the indochinese–sundaic faunal transition at the isthmus of kra: an analysis of resident forest...

The Indochinese–Sundaic faunal transition at theIsthmus of Kra: an analysis of resident forest birdspecies distributionsJennifer B. Hughes1�, Philip D. Round2 and David S. Woodruff1* 1Ecology, Behavior,

Evolution Section, Division of Biological Sciences, University of California, San Diego, La Jolla,

CA 92093-0116, USA, 2Department of Biology, Mahidol University, Bangkok, Thailand

Abstract

Aim To establish the geographical position of the biogeographical transition betweenIndochinese and Sundaic faunas using distributional data for the best-documented taxon,the birds.

Methods Distributional data of 544 resident forest and forest edge bird species ofThailand and the Thai–Malay peninsula were examined at 45 sites spanning 15� oflatitude from northern-most Thailand to the southern peninsular Malaysia. Sites weregrouped into 23 degree or half-degree latitudinal zones and avifaunal similarity coeffi-cients were calculated between each zone.

Results A Mantel test revealed a significant transition between northern Indochineseand southern Sundaic (Indomalay) avifauna assemblages just north of the Isthmus of Kra(10�30¢ N). Northern and southern range limits of 152 species (> 269 species andsubspecies combined) lie between 11� and 13� N.

Main conclusions This transition between zoogeographical subregions is not coincidentwith the widely recognized transition between floristic provinces which is traditionallyplaced 400–500 km further south at the Kangar–Pattani line, but is associated with achange from wet seasonal evergreen dipterocarp rain forest to mixed moist deciduousforest north of the Isthmus of Kra in the northern Thai–Malay peninsula. Climatologicaland ecological factors associated with the distribution of forest types today are reviewedand it is hypothesized that the avian transition tracks the northern phytogeographicalboundary. Palaeogeographical factors, including hypothetical Neogene seaways, whichmay account for the historical development of both phytogeographical and avifaunaltransitions are also described.

Keywords

Geographical range limits, biogeographical boundaries, phytogeography, Malaysia,Thailand.

INTRODUCTION

Wallace (1869, p. 158) correctly recognized a �time when thewhole of the Java sea, the Gulf of Siam, and the Straits ofMalacca were dry land, forming, with Borneo, Sumatra, and

Java, a vast southern prolongation of the Asiatic continent�.This area is now called Sundaland and recognized as adistinct floristic province and zoogeographical subregion.Although considerable research has focused on Wallace’sline and the eastern limits of this biota (Whitmore, 1981,1987; Metcalfe et al., 2001), little attention has been paid tothe Indochinese–Sundaland transition, which Wallace placedin the Tenasserim region of the northern Thai–Malay pen-insula. Finding his dictum (1869, p. 24) that �Birds offer usone of the best means of determining the law of distribution�still holds true today, we base this analysis of the zoogeo-graphical transition on avifaunal records.

*Correspondence: David S. Woodruff, Division of Biological Sciences,

University of California, San Diego, La Jolla, CA 92093-0116, USA. E-mail:

[email protected]�Present address: Jennifer B. Hughes, Department of Ecology and

Evolutionary Biology, Brown University, Providence, RI 02912, USA.

Journal of Biogeography, 30, 569–580

� 2003 Blackwell Publishing Ltd

Provincialism remains a central concern of biogeographers(Myers & Giller, 1988; Williams, 1996; Brown & Lomolino,1998; Cox, 2001) and biogeographical discontinuities andtransitions are of interest to both ecologists and paleogeog-raphers. The rapid turnover of taxa at provincial boundariesbegs both historical and biological explanation. The positionof transitions may be associated with present or formerbarriers to dispersal, and with the effects of dispersal, com-petition and invasibility, and obligate co-distribution (Brown& Lomolino, 1998). Here we are interested in the zoogeo-graphical transition between the Indochinese Subregion andthe Malayan Subregion (Wallace’s Indo-Malayan Subregion)of the Oriental Region, and the corresponding phytogeo-graphical transition between the Continental SE AsiaticFloristic Province and the Malayan Floristic Province of theIndo-Malayan Subkingdom (Good, 1964). Wikramanayakeet al. (2002) recently described this as the transition betweenthe Indochina Bioregion and the Sunda Shelf and PhilippinesBioregion. Herein, we will use the terms Indochinese andSundaic for the northern and southern biotas, respectively.In describing forest types we follow Ashton (1995) andrecognize seasonal evergreen rain forest and mixed moistdeciduous forests; other workers call the seasonal rain forest�semi-evergreen forest� and the deciduous forest �monsoonforest�.

