Top Banner
See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/273450387 Return to the Malay Archipelago: the biogeography of Sundaic rainforest birds Article · March 2015 DOI: 10.1007/s10336-015-1188-3 CITATIONS 26 READS 523 3 authors: Some of the authors of this publication are also working on these related projects: Birds Fiji View project oVert Thematic Collections Network View project Frederick H Sheldon Louisiana State University 154 PUBLICATIONS 6,005 CITATIONS SEE PROFILE Haw Chuan Lim George Mason University 40 PUBLICATIONS 899 CITATIONS SEE PROFILE Robert Glen Moyle University of Kansas 208 PUBLICATIONS 3,122 CITATIONS SEE PROFILE All content following this page was uploaded by Frederick H Sheldon on 18 December 2018. The user has requested enhancement of the downloaded file.
36

Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Jun 17, 2020

Download

Documents

dariahiddleston
Welcome message from author
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
Page 1: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/273450387

Return to the Malay Archipelago: the biogeography of Sundaic rainforest birds

Article · March 2015

DOI: 10.1007/s10336-015-1188-3

CITATIONS

26READS

523

3 authors:

Some of the authors of this publication are also working on these related projects:

Birds Fiji View project

oVert Thematic Collections Network View project

Frederick H Sheldon

Louisiana State University

154 PUBLICATIONS   6,005 CITATIONS   

SEE PROFILE

Haw Chuan Lim

George Mason University

40 PUBLICATIONS   899 CITATIONS   

SEE PROFILE

Robert Glen Moyle

University of Kansas

208 PUBLICATIONS   3,122 CITATIONS   

SEE PROFILE

All content following this page was uploaded by Frederick H Sheldon on 18 December 2018.

The user has requested enhancement of the downloaded file.

Page 2: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

REVIEW

Return to the Malay Archipelago: the biogeography of Sundaicrainforest birds

Frederick H. Sheldon • Haw Chuan Lim •

Robert G. Moyle

Received: 12 November 2014 / Revised: 11 February 2015 / Accepted: 23 February 2015

� Dt. Ornithologen-Gesellschaft e.V. 2015

Abstract During the last 15–20 years, phylogenetic,

phylogeographic, paleontological, geological, and habitat

modeling studies have improved our knowledge of Sundaic

biogeography dramatically. In light of these advances, we

review (or postulate) where Sundaic rainforest birds came

from, the causes of their endemism, and the influence of

Pleistocene climatic perturbations on their diversification.

We suggest that four scenarios make up a coherent, plau-

sible explanation of patterns of extant diversity. First, re-

lictual lineages, which represent hangovers from the warm,

wet Eocene, survived the hard climatic times of the colder,

drier Oligocene and Pliocene in the mountains and adjacent

lowlands of eastern Borneo, where rainforest has existed

continuously for the last 20–30 million years. Second, most

modern SE Asian genera developed during the Miocene.

Third, the rainforest of Sundaland and its avifauna were

largely isolated from the rest of SE Asia during the late

Miocene and Pliocene by seasonal habitats in southern

Indochina and ocean boundaries elsewhere, increasing re-

gional endemism. Finally, the advent of global glaciation in

the Pleistocene introduced a different diversification dy-

namic to Sundaland. Early glacial events caused sufficient

drying in central Sundaland to fragment rainforest and its

avifauna into refugia in eastern and western Sundaland and

to allow dry-habitat taxa to reach Java from Indochina.

More recent glacial events resulted in sufficient perhumid

habitat in central Sundaland to reconnect previously vi-

cariated rainforest populations, creating the lowland and

elevational parapatry we see today. This Pleistocene dy-

namic was probably not simply one period of separation

and one period of connection, but rather a complex inter-

play of isolation and colonization, influenced by highly

variable population sizes, changing levels of gene flow, and

behavioral idiosyncrasies of the species involved.

Throughout all of these events, Borneo played a seminal

role in rainforest bird evolution by providing the habitat

necessary for diversification and the long-term survival of

taxa.

Keywords Avifauna � Borneo � Pleistocene glaciation �Java � Savanna � Sundaland

Introduction

The diversity and distribution of Indo-Malayan birds in-

spired Alfred Russel Wallace as he labored in the forests

and bungalows of Sarawak 160 years ago (Wallace 1876,

1883), and they still intrigue us today. Where did the Rail-

babbler (Eupetes macrocerus), Bornean Bristlehead (Pi-

tyriasis gymnocephala), and other unusual species of the

Greater Sundas come from? Why are so many Sundaic

endemics montane? Why are almost all SE Asian trogons

Communicated by E. Matthysen.

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10336-015-1188-3) contains supplementarymaterial, which is available to authorized users.

F. H. Sheldon (&)

Museum of Natural Science and Department of Biological

Sciences, Louisiana State University, Baton Rouge, LA, USA

e-mail: [email protected]

H. C. Lim

Smithsonian Institution, National Museum of Natural History,

Washington, DC, USA

R. G. Moyle

Biodiversity Institute and Department of Ecology

and Evolutionary Biology, University of Kansas,

Lawrence, KS, USA

123

J Ornithol

DOI 10.1007/s10336-015-1188-3

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 3: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

uniform in morphology and voice (Harpactes), except for

one taxon in the mountains of Java and Sumatra (Apal-

harpactes)? Why do barbets exhibit much the same pattern:

30 species of Megalaima (including Psilopogon)—almost

all with uniformly green bodies and colorful heads,

monotonous ‘‘tooking’’ or ‘‘pooping’’ songs, and solitary

lifestyles—versus one odd brown, wheezing, highly social

taxon (Caloramphus)? Why does Java share some taxa

with Indochina but not with Sumatra and Borneo? Why are

Bornean populations subdivided taxonomically despite

continuous rainforest across the island, such that species

like the Black-thighed Falconet (Microhierax fringillarius)

and Garnet Pitta (Pitta granatina), which inhabit most of

Borneo, are suddenly replaced in the northeast by the

White-fronted Falconet (M. latifrons) and Black-crowned

Pitta (P. ussheri)?

