SEARCH

SEARCH BY CITATION

Keywords:

  • Amphibians;
  • birds;
  • Borneo;
  • island biogeography;
  • mammals;
  • Palawan;
  • Philippines;
  • phylogeny;
  • reptiles;
  • Sunda Shelf

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Aim  Nearly 150 years ago, T. H. Huxley modified Wallace’s Line, including the island of Palawan as a component of the Asian biogeographic realm and separating it from the oceanic Philippines. Although Huxley recognized some characteristics of a transition between the regions, Palawan has since been regarded primarily as a peripheral component of the Sunda Shelf. However, several recent phylogenetic studies of Southeast Asian lineages document populations on Palawan to be closely related to taxa from the oceanic Philippines, apparently contradicting the biogeographic association of Palawan with the Sunda Shelf. In the light of recent evidence, we evaluate taxonomic and phylogenetic data in an attempt to identify the origin(s) of Palawan’s terrestrial vertebrate fauna.

Location  The Sunda Shelf and the Philippines.

Methods  We review distributional and phylogenetic data for populations of terrestrial vertebrates from Palawan. Using taxonomic data, we compare the number of Palawan taxa (species and genera) shared with the Sunda Shelf and oceanic Philippines. Among widespread lineages, we use phylogenetic data to identify the number of Palawan taxa with sister relationships to populations or species from the Sunda Shelf or oceanic Philippines.

Results  Although many terrestrial vertebrate taxa are shared between Palawan and the Sunda Shelf, an increasing number of species and populations are now recognized as close relatives of lineages from the oceanic Philippines. Among the 39 putative lineages included in molecular phylogenetic studies with sampling from the Sunda Shelf, Palawan and the oceanic Philippines, 17 of them reveal sister relationships between lineages from Palawan and the oceanic Philippines.

Main conclusions  Rather than a simple nested subset of Sunda Shelf populations, Palawan is best viewed as having played multiple biogeographic roles, including a young and old extension of the Sunda Shelf, a springboard to diversification in the oceanic Philippines, and a biogeographic component of the Philippine archipelago. Palawan has a long, complex geological history, which may explain this variation in pattern. Huxley originally noted transitional elements in Palawan’s fauna; we therefore suggest that his modification of Wallace’s Line should be recognized as a filter zone, reflecting both his original intent and available taxonomic and molecular evidence.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

A zoogeographic border is not a line without width [our emphasis] … by necessity there is a mixture of faunal elements along the border of two zoogeographic regions, caused by reciprocal penetration.

Pelseneer (1904), translated and quoted by Mayr (1944, p. 9)

Biogeographers have long investigated the similarities and differences among floras and faunas on adjacent landmasses, illuminating the processes of speciation, extinction and community assembly (Simpson, 1940; Wegener, 1966; Brown, 1971; Heaney, 1986). Continental islands, and the biological communities that reside on them, have proven especially crucial to the maturation of biogeographic principles, being pivotal in the development of theories of community assembly, island area–diversity relationships and the processes by which faunas on recently isolated islands may relax to long-term equilibria (Simpson, 1940; MacArthur & Wilson, 1963; Heaney, 1984; Patterson, 1990).

The Palawan island group (including Balabac, Bugsuk, Busuanga, Culion, Palawan and many small islands), which is politically part of the Philippines, lies at the periphery of the continental shelf (= Sunda Shelf) in Southeast Asia (Fig. 1), and has long served as an integral component of biogeographic investigations (e.g. Huxley, 1868; Holloway, 1982). Palawan’s fauna has generally been treated as most similar to that of Borneo (e.g. Dickerson, 1928; Inger, 1954; Heaney, 1985; Esselstyn et al., 2004), but other authors have found equal or greater similarity to the oceanic Philippines (e.g. McGuire & Alcala, 2000; McGuire & Kiew, 2001; Brown & Guttman, 2002; Evans et al., 2003; Beck et al., 2006).

image

Figure 1.  Map of Southeast Asia showing the traditional view of the Sunda Shelf, which includes Palawan. Modern islands are shown in medium grey and the continental shelf is indicated by light grey. Delineation of the shelf approximates the 120 m isobath. However, the narrow, slightly deeper channel (c. 140 m) between Palawan and Borneo is included as part of the shelf in this depiction. Modified from Voris (2000). East of the Sunda Shelf lie the oceanic islands of Wallacea and the Sahul Shelf (Australia and New Guinea). Huxley’s modification of Wallace’s Line delineates the extent of Sundaland.

Download figure to PowerPoint

Wallace (1860), with a very imperfect knowledge of the Philippine fauna, originally grouped the entire country with the Asian region, while simultaneously noting the Philippines’ deficiency in several Asian groups. By 1876, Wallace (1876) knew of only 14 non-volant mammals and 159 land birds from the Philippines, roughly 15% and 40% of current estimates for diversity, respectively (Heaney et al., 1998, 2009; Kennedy et al., 2000; Hutterer, 2007; Esselstyn & Goodman, in press). Among the Philippine mammals of which Wallace had knowledge at that time, nearly all are widespread Asian genera. By the time he wrote Island life, Wallace (1881) knew of 21 species of Philippine mammals, most of which are either widespread species or Palawan endemics. Thus, he had virtually no knowledge of the highly endemic mammal communities in the oceanic Philippines. At the time, even less was known of amphibian and reptile diversity (Boulenger, 1894). Thus, Wallace’s impression of the Philippine fauna, and his biogeographic delineations of it, were taken from a very small, biased sample of the diversity.

Huxley (1868), also relying primarily on bird and mammal distributions, was the first to note that Palawan’s fauna is Asian, but the remaining Philippine islands possess a community of peculiar animals. Huxley (1868, p. 317) commented, ‘It is extremely remarkable; why Borneo [including Palawan] and the Philippines should have…so much and so little in common with Asia [respectively]…’. Hence, while hinting at sea depth as a possible explanation, Huxley (1868) simultaneously named and modified Wallace’s Line (Fig. 1). However, it should be noted that Huxley (1868) recognized that biogeographic boundaries are places where faunas grade into one another, as indicated on p. 317: ‘The eastern boundary between Arctogaea and Australasia is formed, not by a line, but by a broad zone of border islands…’. Following Huxley’s observations, others drew similar conclusions and grouped Palawan with Borneo (Everett, 1889; Boulenger, 1894).

With the publication of Dickerson’s (1928) extensive volume on Philippine biodiversity, knowledge of the Philippine fauna had greatly improved, and the grouping of Palawan with Borneo, and concurrent recognition of the oceanic Philippines as a unique centre of endemism, were well established. Most authors recognized exceptions to these general patterns, but considered the evidence in support of Huxley’s Line to be convincing (e.g. Mayr, 1944). More recent distributional data have supported these conclusions, again with occasional exceptions noted (e.g. Holloway, 1982; Kennedy et al., 2000; Esselstyn et al., 2004).

Although biogeographers occasionally overemphasize the significance of the precise placement of faunal boundaries (Simpson, 1977), assignment of any particular island to a biogeographic region has important implications for both conservation and evolutionary biology. For instance, thorough knowledge of the distribution of biodiversity facilitates the appropriate allocation of scarce resources for conservation efforts and, in the context of evolutionary biology, summary data characterizing distributions and relationships of organisms provide insights into: (1) the events that may have triggered speciation, (2) the directions and timing of colonization events, and (3) the degree of congruence of particular processes among disparate lineages.