Kloss (1915), Robinson & Kloss (1921–1924) and Deignan(1963) provided basic information on avifaunal distributionon the Thai–Malay peninsula, and Wells (1976) provideda preliminary analysis of the data as it affects the transition.Wells found that many forest bird species have their distri-butional range limits at the southern end of the Tenasserim,at the Isthmus of Kra (10�30¢ N) where the peninsula is only45 km wide (Fig. 1). However, he did not conduct a detailedanalysis or address the question of whether species assem-blages differ significantly above and below the isthmus. Herewe report distributional data of resident forest birds ofThailand and assess the statistical significance of a turnoverof species along the latitudinal gradient. We discuss eco-logical and geological evidence that might account for thezoogeographical pattern which, unlike the Central Americanand Asian-Australian transitions, cannot be explained byplate tectonics. Instead, we will focus on the possible rela-tionship between the avian transition and vegetation, asMacArthur & MacArthur (1961) showed how bird speciesdistributions, and the diversity of bird communities, arehighly dependent on vegetation structure. There are twophytogeographical transitions on the peninsula: (1) betweenperhumid evergreen rain forest and wet seasonal evergreenrain forest, 400–500 km south of the Isthmus of Kra nearthe Thai–Malay border (Steenis, 1950), and (2) between wetseasonal evergreen rain forest and mixed moist deciduousforests just north of the isthmus (Richards, 1996). Althoughthe avifauna may be co-distributed with the vegetation typestoday this does not account for the development of eitherplant or avian biogeographical patterns. Here, and in com-panion papers (Woodruff, 2003a,b), the evidence for thehistorical cause of the divergence of Indochinese and Sundaicbiotas will be reviewed.

MATERIAL AND METHODS

One of us (PDR) has assembled the most detailed set ofconfirmed bird records available for Thailand. The recordsused here are reported elsewhere (Round et al., 2003) andare based on personal observations over the period 1979–94,on reliable published records (e.g., Holmes, 1973; Holmes &Wells, 1975), and on bird watcher’s reports reviewedmonthly by a committee of the Bird Conservation Society ofThailand (formerly Bangkok Bird Club). The 1990 versionof these records formed the basis of the species range maps inthe standard field guide to the birds of Thailand (Lekagul &Round, 1991) and, for convenience, we have followed thissource for generic and species names. [The new guide byRobson (2002) uses the same maps with minor updating.]Using the 1994 records for the occurrence of birds at forty-six specific sites, we created a data base of the current dis-tributions of 544 bird species and subspecies from fifty-threetaxa (families, subfamilies and tribes) (Table 1). Recognizingsubspecies in the field is difficult so we were for the most partreliant on older published data to establish subspecific dis-tribution limits. In addition, we added records for Malaysiabased on the work of Medway & Wells (1976). We focusprimarily on rain forest birds but also include species char-acteristic of deciduous forests and forest edges. We excludedfamilies of shorebirds, waterbirds, Palaearctic migrants, non-breeding visitors, species known from only a single sighting,and most open country residents from the analyses as theirdistributions are constrained by different parameters. Wealso excluded a few species restricted to southeast Thailandwhose current ranges are remote to the peninsula. Onlyfamilies with two or more species found in Thailand wereincluded. The forty-six site survey records were used toestablish northern and southern species range limits intwenty-three latitudinal zones (A–W) ranging from Malaysia(lumped as �5� N�) and the southern border of Thailandadjacent to Malaysia (6� N) to the northern border withLaos and Myanmar (> 20� N)(Table 2).

Jaccard’s (1908) coefficient of community (S) was used tocalculate a matrix of similarities between sites

S ¼ a=ða þ b þ cÞwhere a is the number of species present in both sites, and band c are the number of species present at one site and notthe other. Double absences are excluded so as not to indicateresemblance.

Similarity values between two sites are negatively relatedto the distance between those sites (Fig. 2). In the followinganalysis, we used the residuals of a non-linear regression(y ¼ 0.002x2)0.062x þ 0.651, r2 ¼ 0.610) to offset theinfluence of distance. [Here data from Malaysia (<6� N)and north of the Thailand border (> 20� N) were excluded,because these zones cover > 1� of latitude.]

Multidimensional scaling of the similarity matrix pro-duced a two dimensional plot of the localities, where thedistance between the coordinates represents the differencebetween avifaunas at different sites. We used a cluster ana-lysis to determine the significance of the groupings.