In this review, we try to come to grips with these and

other enigmatic patterns evident in the rainforest avifauna

of the Greater Sundas. The tremendous amount of phylo-

genetic, geological, geographic, and paleontological in-

formation generated in the last 15–20 years makes it

possible to propose with some degree of confidence: (1)

where major components of the Sundaic avifauna

originated on a global scale, (2) roughly (very roughly)

when they arrived in SE Asia, (3) what caused major

groups to radiate or decline in the Sunda Islands, and (4)

how diversification occurred in more recent geological

times. Our examples come mainly from Borneo because we

are most familiar with Bornean birds, and Borneo is by far

the best-studied Sundaic landmass in terms of phyloge-

netics and population genetics. We also discuss bird evo-

lution on the other Sunda islands, particularly Java,

because the unique histories of these islands help illumi-

nate biogeographic patterns. What is evident in this telling

is that we have a reasonable idea where some groups of

Indo-Malayan birds ultimately came from and what forces

likely caused Pleistocene diversification—but much of our

understanding of Sundaic bird evolution is shaky at best.

Dates attributed to events, for example, may be off by tens

of millions of years in some instances. Regardless of this

substantial uncertainty, we present a fairly simple, in some

cases provocative, outline of biogeographic history in the

hope of stimulating more rigorous investigations of plau-

sible scenarios in the future.

Major patterns in the Sundaic avifauna may be attributed

to just a few interrelated climatic and geographic forces,

the most important of which were: (1) changes in tem-

perature and precipitation between Cenozoic epochs, (2)

climatic changes associated with global glacial events of

the Pleistocene, (3) persistence of Sundaic rainforest

refuges through hard climatic times, and (4) the topography

and position of Borneo. Climatic shifts between Cenozoic

epochs (Berggren and Prothero 1992; Zachos et al. 2001)

almost certainly fostered cycles of taxic radiation and ex-

tinction in SE Asia (Morley 2000; Mittelbach et al. 2007),

sort of ‘‘taxon cycles’’ written on a large scale (Ricklefs

and Cox 1978). The warm wet Eocene (a hot house epoch)

would have led to a bloom of rainforest species, the cold

dry Oligocene (an ice house epoch) to a reduction in

rainforest species, the warm wet Miocene to a bloom, and

the cold dry Pliocene to a reduction. The Eocene bloom

and Oligocene reduction are suggested by the age and

characteristics of a few rainforest relicts that have survived

to modern times, and the Miocene bloom is evident from

phylogenetic studies of modern taxa. The persistence of

rainforest refuges in and around mountains would have

allowed rainforest species to survive through the cooler,

drier Oligocene and Pliocene. The Pleistocene Ice Age

began at about 2.6 Ma (Mega-annum or million years ago),

and subsequent global glacial and interglacial events in-

troduced a new dimension to the process of diversification

in Sundaland. Habitat alterations wrought by sea level and

climate changes during the glacial events explain much of

the parapatry we see today between populations both

across islands in lowland rainforest and elevationally on

mountains. They also explain the disjunction between Ja-

van and Indochinese taxa. Throughout much of the Ceno-

zoic, Borneo must have played a special role in rainforest

bird diversification and preservation because of its age,

size, extensive mountains, and position on the eastern edge

of Sundaland (de Bruyn et al. 2014). In contrast, the other

Greater Sunda Islands are relatively recent derivatives. As

such, these islands would have inherited much of their

rainforest avifauna from Borneo and to a lesser extent the

Malay Peninsula, which did not enjoy the rainfall or well-

positioned mountains necessary to preserve extensive

rainforest through colder, drier times.

Our review begins with traditional biogeographic de-

scriptions of Sundaland and its avifauna. We then scan the

geological and geographic history of the region from

60–5 Ma, highlighting types of land masses, habitats, and

bird groups likely to have existed in SE Asia at various

points in time. Starting at 5 Ma, in the Pliocene, the pace of

the review slows, and discussion focuses on geographic

changes, especially those driven by global glacial events of

the Pleistocene Ice Age, and how they influenced species

distributions, population structure, and diversification in

general.

The geography and avifauna of Sundaland

The Malay Peninsula, Borneo, Sumatra, Java, Palawan, and

many smaller islands lie on the Sunda Continental Shelf

(Fig. 1), and together they constitute Sundaland (‘‘Sunda

Land’’; Molengraaff 1921). This is an important

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 4: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

biogeographic subregion of SE Asia because of its

relatively non-seasonal (perhumid) rainforest and long-

term existence. To its north, Sundaland is separated from

Indochina by the transition from rainforest to more sea-

sonal forest. The floral demarcation of this shift is the

Kangar–Pattani Line (van Steenis 1950), but most verte-

brate biologists associate the Sundaic border with the

Isthmus of Kra further to the north, at approximately 10�latitude (Woodruff and Turner 2009). Biogeographic issues

related to this transition were reviewed by Hughes et al.

(2003) and Round et al. (2003). To the east, Sundaland is

separated from Wallacea by the deep oceanic trench of the

Makassar Strait, along which runs Wallace’s Line (Whit-

more 1981; Lohman et al. 2011). To the northeast, Sun-

daland is separated from the oceanic Philippine islands by

Huxley’s Line (Esselstyn et al. 2010).