Geology, sea levels and geography

The geological history of Palawan is complex and involves extensive movement across the South China Sea (Hall, 1996, 1998; Zamoras & Matsuoka, 2004; Yumul et al., 2009a,b). Northern Palawan was initially part of the Asian mainland near modern Taiwan, but rifted from the continent during the Oligocene and travelled south for c. 30 Myr (Hall, 2002). After separating from the Asian mainland, the continental fragment was probably mostly submerged, as evidenced by Eocene to early Miocene carbonate deposits layered on top of older rocks (Yumul et al., 2009a). As the Palawan microcontinental block (includes Palawan and parts of Mindoro, Panay and Romblon) continued to travel south, it collided with the Philippine mobile belt c. 20–16 Ma (Hall, 2002; Yumul et al., 2009b), probably resulting in uplift and perhaps the production of islands. Evidence for erosion in the area (Bird et al., 1993) suggests islands were present by c. 20–16 Ma, as does the existence of 15–13 Myr old granite in north Palawan (Encarnación & Mukasa, 1997), the formation of which requires a thick crust. Palawan came into close proximity with Borneo c. 10 Ma (Hall, 2002), and southern Palawan may have been uplifted around this time. Most depictions of the geological history of Palawan distinguish the northern half of the island (marine-capped continental fragments) from the southern (uplifted marine sediments and volcanics), but Durkee (1993) provides an alternative perspective, in which the apparent fault between the northern and southern parts of the island does not exist. Rather, Durkee (1993) refers to southern Palawan as a thrust-pile from northward movement of crust over the south-moving microcontinental block. Although many questions regarding the geological history of Palawan remain unanswered, it is significant that we know that some portion of the island broke away from the Asian mainland and drifted south and that most, but perhaps not all, of this continental fragment was submerged at one time or another, and that islands were possibly emerging as early as 20 Ma.

By the Pleistocene, climatic oscillations were generating major fluctuations in global sea levels (Bintanja et al., 2005; Thomas et al., 2009). The Sunda Shelf, of which Palawan is now a part, is the largest continental shelf in the world and consists of many islands (= Sundaland) and a shallow sea extending south and east from the Malay Peninsula (Fig. 1). During periods of low sea level, the shelf was exposed repeatedly as dry land, and the large islands of Borneo, Java and Sumatra were united into a single contiguous, continental landmass (Kloss, 1929; Inger, 1954; Heaney, 1985; Voris, 2000; Woodruff & Turner, 2009). The terrestrial fauna of Sundaland is thus Asian, with moderate levels of endemism (Inger, 1954, 1966, 1999; Heaney, 1984; Cracraft, 1988; Corbet & Hill, 1992; MacKinnon & Phillipps, 1993; Inger & Tan, 1996). Sundaic endemism is generally attributed to isolation caused by rising sea levels (Heaney, 1985; Inger & Voris, 2001; Woodruff & Turner, 2009) or altered distributions of forest and savanna habitats during the Pleistocene (Heaney, 1991; Meijaard, 2003; Gorog et al., 2004; Bird et al., 2005). However, some studies have inferred or implied invasions of the shelf much earlier than the Pleistocene (e.g. Jansa et al., 2006; Outlaw & Voelker, 2008; Matsui et al., 2010).

Palawan Island is currently isolated from Borneo by a c. 140 m deep channel (Heaney, 1985, 1986). Until very recently, most sea-level reconstructions suggested that Palawan and Borneo were united, or nearly so, with an inferred sea-level minimum of c. −140 m during the penultimate glacial maximum c. 140 ka (Gascoyne et al., 1979; Rohling et al., 1998). However, the most recent sea-level estimates for the penultimate glacial period suggest that Palawan and Borneo were not united at that time, with reconstructed sea-level minima nearer the −120 m typically inferred for the most recent glacial maximum (e.g. Siddall et al., 2003, 2006; Bintanja et al., 2005; Thomas et al., 2009). Earlier glacial periods reduced sea levels to c. −130 m, c. 430 and 630 ka (Miller et al., 2005; Bintanja et al., 2005), suggesting that Palawan has remained isolated by a narrow sea channel for the last million years. However, we note that rates of tectonic change around Palawan have been rapid, and current bathymetry may only be useful for understanding relatively recent (c. < 1 Ma) patterns of inter-island connectedness. Additionally, we note that the breadth of any land bridges or sea channels would be an important factor in determining which organisms would represent potential colonists.

Patterns of faunal similarity, data availability and putative biogeographic histories

Palawan’s vertebrate fauna has been considered similar to that of Borneo, but with moderate levels of endemism (Everett, 1889; Dickerson, 1928; Esselstyn et al., 2004). However, early studies were dominated by investigations of bird and mammal distributions (Huxley, 1868; Everett, 1889), with other terrestrial organisms (e.g. amphibians, reptiles, invertebrates, plants) receiving far less attention (but see Günther, 1872; Boulenger, 1894). More recently, several phylogenetic studies have shown Palawan taxa to be more closely related to species from the oceanic Philippines or Sulawesi than to Sundaic populations (e.g. McGuire & Kiew, 2001; Brown & Guttman, 2002; Evans et al., 2003; Esselstyn et al., 2009). Other researchers have noted that in some groups, diverse Bornean communities are absent from Palawan (e.g. none of the nine Bornean species of flying lizards are found on Palawan: McGuire & Alcala, 2000). Given the early biases in available distributional data and the results of recent phylogenetic inferences, some have questioned the characterization of Palawan as a simple extension of the Sunda Shelf (e.g. McGuire & Alcala, 2000; Atkins et al., 2001; Brown & Guttman, 2002; Beck et al., 2006; Brown & Diesmos, 2009). Furthermore, recent collections of terrestrial vertebrates from the island have provided new distributional records and facilitated taxonomic revisions that potentially shed light on the biogeographic relationships of these areas (Kennedy et al., 2000; Esselstyn et al., 2004; Hutterer, 2007; Brown et al., 2009; Welton et al., 2009).

In this paper we review the distributions and phylogenetic relationships of the terrestrial vertebrates of Palawan, taking into account recent taxonomic changes and new distributional records of extant and fossil taxa. In effect, we consider the universality of Huxley’s Line by exploring the possible origins of Palawan’s terrestrial vertebrate fauna, including whether it is a subset of Borneo’s with a Pleistocene origin, whether a substantial proportion of Palawan’s fauna might originate from the oceanic Philippines or elsewhere, whether Palawan might have served as a colonization route into the oceanic Philippines and whether the island’s fauna has a complex of lineage-specific relationships.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Distribution of terrestrial vertebrates

We gathered distributional information from published sources, as well as unpublished records of recently documented species. Mammal records for Palawan and associated small islands were taken from Esselstyn et al. (2004) and Heaney et al. (1998) and updated with recent discoveries and taxonomic changes (Gaubert & Antunes, 2005; Helgen, 2005; Lucchini et al., 2005; Hutterer, 2007; Piper et al., 2008). We also include unpublished records of an endemic shrew (Suncus) and the widespread hairy-winged bat (Harpiocephalus harpia), each first collected on Palawan in 2007 (D.S. Balete & J.A. Esselstyn, unpublished). Mammal records for the Sunda Shelf and oceanic Philippines were drawn from several sources (Payne et al., 1985; Corbet & Hill, 1992; Heaney et al., 1998). Records of breeding land birds were taken from Kennedy et al. (2000) and MacKinnon & Phillipps (1993), but taxonomy follows Dickinson (2003). Distributional records of reptiles and amphibians were taken from Taylor (1922a,b,c,d,e, 1923, 1925, 1928), Inger (1954) and Brown & Alcala (1970, 1978, 1980), with recent records summarized by Diesmos et al. (2002) and Brown (2007). The most recent discoveries and taxonomic updates are included (e.g. Brown et al., 2009, 2010; Welton et al., 2009; Koch et al., 2010; Linkem et al., 2010).