� 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 569–580

570 J. B. Hughes et al.

If different assemblages of northern and southern avifaunaexist, then the degree of similarity between two localities isdependent upon whether they are in the same region or not.We tested this hypothesis for each latitude. We generated abinary matrix to represent a division of northern andsouthern regions. Sites which occurred on the same side ofthe dividing line were assigned a �1�, those in opposite regionswere assigned a �0�. A matrix of the residual similarity valueswas then compared with the binary matrices using theMantel test statistic (Z) (Mantel, 1967; Sokal & Thomson,1987). The Mantel statistic is computed as the sum of thecell-by-cell multiplication of the two matrices. The larger thecorrespondence between the matrices, the larger the calcu-lated Z statistic. We used a Monte Carlo simulation togenerate a distribution of possible values. For each permu-tation, two random columns and the corresponding rows ofthe binary matrix were transformed, and a Z value wascalculated with a program written by and available fromJBH. The statistical significance of the original value of Zwas then determined by comparison to this distribution.

The same analysis was repeated including subspeciesdivisions among the species, increasing the data set to 724species and subspecies. In cases where subspecies� geo-graphical ranges are not well defined we set range limits inthe middle of the undecided area, usually 1� of latitude or100 km. The nonlinear regression of the similarity coeffi-cients between localities and their distance apart was cal-culated (y ¼ 0.004x2 )0.1x þ 0.652, r2 ¼ 0.729) and, as inthe above case, the residuals of this regression were used totest the statistical significance of a transition between nor-thern and southern avifauna.

RESULTS

The most frequent latitudinal limits of the species examinedare between 11� and 13� N, just north of the Isthmus of Kra(Fig. 3–4). Approximately 152 species had northern orsouthern range limits between these latitudes. This amountsto 28% of the bird species considered and more than half thespecies occurring in this 200 km wide latitudinal zone.

Figure 1 Approximate latitudinal limits of

resident taxa of forest associated birdsoccurring between 15� N and 6� N latitude

on the Thai–Malay Peninsula. The length of

each bar represents the number of distribu-tional limits of species and subspecies at that

latitude. A significant number of taxa have

range limits between 13� N and 11� N lati-

tude just north of the Isthmus of Kra. Thisavifaunal transition is spatially associated

with the transition between rain forest and

mixed deciduous forest that lies near Tavoy

on the west coast and Chumphon on theGulf of Thailand. 500 km further south, the

Kangar–Pattani line marks the approximate

northern boundary of Sundaic rain forest

(Steenis, 1950; Whitmore, 1984) and thetransition between the Malaysian [Indomalay

or Malesian] and the Thai-Burmese [Indo-

chinese] floristic provinces. Elevations above100 m are shaded. Scale bar shows 100 km.


Avian transition at the Isthmus of Kra 571

Table 2 Statistical analyses of avifaunal relationships for species and for subspecies from specific localities grouped into 23 latitudinal zones

(A–W). The Mantel probability (P-values) pertain to the transition between the avifauna of a specific zone and the next most southerly zone.

Latitudes are the northernmost limits of the zones

Zone (� N) Localities

P-value

species only

P-value with

subspecies

A > 20� Doi Pha Hom Pok – –

B 20� Doi Chiang Dao 1.00 1.00

C 19� Doi Inthanon; Doi Suthep-Pui 0.99 1.00

D 18� Om Koi; Phu Luang; Phu Kradeung 0.97 1.00E 17� Mae Sot; Phu Khieo; Nam Nao; Thung Salaeng Luang 0.99 0.98

F 16� Huai Kha Khaeng; Thung Yai; Umphang 0.98 1.00

G 15� Bung Kroeng Kavia 0.81 0.97H 14�30¢ Khao Yai 0.29 0.76

I 14� Sai Yok 0.20 0.71

J 13�30¢ Khao Soi Dao 0.03 0.07

K 13� Kaeng Krachan < 0.001 < 0.001L 12�30¢ Hua Hin; Khao Sam Roi Yot < 0.001 < 0.001

M 12� Prachuap; Khao Luang; Khao Nok Wua < 0.001 < 0.001

N 11� Thasan; Thae Sae 0.22 0.002

O 10� Ranong; Tapli 0.26 0.03P 9�þ9�30¢ Khao Sok; Khlong Saeng, Khlong Nakha 0.86 0.61

Q 8�30¢ Khao Phanom Bencha; Khlong Phraya; Krabi; Khao Nong; Khao Luang 0.91 0.74

R 8� Khao Nor Chuchi; Khao Pu-Khao Ya 0.93 0.89

S 7�30¢ Trang; Khao Banthad 0.82 0.77T 7� Thale Ban; Ton Nga Chang 0.53 0.65

U 6�30¢ Pattani 0.35 0.44

V 6� Yala and Narathiwat provinces – –W �5�� Malaysia – –

Table 1 Families, subfamilies/tribes included in the analysis arranged following Sibley & Monroe (1990)

