauna during a cool and dry climate. That not
only genera but species are disjunct indicates that such conditions prevailed relatively
recently. The most recent events which could have led to widespread aridity
combined with reduced temperatures over the entire Oriental Region are the
Pleistocene glaciations.
ASIAN COLOBINES AS CUMATIC INDICATORS
339
CORROBORATIVE EVIDENCE FOR CUMATIC CHANGE
There is now substantial evidence that forests in the tropical zones of both Africa
(Hamilton, 1974, 1976, 1988; Grubb, 1978, 1982; Livingstone, 1993) and South
America (Haffer, 1969, 1990; Prance, 1973, 1982; Vanzolini, 1973; Duellman, 1982;
Kinzey, 1982; Whitmore & Prance, 1987) were reduced to relic distributions during
arid periods associated with the Pleistocene glaciations. Colinvaux's (1993) doubts
that the Amazon Basin could have been arid, appear to stem from the assumption
that it was a decrease in temperature alone (estimated at 6-9°C below modern levels)
about 30 000 years BP, that drove Andean forest in the Napo refugium, Ecuador,
1500 metres below its current montane level. Plants endemic to high altitudes are
hardier to cold dry conditions. This isolates them from competition with plants
which cannot tolerate such conditions, but does not necessarily imply that they prefer
such conditions. There is no corollary that plants at lower levels have opposite
adaptations, only that they have a lower aridity tolerance. Temperature appears
significant only indirectly in mediating the levels of evaporation and precipitation
which sustain the rainforest. Rainfall charts illustrate the discontinuous distribution
of 1000 mm rainfall in the Amazon Basin between May and October. A temperature
decline of at least 6°C would almost certainly render this discontinuity more
perennial, and create corresponding discontinuity in the rainforest. At all events,
rather than descent at high and low altitudes, as suggested by Colinvaux (1993), such
conditions would more probably produce range contraction of all forest types
towards the most moist available climatic zone. Such a climate is commonly but not
exclusively, available at medium elevations on mountains.
The belief that Asian rainforests survived the glaciations virtually unscathed owing
to their strongly maritime climate is inapplicable to the Indian subcontinent, and
ignores the climatic effects engendered by the emergence of the Sunda shelf (Fig.
4B,D) and the Sahul shelf. These climatic effects were first appreciated by van
Steenis (1935). The simultaneity of the northern and southern hemisphere ice ages
indicates synchronous Pleistocene fluctuations of the Asiatic and Australian
anticyclones. The Intertropical Convergence zone had a more southerly position
than at present in the whole or major part of the region. Observed fluctuations in
annual rainfall strongly correlated with both these climatic factors for Pontianak,
Borneo, for example, amount to 25% of the annual mean if l l-year periods are
averaged and even to 75% if the highest and lowest annual values on record are
considered (Verstappen, 1975). The climate is likely to have been much more
seasonal, the monsoon less developed, and reduced sea surface temperatures would
have meant less frequent generation of tropical cyclones which are now an important
source of rainfall (Woodroffe, 1993). The presence of glaciers on New Guinea,
Borneo and Sumatra prior to about 10 000 years BP, a snowline 1000 m lower than
today, and evidence from palynological studies in west Java, central Sumatra and
New Guinea that montane vegetation zones occurred much lower than currently,
indicate a fall in temperature of 2-6°C (Heaney, 1991). The relic forests in eastern
Indochina can be recognized as a southerly continuum of the previously identified
(Reinig, 1936) east Eurasian glacial relic forests.
From the distributions offive drought indicator plants, van Steenis (1961) inferred
a Pleistocene corridor connecting their disjunctions to the north and south of
Southeast Asia. Smithia sensitiva exemplified a species with a preference for a weak dry
season as it occurs in north peninsula Malaysia, north Sumatra, west Java and
340
D. BRANDON:JONES
scattered localities in New Guinea. At the other extreme was Rhynchosia rothii, a
species bound to a severe dry season and in Malaysia restricted to the driest areas.