We tallied the total numbers of species and genera of birds, mammals, amphibians and reptiles occurring on Palawan. Of those species and genera, we counted how many are shared with the oceanic Philippines versus the Sunda Shelf.

Phylogenetic evidence

We sought phylogenetic studies that used molecular evidence to infer relationships among widespread taxa found on the Sunda Shelf, Palawan and oceanic Philippines. We limited our sources of data to studies that sampled populations of a putative lineage (genus or species) from all three areas, because these studies provide evidence beyond that available from summaries based on taxonomy. Studies that sampled taxa from only two of the three areas are not included because these would be uninformative with regard to the question of whether the Palawan population is more closely related to Sunda Shelf or Philippine populations. We consider the included phylogenies to provide the same information as taxonomic studies, but at a finer level of resolution and with more explicit statements of shared ancestry.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Distribution of terrestrial vertebrates

Most terrestrial vertebrate species documented from Palawan are widespread across the region, are Palawan endemics or are shared with the Sunda Shelf (Fig. 2). However, several species (especially reptiles and birds) occur on Palawan and the oceanic Philippines only, and not on the Sunda Shelf (Fig. 2). When distributional data for genera are examined, Palawan’s fauna is more similar to that of the Sunda Shelf for all groups, but the differences are not great (Fig. 3a). However, this pattern is driven by widespread genera, and stronger similarity is noted between Palawan and the Sunda Shelf when the comparison is limited to genera that occur in only two of the three areas (Palawan, Sunda Shelf, oceanic Philippines: Fig. 3b). Generic distributions reveal that the similarity between the faunas of Palawan and the Sunda Shelf is much stronger in mammals than in other taxa. All distributional data are provided in Appendix S1 in the Supporting Information.

image

Figure 2.  Terrestrial vertebrates from Palawan reveal five common distributional patterns: (a) endemic to Palawan; (b) present on Palawan and the Sunda Shelf; (c) as (b), but also present on Mindoro Island; (d) widespread within the Philippines, including Palawan; and (e) widespread throughout the region occurring on the Sunda Shelf, Palawan and in the oceanic Philippines. The number of species of each higher taxon, and the total, are listed next to each map. Among the species in category (e), several taxa only marginally enter the oceanic Philippines and are restricted to the Mindanao faunal region south of the curved line (two birds, one mammal, four amphibians and two reptiles).

Download figure to PowerPoint

image

Figure 3.  Numbers of genera of terrestrial vertebrates from Palawan and their regional distributions. Panel (a) shows the numbers of genera shared with the Sunda Shelf and oceanic Philippines while panel (b) considers only genera that occur on Palawan and either the Sunda Shelf or oceanic Philippines, but excludes genera that occur in all three areas.

Download figure to PowerPoint

Phylogenetic evidence

We identified 39 Palawan species or populations that have been included in phylogenetic studies (some of which are in progress), with representatives also sampled from both the Sunda Shelf and oceanic Philippines (Table 1). Among these taxa, 17 Palawan populations are sister to Philippine lineages, 10 have sister relationships to Sunda Shelf populations, eight are sister to populations from the oceanic Philippines and Sunda Shelf, two are sister to Sulawesi taxa, and one is sister to populations from the Philippines and Sulawesi. One lineage is genetically homogeneous across the Borneo–Palawan–Philippines arc (Fig. 4, Table 1).

Table 1.   Summary of phylogenetic/phylogeographic evidence showing the distributions of populations that are sister to taxa from Palawan Island.
Species from PalawanSister populationReference
  1. 1We include Iole because some authors synonymize it with Hypsipetes, which is present on the Sunda Shelf and in the oceanic Philippines.

  2. 2Denotes Sunda Shelf taxa sister to Palawan + oceanic Philippines clades.

  3. 3Mitochondrial gene trees reveal two clades from Palawan, one closely related to populations from the oceanic Philippines and one to Sunda Shelf populations.

  4. 4Haplotypes are shared among Philippine, Bornean and Palawan individuals.

  5. 5These five Palawan endemics of Sundasciurus form a clade that is sister to a clade found from the oceanic Philippines and Sunda Shelf.

  6. 6We include Tupaia here because some authors include Urogale, which is present in the oceanic Philippines, within Tupaia, and because molecular evidence supports this arrangement.

  7. 7Polypedates leucomystax may be an introduced species on Palawan (Brown et al., in press).

  8. 8Mitochondrial gene trees show a close relationship between Palawan and oceanic Philippine populations, whereas nuclear gene trees suggest a close relationship between populations from Palawan and Borneo. Siler et al. (2010) hypothesize that the discordance is due to ancestral polymorphism and the Palawan + oceanic Philippines hypothesis is the favoured species tree topology.

  9. 9These three Palawan endemics of Sphenomorphus form a clade that is nested within a clade from the oceanic Philippines.

Birds
 Ficedula platenaeSunda ShelfOutlaw & Voelker (2008)
 Iole palawanensis1Sunda ShelfOliveros & Moyle (2010)
 Pernis ptilorhyncusSunda ShelfGamauf & Haring (2004)
 Phylloscopus trivirgatusPhilippinesJones & Kennedy (2008)
 Prionochilus plateniSunda ShelfNyári et al. (2009)
 Pycnonotus atricepsSunda ShelfOliveros & Moyle (2010)
 Pycnonotus plumosusSunda ShelfOliveros & Moyle (2010)
 Stachyris hypogrammicaPhilippinesMoyle et al. (2009)
Mammals
 Crocidura batakorumSulawesiEsselstyn et al. (2009)
 Crocidura palawanensis2PhilippinesEsselstyn et al. (2009)
 Cynopterus brachyotis3Philippines & Sunda ShelfCampbell (2004)
 Paradoxurus hermaphroditus4Philippines & Sunda ShelfPatou et al. (2010)
 Sundasciurus hoogstraali5Philippines & Sunda Shelfden Tex et al. (2010)
 Sundasciurus juvencus5Philippines & Sunda Shelfden Tex et al. (2010)
 Sundasciurus moellendorffi5Philippines & Sunda Shelfden Tex et al. (2010)
 Sundasciurus rabori5Philippines & Sunda Shelfden Tex et al. (2010)
 Sundasciurus steerii5Philippines & Sunda Shelfden Tex et al. (2010)
 Sus ahoenbarbusPhilippinesLucchini et al. (2005)
 Tupaia palawanensis6Sunda ShelfRoberts et al. (2009)
Amphibians
 Kaloula baleataSulawesiR.M. Brown et al. (in prep.)
 Leptobrachium tagbanorum2PhilippinesBrown et al. (2009)
 Limnonectes palavanensisSunda ShelfEvans et al. (2003)
 Limnonectes acanthiPhilippinesEvans et al. (2003)
 Megophrys ligayaeSunda ShelfR.M. Brown (unpubl.)
 Occidozyga laevisPhilippinesC.D. Siler et al. (unpubl.)
 Polypedates leucomystax7PhilippinesBrown et al. (in press)
 Polypedates macrotisSunda ShelfBrown et al. (in press)
 Rana sanguineaPhilippinesBossuyt et al. (2006)
 Rana moellendorffi2PhilippinesBrown & Guttman (2002)
Lizards, snakes, turtles
 Bronchocela cristatellaPhilippines & SulawesiJ.A. McGuire et al. (in prep.)
 Cuora amboinensisPhilippinesR.M. Brown et al. (unpubl.)
 Cyrtodactylus redimiculus8Philippines & Sunda ShelfSiler et al. (2010)
 Cyrtodactylus tautbatorumPhilippinesWelton et al. (2009); Siler et al. (2010)
 Draco palawanensisPhilippinesMcGuire & Kiew (2001)
 Parias schultzeiSunda ShelfSanders et al. (2004)
 Sphenomorphus victoria9PhilippinesC.W. Linkem et al. (unpubl.)
 Sphenomorphus traanorum9PhilippinesC.W. Linkem et al. (unpubl.)
 Sphenomorphus wrighti9PhilippinesC.W. Linkem et al. (unpubl.)
 Varanus palawanensisPhilippinesL.J. Welton et al. (unpubl.)
image

