pre-glacial bornean primate impoverishmen_brandon-jones

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Bornean primates and Wallaces line 393

Pre-glacial Bornean primate impoverishment and Wallaces line

Douglas Brandon-JonesDepartment of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, UK

Key words: Asia, Australasia, Borneo, climate, dispersal barriers, island hopping, Java, Mentawaiarchipelago, Oriental biogeography, rafting, rainforest refugia, Sumatra, Wallacea

Abstract

Leaf monkeys (Semnopithecus, subgenus Trachypithecus)and lorises (Lorisand Nycticebus) are both geographicallydisjunct between southern India and SE Asia, with endemicrepresentatives in eastern Indochina. These parallels appearto result from restriction to, and re-expansion from, rainfor-est glacial refugia in southern India, northeast Indochinaand west Java. Sureli (Presbytis) and gibbon (Hylobates) dis-tributions reveal further refugia in north Borneo, northSumatra and the Mentawai Islands. Modern Sumatran pri-mate distribution was moulded by at least two cold dry gla-cial periods. The earlier one 190,000 years ago eliminated

all Sumatran primate habitats whereas, after recolonization,the later one 80,000 years ago left a north Sumatran rainfor-est refugium. Not only did the Mentawai Islands provide areservoir for the recolonization of Sumatra, but indirectly foran interglacial invasion of Borneo which, like Sulawesi, hadpreviously been outside the range ofPresbytisand gibbons.Bornean primate zoogeography indicates that before thefirst arid period there may have been fewer than four pri-mate species on Borneo. Most of the present twelve or thir-teen Bornean primate species rafted there interglacially orpost-glacially from Sumatra. Pre-glacial Bornean primate im-poverishment is primarily attributed to a suspected southcoastal dry zone which would have inhibited or precludedcolonization. Colonization of islands further east must gen-erally have bypassed Borneo via Java or the Philippines.The Bornean climatic barrier presented a more severe im-

pediment to faunal exchange across Wallaces line than didthe sea depth along its course. Such climatic barriers, whoseinfluences waxed and waned with the glacial cycles, wouldhave affected most SE Asian islands and were the primeinhibitor of faunal and floral exchange between the Orientaland the Australasian regions.

Introduction

SE Asia has a rich primate fauna, comprisingorang-utans (Pongo), gibbons (Hylobates), colo-

bine monkeys (Nasalis, Pygathrix, Presbytis andSemnopithecus, subgenus Trachypithecus),macaques (Macaca), loris (Nycticebus) andtarsiers (Tarsius). Twelve (or thirteen if the pres-ence of Hylobates agilis is accepted) primatespecies occur on the island of Borneo. And yet,despite the presence of suitable habitats, onlythe macaques on Sulawesi and the Lesser SundaIslands and, to a much lesser extent, the leafmonkeys on Lombok (purportedly by humanintroduction), have crossed Wallaces line.

The effectiveness as a faunal barrier of thismost widely-adopted division of the Orientalfrom the Australasian zoogeographic region, isgenerally attributed to the depth of the sea chan-nel extending from the Bali-Lombok Strait, be-tween Borneo and Sulawesi, to the east of thePhilippines. The deep Makassar Strait remaineda sea barrier when the Sunda and Sahul shelves

were exposed during glacial sea-level depres-sions. Huxleys line coincides approximately

with the eastern edge of the Sunda shelf, andLydekkers line with the western edge of theSahul shelf. These later variations on the divi-

sion have been regarded as clear-cut faunalboundaries enclosing a transitional zone.

However, major recolonization of the vol-canic Krakatau archipelago, 12 km away fromthe next nearest island, has occurred in only amatter of decades (Smith, 1943; Thornton,1996). No convincing explanation has been of-fered as to how a sea barrier such as the Bali-Lombok Strait, little more than three times as

wide, could have inhibited colonization for mil-lennia. Floating islands capable of transporting a

Biogeography and Geological Evolution of SE Asia, pp. 393-404Edited by Robert Hall and Jeremy D. Holloway 1998 Backhuys Publishers, Leiden, The Netherlands


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394 D. Brandon-Jones

viable sample of flora and fauna have been reli-ably reported. Even if these crossed a strait onlyonce a century, their impact on floral and faunalexchange between the two land masses wouldhave been significant. Conditions favouring

such rafting would have been enhanced duringperiods of climatic change (see the discussionbelow).