Accipitridae Hawks Malaconotinae Bushshrikes

Aegithininae Ioras Megalaimidae Asian barbetsAlaudidae Larks Meropidae Bee-eaters

Alcedinidae Kingfishers Muscicapinae/Muscicapini Flycatchers

Apodidae Swifts Muscicapinae/Saxicolini Chats

Batrachostomidae Asian frogmouths Nectarinidae Flowerpeckers, sunbirdsBucerotidae Hornbills Phasianidae Pheasants

Caprimulgidae Nightjars Picidae Woodpeckers

Centropodidae Coucals Pittidae PittasCeryliidae Kingfishers Passeridae/Estrildinae Munias

Chloropseidae Loras, leafbirds Passeridae/Ploceinae Weavers

Cisticolidae African warblers Passeridae/Passerinae Sparrows

Columbidae Pigeons Psittacidae ParrotsCoraciidae Rollers Pycnonotidae Bulbuls

Corvinae/Oriolini Cuckooshrikes Rallidae Rails

Cuculidae Cuckoos Strigidae Owls

Dicrurinae/Rhipidurini Fantails Sturnidae Starlings, mynasDicrurinae/Dicrurini Drongos Sylviidae/Acrocephalinae Warblers

Dicrurinae/Monarchini Monarchs Sylviidae/Megalurinae Grassbirds

Eurostopodidae Eared-nightjars Sylviidae/Garrulacinae LaughingthrushesEurylaimidae Broadbills Sylviidae/Sylviinae Babblers

Falconidae Falcons Tytonidae Barn owls

Hemiprocnidae Tree swifts Trogonidae Trogons

Hirundinidae Swallows Turdinae ThrushesIrenidae Leafbirds Turnicidae Buttonquails

Jacanidae Jacanas Zosteropidae White-eyes

Laniidae Shrikes



Within most of the bird families, some species appear tobe restricted to either northern Indochinese or the southernSundaic provinces, while others occur across the wholelatitudinal range (Fig. 3). About 190 species are exclusivelyIndochinese, 150 are Sundaic, and another 147 are wide-spread; of these latter, eighty-six have both Indochinese andSundaic subspecies (data in Round et al. (2003). Fifty-sixother species are �montane island-hoppers� occurring inthe hills of northern Thailand and the hills of peninsularMalaysia but not in the intervening central Thai–Malaypeninsula. In Fig. 3 all categories of widespread species are

placed arbitrarily below the Sundaic fauna at the base of thefigure. Families that best illustrate these patterns of speciesreplacement, with congeneric Indochinese and Sundaic spe-cies, include the woodpeckers (Picidae), pheasants (Phasi-anidae), and bulbuls (Pycnonotidae) (Figs 5–7). In thewoodpeckers, for example, there are eleven Indochinesespecies, sixteen Sundaic species, and eight widespread spe-cies of which five show significant range gaps in the northernand central peninsula. There are at least five congenericbiogeographical species replacements involving northern andsouthern congeneric species with non-overlapping southernand northern range limits. There are also thirteen caseswhere northern and southern subspecies replace one anotheralong the transect. Only one of eleven Indochinese speciesshow subspecific differentiation, while seven of sixteenSundaic and five of eight widespread species show suchgeographical differentiation. In the pheasants, there are ele-ven Indochinese, seven Sundaic and three widespread spe-cies. In the bulbuls, eleven Indochinese species are replacedby seventeen Sundaic species and seven more are wide-spread. As in the woodpeckers relatively more sub-speciationoccurs in the southern than in the northern species.

The multidimensional scaling plot divides the localitiesinto two groups: (1) the localities from 12� N to the nor-thern border of Thailand (latitudinal zones A–M), and (2)the localities from Malaysia to 11� N (zones N–W) (Fig. 8).The Mantel test detected significant transitions of the nor-thern and southern assemblages of bird species between 11�and 13�30¢ N (P < 0.001)(Table 2). These results also holdwhen the range limits of the subspecific taxa are included(n ¼ 269); the Mantel test is highly significant for transitionsbetween 10� and 12�30¢ N (P < 0.002) and significant at the9�30¢/10� N boundary (P ¼ 0.032) (Table 2).

Figure 3 The latitudinal ranges of all 544resident forest bird species between China

and central Malaysia plotted as stacked bars.

The height of a bar with fifty species is indi-

cated. Species are sorted according to thelatitude of their southern or northern range

limit along the transect from > 20� N to

< 6� N. Three patterns are recognizable:

(1) a group of Indochinese species (top) fol-lowed by (2) a group of Sundaic species

(middle), and (3) species that occur in both

provinces (arbitrarily placed at the bottom ofthe stack). For those species with range limits

along the transect, species borders are not

evenly distributed; sharp steps in the stacking

pattern indicate a disproportionate numberof range limits just north of the Isthmus of

Kra between 11� N and 13� N latitude (data

in Round et al., 2003).