Figure 4.  Map of the Philippines and northern Borneo alongside three common phylogenetic patterns where Palawan species are (a) sister to taxa from the oceanic Philippines, (b) sister to taxa from the Sunda Shelf or (c) have either ambiguous or undifferentiated relationships. Taxa fitting each pattern are listed below the schematic phylogeny. Species revealing other relationships (e.g. sister to Sulawesi populations) are not included. References are listed in Table 1.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Our results reveal that a substantial component of Palawan’s terrestrial vertebrate diversity is indeed closely related to populations from the Sunda Shelf, especially among mammals and birds. However, numerous taxa occur in all three areas (Fig. 2), and many Palawan populations are most closely related to taxa from the oceanic Philippines or Sulawesi (Fig. 4, Table 1), especially among reptiles. We must note that differing taxonomic philosophies may contribute to the distinct patterns observed among groups of vertebrates. For instance, more Palawan endemic genera and species are found among birds and mammals than among reptiles or amphibians (Fig. 2). This may be due to: (1) Palawan’s bird and mammal groups representing older clades, (2) birds and mammals exhibiting faster rates of morphological evolution, or (3) differing taxonomic philosophies among the systematists that focus on these groups. Despite these possibilities, the similarity of the Palawan fauna to that of the Sunda Shelf is apparent from taxonomy, and is supported by some phylogenetic evidence (e.g. bulbuls: Oliveros & Moyle, 2010; flowerpeckers: Nyári et al., 2009; and flycatchers: Outlaw & Voelker, 2008), but apparently is contradicted by the commonness of close phylogenetic relationships with taxa from the oceanic Philippines or Sulawesi (e.g. flying lizards: McGuire & Kiew, 2001; frogs: Brown & Guttman, 2002; Evans et al., 2003; and shrews: Esselstyn et al., 2009).

We note that sister relationships between Palawan and oceanic Philippine populations do not necessarily contradict the view of Palawan as a Sundaic peninsula, but expand it beyond the simplicity of a ‘nested subset’ prediction. Rather, this pattern is precisely what would be expected if Palawan served as a colonization route into the oceanic Philippines. In cases where taxa colonized the oceanic Philippines via Palawan, we expect to see Bornean populations inferred as sister to clades composed of Palawan + oceanic Philippines populations. Among the 17 groups that show a Palawan + oceanic Philippines relationship, this pattern is evident in a shrew (Crocidura palawanensis: Esselstyn et al., 2009) and three frogs (Leptobrachium tagbanorum: Brown et al., 2009; Limnonectes acanthi: Evans et al., 2003; Rana moellendorffi: Brown & Guttman, 2002). A similar pattern is noted in a gecko lineage (Cyrtodactylus), where two species from Palawan are each sister to small radiations from the oceanic Philippines (Siler et al., 2010). These two clades (including the Palawan species), are sister groups, and taxa from the Sunda Shelf are sister to the entire clade (Siler et al., 2010). These cases suggest that Palawan may indeed have served as an important point of entry to the oceanic Philippines (e.g. Myers, 1949; Diamond & Gilpin, 1983; de Jong, 1996).

If Palawan were a peninsula of Borneo, with frequent connections emerging during periods of low sea level, then many Palawan populations should be closely related to Bornean taxa, having been isolated since the Pleistocene. However, when Palawan taxa are sister to Sunda Shelf populations, these relationships often appear to be old divergences that pre-date Pleistocene, and in some cases Pliocene, sea-level fluctuations. For instance, Oliveros & Moyle (2010) found that all four species of bulbul from Palawan are sister to Bornean taxa, but three of the four are old lineages long isolated from their Bornean sisters. To obtain divergence time estimates, we inferred maximum likelihood (ML) divergences between the three highly divergent Palawan–Borneo pairs of bulbuls using the data and models of sequence evolution reported by Oliveros & Moyle (2010). We optimized branch lengths on their ML topology in paup* 4.0b (Swofford, 1999), resulting in ML divergences of 0.45 in Iole, 0.24 in Pycnonotus plumosus and 0.20 in Alophioxus bres. If one were willing to assume a molecular clock, even with a fast rate of divergence (0.054 Myr−1: Drovetski et al., 2004), these lineages would have been isolated for c. 4–8 Myr. Given the deep isolation of Palawan populations and the apparent lack of successful invasion of the oceanic Philippines via Palawan, Oliveros & Moyle (2010) characterized Palawan as an evolutionary dead end for bulbuls, rather than a biogeographic umbilicus (sensuDiamond & Gilpin, 1983). Similarly, den Tex et al. (2010) estimated the divergence of Palawan tree squirrels (Sundasciurus) from their Sundaic relatives to have occurred more than 6 million years ago. Thus, although the results of Oliveros & Moyle (2010) and den Tex et al. (2010) are consistent with the topological expectation of Palawan representing a recently isolated peninsula of Borneo, they qualitatively reject the temporal expectation of recent divergence.

Diversification within Palawan has probably not made major contributions to extant diversity. Most genera on the island are represented by a single species, but where multiple species within deeper lineages are present on Palawan most studies found that they are distant relatives derived from independent colonization events (e.g. Evans et al., 2003; Brown et al., 2009; Esselstyn et al., 2009; Oliveros & Moyle, 2010). However, a few remaining potential cases of in situ diversification exist, including the five allopatric species of tree squirrels (Sundasciurus), two allopatric species of tree shrews (Tupaia) and several sympatric species of Sphenomorphus (Brown & Alcala, 1980; Heaney, 1979; Heaney et al., 1998; Esselstyn et al., 2004; Helgen, 2005). Preliminary evidence from Sphenomorphus suggests that three species from Palawan form a clade most closely related to taxa from the oceanic Philippines (Linkem et al., 2010; C. W. Linkem & R. M. Brown, unpublished). Similarly, den Tex et al. (2010) found that several species of tree squirrel (Sundasciurus) from Palawan form a clade, but the divergences among them are limited.

Although there is little evidence for in situ diversification as a significant generator of diversity on Palawan, potential mechanisms do exist. Bird et al. (2007) suggested that plant communities on the island shifted between forest and savanna during the Pleistocene, perhaps providing opportunities for isolation of populations of forest-dependent animals. Hutterer (2007) hinted that the population of shrews (Crocidura palawanensis) on Balabac Island at the southern end of the Palawan group may represent a species distinct from populations on the main Palawan Island, and we suspect that this could be a common pattern. The long, narrow shape of Palawan (Fig. 1) has the potential to promote diversification along its long axis, by allowing relatively small areas of unsuitable habitat to represent substantial barriers to dispersal, or simply by generating strong isolation-by-distance over contiguous habitats.