The inference (Brandon-Jones, 1996a) thatduring the glaciations Asian rainforest wasreduced by drought to a few scattered pocketsof distribution provides a more plausibleexplanation for these biogeographic barriers.Not only could rainforest communities on suchislands as the Philippines and Sulawesi, havebeen entirely eliminated, leaving only severelydegraded forest or no forest at all, but therecession of rainforest from some coastal areas,

would have seriously impaired the ability ofrainforest to disperse by rafting. Contraction andexpansion of rainforest distribution has been theprime mediator of present primate speciesdiversity on Borneo (Brandon-Jones, 1996b), insharp contrast to the probable presence there,demonstrated in this paper, of only two primatespecies before the penultimate glaciation. Ifsuch a faunal turnover can be established forBorneo, seemingly in the heart of the Asianmoist rainforest, extending such analysis toother Indo-Pacific islands should producefurther insights into the effects of climate changeon floral and faunal migration and diversity.

Glacial effects on Asian primate distribution

Both the pied leaf monkeys (Semnopithecusauratus, S. francoisi, S. hatinhensis, S. laotum,S. delacouriand S. johnii) of Java (Indonesia),northeast Indochina and southern India(Brandon-Jones, 1995), and the grizzled surelis(Presbytis comata) of Java, north Sumatra andnorth Borneo (Brandon-Jones, 1993, 1996a, b)display a tripartite disjunction. Brandon-Jones(1996a) inferred that the once continuous sub-

continental Indian, Chinese and SE Asian rain-forest was fragmented by a glacial drought190,000 years ago. It subsequently re-expanded,although probably not to its former extent, onlyto contract again during a second, less severedrought 80,000 years ago. Asian colobine mon-key zoogeography suggests that these droughtseliminated all but a few small pockets of rainfor-est. Such rainforest refugia survived in northSumatra, the Mentawai Islands (off westSumatra), north Borneo, west Java, northeast

Indochina and southern India (Brandon-Jones,1993, 1995, 1996a, b, 1997). Some of theserefugia are located at one thousand metres ormore in altitude, but most are areas which

would have remained sea-bound, either as

promontories or islands, or are coastal areas which retained a maritime climate duringdesiccative glacial sea-level depressions.

The dual contraction and re-expansion of therainforest led to the fracturing of the distributionof the pied leaf monkeys from continuity be-tween Java, northeast Indochina and southernIndia, to survival in those areas alone (Fig.1;Brandon-Jones, 1995). The prosimian loris has aparallel distribution, with an endemic represent-ative, Nycticebus pygmaeus, in eastern Indochi-na (Fig.2). This suggests a similar history of dis-junction and partial recolonization. In both cas-

es recolonization has been northward, undoubt-edly from Java in the case of the leaf monkeys,and probably so in the case of the loris. Gibbon(Hylobates) distribution is similar, but withoutan outlying population in southern India. Recol-onization has been extensive but incomplete. Atleast four primate genera (Hylobates, Presbytis,Semnopithecus and Macaca) have added Bor-neo to their pre-glacial distribution, but others(Pongo, Nasalisand Pygathrix) have undergonelittle or no post-glacial dispersal.

The Mentawai archipelago is the key to inter-preting the biogeography of Sumatra and Bor-neo. Ancestors of its endemic primates

(Hylobates klossii, Nasalis concolor, Presbytispotenzianiand Macaca pagensis) must formerlyhave existed on Sumatra, but no longer occurthere. The ebony leaf monkey (Semnopithecusauratus) can only have reached Java by way ofSumatra, from which it is also now absent.Presbytis potenzianiis sister-taxon to P. comataof north Sumatra, north Borneo and west Java(Brandon-Jones, 1993). An ancestral taxon simi-lar to P. potenziani is presumed to have beenthe initial coloniser of SE Asia. Hylobates klossiiand the gibbons of Java and (with some varia-tion) north Borneo, are chromatically monomor-

phic, unlike those of the Malay peninsula andSumatra. H. lar' vestitusof north Sumatra is re-placed in southern Sumatra by the polymorphicH. agilis. The call of the south Bornean gibbon(whose specific allocation, like that of H. larvestitus, remains debatable) is virtually identicalto that ofH. agilis(Geissmann, 1995). This indi-cates a geographic relationship between theMentawai Islands gibbon and other gibbonsanalogous to that between P. potenzianiand P.comata. H. klossiitodayis suggested to be mor-