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

0 2 4 6

Latitude distance

Sim

ilarit

y

8 10 12 14

Figure 2 Avifaunal similarity between two latitudinal zones in

relation to the distance between the zones.



Our prime result is therefore that there is a markedavifaunal transition north of the Isthmus of Kra and nodetectable cluster of species boundaries further south near

the transition between perhumid and wet seasonal evergreenrain forest types (see below) at 7� N.

Figure 4 The number of species taxa reach-

ing their distributional limit at the latitudeindicated.

ID#

>20 20 19 18 17 16 15

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PicidaeGecinulus grantia 400Dendrocopus cathpharius 422D. mahrattensis 426D. hyperythrus 423D. atratus 424Picus erythropygius 406Meiglyptes jugularis 419P. xanthopygaeus 404D. macei 425Sasia ochracea 394 ++ ++ ++ ++ ++ ---- ----Hemicircus canente 420Reinwardtipicus validus 396P. mentalis 411H. concretus 421S. abnormis 395Dinopium rafflesii 399P. miniaceus 409 +++ ++ ++ ++ ++ ++ +++P. puniceus 410Blythipicus rubiginosus 413M. tukki 418M. tristis 417P. viridanus 403 ++ ++ ++ ++D. javanense 398 +++ ++ ++ ++ ++ +++Muelleripicus pulverulentus 415 +++ +++ ++ ++ ++ ++ ++ +++Dryocopus javensis 416 +++ ++ ++ ++ ++ ++ +++Celeus brachyurus 412 ++ ++ ++ ++ ++ ---- ---- ---- ---- ---- ---- ---- ----P. vittatus 402 +++Picumnus innominatus 393G. viridis 401 +++ ++ ++ ++ ++ +++P. canus 405 +++P. flavinucha 407 ++ ++ ++ ++ ----P. chlorolophus 408 +++B. pyrrhotis 414D. canicapillus 427 ++ +++ +++ ++ ++ ++ ---- ---- ----Chrysocolaptes lucidus 397 +++ ++ ++ ++ ++ ++ +++

Figure 5 The latitudinal distribution of species and subspecies of the woodpecker family (Picidae). The occurrence/absence of each taxon

(species ID #�s from Lekagul & Round, 1991) with sites grouped by latitudinal zone. Column headings are latitudes (� N) with �Malay� beingpeninsular Malaysia (<6� N). Generic names can be discerned from the species numbers. Different symbols show the ranges of different

subspecies; the shaded cell marks an uncertain subspecies break.



DISCUSSION

These analyses support the hypothesis that a significantturnover in bird species assemblages occurs between 11� and13� N on the Thai side of the Thai–Malay peninsula. At thespecies level the Sundaic avifauna is clearly different fromthat of the Indochinese subregion. Comparable documenta-tion of the magnitude and geographical position of thezoogeographical transition in other terrestrial animals arestill lacking but, as a broad generalization, mammals, rep-tiles, amphibians and butterflies appear to exhibit similarpatterns (Lekagul et al., 1970; Corbet & Pendlebury, 1992;J. Nabhitabhata, pers. comm., 1996). The geographicalranges of mammals described by Lekagul & McNeely (1988)and Corbet & Hill (1992) show that numerous species andsubspecies boundaries lie near the Isthmus of Kra. Morerecently, Chaimanee (1997) has analysed the extant rodentfauna and found that, of sixty-one species, 61% have rangelimits associated with the Isthmus of Kra. Amphibian speciesalso show turnover at the isthmus but more Indochinesespecies extend south than Sundaic species extend north of thetransition (Inger, 1966). Interestingly, Corbet & Pendlebury(1992) reported the opposite tendency in butterflies.

In contrast to the patterns in terrestrial animal distribu-tions there are two phytogeographical transitions on theThai–Malay Peninsula (Fig. 1). The southern transition,between perhumid and wet seasonal evergreen dipterocarprain forests, lies near the Thai–Malay border. The northerntransition, between seasonal evergreen rain forest and mixedmoist deciduous forests, lies north of the Isthmus of Kra.