The shape of Palawan may explain another pattern noted by McGuire & Alcala (2000), in which none of the nine Bornean species of flying lizards (Draco) are found on Palawan. This may be an isolated phenomenon, or a general pattern. Numerous Bornean genera are absent from Palawan, but this is expected because Palawan is so small relative to Borneo. Future research may demonstrate that the Palawan fauna includes fewer Bornean taxa than are present on other, demonstrably land-bridge, islands. If Palawan does indeed hold fewer Bornean species than other land-bridge islands, it may be that the island’s long narrow shape and northerly orientation (Fig. 1) simply presents a small ‘target’ for potential colonists originating from northern Borneo (e.g. Lomolino, 1990).

Finally, the possible existence of Palawan as an oceanic island prior to its approach to Borneo would explain many of the patterns we note. In particular, the ancient divergences between Palawan and Bornean taxa would make sense if Palawan were colonized over water several million years ago. Similarly, faunal exchange with the oceanic Philippines might have occurred frequently when a proto-Palawan was nearest the oceanic parts of the Philippines, perhaps explaining the close relationships between some taxa in these areas.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

We conclude that attempting to assign a single historical process to Palawan’s vertebrate biodiversity is overly simplistic. It is unreasonable to expect all organisms living on an island to have experienced identical evolutionary processes, especially when the island in question has such a long, complex geographic history. Distributional and phylogenetic data on Palawan vertebrates contain signals consistent with a variety of evolutionary histories. Many species and genera are shared with Borneo, including some recently diverged taxa, but other populations have been isolated on Palawan for millions of years (e.g. Oliveros & Moyle, 2010). Several other Palawan lineages have close relationships with populations from the oceanic Philippines. Some of these relationships are probably due to invasion of the oceanic Philippines via Palawan (e.g. Esselstyn et al., 2009; Siler et al., 2010), but in other cases Palawan populations are nested within clades otherwise restricted to the oceanic Philippines (e.g. McGuire & Kiew, 2001), suggesting invasion of Palawan from the oceanic Philippines. Given the prevalence of deep divergences between Bornean and Palawan populations and close relationships between Palawan and oceanic Philippine populations, along with evidence for thickened crust and erosion in the area c. 20–13 Ma (Bird et al., 1993; Encarnación & Mukasa, 1997; Yumul et al., 2009b), we consider it likely that Palawan existed as an oceanic island prior to its approach to Borneo. If this is the case, it might explain the complex set of relationships exhibited by Palawan’s terrestrial vertebrates.

Available evidence suggests that Palawan represents both a young and old extension of the Sunda Shelf (Oliveros & Moyle, 2010), a springboard to diversification in the oceanic Philippines (Esselstyn et al., 2009; Siler et al., 2010), a biogeographic component of the Philippine archipelago (McGuire & Alcala, 2000; Brown & Diesmos, 2009) and, in some cases, a ‘dead end’ for faunal elements that dispersed from the oceanic Philippines but never made it as far as Borneo (e.g. emerald green tree skinks, Lamprolepis smaragdina). It remains possible that Palawan played these various roles at different times in its history. However, given the extensive variation in dispersal capacity among Southeast Asian vertebrates, it seems reasonable that when Palawan was in a particular geographic position it may have served, for example, as a springboard to the oceanic Philippines for some organisms, while simultaneously representing a dead-end Sundaic peninsula for others.

Thoroughly testing these hypotheses will require improved geological and sea-level reconstructions and many more phylogenies than are currently available, each with precise and accurate time-scales alongside dense geographic sampling. Future taxonomic updates will probably lead to the increased recognition of Palawan populations as endemic species (Peterson, 2006; Brown & Diesmos, 2009). However, we anticipate that the complex pattern of biogeographic relationships we summarize here will remain, even as new data are collected and gradually refine our knowledge of the relationships among organisms in the region.

Given the evidence presented here, Huxley’s Line, which has long ‘divided’ the oceanic Philippines from Palawan, is best viewed as a filter barrier that strongly impacts some lineages, others moderately so, and some not at all. Perhaps, when discussing the importance of biogeographic boundaries such as Huxley’s Line, biogeographers would be advised to acknowledge the combined effect of geographic history, lineage-specific dispersal characteristics and historical contingencies, which gives rise to everything from strict adherence to complete defiance of the line (Evans et al., 2003). We therefore suggest adoption of the more accurate terminology ‘Huxley’s Filter Zone’. This terminology recognizes Huxley’s significant contributions and original intent, and imparts a biologically meaningful characterization of this classic biogeographical theme.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