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CHINA

INDOCHINA

Vietna

m

INDIA

Sumatra

M

alayPeninsula

BORNEO

Sarawak

Sabah

Sulawesi MOLUCCAS

LESSER SUNDA ISLANDSJava

Kraka

tau

Belitung

Bali Lombok

Flores

Timor

Siwaliks

Mindanao

PHILIPPIN

ES

0

20N

80W 100W 120W

Singapore

Kalimantan

Luzon

phologically conservative, descended directlyfrom the Mentawai progenitor of most, if not allother extant gibbons, except for the concolorgibbons and the siamang. Brandon-Jones (1993,1996a) inferred that all Sumatran primates (andSumatran primate habitats) disappeared duringthe earlier glacial drought, persisting only on theMentawai Islands, whose maritime climate pro-tected it from the desiccating effect of the glacialemergence of the Sunda shelf.

During the interglacial, Presbytis comatadi-verged from P. potenziani, and Hylobates larvestitus, H. muelleri and H. moloch divergedfrom H. klossii, as moist rainforest recolonisationof Sumatra, Java and southern Borneo facilitateddispersal from the Mentawai Islands. Pongore-invaded Sumatra, probably from Borneo, butpossibly from Indochina. During the later, andlesser drought, rainforest area contracted lessthan during the previous dry period, enablingthese recolonisers to survive in north Sumatra,

north Borneo and west Java. The absence ofNasalis, and of endemic subspecies ofSemno-pithecusand Macacain the Sumatran refugium, which sustained the more moist rainforest-associated Pongo, Hylobates and Presbytis,indicates that two deforestations occurred. Afterthe second dry period, independent evolutionof brownish species occurred on Sumatra (P.femoralis), Borneo (P. frontata) and Java (P.fredericae) from the populations of Presbytis

comatawithin those islands. P. femoralis disp-ersed to Borneo. Two reddish species, theSumatran P. melalophos, and the Bornean P.rubicunda are the end-products of chromaticsuccessions from black, through grey, thenbrown to red, and in some cases to albinistic,

which characterise colobine post-glacial disp-ersal (Brandon-Jones, 1996b). Each stage in thesuccession was probably correlated with aphase of rainforest regeneration. This suggeststhat climatic remission was punctuated, rather

Fig.1. The glacial refugial distribution of the pied leaf monkeys (Semnopithecus auratus, S. francoisi, S. hatinhensis, S. laotum, S.delacouriand S. johnii) after deforestation 190,000 years ago, with an estimate (dashed line) of their distribution before that date.


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than continuous.The endemic Mentawai Islands macaque,

Macaca pagensis, is closely related to thepigtailed macaque, M. nemestrina. Externallyhowever, the population on Siberut (thenorthernmost Mentawai island) is more similarto other members of its species group, such asthe lion-tailed macaque, M. silenus, isolated insouthern India, and the Sulawesi macaque, M.tonkeana. These Siberut, Sulawesi and southIndian macaques probably also have a glacially-fragmented distribution (Fig.3; Brandon-Jones,

1998). The distribution of Macaca nemestrinadwindles to a narrow corridor as it entersMeghalaya, India (Fooden, 1975; Biswas andDiengdoh, 1978), indicating it is a northward-dispersing species, yet to colonize Java andnorth Vietnam. The northern subspecies is palerin pelage colour which, by Hershkovitzs (1968)principles of metachromism, supports thisinterpretation. Although it had an earliercommon ancestor with the Sulawesi species, itsmost recent common ancestor was probably

with the macaque of the two southernmostMentawai islands.

Dating the deforestations

The silvered leaf monkey, Semnopithecuscristatus has reached islands such as Belitungand Serasan, and the long-tailed macaque,Macaca fascicularismany more. Their failure tocolonize the Mentawai Islands seems to reflect ashortage of time rather than ability, and

indicates that their geographic radiationsoccurred recently. S. auratus (a close relativeof S. cristatus) evidently did not spread from

Java between the two arid periods, suggestingthis interval was short. S. cristatus, Macacafascicularis and M. nemestrina are unrepres-ented by endemic taxa in the north Borneanrefugium and thus appear to have been absentfrom Borneo until after the second arid period.Subfossil evidence from Niah Cave in northwestBorneo indicates the presence there ofMacaca

Fig.2. The geographic distribution of the lorises (Lorisand Nycticebus).

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?