Pollen grains of the mangrove genus, Aegialites occur in the Pliocene of north-western
Borneo, about midway between its nearest modern distribution in the BengalThailand coastal area to the north-west, and in eastern Malesia and northern
Australia to the south-east. The geologically recent Bornean immigration from the
direction of New Guinea, of the conifers Podocarpus imbricatus and Phyllocladus in the
upper Pliocene and Plio-Pleistocene transition respectively, suggests that in order to
achieve this, their distribution was not always montane. P. imbricatus, but not
Phyllocladus, also reached Indochina, Sumatra and Java (Muller, 1972). Climatic
instability is also indicated by the Pliocene presence in Borneo of two fern species of
the genus Stenochaena, now distributed no closer than the Philippines; and by the
disappearance from north-western Borneo during the Pleistocene of the mangrove
genus, Comptostemon, now restricted to its south-east coast, the Philippines, Sulawesi,
Moluccas and New Guinea (Muller, 1972). Southern Borneo probably had a more
seasonal climate in the early Holocene, about 9000 years BP. Pollen analysis
indicates that pine-grassland savanna similar to the open woodlands of Thailand and
northern Luzon (Philippines) replaced lowland rainforest at a Middle Pleistocene site
near Kuala Lumpur, Malaysia, during a period oflow sea level, about 160 000 years
BP. Fossil pollen studies show that the Atherton Plateau in Queensland, Australia,
the Bay of Bengal and eastern India, and the Western Ghats of southern India, all
experienced drier and more seasonal climates during the last glacial maximum
(Heaney, 1991).
Stresemann (1939) stressed the presence of localized species and well-defined
subspecies of grassland birds as implying that such habitat had existed in the Malay
archipelago long before the advent of man. Two such birds, Centropus purpureus and
Prinia po!Jchroa, were endemic to the Javan open country dominated by alang-alang
grass, Imperata cylindrica. Further examples, the rice finches, Lonchura (Padda) oryruora
and Lonchura leucogastroideswere probably restricted to Java and Bali. Another one, the
weaver bird, Lonchurafuscans, was endemic to the rice fields or alang-alang of Borneo.
Marked subspeciation in Centropus bengalensis, Saxicola caprata, Tumix suscitator and
Tumix sylvatica demonstrated prolonged residency in the subregion. In New Guinea,
Megalurus timoriensis was differentiated into a lowland and montane subspecies, and
Lonchura caniceps and the grassland quail Synoicus ypsilophorus both comprised three
altitudinal subspecies. From bird distribution he concluded that extensive Pliocene
grassland areas had survived at least in south Borneo, east Java, the Lesser Sunda
Islands, (south) Sulawesi, Luzon (Philippines) and eastern New Guinea.
Previously extensive Sundaic grassland is indicated by the distribution of the genus
Caprolagus, now reduced to a single species, the hispid hare, inhabiting the grass
jungles of the Himalayan foothills, but represented by three or four species in Middle
Pleistocene Java (Dawson, 1971). Their contemporaries, the hippopotamus,
antelope, cattle, chital and other deer are all obligate grazers. The diversified group
of Middle Pleistocene terrestrial predators, including hyenas, three genera of dogs,
sabre-toothed 'cats', possibly two 'tigers', a leopard, leopard cat and civets, is more
reminiscent of plains communities in India or the African savanna than the
impoverished carnivore fauna of modern Sundaic forests (Medway, 1972). The
survival at Niah Cave, Sarawak, Borneo until the later Upper Pleistocene of a giant
pangolin, Manis palaeojaoanica, otherwise known only from Middle Pleistocene
deposits in Java, conveys some impression of the then prevalent conditions. This
ASIAN COLOBINES AS CUMATIC INDICATORS
341
extinct species, almost a metre longer than the largest living pangolin, Manisgigantea,
coexisted with the extant Manisjavanica. Manisgigantea is widely distributed in forestsavanna-cultivation mosaic from the west coast to Uganda in equatorial Africa,
feeding in wooded and open country and visiting papyrus swamps. Most forestdwelling termites of peninsular Malaysia nest underground. None construct the tall
termite mounds characteristic of the African savanna, which the extinct pangolin
must have required (Medway, 1972).