We thank the Philippine Department of Environment and Natural Resources and the staff from the Palawan Council for Sustainable Development for supporting our research. Financial assistance was provided by the American Society of Mammalogists to J.A.E. and National Science Foundation (DEB 0743491) to R.M.B. and R.G.M. N. Antoque, J. Cantil, J. Fernandez, A. Regalo and V. Yngente provided invaluable assistance with fieldwork. We thank the KU herpetology and mammal reading groups, L.R. Heaney and two anonymous referees for their constructive and insightful criticisms of the manuscript. R. Hall and G. Yumul were especially helpful with interpretations of the geological literature.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information
  • Atkins, H., Preston, J. & Cronk, Q.C.B. (2001) A molecular test of Huxley’s line: Cyrtandra (Gesneriaceae) in Borneo and the Philippines. Biological Journal of the Linnean Society, 72, 143159.
  • Beck, J., Kitching, I.J. & Linsenmair, K.E. (2006) Wallace’s line revisited: has vicariance or dispersal shaped the distribution of Malesian hawkmoths (Lepidoptera: Sphingidae)? Biological Journal of the Linnean Society, 89, 455468.
  • Bintanja, R., van de Wal, S.W. & Oelemans, J. (2005) Modelled atmospheric temperatures and global sea levels of the past million years. Nature, 437, 125128.
  • Bird, M., Boobyer, E., Bryant, C., Lewis, H., Paz, V. & Stephens, W. (2007) A long record of environmental change from bat guano deposits in Makangit Cave, Palawan, Philippines. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 98, 111.
  • Bird, M.I., Taylor, D. & Hunt, C. (2005) Palaeoenvironments of insular Southeast Asia during the Last Glacial Period: a savanna corridor in Sundaland? Quaternary Science Reviews, 24, 22282242.
  • Bird, P.R., Quinton, N.A., Beeson, M.N. & Bristow, C. (1993) Mindoro: a rifted microcontinent in collision with the Philippines volcanic arc; basin evolution and hydrocarbon potential. Journal of Southeast Asian Earth Sciences, 8, 449468.
  • Bossuyt, F., Brown, R.M., Hillis, D.M., Cannatella, D.C. & Milinkovitch, M.C. (2006) Phylogeny and biogeography of a cosmopolitan frog radiation: Late Cretaceous diversification resulted in continent-scale endemism in the family Ranidae. Systematic Biology, 55, 579594.
  • Boulenger, G.A. (1894) On the herpetological fauna of Palawan and Balabac. Annals and Magazine of Natural History, 80, 690.
  • Brown, J.H. (1971) Mammals on mountain tops: nonequilibrium insular biogeography. The American Naturalist, 105, 467478.
  • Brown, R.M. (2007) Introduction to Robert F. Inger’s systematics and zoogeography of Philippine Amphibia. Systematics and zoogeography of Philippine Amphibia (by R.F.Inger), pp. 117. Natural History Publications, Kota Kinabalu, Malaysia.
  • Brown, R.M. & Diesmos, A.C. (2009) Philippines, biology. Encyclopedia of islands (ed. by R.G.Gillespie and D.A.Clague), pp. 723732. University of California Press, Berkeley, CA.
  • Brown, R.M. & Guttman, S.I. (2002) Phylogenetic systematics of the Rana signata complex of Philippine and Bornean stream frogs: reconsideration of Huxley’s modification of Wallace’s Line at the Oriental–Australian faunal zone interface. Biological Journal of the Linnean Society, 76, 393461.
  • Brown, R.M., Siler, C.D., Diesmos, A.C. & Alcala, A.C. (2009) The Philippine frogs of the genus Leptobrachium (Anura; Megophryidae): phylogeny-based species delimitation, taxonomic revision, and descriptions of three new species. Herpetological Monographs, 23, 144.
  • Brown, R.M., Diesmos, A.C., Duya, M.V., Garcia, H.J.D. & Rico, E.L. (2010) A new forest gecko (Squamata; Gekkonidae; genus Luperosaurus) from Mt. Mantalingajan, southern Palawan Island, Philippines. Journal of Herpetology, 44, 3748.
  • Brown, R.M., Linkem, C.W., Siler, C.D., Sukumaran, J., Esselstyn, J.A., Diesmos, A.C., Iskandar, D.T., Bickford, D., Evans, B.J., McGuire, J.A., Grismer, L., Supriatna, J. & Andayani, N. (2010) Phylogeography and historical demography of Polypedates leucomystax in the islands of Indonesia and the Philippines: Evidence for recent human-mediated range expansion? Molecular Phylogenetics and Evolution, doi: 10.1016/j.ympev.2010.06.015.
  • Brown, W.C. & Alcala, A.C. (1970) The zoogeography of the Philippine Islands, a fringing archipelago. Proceedings of the California Academy of Sciences, 38, 105130.
  • Brown, W.C. & Alcala, A.C. (1978) Philippine lizards of the family Gekkonidae. Silliman University Press, Dumaguete City, Philippines.
  • Brown, W.C. & Alcala, A.C. (1980) Philippine lizards of the family Scincidae. Silliman University Press, Dumaguete City, Philippines.
  • Campbell, P. (2004) Phylogeny and phylogeography of Old World fruit bats in the Cynopterus brachyotis complex. Molecular Phylogenetics and Evolution, 33, 764781.
  • Corbet, G.B. & Hill, J.E. (1992) The mammals of the Indomalayan region. Oxford University Press, New York.
  • Cracraft, J. (1988) From Malaysia to New Guinea: evolutionary biogeography within a complex continent–island arc contact zone. Proceedings of the 19th International Ornithological Congress, 2, 25812593.
  • Diamond, J.M. & Gilpin, M.E. (1983) Biogeographic umbilici and the origin of the Philippine avifauna. Oikos, 41, 307321.
  • Dickerson, R.E. (1928) Distribution of life in the Philippines. Philippine Bureau of Science, Manila.
  • Dickinson, E.C. (2003) The Howard & Moore complete checklist of the birds of the world. Princeton University Press, Princeton, NJ.
  • Diesmos, A.C., Brown, R.M., Alcala, A.C., Sison, R.V., Afuang, L.E. & Gee, G.V.A. (2002) Philippine amphibians and reptiles. Philippine biodiversity conservation priorities: a second iteration of the National Biodiversity Strategy and Action Plan (ed. by P.S.Ong, L.E.Afuang and R.G.Rosell-Ambal), pp. 2644. Department of the Environment and Natural Resources, Quezon City, Philippines.
  • Drovetski, S.V., Zink, R.M., Rohwer, S., Fadeev, I.V., Nesterov, E.V., Karagodin, I., Koblik, E.A. & Red’kin, Y.A. (2004) Complex biogeographic history of a Holarctic passerine. Proceedings of the Royal Society B: Biological Sciences, 271, 545551.
  • Durkee, E.F. (1993) Oil, geology and changing concepts in the Southwest Philippines (Palawan and the Sulu Sea). Bulletin of the Geological Society of Malaysia, 33, 241262.
  • Encarnación, J. & Mukasa, S.B. (1997) Age and geochemistry of an ‘anorogenic’ crustal melt and implications for I-type granite petrogenesis. Lithos, 42, 113.
  • Esselstyn, J.A. & Goodman, S.M. (in press) A new species of shrew (Soricidae: Crocidura) from Sibuyan Island, Philippines. Journal of Mammalogy.
  • Esselstyn, J.A., Widmann, P. & Heaney, L.R. (2004) The mammals of Palawan Island, Philippines. Proceedings of the Biological Society of Washington, 117, 271302.
  • Esselstyn, J.A., Timm, R.M. & Brown, R.M. (2009) Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asian shrews. Evolution, 63, 25952610.
  • Evans, B.J., Brown, R.M., McGuire, J.A., Supriatna, J., Andayani, N., Diesmos, A., Iskandar, D., Melnick, D.J. & Cannatella, D.C. (2003) Phylogenetics of fanged frogs: testing biogeographical hypotheses at the interface of the Asian and Australian faunal zones. Systematic Biology, 52, 794819.
  • Everett, A.H. (1889) Remarks on the zoogeographical relationships of the island of Palawan and some adjacent islands. Proceedings of the Zoological Society of London, 1889, 220228.
  • Gamauf, A. & Haring, E. (2004) Molecular phylogeny and biogeography of honey-buzzards (genera Pernis and Henicopernis). Journal of Zoological Systematics and Evolutionary Research, 42, 145153.