Nycticebus pygmaeus

Nycticebus coucang

Loris tardigradus

0N

20N

80W 100W 120W


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MentawaiIslands

Macaca silenus, M. pagensis and theSulawesi macaques

Macaca nemestrina

0N

20N

80W 100W 120W

before the most recent glacial maximum(Brandon-Jones, 1996a). The two most recentglacial maxima at about 135,000 and 21-22,000years ago, are indistinguishable in severity.Instead, they were preceded by a fluctuating,but persistent, temperature decline and suc-ceeded by a rapid temperature increase. Neitherof the two most recent glaciations included acold period preceded by a significantly colderone (Martinson et al., 1987). The more abrupt

onset of the earlier glaciation seems the onlyrelevant difference between the two glaciations.

At the end of each interglacial, precipitation ortemperature seems to have suddenly droppedbelow a critical threshold for widespread forestmaintenance, and this threshold was not re-attained until the beginning of the subsequentinterglacial. In the penultimate glaciation, thisthreshold was broken more abruptly, and thesucceeding interstadials offered little remission.The deforestations appear to have occurred

quite rapidly as the interglacials ended about190,000 and 80,000 years ago (Brandon-Jones,1996a), and the appearance of Macaca onBorneo before the most recent glacialmaximum, indicates that some reafforestationhad occurred by then.

An Indonesian deep-sea core, about 850 kmNNW of Australia, yielded grass pollen associ-ated with low sea-level dry glacial periods at190,000-130,000 years and 38,000-12,000 years

ago. Interglacial periods supported woodland/fern vegetation (Kaars, 1991). During the MiddlePleistocene, pine-grassland savannah similar tothe open woodlands of Thailand and Luzon(Philippines) occupied areas now characterisedby lowland rainforest near Kuala Lumpur, Ma-laysia (Batchelor, in Morley and Flenley, 1987).Palaeosol development in the intramontaneBandung basin, west Java, indicated an anoma-lously dry climate at the end of the penultimateglaciation about 135,000 years ago, followed by

Fig.3. The geographic distribution of the Macaca silenusspecies group.


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very warm and humid interglacial conditionsfrom 126,000 to 81,000 years ago (Kaars andDam, 1995).

At the advent of the last glacial period, about81,000 years ago, freshwater swamp forest on

the Bandung plain was replaced by an opengrass-and-sedge-dominated swamp vegetation,indicating a considerably drier climate. A similarclimate from 81,000 to 74,000 years ago in theadjacent mountains, is suggested by the strongdecline in Asplenium ferns. Their resurgencefrom 74,000 to 47,000 years ago, indicates a re-turn to slightly warmer conditions. Inferred de-pression of montane vegetation zones and fernscarcity from 47,000 to about 20,000 years ago,suggest distinctly cooler and possibly drier cli-matic conditions in the Bandung area (Kaars andDam, 1995). The survival at Niah until about

40,000 years ago of a giant pangolin, otherwiseknown only from the Middle Pleistocene of Java,conveys some impression of the then prevalentconditions. The tall termite mounds necessary tosustain this extinct species, almost a metrelonger than the largest living pangolin, are nowcharacteristic of savannah areas. Its MiddlePleistocene contemporaries, the hippopotamus,antelope, cattle, chital and other deer are all ob-ligate grazers. The terrestrial predators of thatera, which include hyenas, three genera of dogs,sabre-toothed cats, possibly two tigers, a leop-ard, leopard cat and civets, accord with this im-pression of a plains community. Data from Niah

Cave, the Tabon Cave in the Philippines, and theNgoum Rock shelter in Vietnam, indicate a cooldry period from 32,000 to 23,000 years ago. Theend of this period was even colder, producing arubble layer in the Ngoum Rock shelter, andprobably explaining the scarcity of monkeysand arboreal squirrels at Niah about 19,000years ago, and the disappearance from this lo-cality almost at sea-level, of two mammal gen-era, Hylomys and Melogale, now exclusivelymontane. This latter drought probably coincided

with the most recent glacial maximum when west Javan temperatures fell by 4-7oC. A syn-

chronous dry period occurred in Africa andSouth America. Since 23,000 years ago the cli-mate moderated, producing a stalagmitic floorin the Tabon Cave (Brandon-Jones, 1996a).