The two Nasalis species feed heavily on leaves (Witkamp, 1932; Kern, 1964;
Kawabe & Mano, 1972; Tilson, 1977; Salter et al., 1986; Bennett & Sebastian, 1988;
Yeager, 1990). Odontometric analysis (Kay, 1978) indicates that potentially they are
the most folivorous of Old World monkeys. Such specialization, which entails the
evolution of a modified and bacteria-infested stomach, confers the advantage of
enabling the animal to exploit seasonal rainforest where the supply of more readily
digestible and more nutritious foods is unreliable. That species so equipped should be
endemic to the equatorial islands of Borneo and Mentawai where fruits, flowers,
buds and shoots are perennially available, is incongruous. This anomaly is
compounded by their resemblance to semi-terrestrial cercopithecines. Their limb
proportions, alveolar prognathism, and hair coloration are all macaque-like; as are
the facial and genital skin coloration in Nasalis larvatus, the short and almost hairless
tail in N. concolor, and the marked body-weight sexual dimorphism in N. larvatus
(Napier & Napier, 1967; Groves, 1970; Brandon-Jones, 1984). These adaptations
indicate that the genus evolved in woodland characterized by an openness
demanding considerably more terrestrial locomotion than the mangrove and
lowland rainforest it currently inhabits.
West Bornean freshwater fish show closer affinities with those of south-eastern
Sumatra than with those of eastern Borneo. This resemblance has been cited as
evidence that during the glacial emergence of the Sunda shelf, the rivers of western
Borneo and south-eastern Sumatra formed a single drainage system serving northern
Sundaland. Drainage eastwards into the Flores Sea would be expected to combine
the rivers of southern Bornean and northern Java. However, the south Bornean fish
resemble those of western Borneo and south-eastern Sumatra, the whole comprising
a Pleistocene fauna (de Beaufort, 1951). It is the fish of eastern Borneo which
resemble those of northernJava. Both are considered to represent an older fauna (de
Beaufort, 1951). A more compatible explanation is that the older fauna was
extirpated by the glacial dry conditions in central Sundaland where it is known from
fossil evidence (de Beaufort, 1951), and was replaced by post-glacial colonizers.
All this evidence reinforces the conclusion that the Oriental Region was
predominantly deforested during a Pleistocene glacial drought and subsequently
reafforested with climatic recovery. The zoogeography of Sumatra requires further
explanation.
EVIDENCE INDICATING A SECOND DEFORESTATION
The Mentawai Islands primates and Semnopithecus auratus ofJava could only have
reached these islands by way of Sumatra. They are however, unrepresented in its
northern glacial refugium whose endemic primate fauna includes only the sureli
(Presby tis cornata), the gibbon (Hylobates lar) and the orang-utan (Pongo pygmaeus). This
implies that the ebony leaf monkey and the ancestors of the Mentawai Islands
342
D. BRANDON:JONES
primates were absent from Sumatra at the time the Sumatran distribution of the
others became refugial only. It is inconceivable that a drought severe enough to
eliminate macaques, leaf monkeys and Nasalis which are not especially associated
with moist rainforest, would have spared the present refugial primates. The absence
of the ebony leaf monkey and the ancestors of the Mentawai Islands primates
therefore implies elimination by an earlier and more severe arid period, when no
refugium survived, and when all primates were eliminated from Sumatra (Fig. 4B).
This earlier dry period was presumably also responsible for the absence of the
significant number of animals found on the Asian mainland and Java, but not on
Sumatra (Dammerman, 1929). Presby tis, Hylobates and Pongo must have recolonized
Sumatra since then, and their present distribution demonstrates the occurrence of a
second and less severe glacial drought (Fig. 4D).