Sundaland shares the largest proportion of its resident

forest birds with Indochina, and fewer with the Philippines

and Wallacea (Mayr 1944; Darlington 1957). Despite this

commonality, much of Sundaland’s avifauna is distinct

because of the habitat and physical barriers that have iso-

lated it for millions of years. About 691 resident land bird

species inhabit Sundaland, of which 264 (38 %) are en-

demic to the region [Table 1; Electronic Supplementary

Material (ESM) 1]. Among the Sundaic landmasses, the

Malay Peninsula has the most species (420) and the fewest

endemics (4). This odd numerical combination stems from

the Peninsula’s position, which results in it sharing large

numbers of species with Indochina and the Sunda Islands

(Wells 1999). Sumatra has the most species of any of the

Sunda islands (414), but not the most endemics (33), even

though it includes the endemic-rich Mentawai and

Enggano islands to its southwest. Borneo ranks third in

terms of number of species (373), but it has the most en-

demics (52), most of which are montane (Smythies 1999;

Phillipps and Phillipps 2014). Borneo also has the most

frogmouths, trogons, hornbills, barbets, pittas, broadbills,

flowerpeckers, and spiderhunters of any place in the world

(Phillipps and Phillipps 2014). Palawan possesses the

fewest species of any major Sunda island, presumably

because of its small size and relative isolation (Esselstyn

et al. 2010; Lim et al. 2014). Java has the most distinct

avifauna of any Sunda island by virtue of its position next

to the Lesser Sundas and its drier and more seasonal

Fig. 1 Map of Sundaland, with

the Greater Sunda Islands and

outlying biogeographic regions

(Indochina, Philippines, and

Wallacea) indicated. Black lines

Borders of Sundaland

Table 1 Total number of resident and endemic land bird species in

Sundaland

Area Total species (n) Endemics (n) % Endemism

Malay Peninsula 420 4 1

Borneo 373 52 14

Sumatra 414 33 8

Java 313 41 13

Palawan 153 18 12

Sundaland 691 264 38

Based on the list of Sundaic species in the ESM 1 and the classifi-

cation of Gill and Donsker (2014)

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 5: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

lowlands (Whitten et al. 1996). Java’s avifauna also com-

prises about 30 species with disjunct relationships to taxa

in Indochina (MacKinnon and Phillipps 1999).

The Malay Peninsula and Sumatra share the most resi-

dent land bird species (342) of any of the Sundaic land-

masses (Table 2), as would be expected by their proximity

and parallel geographic positions. These two areas are most

similar to Borneo in habitat and size and, thus, share the

most species with that island, about 280 and 289, respec-

tively. Java shares about 200 species each with the Malay

Peninsula, Borneo, and Sumatra, and Palawan shares about

85 species with each of the other areas.

From the Eocene to the Pliocene

Biogeography of the Indian Ocean

The birds of Sundaland come not only from adjacent Asia

but also from India, Africa, and Australia (Fig. 2). Re-

constructing the evolutionary history of Sundaland thus

requires an understanding of the Cenozoic geography of

the entire Indian Ocean region.

At the beginning of the Cenozoic, at around 66 Ma,

Sundaland was a peninsula jutting south from SE Asia

(Fig. 3), and its flora and fauna were presumably Laur-

asian. India was the first landmass with the potential to

bring Gondwanan land birds to Laurasia, at between 50 and

35 Ma (Morley 1998b; Aitchison et al. 2007; Kumar et al.

2007; Morley 2012; Hall 2013; Li et al. 2013). The timing

of India’s collision with Asia is not known precisely.

However, any exchange of organisms between India and

SE Asia would have been complicated by the development

of land bridges before complete continental unification and

the habitat barriers that followed unification (Hall 2013),

not to mention overwater dispersal. Indian flora arrived in

Sundaland in the mid-Eocene, suggesting a moist corridor

between the two regions (Morley 1998b, 2012). Whether

India carried birds to SE Asia from Madagascar (and by

extension from Africa) is not known. It certainly

transported ancient birds, but obvious descendants of these

may not have survived to modern times.

Africa was separated from western Laurasia by the

Tethys Sea until at least the Oligocene (Meulenkamp and

Sissingh 2003; Harzhauser et al. 2007; Allen and Arm-

strong 2008; Pook et al. 2009). A strong connection be-

tween African and SE Asian avifaunas is well known

(Olson 1973, 1979; Dinesen et al. 1994; Crowe et al. 2006;

Fuchs et al. 2006b; Jønsson et al. 2011; Ericson 2012;

Gonzalez et al. 2013), but it is difficult to determine how

and when bird groups were exchanged. Evidence from a

variety of plants and animals indicates that dispersal oc-

curred between Africa and SE Asia across Arabia and India

starting in the late Oligocene in what has been described by

Gonzalez (2012) as the ‘‘palaeotropical biotic exchange’’

(Morley 2000; Antoine et al. 2003; Zhou et al. 2012; Li

et al. 2013). Another ‘‘exchange’’ occurred at ap-

proximately 18–17 Ma during the height of the wet, warm

Miocene—this time by way of the Gomphotherium land-

bridge—and periodically thereafter (Barry et al. 1985,

1991; Rogl 1998, 1999; Koufos et al. 2005). The exchange

was closed toward the end of the Miocene with aridifica-

tion in the Middle East. Even during times when birds

could move back and forth between Africa and SE Asia,

the avifaunal connection was complicated by intervening

Laurasian and Indian avifaunas. Although Africa and SE

Asia share phasianids, cuckoos, trogons, hornbills, barbets,

woodpeckers, honeyguides, sub-oscines, among others,

these groups may well be Laurasian (Mayr 2005, 2014; but

see Ericson 2012). As such, they could have invaded Africa

and SE Asia independently. Thus, with the exception of a

few well-studied taxa, such as hornbills and oscine pas-

serines, it is difficult to stipulate with confidence a direct,

cross-India connection between Africa and SE Asia.

Numerous authors have also proposed that with respect to

some oscines, invasion may have occurred directly over the

Indian Ocean from Asia to Africa and vice versa (Jønsson

and Fjeldsa 2006; Samonds et al. 2012; Fjeldsa 2013;

Voelker et al. 2014).

