The avian fossil record in Insular Southeast Asia and its implications for avian biogeography and palaeoecology

Introduction

Ever since the seminal observations of Wallace (1863) and Wallace (1869), a plethora of studies has highlighted the avian species richness, high levels of endemism, and unique biogeographical patterns, as well as the conservation threats across Insular Southeast Asia (i.e., Huxley, 1868; Mayr, 1944; Butchart et al., 1996; Brooks, Pimm & Collar, 1997; Brooks et al., 1999; Stattersfield et al., 1998; Myers et al., 2000; Trainor & Lesmana, 2000; Birdlife International, 2001; Jones et al., 2001; Jones, Marsden & Linsley, 2003; Ding et al., 2006; Jønsson et al., 2008; Jønsson et al., 2010; Holt et al., 2013). However, very little is known regarding the evolutionary history of birds in this region. Evidence for extinction events and faunal turnovers in Insular Southeast Asia comes mainly from the mammalian fossil record, particularly proboscideans and primates (i.e., van den Bergh, 1999; Meijaard, 2003; de Vos, van den Hoek Ostende & van den Bergh, 2007; Van der Geer et al., 2010; Louys & Meijaard, 2010). How past events have shaped current patterns of avian distributions remains unexplored. Here, I provide a synthesis of the current fossil record of birds in Insular Southeast Asia. I describe sites with fossil avian remains, interpret the fossil evidence in terms of avian biogeography and dispersal, and discuss the significance of avian assemblages for Southeast Asian palaeoecology.

Material and Methods

Data on fossil occurrences of avian taxa in Insular Southeast Asia were acquired through the database www.Fossilworks.org (search terms ‘Aves’ and ‘Asia’), from published accounts, and from my own observations. Insular Southeast Asia is defined as the islands in the archipelagos of Indonesia, the Philippines, Malaysia, Singapore, Brunei, East Timor, and Christmas Island.

Sumatra

The oldest bird remains from Insular Southeast Asia are represented by an almost complete skeleton of the pelecaniform Protoplotus beauforti (Lambrecht, 1931) from Sibang in the Sangkarewang Formation, West Sumatra (Fig. 1). The age of the sediments has been disputed, but they are thought to be at least of Eocene age (Van Tets, Rich & Marino-Hadiwardoyo, 1989). Avian footprints have been described from the Oligocene Sawahlunto Formation near Kandi in West Sumatra. These footprints are attributed to two distinct ichnospecies of Aquatilavipes, A. wallacei (Zonneveld et al., 2011) and Aquatilavipes sp. A (Zaim et al., 2011; Zonneveld et al., 2011; Zonneveld et al., 2012), and are most similar to tracks produced by small shorebirds such as sandpipers, rails and plovers (Zonneveld et al., 2011).

The Fossil Bird Record in Insular Southeast Asia

To date, sixty-three species of fossil birds have been identified in Insular Southeast Asia, representing at least 54 genera and 27 families (Table S1). Two taxa are represented by fossil footprints only. While the avian fossil record covers the Eocene through to the Holocene, the majority of fossil avians come from Quaternary sediments. Raptors, owls, and swiftlets are present and abundant in all cave sites excavated, and remain ubiquitous elements in the modern Southeast Asian avifauna today. The current fossil record for birds forms a significant extension of the last overview of Southeast Asian fossil birds (Rich et al., 1986), which only listed a record for Java. The recent expansion reflects both renewed interest in existing collections (Borneo) as well as new excavation efforts on Sumatra, Flores and Palawan.

It is important to note the differences in taphonomy between some of the sites. Open-air sites in fluvial deposits, such as the localities of Watualang and Trinil, are less likely to preserve microfauna, whereas the cave sites on Borneo, Palawan and Flores are more favourable for the preservation of smaller bones. Bone accumulations in caves may result from fluvial transport, pitfalls, burrow deaths, predation and hibernation/aestivation (Andrews, 1990). For Niah Caves, deposition of swiftlets likely resulted from natural death, as the caves have sustained populations of swiftlets for at least 48,000 years (Stimpson, 2013). At Liang Bua (Flores), signs of digestions on the bone surfaces suggest that birds of prey, most likely a species of barn owl (Tyto sp.), are responsible for the accumulation of the majority of non-predatory birds (Meijer et al., 2013). Although many bird bones have been found in association with hominid (Java, Flores) or modern human (Borneo and Palawan) remains, no cut marks or other signs indicative of human hunting have been reported for any bird bones, in contrast to the remains of the pygmy elephant Stegodon florensis insularis (van den Bergh et al., 2008; van den Bergh et al., 2009).