Presbytis comata and the Mentawai Islands Presby tis potenziani are so similar in pelage
colour and vocalization, that it has been suggested they may be only subspecifically
separable (Chasen, 1940; Wilson & Wilson, 1977). The characters which distinguish
P. poteneiani, establish it as more ancestral (Brandon-jones, 1993). Its distinctiveness
emphasizes the homogeneity of the Sumatran, Javan, and Bornean subspecies of P.
comata, and reinforces the view that they are remnants of a recently fragmented single
population. If this fragmentation was wrought by the second dry period, and its
Sumatran section could not have survived the first, then the relationship between the
two species is most economically explained by deducing that the genus, Presbytis was
absent from Borneo before the first arid period, when it survived only on the
Mentawai Islands as P. potenriani. P. comata developed from it during the interval
between the dry periods, and gave rise to the remaining extant species of the genus
after the second dry period (Fig. 4B-D; Brandon-jones, 1993, 1996a). By analogy,
the endemic Mentawai Islands gibbon, Hylobates klossii is probably the progenitor of
most, if not all gibbons, other than the concolor gibbons and the siamang (BrandonJones, in Chivers, 1977). The absence of a macaque taxon endemic to the north
Bornean refugium indicates that Macaca nemestrina did not colonize Borneo until after
the second arid period and that in the Sunda subregion its close relatives survived the
arid periods only on the Mentawai Islands and Sulawesi. One of these populations,
probably the former, presumably gave rise to M. nemestrina after the second arid
period. The systematics of the ten Mentawai Island endemic rodent species (Musser
& Carleton, 1993) are insufficiently advanced to be able to determine whether they
too conform to this pattern, but speciation in Chiropodomys (see Musser, 1979) and
Iomys for example, seems conducive to such an explanation. Survival on the
Mentawai archipelago (probably only on Siberut) was facilitated by its maritime
climate which buffered it from the desiccating effect of the emergence of
Sundaland.
CHRONOLOGY
Absent from the Mentawai Islands, but present on many others, are the long-tailed
macaque, Macacafascicularis and the silvered leaf monkey, Semnopithecus cristatus. This
indicates they are relative newcomers to the region, and reinforces the impression
that the events which brought about the geographic disjunctions occurred very
recently. The progenitor of the silvered leaf monkey, the ebony leaf monkey,
Semnopithecus auratus, evidently failed to disperse from Java between the first and
ASIAN COLOBINES AS CLIMATIC INDICATORS
343
second arid periods. This suggests this interval was short. The most recent events to
fit these criteria are the two periods of low sea level with low annual precipitation of
100 to 500 mm, at 190 000-130 000 years BP and at 38 000-12 000 years BP,
revealed by van der Kaars' (1991) palynological investigation of an eastern
Indonesian deep-sea core. This core, Lombok Ridge G6-4 at c. 850 km NNW of
Australia, extends to 300 000 years BP and demonstrates that glacial periods were
characterized by expanding grassland vegetation and high pollen concentrations in
marine sediments. During interglacials, woodland and fern cover increased.
Sedimentological and palynological analyses of sediment cores from the intramontane Bandung basin, west Java (Indonesia), provided a continuous palaeoclimatic record for the last 135000 years. Van der Kaars & Dam's (1995) data on
palaeosol development indicated anomalously dry conditions for the final part of the
penultimate glacial period, about 135 000 years BP, and very warm and humid
interglacial conditions from 126 000 to 81 000 years BP. During the transition to the
last glacial period, about 81 000 years BP, freshwater swamp forest of the Bandung
plain was replaced by an open swamp vegetation dominated by grasses and sedges,
indicating a change to considerably drier conditions. A strong reduction in Asplenium
ferns from 81 000 to 74 000 years BP suggests that drier conditions may also have
occurred in the mountains of the Bandung area, while increased numbers indicate
that from 74 000 to 47 000 years BP, it was slightly warmer again. Inferred
depression of montane vegetation zones and reduced fern percentages suggest
distinctly cooler and possibly drier climatic conditions prevailed in the Bandung area
from 47 000 to about 20 000 years BP. Temperature depressions of 4-7°C were
recorded for the last glacial maximum.