The southern transition is widely and prominently por-trayed as the major Indochinese–Sundaic plant boundary(Steenis, 1950; Good, 1964; Udvardy, 1969; Keng, 1970;

Whitmore, 1984; Ashton, 1992; Richards, 1996; Wikra-manayake et al., 2002)(Fig. 1). Steenis first characterizedthis major transition on the basis of distribution maps heprepared for 1200 genera of plants. He found that 375genera of Sundaic plants reach their northern limits, and200 genera of Indochinese plants reach their southern lim-its, at a north–south line between Songkhla (Thailand) andAlor Setar (Malaysia)(Steenis, 1950, p. lxxi–lxxii). Whit-more (1984), as a result of additional fieldwork on speciesof dipterocarps, subsequently rotated this boundarybetween the floral provinces by 90� to a line running west–east between Kangar (Malaysia) and Pattani (Thailand) atc. 7� N latitude along the Thai–Malay border. The positionof the Kangar–Pattani line forest transition has beenattributed to the increasing seasonality north of this line(Whitmore, 1984; Ashton, 1992). Baker et al. (1998) alsoput the boundary of the Malesian flora on the Thai–Malayborder.

The Kangar–Pattani phytogeographical transition is notwell explored ornithologically and additional species andsubspecific borders may be discovered in this area. Forexample, some species (e.g. black-capped babbler, Pellor-neum capistratum) treated as belonging to the same sub-species throughout Malaysia and Thailand, call withdifferent dialects on either side of the Kangar–Pattanitransition (PDR, own data). Others like the banded pitta,Pitta guajana are insufficiently known in this area; theextreme southern Thai birds may be referable to theMalaysian subspecies irena rather than the peninsular Thairipleyi. Regardless of such minor revisions, it is clear thatmost of the birds simply ignore the Kangar–Pattani line.

Whitmore (1984, p. 201) and Richards (1996, p. 403–4)have described this southern transition at Kangar–Pattani

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PhasianidaeSyrmaticus humiae 123Bambusicola fytchii 136Lophura nycthemera 119L. diardi 121Arborophila rufogularis 128A. brunneopectus 129Coturnix coromandelica 139Francolinus pintadeanus 137L. leucomelanos 118A. chloropus 131 ++ ++ ++Polyplectron bicalcaratum 124P. malacense 125L. ignita 120A. charltonii 132Rollulus rouloul 134Rhizothera longirostris 135Argusianus argus 126Caloperdix oculea 133Pavo muticus 127 +++ ++ ++Gallus gallus 122C. chinensis 140

Figure 6 The latitudinal distribution of species and subspecies of the pheasant family (Phasianidae). See Fig. 5 for details.



line as the �Kra ecotone� despite the fact that it lies c. 500 kmsouth of the Isthmus of Kra. Soepadmo (1995) explicitlyequates the Isthmus of Kra with Steenis� turnover of plantgenera at the Thai–Malay border and Hirai et al. (2002)2

similarly misuse the term Isthmus of Kra for sites 400 kmfurther south.

Immediately north of the Isthmus of Kra (at 10�30¢N)there is a second less well-known floristical transition. Thisnorthern transition, between wet seasonal evergreen dip-terocarp rain forest and mixed moist deciduous forestoccurs, on the east side of the peninsula, near the town ofChumphon. The mixed moist deciduous forest differs pro-foundly from the rain forest in stature, absence of emergents,deciduousness (essentially 100%), soil surface environment,and generic composition (Ashton, in litt. 19993 ). This nor-thern phytogeographical transition is described by Richards(1996, p. 162) as a transition between semi-evergreen rainforest and monsoon forest. On the wetter west coast of thepeninsula, in lower Burma (Tenasserim), the transition isbroader and extends north to Tavoy (14� N).

Thus both Whitmore and Ashton view the avifaunaltransition as coincident with the northern phytogeographicaltransition between rain forest and mixed deciduous forestand neither are surprised that we found no ornithologicalboundary at the southern transition as the forest there showsonly minor change in structure (Whitmore, in litt. 1995;Ashton, in litt. 1999)4 . Unfortunately, the distributionalrecords of the Malesian and Indochinese plant genera andspecies upon which their insights are based have never beenpublished. Our current understanding rests on their exten-sive personal fieldwork and the scattered herbarium sheetsknown to only a few botanists. Until the range limits of plantspecies and genera are collected into one data base andplotted out against the geography of the peninsula it is dif-ficult to compare the avifaunal and phytogeographicaltransitions.

We provide a detailed analysis of the underlying birddistributional data elsewhere (Round et al., 2003). A moredefinitive analysis of the northern and southern range limitscan be prepared when the revised distribution data for

Figure 7 The latitudinal distribution of species and subspecies of the bulbul family (Pycnonotidae). See Fig. 5 for details.