Discussion

Avian Dispersal Routes

For the Lesser Sunda Islands, different dispersal scenarios have been proposed. Stresemann (1939) suggested that certain terrestrial birds colonized the Sunda Islands from the north (Sulawesi), but others have argued for a route via Southeastern Sundaland based on the similarities between the extant avifaunas of Flores, Java and Bali (Mayr, 1944; Mees, 2006). Such a route agrees with the presence of giant storks in the Late Pleistocene of both Java and Flores, as their large size might represent an adaptation to a more terrestrial life style (though it should be noted here that L. robustus from Flores displays wing morphology similar to modern L. dubius, Meijer & Due, 2010). Both the Javan and Flores giant stork may represent late offshoots of the lineage that also contains L. falconeri (Milne-Edwards, 1867–1871) from the Siwalik Hills in India (Louchart et al., 2005). Living Ciconidae display significant sexual dimorphism (Louchart et al., 2005), but Weesie (1982) does not consider the possibility that the stork remains from the Middle Pleistocene of Java (which he attributed to the modern black-necked stork Ephippiorhynchus cf. asiaticus and the greater adjutant L. cf. dubius) might, in fact, be smaller (female) specimens of the giant stork L. titan.

Although most of the Sunda Shelf was dry land at some point during the Pleistocene (Hall, 2002), there is no unambiguous geological evidence that Palawan was once connected to Sundaland (see discussion in Reis & Garong, 2001). Fossil and modern faunal data suggest that Palawan might have been a stepping stone between Borneo and the Philippines. In that light, the fossil presence of the mossy-nest swiftlet Aerodramus cf. salanganus in the very early Holocene is interesting, since it is currently absent on Palawan, but present in the Greater Sundas as well as in the Philippines. Its presence in the early Holocene could indicate that Palawan served as a stepping-stone for the dispersal of A. salanganus from the Greater Sundas into the Philippines.

Palaeoecological Implications

The climatic and ecological conditions of Pleistocene Sundaland have been subject of much debate. Heaney (1991) proposed the presence of a continuous savannah corridor during glacial maxima, which stretched from the Malaysian Peninsula through central Sundaland all the way to the Lesser Sunda Islands. This savannah corridor presumably facilitated the dispersal of hominins and other terrestrial megafauna across Sundaland, and acted as a dispersal barrier for forest-dependent taxa between Sumatra and Borneo. Although geomorphological, biogeographical, and palynological evidence, as well as vegetation modelling indicate that drier conditions prevailed over Insular Southeast Asia during the Last Glacial Period (for a review, see Bird, Taylor & Hunt, 2005), there is only very limited support for a continuous savannah corridor at the scale proposed by Heaney (1991). The savannah corridor hypothesis is based on the climatic conditions that occurred during glacial maxima, a situation that existed only for short periods of time during the Pleistocene (Voris, 2000). Furthermore, Slik et al. (2011) argue that the biogeographic difference between Sumatra and the Malay Peninsula, and Borneo can also be explained by exposed sandy sea-bed soils that acted as a dispersal barrier. Instead of savannah vegetation, swamps and heath forest dominated central Sundaland.

Birds are closely associated with vegetation, and their abundance and diversity in fossil assemblages adds valuable palaeoecological insights. The habitat spectrum inferred from Liang Bua’s avifauna (Meijer et al., 2013) shows that, during the Late Pleistocene, forest habitats, as well as wetland and open grassland habitats dominated around Liang Bua, and provided ample resources for hominins. Studies of the fossil bird assemblage from Niah Cave on Borneo (Stimpson, 2010; Stimpson, 2013) showed that swiftlets, obligate insectivores, had been persistently present from well into the Late Pleistocene until today (Stimpson, 2013). Their continuous presence indicates that habitats within the feeding range of these birds supported a sufficient base of aerial arthropods to support swiftlet populations. Despite ample evidence for drier conditions based on geomorphological, palynological, biogeographical data and climate modelling (see references in i.e., Bird, Taylor & Hunt, 2005; Westaway et al., 2009), and the concomitant contraction of forests, Late Pleistocene fossil bird assemblages from both Flores and Borneo suggest that forests persisted at least locally. These findings are consistent with other lines of evidence (Cannon, Morley & Bush, 2009; Wurster et al., 2010; Stimpson, 2012) that suggest that forest habitats were maintained across Insular Southeast Asia throughout the Late Pleistocene and Holocene.

Conclusion

The avian fossil record in Insular Southeast Asian has significantly increased in abundance and diversity over the last decades, and now consists of at least 63 species, representing 54 genera in 27 families, and 2 ichnospecies. Fossil bird remains span the last 50 million years, from the Eocene to the Holocene, but most remains have been found in Quaternary sediments. Swiftlets, birds of prey and owls are present and abundant in all cave sites excavated, and are ubiquitous elements in the modern Southeast Asian avifauna.

Extinctions seem to have been few, as the majority of the species in the fossil record are extant taxa. A number of species have undergone range shifts and are currently restricted to cooler regions. Similarities between the Late Pleistocene avifaunas of Flores and Java suggest a dispersal route across southern Sundaland. The mossy-nest swiftlet A. salanganus might have dispersed into the Philippines via Palawan. The Late Pleistocene record of forest birds, particularly swiftlets, suggest that the structural diversity of forest habitats was maintained, at least locally, throughout the Late Pleistocene and into the present.

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