In contrast, Australia’s influence on SE Asian birds is

much less speculative. At the beginning of the Cenozoic,

Australia was distant from SE Asia (Fig. 2), but by the end

of the Oligocene (approx. 23 Ma) the Australian plate had

pushed into the region of Sulawesi, closing the deep ocean

trench that had separated the two continents (Morley 2012;

Hall 2013). At this time, birds would have begun moving

from Australia to SE Asia (and vice versa) across inter-

vening islands (Barker et al. 2004; Schweizer et al. 2010;

Jønsson et al. 2011; Aggerbeck et al. 2014; Cibois et al.

2014), but the degree of avifaunal exchange is uncertain;

floral exchange at this point was minimal (Richardson et al.

2012). Extensive exchange between Australia and Sunda-

land would probably have proceeded with the Miocene,

Table 2 Number of resident land bird species shared between major

landmasses in Sundaland

Area Malay Peninsula Borneo Sumatra Java

Malay Peninsula –

Borneo 280 –

Sumatra 342 289 –

Java 205 174 222 –

Palawan 88 84 82 84

Based on the list of Sundaic species in the ESM 1 and the classifi-

cation of Gill and Donsker (2014)

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 6: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

after fuller development of Wallacea (Fig. 3) caused by the

amalgamation of the Sundaic and Australian continental

plates (Stelbrink et al. 2012; Holt et al. 2013; de Bruyn

et al. 2014).

Geological history of Sundaland

Sundaland is a subregion of Malesia, which also includes

the Philippines, Wallacea, and New Guinea (van Steenis

1950; Whitmore 1981). The tectonic force that built

Malesia was the clash between the Pacific, Indian, Aus-

tralian, Asian, and many smaller continental plates, starting

at approximately 45 Ma. These events have been reviewed

by Robert Hall of the Royal Holloway University of

London (Hall 1998, 2002, 2009, 2012, 2013), and here we

rely heavily on his synopses. Plate subduction, twisting,

and collision resulted in the formation of modern Sumatra,

Java, parts of Borneo, Palawan, and thousands of conti-

nental and oceanic islands east of Sundaland. It also re-

sulted in the mingling of plants and animals of Asian and

Australian heritage across the entire region (Whitmore

1981, 1987; Morley 2012). To a large extent these geolo-

gical events coincided with the radiation of modern birds

and help explain the origin of the Sundaic avifauna. As

already noted, two especially important geological events

were the Eocene collision of the Indian and Asian plates

and the late Oligocene collision of the Australian and Asian

plates (Hall 2012; Morley 2012). The latter event cut the

connection between the Pacific and Indian oceans at the

Indonesian Throughflow, so that moisture previously car-

ried from the Pacific Warm Pool was shed on Sundaland

rather than further west in the Indian Ocean (Morley 2003,

2012; Hall 2013). The increase in rainfall accompanied

global warming in the Miocene, and it fed the rainforest of

Sundaland throughout most of the epoch. Toward the end

of the Miocene, the global climate became cooler and drier,

reaching a dry peak in the Pliocene. At the end of the

Pliocene, from 2.6 Ma onward, effects of global glacial

events came into play as powerful causal forces in avian

diversification in Sundaland.

Since the Mesozoic, the Sunda Core has extended as a

continental peninsula south from Asia (Fig. 3: 60 Ma). The

main central mountain range of the Malay Peninsula was in

place and above sea level throughout the Cenozoic. It and

other elevated parts of the Core, especially the Schwaner

Mountains of western Borneo and possibly areas in the

northern Java Sea, provided sediments to build surrounding

lowlands in the early Cenozoic. In contrast to this stable

center, the outer edges of Sundaland, namely, Sumatra,

Java, and eastern Borneo, experienced the effects of sub-

duction and mountain-building starting approximately

45 Ma and underwent much change.

Portions of western and northern Borneo were probably

emergent throughout the Cenozoic (Moss and Wilson

1998). At its beginning, Borneo was a fairly linear

promontory extending eastward from the Sunda Core

(Fig. 3). At approximately 20 Ma, mountain-building was

extensive on Borneo’s northern margin as the island rotated

counterclockwise on its axis. The growth rate of these

mountains was perhaps equivalent to that of the Himalayas

(Hall and Nichols 2002: 18), and the resulting erosion was

massive, filling large basins with sediment and creating the

northwestern, southeastern, and eastern lowlands of Bor-

neo. Subduction in the middle to late Miocene also created

a volcanic arc in the region of the Dent and Semporna

peninsulas, extending across the Sulu region to the

Philippines (Fig. 3: 10 Ma). The Meratus Mountains of

southeastern Borneo arose in the middle to late Miocene

(Witts et al. 2012). Mt. Kinabalu, Borneo’s most dominant

peak at 4095 m a.s.l., derives from granitic magma forced

into weak zones and fractures in Borneo’s northernmost

mountains. Subsequent uplift at approximately 7–8 Ma and

Fig. 2 Potential sources of birds in SE Asia (black arrows) at various

times in the Cenozoic: 60 Ma Laurasia, 40 Ma India, 30–10 Ma

Australia and Africa. For non-corvoid oscines (Passerides), biogeog-

raphers have speculated on a route to SE Asia first from Australia to

Africa over the Indian Ocean (approx. 40 Ma), and then more

recently from Africa to SE Asia (Ericson et al. 2003; Fuchs et al.

2006a; Jønsson and Fjeldsa 2006; Fjeldsa and Bowie 2008).

Continental positions were estimated from Li and Powell (2001) via

Schweizer et al. (2010)

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 7: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

erosion of overlying softer rock (Choi 1996; Cottam et al.

2010) yielded the mountain we see today.