Malaysian passerines are available (Wells, 1999, unpubl.data) and when current data become available for the Ten-asserim (now Thanintharyi State) and the rest of southernMyanmar. However, before leaving this issue we shouldpoint out some readily apparent features of the pattern.First, the overall pattern (Fig. 3) is not simply one of Indo-chinese species replacing Sundaic species in the transition.Some of the Thai species have southern range limits north ofthe transition and are montane-adapted species lackingsuitable habitat in the peninsula (e.g. stripe-breasted wood-pecker, Picoides atratus). Others are more flexible and shiftfrom lowland habitat in Thailand to hill habitat in Malaysia,perhaps in response to competition with Sundaic lowlandcongeners (e.g. orange-breasted trogon, Harpactes oreskios).Simple species replacement may therefore be rarer than theabove discussion suggests. Overall the pattern is of a muchricher lowland forest fauna in the Sundaic than the Indo-chinese province and perhaps this is linked to the greaterstructural complexity of the less seasonal rain forests. ManySundaic species have no ecological equivalents in the Indo-chinese fauna. In other cases, one or two Indochinese gen-eralists are either replaced, or added to, by further congenersin the Sundaic province. Among leafbirds, Chloropsis spp.,for example, the golden-fronted leafbird,C. aurifrons, isfound exclusively north of the Kra Isthmus within the regioncovered by our analysis (although it reappears in north Su-matra); the blue-winged leafbird C. cochinchinensis, occurson both sides of the divide, as does a montane species,orange-bellied leafbird, C. hardwickii. Two other lowlandspecies, the greater green leafbird, C. sonnerati, and lessergreen leafbird, C. cyanopogon, are exclusively Sundaic.Finally, there are a few species that have expanded their

ranges during the last century in response to lowland de-forestation (e.g. Indochinese black-collared starling, Sturnusnigricollis, has spread into the southern peninsula) andtherefore tell us little about the historical pattern.

Although the position of the phytogeographical transi-tions involving > 500 genera may be determined by climaticfactors today and the avifaunal transition may be linkedcausally (directly or indirectly) to the plants, we still have toexplain the origination of the different Indochinese andSundaic biotas. Unlike the Central American biogeographi-cal transition or that associated with Wallace’s Line, theavifaunal transition near the Isthmus of Kra cannot beattributed to plate tectonics and former open ocean barriersto dispersal. Yet the significant transitions on the Thai–Malay peninsula require that some sort of barrier existed inthe past in order to permit the provincial biotas to diverge inallopatry. In a companion paper, Woodruff (2003a) arguesthat marine transgressions during the Miocene and thePliocene breached the peninsula and permitted the evolu-tionary differentiation of some terrestrial animals north andsouth of the seaways. A consideration of Tertiary eustaticchanges (Vail & Hardenbol, 1979; Haq et al., 1987; Hallam,1992; Abreu & Anderson, 1998) leads to the conclusion thatthe Thai–Malay peninsula may have been breached bymarine seaways for two periods relevant to modern birddistributions: during both a mid-Miocene and an earlyPliocene high stand. Sea levels of at least þ150 m (þ220 maccording to Hutchison, 1989) during the middle Mioceneprobably flooded the isthmus from 24 to 13 Ma and possiblylonger. Straits probably formed again during the early Plio-cene from 5.5 to 4.5 Ma when sea level rose to þ140 maccording to Hutchison (1989). Today a sea level at þ100 mwould flood the peninsula in two places (Woodruff, 2003a):in the north, a strait would open between Surat Thani andKrabi, in the south, a strait would open between Songkhlaand Kangar. In both cases the seaways would be orientedroughly north–south and contain a number of prominentislands. The northern strait would be 30–100 km wide andthe southern strait would be 40–50 km wide. Between thesetwo straits 80% of southern Thailand would be submergedand forest habitat would remain only on the emergentNakhon si Thammarat Range (Banthad Range) and westernhills.

The Pliocene transgression and hypothetical seaways aremore relevant to the differentiation of extant avian speciesand subspecies than the Miocene events. Contrary to earlierviews that avian speciation was closely linked to Pleistoceneclimatic cycles (and geographical differentiation in forestrefugia during glacial periods), recent molecular geneticstudies indicate that many north temperate species originatedin the Pliocene (Bermingham et al., 1992; Blondel et al.,1996; Blondel & Mourer-Chauvire, 1998; Klicka & Zink,1997, 1999). Similarly, there is no clear relationship betweenthe inferred positions of the rain forest refugia in southeastAsia and the position(s) of today’s transitions (Morley, 2000;Kershaw et al., 2001; Gathorne-Hardy et al., 2002). This isnot to deny that Pleistocene environmental changes leaverecognizable imprints on modern phylogeography (Avise,

Figure 8 Multidimensional scaling plot of species in 23 latitudinal

zones (zones A–W, Table 2).