The Javan Quaternary fossil and climaterecord

Recent clarification, and improved dating, of the Javan fossil mammal record reveals several

faunal successions, and has been interpreted toindicate rainforest existence on the island foronly 80,000 years. Evidence is absent for mam-mals on Java before the first major sea level re-cession at 2.4 Ma. This suggests that before that

time, Java may have been largely submerged.The Ci Saat and Trinil faunas of 1.2 and 0.9 Marespectively, which mark the first appearancethere ofHomo erectus, were preceded by theoldest recognizable fauna, the Upper PlioceneSatir fauna at 2-1.5 Ma. This fauna includedGeochelone atlas, which persisted until at least1.2 Ma, after the first immigration ofStegodonto

Java, implying a more protracted faunal turnoverthan had been thought. The distribution of thisgiant tortoise at some time extended from Javato the Siwaliks in north India, and further under-mines the concept of rainforest stability. Be-

tween the impoverished Satir and the Ci Saatfaunal stage, both Tetralophodon bumiajuensisand Hexaprotodon simplexwere replaced by thenew immigrants, Stegodon and Hexaprotodonsivalensis.

A major faunal immigration, the KedungBrubus fauna, with the greatest abundance ofmedium to large-sized mammals, indicatingrelatively open and dry conditions, coincided

with a marked sea-level depression at 0.8 Ma. Ofits maximum number of 25 species, ten are newrecords, five of which are probably SE Asianmainland immigrants (Rhinoceros unicornis,Tapirus indicus, Manis palaeojavanica, Hyaena

brevirostrisand Lutrogale palaeoleptonyx). Mosttaxa from the Trinil fauna persist in the KedungBrubus fauna, and extinctions were negligible.Large bovids dominate both faunas, but withdouble the number of megaherbivores (eightagainst four) in the latter fauna. Palynologicalresults from the Sangiran area (with the excep-tion of an anomalous meter section whoseabundance of spores and Podocarpus tree pol-len indicates increased humidity) are poor intree pollen and spores, but rich in herbaceousplant pollen. Little change, other than a slightimpoverishment, is evident in the imprecisely

dated Ngandong fauna.The earliest evidence of both tropical rainfor-

est and Homo sapiensderives from the UpperPleistocene Punung fauna, probably correlated

with the warm interglacial from 125,000 yearsago onwards. Seventeen Kedung Brubus taxahad disappeared, with ten replacements. Thesereplacements include large numbers of primatessuch as Pongoand Hylobates, indicating a majorenvironmental change to humid conditions. Thepresence ofHomo sapiens, suggests an age less


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than 110,000 years. Bergh et al. (1996) dated thisfauna to 60-80,000 years, based on its similarity

with the Jambu and Lida Ajer Sumatran cave fau-nas, for which aspartic acid racemization datinggave ages of 60-70,000 years and 80,000 years

respectively. The invasion probably occurredbetween 80-110,000 years during the later partof the interglacial. Multiple extinctions with lim-ited replacement, are demonstrated by theHolocene fossil cave faunas, such as Wajak,Sampung and Hoekgrot. Pongo is absent fromthis composite cave fauna, and probably disap-peared from Java during the last glacial.

Variations in oxygen isotope levels frombenthic and tropical planktonic foraminiferasuggest that from about 2.8 Ma to 2.4 Ma icevolumes and sea levels fluctuated, with an over-all increase in the former and a decrease in the

latter, culminating at about 2.4 Ma in the firstmajor glaciation. Sea level fluctuations thenmoderated, remaining constant until 0.8 Ma,

with a mean of about 70 m below present daylevel (PDL), and lowest sea levels at about 100m below PDL. Although insensitive to short-term fluctuations, the one global Pleistocenelow sea level event detected by seismo-stratigraphy commenced at 0.8 Ma when sealevels were apparently exceptionally low forlong enough to register on many seismic pro-files. Sea level fluctuations then abruptly in-creased in amplitude, averaging about 90 m be-low PDL, with sea levels falling as low as 170 m

below PDL. This fluctuation mode persisted un-til recent times (Bergh et al., 1996).