Sumatra experienced periods of mountain-building on

its southwestern side from the subduction of the Indian

plate, but the island also subsided and was largely inun-

dated several times. Volcanic activity was widespread in

the middle Eocene. From 30–25 Ma, Sumatra consisted of

mostly dry land, with small areas of high elevation and

some volcanoes, but from 20–10 Ma most of the lower

elevation sites were submerged, and only the mountains

remained above sea level. In the late Miocene, the Barisan

mountains rose and expanded (Fig. 3: 10 and 5 Ma). The

large islands off Sumatra’s southwestern coast (e.g., Nias

and Siberut) were probably connected to the main island

Fig. 3 Geography of Sundaland during the Cenozoic, based on maps provided by Hall (2013)

J Ornithol

123

Highlight
Page 8: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

since the middle Miocene, but this is less likely for islands

further to the east. At approximately 1 Ma, Sumatra ex-

perienced a large amount of volcanism along its western

side, and erosion of these mountains helped produce the

island’s current northern lowlands.

Java is a newer island than Borneo and Sumatra, having

emerged in its modern form only in the last 2 Ma, although

western Java existed as a land mass before then (Fig. 3).

The rocks underlying the modern island were roughly

aligned north–south with Sumatra at the beginning of the

Cenozoic, and its northern end (modern western end) was

connected and emergent at 30–25 Ma. From the end of the

Oligocene to about 5 Ma, however, Java was basically an

arc of volcanic islands rather than a single island. Like

Sumatra, it experienced a great deal of volcanism during

the last million years due to subduction. Unlike Sumatra,

however, it does not have a continuous mountain range; its

highlands and volcanos, which were previously separated

by water, are now separated by drier lowlands. Thus, the

mountains still act as geographic islands (Whitten et al.

1996).

Palawan’s history differs substantially from that of the

other Sunda islands. Palawan began as a continental frag-

ment that broke off southern Asia about 30 Ma and drifted

south until becoming lodged on the Sunda shelf about

10 Ma (Hall 1998, 2002; Zamoros and Matsuoka 2004;

Zamoros et al. 2008). Originally, Palawan was thought to

have been submerged during most of its journey, but

Blackburn et al. (2010) and Siler et al. (2012) have argued

on biological and geological grounds that parts of Palawan

were continuously subaerial, so that the island could have

acted as an ‘‘ark’’, transporting organisms from continental

Asia to Sundaland, Philippines, and Sulawesi. Hall’s most

recent maps (Fig. 3) depict Palawan as continuously

emergent as well. Much of modern-day Palawan was thrust

upward after it hit the Sunda shelf (Durkee 1993; Hall

2002; Yumul et al. 2009). Despite its attachment to the

Sunda shelf, Palawan may not have been connected di-

rectly by land to greater Borneo for at least 1 Ma, if ever

(Bintanja et al. 2005; Esselstyn et al. 2010).

In terms of avian evolution, the most important con-

clusion to be drawn from this geological summary is that

Borneo is by far the oldest and largest continuously sub-

aerial island in Sundaland. Its central mountain chain has

been dominant for at least 20 (perhaps 30) million years,

and its lowlands were extensive during that period. Su-

matra has come together as a stable, whole island only in

the last 5–10 Ma, and Java only in the last 2–5 Ma.

Geographic history of Sundaland

Geologists and paleontologists have made great strides in

identifying land areas and reconstructing climate and

habitats of Sundaland in the Cenozoic. Advances in un-

derstanding Sundaic geography have been reviewed and

updated for non-geologists by palynologist Robert J.

Morley of the Royal Holloway University of London

(Morley 1998a, b, 2000, 2011, 2012). Most of the evidence

for paleo climates and habitats comes from pollen derived

from drilling cores produced during hydrocarbon explo-

ration, but some also comes from lithographic indicators

such as coal, which was deposited during wet times, and

from paleosols (Morley and Morley 2013).

The Paleocene and Eocene of Sundaland were warm,

wet epochs, referred to as the Early Eocene Climatic Op-

timum (Yapp 2004). At this time, Sundaland would have

had extensive rainforest composed of a Laurasian flora

(Morley 2012). Modern plants did not occur in Sundaland

until the mid to late Eocene (Morley 2012), when many of

the older indigenous forms were replaced by invading In-

dian flora (Morley 2012: fig. 4.2). Forest birds of the early

and mid-Eocene would have been Laurasian as well, and

few would have been recognizable as modern taxa (Mayr

2014). Although cooling occurred toward the end of the

Eocene, it appears that the entire epoch would have suited

rainforest species, and we can expect they radiated sub-

stantially. From about 40 Ma, modern forms might have

included galliforms, cuckoos, owls, nightjars, frogmouths,

swifts, trogons, kingfishers, colies, coraciiforms, wood-

peckers, broadbills, and pittas (James 2005; Mayr 2005,

2014; Moyle et al. 2006a; Clarke et al. 2009; Ksepka and

Clarke 2009; Nesbitt et al. 2011).

During the Oligocene, Sundaland had seasonal forest in

its north and west and wetter forest along its eastern and

southern edges. Extensive drying in the mid-Oligocene

gave way to wetter forest in the equatorial zone and east

coast toward the end of the epoch (Morley 2012). Mid-

Oligocene (28 Ma) dry habitats are suggested by the ex-

tensive presence of conifers in the lowlands of the South

China Sea region and a lack of coal deposits (Morley 2012:

fig. 4.7). Sumatra also appears to have had a seasonal cli-

mate at this time. In the Java Sea, the early Oligocene was

wet but became drier as the epoch proceeded. Peatswamp

forest is evident in this region in the late Oligocene. Most

important for our story is that the mountains of equatorial

Borneo appear to have retained an ‘‘everwet’’ climate

throughout the epoch (Morley 2012).

At the end of the Oligocene, the collision between the

Australian and Asian plates closed the Indonesian

Throughflow, causing the warm, moist Pacific air to con-

centrate on Sundaland (Morley 2003). This moisture,

combined with global warming, ended the relatively cold,

dry Oligocene and began the long, warm, wet Miocene.

Extensive rainforest is thought to have developed across

Sundaland by the early Miocene, except perhaps in

southern Sumatra and western proto-Java (Morley 2012:

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 9: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

fig. 4.7). Phylogenetic studies indicate that rainforest bird

groups, including galliforms, trogons, barbets, hornbills,

and oscine passerines, radiated substantially during this

epoch.