Ha Van Tan (1985) compared data from Niah Cave in north-west Borneo, the
Tabon Cave on Palawan in the Philippines, and the Ngoum Rock shelter in
Vietnam, and concluded that a cold dry period occurred in Southeast Asia from
32 000 to 23 000 years BP. Shortly before 23 000 years BP, the cold climate
intensified, and caused the formation of a rubble layer in the Ngoum Rock shelter.
An intact orang-utan mandible was recovered from the base of the overlying layer.
After 23 000 years BP, the climate became mild and humid, producing a stalagmitic
floor in the Tabon Cave. The scarcity of monkeys and arboreal squirrels at Niah
cave below the 122 em depth (carbon-14 dated at about 19 000 years BP), noted by
Medway (1960), is perhaps attributable to the more severe drought which concluded
this arid period. This drought probably coincided with the most recent glacial
maximum usually dated to 18 000 years BP (Martinson et al., 1987) but now more
accurately revised by higher precision mass-spectrometric uranium-series dating to
21 000-22 000 years BP (Bard et al., 1990). A synchronous dry period occurred in
Africa (Hamilton, 1974) and South America (Van der Hammen, 1974). This more
severe drought might also explain why two mammal genera, Hylomys and Melogale,
identified at depths of236-244cm and 137-152 em respectively (Medway, 1964), no
longer occur at Niah, little above sea level, and are now exclusively montane
(Medway, 1972).
It might be concluded that the two deforestations correspond with the two most
recent glacial maxima at about 135 000 years BP (Martinson et al., 1987) and
21-22 000 years BP (Bard et al., 1990). The silvered leaf monkey, Semnopithecus
cristatus, the long-tailed macaque, Macaca fascicularis, and the pigtail macaque, M.
nemestrina are unrepresented by endemic taxa in the north Bornean refugium and
thus appear not to have reached Borneo until after the second arid period. Niah
344
D. BRANDON:JONES
cave, Sarawak, Malaysia is a vast natural cave which occurs in an isolated coastal
limestone outcrop. In the Upper Pleistocene deposits at its west mouth, Hylobates has
been identified to a depth of 152-158 em (Medway, 1959), Presby tis to a depth of
305-3l2cm, Semnopuhecus to a depth of l22-l52cm and Macaca to a depth of
25l-259cm (Hooijer, 1963). The c. 254cm depth has been carbon-14 dated at
41 500 ± 1000 years BP and the 244-254 em depth to 39600 ± 1000 years BP
(Harrisson, 1960). More recently the 213-229 ern depth has been carbon-l 4 dated at
21 410 ± 1000 years BP (Majid, 1982). Although these dates are unreliable, they
indicate that Macaca was present at the site before the most recent glacial
maximum,
That the deforestations are not attributable to the two most recent glacial maxima
is corroborated by the orbitally based chronostratigraphy of Martinson et at. (1987),
which indicates no significant difference between them in severity. A fluctuating but
persistent temperature decline towards the glacial maxima is revealed, with a rapid
increase at the advent of the interglacials. Neither of the two most recent glaciations
included a cold period preceded by a significantly colder one. The more abrupt onset
of the earlier glaciation seems to distinguish it from the later one. A presumably
critical threshold was passed at the end of oxygen-isotope Stages 7 and 5, which was
not reattained until the interglacials. In the penultimate glaciation, this threshold was
crossed more abruptly, and the succeeding interstadials offered little remission. The
deforestations therefore appear correlated with the termination of the interglacials at
about 190000 years and 80000 years BP.