  • Gascoyne, M., Benjamin, G.J., Schwarez, H.P. & Ford, D.C. (1979) Sea-level lowering during the Illinoian Glaciation: evidence from a Bahama ‘Blue Hole’. Science, 205, 806808.
  • Gaubert, P. & Antunes, A. (2005) Assessing the taxonomic status of the Palawan pangolin Manis culionensis (Pholidota) using discrete morphological characters. Journal of Mammalogy, 86, 10681074.
  • Gorog, A.J., Sinaga, M.H. & Engstrom, M.D. (2004) Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biological Journal of the Linnean Society, 81, 91109.
  • Günther, A. (1872) On the reptiles and amphibians of Borneo. Proceedings of the Zoological Society of London, 1872, 586600.
  • Hall, R. (1996) Reconstructing Cenozoic SE Asia. Tectonic evolution of Southeast Asia (ed. by R.Hall and D.Blundell), pp. 153184. Geological Society of London Special Publication No. 106. The Geological Society, London.
  • Hall, R. (1998) The plate tectonics of Cenozoic SE Asia and the distribution of land and sea. Biogeography and geological evolution of SE Asia (ed. by R.Hall and J.D.Holloway), pp. 99131. Backhuys Publishers, Leiden.
  • Hall, R. (2002) Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions and animations. Journal of Asian Earth Sciences, 20, 353434.
  • Heaney, L.R. (1979) A new species of tree squirrel (Sundasciurus) from Palawan Island, Philippines (Mammalia: Sciuridae). Proceedings of the Biological Society of Washington, 92, 280286.
  • Heaney, L.R. (1984) Mammalian species richness on islands of the Sunda Shelf, Southeast Asia. Oecologia, 61, 1117.
  • Heaney, L.R. (1985) Zoogeographic evidence for middle and late Pleistocene land bridges to the Philippine Islands. Modern Quaternary Research in Southeast Asia, 9, 127144.
  • Heaney, L.R. (1986) Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Biological Journal of the Linnean Society, 28, 127165.
  • Heaney, L.R. (1991) A synopsis of climatic and vegetational change in Southeast Asia. Climate Change, 19, 5361.
  • Heaney, L.R., Balete, D.S., Dolar, M.L., Alcala, A.C., Dans, A.T.L., Gonzales, P.C., Ingle, N.R., Lepiten, M.V., Oliver, W.L.R., Ong, P.S., Rickart, E.A., Tabaranza, B.R. & Utzurrum, R.B. (1998) A synopsis of the mammalian fauna of the Philippine Islands. Fieldiana: Zoology n.s., 88, 161.
  • Heaney, L.R., Balete, D.S., Rickart, E.A., Veluz, M.J. & Jansa, S.A. (2009) A new genus and species of ‘small tree-mouse’ (Rodentia, Muridae) related to the Philippine giant cloud rats. Bulletin of the American Museum of Natural History, 331, 205229.
  • Helgen, K. (2005) Order Scandentia. Mammal species of the world, 3rd edn (ed. by D.E.Wilson and D.M.Reeder), pp. 104109. Johns Hopkins University Press, Baltimore, MD.
  • Holloway, J.D. (1982) Mobile organisms in a geologically complex area: Lepidoptera in the Indo-Australian tropics. Zoological Journal of the Linnean Society, 76, 353373.
  • Hutterer, R. (2007) Records of shrews from Panay and Palawan, Philippines, with the description of two new species of Crocidura (Mammalia: Soricidae). Lynx, 38, 520.
  • Huxley, T.H. (1868) On the classification and distribution of the Alectoromorphae and Heteromorphae. Proceedings of the Zoological Society of London, 1868, 296319.
  • Inger, R.F. (1954) Systematics and zoogeography of Philippine Amphibia. Fieldiana, 33, 181531.
  • Inger, R.F. (1966) The systematics and zoogeography of the Amphibia of Borneo. Fieldiana, 52, 1402.
  • Inger, R.F. (1999) Distributions of amphibians in southern Asia and adjacent islands. Patterns of distribution of amphibians, a global perspective (ed. by W.E.Duellman), pp. 445482. Johns Hopkins University Press, Baltimore, MD.
  • Inger, R.F. & Tan, F.L. (1996) Checklist of the frogs of Borneo. The Raffles Bulletin of Zoology, 44, 551574.
  • Inger, R.F. & Voris, H.K. (2001) The biogeographical relations of the frogs and snakes of Sundaland. Journal of Biogeography, 28, 863891.
  • Jansa, S.A., Barker, F.K. & Heaney, L.R. (2006) The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Systematic Biology, 55, 7388.
  • Jones, A.W. & Kennedy, R.S. (2008) Evolution in a tropical archipelago: comparative phylogeography of Philippine fauna and flora reveals complex patterns of colonization and diversification. Biological Journal of the Linnean Society, 95, 620639.
  • de Jong, R. (1996) The continental Asian element in the fauna of the Philippines as exemplified by Coladenia Moore, 1881 (Lepidoptera: Hesperiidae). Cladistics, 12, 323348.
  • Kennedy, R.S., Gonzales, P.C., Dickinson, E.C., Miranda, H.C. & Fisher, T.H. (2000) A guide to the birds of the Philippines. Oxford University Press, Oxford.
  • Kloss, B. (1929) The zoo-geographical boundaries between Asia and Australia and some oriental sub-regions. Bulletin of the Raffles Museum, 2, 110.
  • Koch, A., Gaulke, M. & Böhme, W. (2010) Unravelling the underestimated diversity of Philippine water monitor lizards (Squamata: Varanus salvator complex), with the description of two new species and a new subspecies. Zootaxa, 2446, 154.
  • Linkem, C.W., Diesmos, A.C. & Brown, R.M. (2010) A new scincid lizard (genus Sphenomorphus) from Palawan Island, Philippines. Herpetologica, 66, 6779.
  • Lomolino, M.V. (1990) The target area hypothesis: the influence of island area on immigration rates of non-volant mammals. Oikos, 57, 297300.
  • Lucchini, V., Meijaard, E., Diong, C.H., Groves, C.P. & Randi, E. (2005) New phylogenetic perspectives among species of South-east Asian wild pig (Sus sp.) based on mtDNA sequences and morphometric data. Journal of Zoology, 266, 2535.
  • MacArthur, R.H. & Wilson, E.O. (1963) An equilibrium theory of insular zoogeography. Evolution, 17, 373387.
  • MacKinnon, J. & Phillipps, K. (1993) The birds of Borneo, Sumatra, Java, and Bali, the Greater Sunda Islands. Oxford University Press, Oxford.
  • Matsui, M., Tominaga, A., Liu, W., Khonsue, W., Grismer, L.L., Diesmos, A.C., Das, I., Sudin, A., Yambun, P., Yong, H. & Brown, R.M. (2010) Phylogenetic relationships of Ansonia from Southeast Asia inferred from mitochondrial DNA sequences: systematic and biogeographic implications (Anura: Bufonidae). Molecular Phylogenetics and Evolution, 54, 561570.
  • Mayr, E. (1944) Wallace’s Line in the light of recent zoogeographic studies. The Quarterly Review of Biology, 19, 114.
  • McGuire, J.A. & Alcala, A.C. (2000) A taxonomic revision of the flying lizards (Iguania: Agamidae: Draco) of the Philippine islands, with a description of a new species. Herpetological Monographs, 14, 81138.
  • McGuire, J.A. & Kiew, B.H. (2001) Phylogenetic systematics of Southeast Asian flying lizards (Iguania: Agamidae: Draco) as inferred from mitochondrial DNA sequence data. Biological Journal of the Linnean Society, 72, 203229.
  • Meijaard, E. (2003) Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of Biogeography, 30, 12451257.
  • Miller, K.G., Kominz, M.A., Browning, J.V., Wright, J.D., Mountain, G.S., Katz, M.E., Sugarman, P.J., Cramer, B.S., Christie-Blick, N. & Pekar, S.F. (2005) The Phanerozoic record of global sea-level change. Science, 310, 12931298.
  • Moyle, R.G., Filardi, C.E., Smith, C.E. & Diamond, J.M. (2009) Explosive Pleistocene diversification and hemispheric expansion of a ‘great speciator’. Proceedings of the National Academy of Sciences USA, 106, 18631868.
  • Myers, G.S. (1949) Ability of amphibians to cross sea barriers with especial reference to Pacific zoogeography. Proceedings of the Seventh Pacific Science Congress, 4, 1927.
  • Nyári, A.S., Peterson, A.T., Rice, N.H. & Moyle, R.G. (2009) Phylogenetic relationships of flowerpeckers (Aves: Dicaeidae): novel insights into the evolution of a tropical passerine clade. Molecular Phylogenetics and Evolution, 53, 613619.