Rainforest dispersal by island hopping

The correlation between glacial landmass emer-gence and aridity, refutes the notion that rainfor-est could readily have dispersed across the ex-posed Sunda and Sahul shelves. Conditions fa-vourable to dispersal returned only when thesea re-attained its interglacial level. This impliesthat SE Asian rainforest has perhaps perma-

nently been disjunct or insular in distribution,and has dispersed across sea barriers. Extensiveareas of grassland or desert on the other hand,

would pose insurmountable barriers. The pres-ence of Presbytis femoralis, but not Semno- pithecus obscurus, for example on Singapore,suggests the absence of an overland rainforestconnection even between Singapore and penin-sular Malaysia, although the dispersal route ofP.femoralis probably brought it within range ofSingapore earlier than did the dispersal route of

S. obscurus. Such distributional differences tendto confirm that, when exposed, Sundaland wasinimical to rainforest dispersal. This would sug-gest it was predominantly grassland-encom-passed desert, perhaps comparable to the dry

zone in present-day north Burma.If marine rainforest dispersal seems implausi-ble, a reliable account exists of a floating island

with unusually tall nipa palms being mistakenfor a three-masted vessel. The same report tellsof a pirate marooned on the bank of a hostileriver when his companions were forced to makea hurried embarkation. On seeing a small islandfloating to the sea, he swam to it and for manydays subsisted on its palm fruits. These islandsare created by floods undermining the mattedroots of riverside nipas (St. John, 1862, pp. 16-17). Natural rafts, sometimes carrying living

mammals, have been recorded over a hundredmiles off the mouths of tropical rivers, such asthe Ganges, the Amazon, the Zaire and theOrinoco (Matthew, 1915, p. 206). Such rafts arelikely to have been much more frequent duringthe post-glacial period of vegetational succes-sion, when primary rainforest graduallyreestablished itself at the expense of lowercanopy vegetation. Under-storey vegetation,steadily dying off as it became shaded out,

would have been increasingly vulnerable to theaction of river spates.

Needless to say however, the odds arestacked against successful rafting. Ironically, the

better the swimmer the less likely an animal is tocross a strait, because it will have less reluctanceabout deserting a raft and a greater ability to re-sist wind and currents. This is probably a majorfactor in the endemism of the ably swimmingproboscis monkey on Borneo, and the absencefrom Borneo of the tiger which occurs onSumatra, Java and Bali. To succeed, the raft mustoffer ample food and protection from the ele-ments, and the animal must be pregnant or ac-companied by a member of the opposite sex.These undoubtedly rare coincidences have en-couraged the belief that the deep sea channels

which remained as barriers when the Sunda andSahul shelves were exposed were sufficient tohave created Wallaces line and other suchfaunal divides. This ignores the most importantconsideration that, for successful rafting, landfallmust be accompanied by an appropriate cli-mate. Rainforest flora and fauna on a raft willnot flourish on arrival unless the raft lodges at alocality with adequate precipitation and tem-perature.

The deep sea channels were undoubtedly sig-


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nificant in maintaining localised maritime cli-mates when these disappeared elsewhere but,compared to climatological barriers, they wererelatively trivial in impeding dispersal. The lon-gevity of the potential dispersal route between

Asia and Australia is demonstrated by the pre-sumably Asian origin (other than of those intro-duced by man) of the New Guinea and Austral-ian rats (Muridae), which are now almost exclu-sively either endemic species, endemic generaor even endemic subfamilies (Simpson, 1977, p.115). These successful dispersers are compara-tively well able to cope with a range of climates,and perhaps exceptionally adept at survival onthe inimical conditions of a raft.

Pre-glacial Bornean primate impoverish-

ment

Although lingering on in Vietnam until about23,000 years ago (Ha Van Tan, 1985), and for-merly occurring in China (Kahlke, 1973) and

Java, the main stronghold of the orang-utan ap-pears to be Borneo. This suggests the existencethere of both orangs and their rainforest habitatbefore the first deforestation. Establishing thepresence of rainforest on Borneo may seem su-perfluous but, before this deforestation, the onlyprimate undoubtedly present was the endemicproboscis monkey, Nasalis larvatus. Its anatomy,and that of its only close relative, Nasalis

concolor, on the Mentawai Islands, is that of apredominantly terrestrial monkey, and is veryreminiscent of macaques. The genus evidentlyevolved in forest-woodland (Brandon-Jones,1996a). Its natural habitat must intermittentlyhave been overwhelmed by mangrove and rain-forest. The proboscis monkey remained on Bor-neo only because its island distribution pre-vented it from following the climatic and geo-graphic recession of its native vegetation. Evenin isolation, this is clear evidence of former ex-tensive areas of open woodland on Borneo.Nevertheless, the fact that the proboscis monkey

and the orang-utan have not reclaimed centralSarawak suggests that, at glacial extremes, mostof the open woodland disappeared, leaving thetwo primate species with a very localised distri-bution in north (and perhaps west) Borneo.