2000), but rather to recognize that the majority of speciationevents are older. Hewitt (1996, 2000) and others have arguedthat Early Pliocene climatic events were a major impetus tospeciation, and that cyclical Pleistocene changes have hadmore impact on subspecific patterning and extinctions.

If a seaway created a barrier to the dispersal of forestplants and birds along the Thai–Malay peninsula, the studyof phylogenetic relationships within the genera involvedshould reveal evidence of genetic differentiation associatedwith the time of the barrier’s existence. For species-pairsthat originated by allopatric divergence on either side of thehypothetical Pliocene straits some predictions can be made.If the resulting species were poorly differentiated after theseaway disappeared, then they are likely to have come backinto contact with insufficient niche divergence to live inbroad sympatry, and instead may show competitive replace-ment. Alternatively, we may see hybridization betweenimperfectly isolated semispecies, although hybrid zones arenot known to persist for 4 Myr. The avifaunal records havenot yet been formally examined for evidence of competitivereplacement, but there is little evidence for multiple zonesof interspecific hybridization so the transition is probablyancient rather than recent. In contrast, younger species thatoriginated elsewhere and have entered the region since thebarrier disappeared, may have distributions unaffected bysuch historical features.

The degree to which these hypothetical seaways func-tioned as barriers to dispersal of individual species wouldvary tremendously across avian taxa. Some birds, includingmost raptors and migratory birds, would not recognize a30 km wide marine strait as an obstacle, while to others a1-km water gap constitutes a near absolute barrier (e.g. somebabblers, Sylviinae, barbets, Megalaimidae, and the honey-guide, Indicator archipelagigus, Wells, 1976, 1988). Amongthe resident forest birds we have to expect a great diversity ofresponses to water gaps and it would be informative there-fore to further examine the present distribution of species onthe 300 sea islands around the peninsula (see brief review byWells, 1999). Such an analysis may suggest both assemblyrules for these bird communities and limits on the size andduration of hypothetical barriers.

In conclusion, historical and ecological hypotheses toexplain the origin and current position of the transitionbetween Indochinese and Sundaic avifaunas north of theIsthmus of Kra have been developed involving Neogeneseaways, and seasonality as it affects forest type. Testingthese hypotheses can now begin but will be difficult for, asWells (1999) and others have pointed out, there is still noclear understanding of the linkage between climatologicalfactors, forest phenology, floristic diversity, and bird distri-bution. Answers to these complex issues may come from theresolution of a host of smaller questions including the fol-lowing. Are Indochinese species (both birds and plants) moresuccessful in invading Sundaland than Sundaic species are ininvading the Indochinese province? What do comparativepenetrance and invasibility tell us about the history ofthe interaction? Have repeated major changes in lowlandforest area during the Pleistocene favoured Sundaic over

Indochinese species? How have Neogene palaeogeographicalchanges altered the position of the transition? Are today’splant distributions better indicators of palaeogeographicalhistory than the birds? In contrast, do birds track recenthabitat changes more rapidly than plants? Further study ofthe Neogene history of the region and the behaviouralecology and phylogeography of the species associated withthe transition will permit exploration of these questions andtests of these and other hypotheses.

ACKNOWLEDGMENTS

We thank Warren Brockelman for facilitating this study,Jack Bradbury for advice on statistical analyses, David Wellsfor sharing unpublished distributional data, and Peter Ash-ton, Trevor Price, Sukamol Srikwan and two reviewers fortheir critical reading of the manuscript. Research was sup-ported by grants from the Meeker Foundation (Hughes) andthe US National Science Foundation (Woodruff).

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BIOSKETCHES

Jennifer Hughes (PhD, Stanford), is an Assistant Professor of Biology at Brown University. She completed the analyses reportedhere while an undergraduate in Woodruff’s laboratory at UCSD. Her interests in biodiversity and conservation biology aredescribed at: http://www.brown.edu/Departments/EEB/faculty/Hughes.html.

Philip Round has worked as an ornithologist in Thailand for 20 years and is the author of the standard national field guideto the 900 species. He is a Visiting Professor at the Department of Biology, Mahidol University, Thailand’s preeminent universityin biomedicine and science.

David Woodruff is a Professor of Biological Sciences interested in genetic aspects of the evolution and conservation ofanimal species in southeast Asia and elsewhere. A study of genetic erosion in fragmented mammal populations near the Isthmusof Kra led to the initiation of a series of projects on the Indochinese–Sundaic biogeographical transition, the first of which ispresented here.



the indochinese–sundaic faunal transition at the isthmus of kra: an analysis of resident forest...

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