Sundaic bird biogeography from the Eocene to Pliocene

Here we describe patterns of Eocene–Pliocene evolution in

a few SE Asian rainforest bird groups that have been well

sampled and studied using modern phylogenetic methods.

One problem to be faced in reconstructing older biogeo-

graphic events in Sundaland, however, is that molecular

estimates of group ages (e.g., Brown et al. 2008; Wright

et al. 2008; van Tuinen 2009; Brown and Van Tuinen

2011) tend to be greater than those based on fossil or

geographic evidence of those ages (Feduccia 2003; Mayr

2013, 2014), sometimes by tens of millions of years. In SE

Asia, dating of phylogenetic events has depended on as-

sumed molecular rates because calibrating potentially more

appropriate rates is difficult given the region’s complex

geography and lack of rainforest bird fossils (Meijer 2014).

However, the timing of modern bird occurrence in Sun-

daland can be judged roughly by the age of modern

(crown) group fossils found elsewhere. Such fossils do not

occur in substantial numbers until the late Eocene (approx.

40 Ma; Mayr 2005, 2014). Also, newer molecular phylo-

genetic methods employing Bayesian relaxed clock ana-

lyses (Drummond et al. 2006; Drummond and Rambaut

2007; Ho and Phillips 2009) provide dates of bird-group

radiations that are more in accord with geological and

fossil evidence (Gonzalez 2012; Gonzalez et al. 2013; Stein

2013; Aggerbeck et al. 2014). These two lines of evidence

point circumstantially toward the Oligocene as the best

starting point for a discussion of the evolution of modern

Sundaic birds. At this time, the Eocene rainforest was re-

ceding because of a drier, cooler climate, and Eocene bird

groups probably faced substantial competition from Afri-

can and Australian invaders. After the Oligocene, with

climate amelioration, all phylogenetic studies agree that

modern rainforest bird groups flourished.

Galliformes Stein (2013) produced a comprehensive

phylogeny of galliforms employing[14,500 nucleotides of

mitochondrial and nuclear DNA isolated from 233 taxa,

with four fossils for calibration, and Bayesian relaxed clock

analyses. One of the most interesting early events evident

in Stein’s tree is the late Eocene–Oligocene connection

between the east African partridge Xenoperdix and the

Sundaic genera Caloperdix, Rollulus, and Arborophila

(Fig. 4). Such a relationship was predicted by Dinesen

et al. (1994) when they discovered Xenoperdix in the

mountains of Tanzania. Aging from the phylogeny com-

bined with modern distributions also suggests that

Caloperdix and Haematortyx (and possibly Rollulus) are

relicts that survived in Bornean refugia (Fig. 4). As with

other phylogenetic studies, Stein’s study demonstrates that

the late Miocene and Pliocene were most important to the

derivation of the modern pheasant and partridge species in

SE Asia.

Fruit pigeons and doves Sundaland’s main columbids are

fruit pigeons, among which Treron is the most speciose

group, being sister to all other fruit pigeons, doves, and

allies (including Chalcophaps, Turtur, Goura, Caloenas,

Trugon, Phapitreron, Hemiphaga, Lopholaimus, Gymno-

phaps, Ducula, and Ptilinopus), and appears to have arisen

in Asia (Johnson, personal communication). Ptilinopus

represents a Pacific radiation, with P. jambu reaching

Sundaland approximately 10 Ma (Cibois et al. 2014).

Parrots Parrots of Sundaland derived from Australia,

possibly in three waves toward the end of the Oligocene,

leading to Psittacula, Psittinus, and Loriculus. Psittacula

and Psittinus are relatively closely related to one another,

and Loriculus is related to lories (Schweizer et al. 2010).

Ground cuckoos Asian ground cuckoos (Carpococcyx)

form the sister group of couas (Coua) of Madagascar, and

the two genera diverged from one another 25–45 Ma

[Sorenson and Payne (2005) and personal communication].

Thus, it is tempting to say that the ancestors of Asian birds

rafted on India from Africa. However, cuckoos are possibly

a Laurasian group (Mayr 2005), and Madagascar is

Gondwanan. Thus, any number of evolutionary scenarios is

possible, including those of Carpococcyx and Coua being

relicts of a once widespread taxon or representative of in-

dependent invasions of Africa and Asia.

Trogons and barbets Trogons and barbets probably are

Eocene groups of Laurasia (Mayr 2005, 2014; but see

Ericson 2012). Both apparently invaded the Neotropics,

Africa, and Asian tropics at about the same time in the mid-

Cenozoic, thereby complicating the determination of basal

phylogenetic branching among the three tropical areas in

both groups (Moyle 2002, 2004, 2005; Johansson and

Erickson 2004). An early arrival of trogons and barbets in

SE Asia explains their parallel pattern of diversification in

the region. Both groups comprise what appears to be a

single relictual taxon—Apalharpactes in trogons and

Caloramphus in barbets—and a single speciose genus,

Harpactes and Megalaima (including Psilopogon), re-

spectively. Phylogenetic studies (Hosner et al. 2010; den

Tex and Leonard 2013) indicate a split between the re-

lictual and speciose genera approximately in the Oligo-

cene, and substantial diversification within Harpactes and

Megalaima in the Miocene (Fig. 5). One explanation for

this parallel pattern is that trogons and barbets proliferated

in the Eocene of SE Asia, then were largely extirpated in

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 10: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Fig. 4 Clades from the

galliform phylogeny of Stein

(2013) selected for their

Sundaic representation. Gray

boxes 95 % Highest posterior

densities of nodal ages. Where

taxa overlap, the branching

patterns here have been

corroborated by Wang et al.

(2013) and Sun et al. (2014)

Fig. 5 Similarity in pattern of

SE Asian trogon and barbet

phylogenies, given highly

speculative divergence dates.