Presbytis and Hylobates are represented inthe Bornean refugium by the second-wavecolonizers, Presbytis comata and Hylobatesmuelleri, but not by the initial colonizing ances-tors ofP. potenzianiand H. klossii. Having es-tablished the probability of rainforest there dur-

ing the first dry period, the absence of these ini-tial colonizing species implies their genera werethen absent, otherwise they would be expectedto persist in Borneo, cohabiting with their de-scendent congeners. Such areas of sympatric

distribution in Borneo do exist for both surelispecies and gibbon species (see Brandon-Jones,1996b; Mather, 1992). It is possible that thetarsier was also absent and survived the first aridperiod only on Sulawesi, where its vertical cling-ing and leaping adaptation would have equip-ped it well for survival in shrub vegetation, evenif rainforest disappeared. Despite Simpsons (1977)reservations, this accords with Groves (1976)view that Sulawesi might have been a centre oforigin for the tarsier. The loris may have sur-vived only in Java, Indochina and southern In-dia. Thus there is the distinct possibility that,

until 190,000 years ago at the earlier deforesta-tion, or even until 135,000 years ago at the pe-nultimate glacial maximum, there were only twoprimate species on Borneo. This does not estab-lish that Bornean rainforest is necessarily ofsimilar age, but it implies that gibbons, a familyendemic to Asia, are latecomers to Borneo.

Modern Bornean primate diversity

How then do we account for the present pri-mate diversity on Borneo? Probably the first ar-rivals after the orang-utan and the proboscis

monkey, were Presbytis comata and Hylobatesmuelleri, which reached Borneo between thedeforestations. It is possible that the loris andthe tarsier also invaded during this interval, butmore probable that, with the macaques and sil-vered leaf monkey, they did not arrive until afterthe second deforestation. The white-frontedsureli, Presbytis frontatadiverged in situfrom P.comata sabana after the latter event. Its otherBornean congeners, P. femoralis (directly) andP. rubicunda (indirectly), diverged from P.comata thomasi on Sumatra (Brandon-Jones,1996b). If the south Bornean gibbon is a subspe-

cies ofHylobates agilis, it was another Sumatranimmigrant to arrive on Borneo since the seconddeforestation, otherwise it presumably evolvedin situfrom H. muelleri. All the extraneous pri-mates evidently rafted to Borneo, because of theunavailability of suitable habitats for dispersalacross Sundaland. P. femoralis and P. rubi-cunda seem to confirm this by their allopatricdistribution in Kalimantan, compared to theirsympatric distribution in Sarawak, Borneo. Thisgeographic variation in sympatry is virtually ir-


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reconcilable with the concept of prolonged rain-forest stability. It is readily explained by infer-ring recent arrival in separate localities on the

west coast (the only other island occupied by P.rubicunda is Karimata which it presumably

colonized en route), followed by parallel east- ward dispersal, which was more extensive orrapid in P. rubicunda. If rainforest had existedin central Sundaland, the two species wouldsurely have become sympatric much further

westward than they do. As predicted byHershkovitzs (1968) principles of meta-chromism, pelage colour in both P. rubicundain north Borneo, and P. melalophos in southSumatra, dilutes to a pale colour.

Borneo as a dispersal barrier

It is possible that primate impoverishment onBorneo, before the first deforestation, was sim-ply due to an arid coastal climate which pre-vented rafted rainforest from establishing itself.This is supported by Stresemanns (1939) con-clusion that grassland widespread in SE Asiaduring the Pliocene persists in south Borneo,and by the apparent entire extirpation and re-placement during the Pleistocene of the south-

west Bornean freshwater fish fauna (Brandon- Jones, 1996a). By restricting animal and plantcolonization of south Borneo the dry zone re-sponsible would have diminished its potential as

an intermediate route to Sulawesi. Virtually allthe 183 butterfly genera on Sulawesi are Asian,

with no special link to Borneo. A set of youngerpatterns based on the distribution of the 470species (200 of which are regional endemics)links Sulawesi to the Philippines, Lesser SundaIslands and especially the Moluccas, in additionto Asia (Vane-Wright, 1991). This circum-Bornean faunal zone is also reflected in Hooijers(1975) suggestion that Sulawesi, Flores, Timorand intervening small islands had Pleistocenegeographic continuity as Stegoland. The propo-sition of such broad land connections across

waters now nearly 3000 metres deep is geologi-cally tenuous and is rendered superfluous by thepresence of indistinguishable large Pleistocenestegodonts on Mindanao (in the Philippines)and on Java (Simpson, 1977, p. 113). The possi-bility of a physical connection of the latter is-lands with the others is almost negligible. Al-though Groves (1976) believed that mammalmigration between Sulawesi and the Philippines

was insignificant, the stegodont dispersal be-tween these islands must have crossed sea barri-

ers. Sulawesi organisms with Indomalayan af-finities evidently circumvented Borneo, via Javaor the Philippines, many of their ancestors alongthe route, being eliminated by subsequent gla-cial drought.