CONCLUSION
A biogeographic analysis of the extant Asian Colobinae indicates that about
190000 years BP, a major deforestation exterminated Nasalis in Sumatra and
fragmented the geographic distribution of Iygathrix which was eliminated from
western Indochina, and possibly elsewhere. At the same time Presby tis (sensu stricto)
was eradicated from most of its former range, which excluded Borneo but included
east Java, where its Middle Pleistocene presence at Sumberkepuh (7°29'S 112°04'E)
was recorded by Hooijer (1962). Like Pongo (see Kahlke, 1973), it conceivably
occurred as far afield as China (Fig. 4A). The survival of Hylobates klossii, Nasalis
concolor, Presby tis potenriani and Macaca pagensis solely on the Mentawai archipelago
(probably only on Siberut) was facilitated by its maritime climate which alleviated the
desiccative effect of the emergence of the Sunda shelf. The preglacial distribution of
the Semnopithecus subgenus, Trachypithecus, excluded Borneo and the Mentawai
Islands, but extended fromJava to the Indian subcontinent and conceivably along a
seasonal rainforest corridor into Africa (Fig. 4A). The cool dry period contracted its
distribution to west Java, north-east Indochina, southern China and the Western
Ghats of southern India (Fig. 4B).
During the interglacial Presby tis potendani rafted to Sumatra, transmuting into P.
cornata which rafted to Borneo and Java and possibly also to the Malay peninsula.
Hylobates klossii dispersed similarly, and Pongo recolonized Sumatra. It was probably
also during this period that Semnopithecus johnii invaded Sri Lanka, evolving into S.
oetulus.
The second and less severe deforestation at about 80000 years BP eradicated the
central area of P. cornata distribution, restricting it to west Java, north-western
ASIAN COLOBINES AS CUMATIC INDICATORS
345
Sumatra and northern Borneo. From these areas, dispersal into rainforest
regenerated in the vacated areas appears to have proceeded in phases, each one
marked by a pelage colour alteration. These phases probably correspond with
punctuated increases in precipitation, facilitating range extension of the rainforest. S.
(Trachypithecus) species radiated from S. auratus, and in southern Sri Lanka S. entellus
evolved from S. vetulus.
The present distribution of Asian colobines indicates the principal areas where
everwet and seasonal rainforest survived these two arid periods (Fig. 4B, D).
Presumably rainforest survived both periods in areas outside colobine range, such as
New Guinea. Further biogeographic investigation might identify additional minor
relic zones within their range. The exact nature of the non-rainforest vegetation in
the area during the arid periods remains to be determined, but there was probably
extensive grassland and even desert.
This study indicates that climatic barriers have been much more significant than
topographical barriers in delineating the Oriental zoogeographic region. It also
implies that speciation rates are more rapid than has been assumed. It indicates that
morphological change is generated by geographic dispersal, rather than geographic
isolation.
ACKNOWLEDGEMENTS
I thank G.B. Corbet and other members of the Mammal Section and library staff
at the Natural History Museum, London; and C. Smeenk of the Nationaal
Natuurhistorisch Museum, Leiden, for their co-operation and forbearance;J.C. M.
Dring for information on amphibian and reptilian zoogeography; and C.R. Vardy
for assistance with the translation of Stresemann (1939). T.H. van Andel supplied
valuable information on recent tectonics and sea level and temperature changes, with
figures from an unpublished manuscript. He and AA Barnett drew my attention to
many pertinent references. I am also deeply indebted to K.M. Hiiemae for her
collaboration in the drafting; to P. Elson and S. Kariyawasam for their assistance in
the preparation; and to PJ. Andrews, P.S. Ashton, DJ. Chivers, the Earl of
Cranbrook (formerly Lord Medway), E. Delson, C.P. Groves, AG. Marshall, P.H.
Napier and T.R. Olson for their constructive criticism of earlier versions of the
manuscript; and to my wife, Chris, for her assistance and patience in locating
references, with the compilation of the appendix, and in the preparation of the maps
and typing and reformatting the present version of the manuscript, which received
valuable comment from P J. Andrews, C. Brandon-jones, C.P. Groves, A Turner
and an anonymous referee who was particularly helpful with glacial terminology.