Both groups are represented in

SE Asia by a singular, relictual

taxon of approximately

Oligocene age (Apalharpactes

in trogons and Caloramphus in

barbets), and both have

undergone substantial Sundaic

radiations in the Miocene and

Pliocene (Hosner et al. 2010;

den Tex and Leonard 2013)

J Ornithol

123

Highlight
Page 11: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

the colder, drier Oligocene, and finally re-radiated in the

Miocene. Apalharpactes and Caloramphus would be relicts

of the Eocene that survived the Oligocene (and Pliocene) in

rainforest refuges.

Hornbills Gonzalez et al. (2013) compared 1846 nu-

cleotides of the mitochondrial cytochrome b and nuclear

AK1 intron 5 to produce a dated phylogeny of all 61

species of hornbills. These authors calibrated the tree using

a combination of the coraciiform molecular rate (Pacheco

et al. 2011) and three hornbill-fossil dates. With the ex-

ception of Berenicornis (White-crowned Hornbill), they

found that Asian hornbills are monophyletic and invaded

from Africa in the late Oligocene. Berenicornis represents

a separate invasion from Africa in the early Miocene.

Gonzalez (2012) also estimated phylogenies of hornbill

food-trees to assess the co-evolution of the birds and their

food. The hornbills’ Asian invasion followed their devel-

opment of frugivory, and hornbills probably helped dis-

perse food-trees from Africa to SE Asia. An alternative

view had been proposed earlier by Viseshakul et al. (2011),

who believed that hornbills derived from Laurasia much

earlier (in the mid-Eocene) and dispersed Indian fruits to

insular SE Asia. The hornbills of modern Sundaland are

distributed in four main clades, with most members having

proliferated in the late Miocene.

Passerines Distribution, phylogeny, and the fossil record

suggest that Old World suboscines may have radiated in

the Eocene, only to be culled by the climate in the Oli-

gocene, and then largely replaced in the Miocene by

oscines. If true, the suboscines’ fate would mirror the

suspected replacement of other small-bodied Eocene

groups, such as colies and coraciiforms, by Miocene

oscines (Feduccia 1999; Mayr 2005; Clarke et al. 2009).

Evidence of Old World suboscines in the Eocene includes

phylogenetic estimates of lineage ages (Irestedt et al. 2001;

Moyle et al. 2006a) and fossils in the lower Oligocene of

Europe (Mayr 2013). Among Sundaic suboscines (broad-

bills and pittas), the frugivorous green broadbills (Calyp-

tomena) appear to be the only descendants of one ancient

lineage of broadbills, and the insectivorous broadbills

(Corydon and Eurylaimus) descendants of another. Pittas

are also ancient, but the modern taxa have diversified more

recently and extensively (or survived extinction more

successfully) than broadbills.

Oscines presumably arrived in SE Asia later than

suboscines, as indicated by phylogenetic and fossil

evidence (Ericson et al. 2003; Barker et al. 2004; Mayr

2005). Patterns of their likely derivation, dispersal, and

radiation have been reviewed by Fjeldsa (2013). Corvoid

oscines of SE Asia, i.e., members of Infraorder Corvides

(Cracraft 2014)—including orioles, vireos, whistlers,

minivets, cuckoo-shrikes, trillers, wood swallows, wood

shrikes, flycatcher-shrikes, Bornean Bristlehead, ioras,

fantails, drongos, monarchs, jays, and crows—most likely

reached Sundaland by island hopping from the Australian

region, starting in the late Oligocene, based on phyloge-

netic (e.g., Jønsson et al. 2008, 2010a, b, c, 2011; Fabre

et al. 2012; Aggerbeck et al. 2014) and geographic

evidence (Morley 2012; Stelbrink et al. 2012; Hall 2013).

Some of the corvoids then moved to Africa, probably

overland, and some of their descendants reinvaded SE

Asia.

The other SE Asian oscines are in the Infraorder

Passerides (Cracraft 2014) and include such groups as

parids, nuthatches, swallows, warblers, babblers, bulbuls,

flycatchers, starlings, flowerpeckers, and sunbirds. Their

route to SE Asia is more speculative than that of the

corvoids (Ericson et al. 2014). One proposal is that their

ancestors first invaded Africa from Australia in the Eocene

over the Indian Ocean, perhaps via the Kerguelen Plateau

or Indian Ocean islands (Fig. 2; Ericson et al. 2003; Fuchs

et al. 2006a; Jønsson and Fjeldsa 2006; Fjeldsa and Bowie

2008). Members of Passerides presumably arrived in SE

Asia overland after diversifying in Africa, although some

researchers have also suggested an invasion of SE Asia

from Africa directly over the Indian Ocean (Voelker et al.

2014). The earliest overland connection between Africa

and SE Asia would have been in the late Oligocene,

followed by periodic opportunities in the Miocene.

Molecular phylogenetic investigations have clarified the

relationships of the two iconic passerines, the Bornean

Bristlehead and Malaysian Rail-babbler, mentioned earlier

in this article. The Bristlehead is a classic corvoid, similar

in body plan (if not plumage) to Australian cracticids

(butcherbirds and magpies). It is probably a relict of the

Australian corvoid invasion of Sundaland, whose descen-

dants subsequently reached Africa (Ahlquist et al. 1984;

Moyle et al. 2006b; Jønsson et al. 2011; Aggerbeck et al.

2014). The Rail-babbler is sister to the African Chaetops

(rockjumpers), and together they are sister to the African

Picathartes (rockfowl) (Jønsson et al. 2007). Chaetops and

Picathartes are thought to be relicts of early Passerides

radiation in Africa (Ericson et al. 2014). Thus, the Rail-

babbler would be a relict of an early invasion of SE Asia by

ancestral African oscines.