The climatic origin of Wallacea

Simpson (1977, p. 117) concluded that Huxleysline, which approximately coincides with theeastern edge of the Sunda shelf, and Lydekkersline, which roughly corresponds to the westernedge of the Sahul shelf, are clear-cut faunalboundaries separated by an unstable zone, nowoften termed Wallacea. He declined to catego-rize the intermediate zone as transitional, in or-der to encourage further research on its bioge-

ography. The possibility that this unstable zonewas at least partly created by climatic barrierswas appreciated as early as 1845 (Mller, 1846).Lincoln (1975) concluded that Wallaces line

was primarily an ecological division, with theLesser Sunda Islands to the east of the line beingdrier and smaller with an impoverished butdominantly Oriental avifauna. Smith (1943, p.140) remarked that the Philippines, Sulawesiand the Lesser Sunda Islands, as compared toBorneo, Java and Sumatra, are notable for theabsence of large mammals, not because theycould not have reached them, but because theycould not survive upon them if they got there.

Pleistocene mammals contradict this. Theformer presence of somewhat diverse probosci-deans on islands between the Huxley andLydekker Lines remains a puzzling fact that mustbe taken into account The large stegodonts,ubiquitous where any Pleistocene mammals areknown, surely were not all victims in the firstgeneration of occupants (Simpson, 1977, p. 113).Perhaps these elephant-like mammals thrivedduring relatively dry glacial periods of extensivegrassland, and died out during excessive aridity

when much of it turned to desert. As the climatechanged their island distribution would have, as

with the proboscis monkey, curtailed their abil-ity to follow their preferred habitat.

Australasian organisms spreading northwest-wards would have experienced a similar seriesof advances and local extinctions on their pre-carious stepping-stone route to Asia. Relativelyfew of them, such as the Sulawesi phalangers,have successfully negotiated the climatic adver-sities (and perhaps superior competition) inter-mittently intervening to obstruct their passage.Islands along the route have varied (according


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to their size, topography and geographic situa-tion) in their ability to sustain varying grades ofvegetation for varying periods of time. Manyspecies presumably had precursors eliminatedfrom islands behind them on the route, and pos-

sibly their descendants from islands ahead ofthem. Steenis (1935, p. 404) for example, notedthat Mount Kinabalu in Sabah, Borneo, is farricher than Timor in Australian temperate plants.Hence the need for caution in inferring dispersalroutes from existing distributions. A species ab-sence can be as informative as its presence. Thenet result has been an ebb and flow of dispersalcorrelated with the glacial cycles. Wallaces lineand other faunal divides such as Mllers and

Webers, may therefore mark only the approxi-mate midpoint between two or more rainforestglacial refugia in Australasia and SE Asia.

Conclusions

Asian primate distribution indicates that mostAsian rainforest was eliminated by glacial drought.Sumatran primate distribution indicates that thisoccurred at least twice, and that the most recentdeforestation was less drastic than its predeces-sor. The two deforestations appear correlated

with the terminations of the two most recentinterglacial periods. The Javan fossil record sug-gests that before these interglacials, conditionsgenerally favoured open country animals. The

correlation between landmass emergence andaridity implies that SE Asian rainforest dispersal,successfully negotiated sea barriers. Indicationsthat southwest Borneo had a prolonged arid cli-mate which would have prevented rafted rain-forest from establishing itself, provides an expla-nation for the apparent necessity for most faunato bypass it on their route to islands further east.The contrast between evident pre-glacial Borneanprimate impoverishment and its present primatediversity, provides a model for the effects of cli-mate change on SE Asian island biogeography,and demonstrates how such effects could have

restricted faunal and floral interchange betweenAustralasia and SE Asia.

Acknowledgements

I am most grateful to my wife, Chris Brandon- Jones, for the preparation of the maps and toher, Peter Andrews, Jeremy Holloway and MarkPilkington for constructive criticism of themanuscript.

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