  • Oliveros, C.H. & Moyle, R.G. (2010) Origin and diversification of Philippine bulbuls. Molecular Phylogenetics and Evolution, 54, 822832.
  • Outlaw, D.C. & Voelker, G. (2008) Pliocene climatic change in insular Southeast Asia as an engine of diversification in Ficedula flycatchers. Journal of Biogeography, 35, 739752.
  • Patou, M.L., Wilting, A., Gaubert, P., Esselstyn, J.A., Cruaud, C., Jennings, A.P., Fickel, J. & Veron, G. (2010) Evolutionary history of the Paradoxurus palm civets – a new model for Asian biogeography. Journal of Biogeography, doi: 10.1111/j.1365-2699.2010.02364.x.
  • Patterson, B.D. (1990) On the temporal development of nested subset patterns of species composition. Oikos, 59, 330342.
  • Payne, J., Francis, C.M. & Phillips, K. (1985) A field guide to the mammals of Borneo. Sabah Society, Kota Kinabalu, Malaysia.
  • Pelseneer, P. (1904) La ‘Ligne de Weber,’ limite zoologique de l’Asie et de l’Australie. Bulletin de la Classe des Sciences Académie Royale de Belgique, 1904, 10011022.
  • Peterson, A.T. (2006) Taxonomy is important in conservation: a preliminary reassessment of Philippine species-level bird taxonomy. Bird Conservation International, 16, 155173.
  • Piper, P., Ochoa, J., Lewis, H., Paz, V. & Ronquillo, W. (2008) The first evidence for the past presence of the tiger Panthera tigris (L.) on the island of Palawan, Philippines: extinction in an island population. Palaeogeography, Palaeoclimatology, Palaeoecology, 264, 123127.
  • Roberts, T.E., Sargis, E.J. & Olson, L.E. (2009) Networks, trees, and tree shrews: assessing support and identifying conflict with multiple loci and a problematic root. Systematic Biology, 58, 257270.
  • Rohling, E.J., Fenton, M., Jorissen, F.J., Bertrand, G., Ganssen, G. & Caulet, J.P. (1998) Magnitude of sea level lowstands of the last 500,000 years. Nature, 394, 162165.
  • Sanders, K., Malhotra, A. & Thorpe, R. (2004) Ecological diversification in a group of Indomalayan pitvipers (Trimeresurus): convergence in taxonomically important traits has implications for species identification. Journal of Evolutionary Biology, 17, 721731.
  • Siddall, M., Rohling, E.J., Almogi-Labin, A., Hemleben, C., Meischner, D., Schmelzer, I. & Smeed, D.A. (2003) Sea-level fluctuations during the last glacial cycle. Nature, 423, 853858.
  • Siddall, M., Bard, E., Rohling, E.J. & Hemleben, C. (2006) Sea-level reversal during Termination II. Geology, 34, 817820.
  • Siler, C.D., Oaks, J.R., Esselstyn, J.A., Diesmos, A.C. & Brown, R.M. (2010) Phylogeny and biogeography of Philippine bent-toed geckos (Gekkonidae: Cyrtodactylus) contradict a prevailing model of Pleistocene diversification. Molecular Phylogenetics and Evolution, 55, 699710.
  • Simpson, G.G. (1940) Mammals and land bridges. Journal of the Washington Academy of Sciences, 30, 137163.
  • Simpson, G.G. (1977) Too many lines; the limits of the Oriental and Australian zoogeographic regions. Proceedings of the American Philosophical Society, 121, 107120.
  • Swofford, D.L. (1999) PAUP* 4.0. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA.
  • Taylor, E.H. (1922a) The lizards of the Philippine Islands. Philippine Bureau of Science Monograph 17. Philippine Bureau of Science, Manila, Philippines.
  • Taylor, E.H. (1922b) Additions to the herpetological fauna of the Philippine Islands, I. Philippine Journal of Science, 21, 161206.
  • Taylor, E.H. (1922c) Additions to the herpetological fauna of the Philippine Islands, II. Philippine Journal of Science, 21, 257303.
  • Taylor, E.H. (1922d) Herpetological fauna of Mount Makiling. The Philippine Agriculturist, 5, 127139.
  • Taylor, E.H. (1922e) The snakes of the Philippine Islands. Department of Agriculture and Natural Resources, Bureau of Science, Manila.
  • Taylor, E.H. (1923) Additions to the herpetological fauna of the Philippine Islands, III. Philippine Journal of Science, 22, 515557.
  • Taylor, E.H. (1925) Additions to the herpetological fauna of the Philippine Islands, IV. Philippine Journal of Science, 26, 97111.
  • Taylor, E.H. (1928) Amphibians, lizards, and snakes of the Philippines. Distribution of life in the Philippines (ed. by R.Dickerson), pp. 214241. Philippine Bureau of Science, Manila, Philippines.
  • den Tex, R.-J., Thorington, R., Maldonado, J.E. & Leonard, J.A. (2010) Speciation dynamics in the SE Asian tropics: putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. Molecular Phylogenetics and Evolution, 55, 711720.
  • Thomas, A.L., Henderson, G.M., Deschamps, P., Yokoyama, Y., Mason, A.J., Bard, E., Hamelin, B., Durand, N. & Camoin, G. (2009) Penultimate deglacial sea level timing from uranium/thorium dating of Tahitian corals. Science, 324, 11861189.
  • Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography, 27, 11531167.
  • Wallace, A.R. (1860) On the zoological geography of the Malay Archipelago. Journal of the Proceedings of the Linnean Society: Zoology, 4, 172184.
  • Wallace, A.R. (1876) The geographical distribution of animals, with a study of the relations of living and extinct faunas as elucidating the past changes of the Earth’s surface. Harper & Brothers, New York.
  • Wallace, A.R. (1881) Island life. Harper & Brothers, New York.
  • Wegener, A. (1966) The origin of continents and oceans. Dover Publications, New York.
  • Welton, L.J., Siler, C.D., Diesmos, A.C. & Brown, R.M. (2009) A new bent-toed gecko (genus Cyrtodactylus) from southern Palawan Island, Philippines, and clarification of the taxonomic status of C. annulatus. Herpetologica, 65, 328343.
  • Woodruff, D.S. & Turner, L.M. (2009) The Indochinese–Sundaic zoogeographic transition: a description and analysis of terrestrial mammal species distributions. Journal of Biogeography, 36, 803821.
  • Yumul, G., Dimalanta, C., Queaño, K. & Marquez, E. (2009a) Philippines, geology. Encyclopedia of islands (ed. by R.G.Gillespie and D.A.Clague), pp. 732738. University of California Press, Berkeley, CA.
  • Yumul, G.P., Dimalanta, C.B., Marquez, E.J. & Queaño, K.L. (2009b) Onland signatures of the Palawan microcontinental block and Philippine mobile belt collision and crustal growth process: a review. Journal of Asian Earth Sciences, 34, 610623.
  • Zamoras, L.R. & Matsuoka, A. (2004) Accretion and postaccretion tectonics of the Calamian Islands, North Palawan block, Philippines. The Island Arc, 13, 506519.

Biosketch

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

The authors share a general interest in historical biogeography, especially in Southeast Asia. All are involved in research programmes investigating the evolutionary history of various Southeast Asian vertebrate lineages. By combining active field programmes with modern molecular and bioinformatic techniques, we hope to contribute to a synthetic understanding of why there are so many species in Southeast Asia.

Author contributions: J.A.E., J.M.G. and R.M.B. conceived the project; J.A.E. compiled the mammal data, C.H.O. and R.G.M. the bird data, and R.M.B the reptile and amphibian data; all authors contributed to the interpretation of data and writing.

Editor: Lawrence Heaney

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Appendix S1 List of the species of terrestrial vertebrates recorded from Palawan Island and its satellites, with details of their occurrence on the Sunda Shelf and in the oceanic Philippines.

As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.

FilenameFormatSizeDescription
JBI_2378_sm_Apps1.txt10KSupporting info item

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.