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APPENDIX
Examples of Indomalayan animals and plants with a North Indian subcontinental hiatus in their distribution
Blanford (190 I) tabulated the following vertebrate examples: the mammal genera, Hemitragus, Mustela and
Sciuropterus; the bird genera, Arachnothera, Batrachostomus, Cephalopyrus, Chaptia, Cissa, Collocalia, Dichoceros, Ducula,
Eurystomus, Garrulax, Gorsachius, Hemicercus, Hodgsonius, Huhua, Hypsipetes, Iole, Irena, Loruulus, Lyncomis, Micropus,
Photodilus, Picumnus, Sauropatis, Scolopax, Thnponax, Tzga and Trochalopterum; the reptile genera, Ancistrodon, Cylindrophis,
Dendrelaphis, Draco, Dryocalamus, Gerardia, Liolepis and Rhabdops; and the caecilian, Ichthyophis. He also mentioned Loris
and Nycticebus, two closely related prosimian genera occurring respectively in Sri Lanka and southern India, and east
of the Bay of Bengal; and the cuckoo, Phoenicophaus, then known only from Sri Lanka, but subsequently reported from
southern India (Baker, 1927; Biddulph, 1956), and allied to Ramphococcyx and Rhinortha, from southern Tenasserim
and "the Malay countries".
Kurup (1974) listed the similarly disjunct mammal subfamily, Platacanthomyinae; the disjunct mammal genera,
Martes, Petinomys and Tragulus; and the disjunct mammal species, Aonyxcinerea, Harpiocephalus harpia, Mus famulus and
Viverra megaspila. Jayaram (1974) added the lizard genera, Cnemaspis, Dasia, Lygosoma, Platyurus and Riopa; the snake
species, Chrysopelea omata; the toad, Nectophryne; the tree frog, Philautus; the freshwater fish genera, Batasio, Homaloptera,
Osteocheilus, Rohtee, Silurus and Thynnichthys, and the freshwater fish species, Balitara brucei and Glyptothorax conirostrae.
Sen-Sarma (1974) indicated the termite species, Odontotermes homiand O. wallonensis, and the genera, Homallotermes and
Procapntermes. Singh (1974) listed the dipteran species, Anopheles aconitus, A. insukufiorum, Cainsa testacea, Lucilia papuensis
and the genera, Agromyza and Phytomyra. Mani (1974b) cited the Lepidoptera, Discophora sondaica, Graphium agamemnon,
Papilio pario and Polydorus aristalochiae; the phasmids, Ocellata, Phamacia ingens and P. serratipes; and the oligochaetes,
Megascolex, Notoscolex, Plutellus and Woodwardia.
Among plants, Mani (1974a) instanced Willoughbeia (Apocynaceae); Lonicera, Vibumum (Caprifoliaceae); Arenaria,
Silene, Stellana (Caryophyllaceae); Rhodomyrtus tomentosa (Combretaceae); Corydalis, Fumana (Fumariaceae); Geranium
nepalense (Geraniaceae); Beilschmedia, Cinnamomum, Litsea, Machilus, Phoebe (Lauraceae); Saraca, Trifolium repens
(Leguminosae); Medinilla (Melastomataceae); Myristica (Myristicaceae); Nepenthes (Nepenthaceae); Circaea (Onagraceae); Pittasporum (Pittosporaceae); Polygala sibirica (Polygalaceae); Aconitum, Anemone rioulans, Aquilegia, Callianthemum,
CimicijUga, Clematis, Coptis, Delphinium, Isopyrum, Paeonia, Trollius (Ranunculaceae); Rhamnus oirgatus (Rhamnaceae);
Prinsepia utilis (Rosaceae); Galium, Rubia, Sarcocephelus (Rubiaceae); and Valeriana (Valerianaceae).