Among Passerides that have proliferated in SE Asia, the

babblers (Timaliidae) are perhaps the best group for the

study of Sunda biogeography and community assembly

because of their taxonomic and morphological diversity,

approximately 275 species in 50 genera, and extensive

sympatry in rainforest habitats. Moyle et al. (2012)

provided a comprehensive phylogeny of the group and a

general biogeographic analysis. These authors found that

babblers are divided into four main clades—Leiothrichi-

nae, Timaliinae, Pellorneinae, and Zosteropidae—all of

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Highlight
Page 12: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

which presumably radiated in the Miocene (Fig. 6). As a

whole, Sundaic babblers appear to have a mainland Asian

origin. In Leiothrichinae, only a few taxa have invaded

Sundaland (some laughingthrushes and Brown Fulvetta,

Alcippe bruneicauda). The most diverse Sundaic groups,

Timaliinae and Pellorneinae, comprise clades that are

endemic and probably diversified in Sundaland (this is

especially true of the Pellorneinae), as well as taxa that

may have originated in Sundaland and invaded Indochina

and other mainland areas, such as the Scaly-crowned

Babbler (Malacopteron cinereum) and Grey-throated Bab-

bler (Stachyris nigriceps). The Zosteropidae differs from

other babblers in that most of the early diversification of

these birds may have been centered in Wallacea and the

Philippines (Cibois et al. 2002; Moyle et al. 2009). This

family also includes two Bornean endemics, Chlorocharis

and Oculocincta, which are aberrant morphologically but

close genetically to other white-eyes.

Among passerines arriving most recently in Sundaland

from Australia and the Pacific are Gerygone and Pachy-

cephala (Gardner et al. 2010; Jønsson et al. 2014). For the

most part, these invaders are coastal, but one species, P.

hypoxantha (Bornean Whistler), is endemic to the moun-

tains of Borneo.

Sundaland from the Pliocene to present

Regional endemism of Sundaic birds

During the peak of the Miocene, tropical forest reached

from the equator northeast as far as Japan and northwest as

far as India (Morley 1998b). The strong taxonomic con-

nection between Sundaic, Indochinese, and southern Chi-

nese avifaunas (such as shown in Fig. 1 of Packert et al.

2012) probably stems from this widespread Miocene

rainforest. Toward the end of the Miocene and especially in

the Pliocene, however, perhumid forest retracted with

global cooling and drying and became restricted to Sun-

daland (Morley 2012) and parts of northern Indochina (Li

and Walker 1986). Between these two areas, drier seasonal

forest developed. Within Sundaland during the Pliocene,

rainforest retreated still further, occurring mainly in Bor-

neo’s eastern mountains and its Makassar Strait and Ma-

hakam catchments on the eastern side of the island (Morley

and Morley 2011; Morley 2012; de Bruyn et al. 2014).

Rainforest persisted in eastern Borneo throughout the

Pliocene and Pleistocene, even when the rest of Sundaland

was drier. The forest situation in western Sundaland is not

as clear, but the mountains and islands of western Sumatra

were likely wet from orographic precipitation throughout

the Pliocene–Pleistocene. In Java, at approximately 2 Ma,

the eastern lowlands were savanna and nearly treeless, and

temperate flora was invading from the Australian side

(Morley 2012).

The separation of Sundaic and Indochinese rainforest for

the last 5–10 Ma (Morley 2012: Fig. 4.7) led to substantial

regional endemism (Table 1). Nevertheless, some taxa still

managed to move between Sundaland and Indochina

(Medway and Wells 1976; Hughes et al. 2003; Reddy

2008; Moyle et al. 2012), as evidenced by the low number

of endemic genera (23) in Sundaland (Table 3). Dispersal

of rainforest taxa between Sundaland and Indochina may

have occurred during relatively short wetter periods or

involved eurytopic intermediates able to move through

drier more open forest.

To reconstruct the development of Sundaic endemism, it

would be helpful to date vicariance and dispersal events

between Sundaland and Indochina, but few studies provide

the necessary information. Stein’s (2013) phylogeny of the

Galliformes (Fig. 4) has an approximate date for the di-

vergence of two relevant Arborophila species, A. javanica

(Java) and A. ardens (Hainan), which diverged ap-

proximately 5.1 Ma. Stein’s phylogeny also contains dates

relevant to intra-Sundaic diversification. Among the low-

land peacock–pheasants, Polyplectron schleiermacheri

(Borneo) diverged from P. malacense (Thai-Malay Penin-

sula) at approximately 4.4 Ma (see also Kimball et al.

2001), and among the lowland fireback pheasants, Lophura

Fig. 6 Outline of the babbler phylogeny (Moyle et al. 2012), with

Sundaic genera listed in major clades. Diversification times are highly

speculative

J Ornithol

123

Highlight
Highlight
Page 13: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

bulweri (Borneo) diverged from its congeners (including

Sundaic and SE Asian taxa) approximately 7.4 Ma.

Two other studies that provide insight into the Sundaic–

Indochinese divergence are Reddy’s phylogeographic

comparisons of shrike-babblers and scimitar babblers

(Reddy 2008; Reddy and Moyle 2011). Among scimitar

babblers, she found that the endemic Sundaic species Po-

matorhinus montanus (Borneo, Sumatra, Java, and the

Malay Peninsula) was isolated near the beginning of the

Pleistocene from its Indochinese sister group, which con-

tains all other Pomatorhinus species. Among shrike-bab-

blers, she discovered two rounds of diversification. The

Javan species Pteruthius aenobarbus and P. flaviscapis

diverged from their closest Indochinese relatives at 4 and

2.5 Ma, respectively.

Finally, first Johansson et al. (2007) and then Packert

et al. (2012) examined the relationships of Sundaland’s

Phylloscopus and Seicercus warblers as tangents to their

Himalayan studies. As with shrike-babblers and scimitar

babblers, Sundaland has few representatives of these

otherwise speciose groups. P. trivirgatus (Mountain

Leaf-Warbler) diverged from its closest mainland rela-

tives between the late Pliocene and the mid-Pleistocene.

The Sundaic yellow-breasted warblers (S. montis, S.

castaniceps, and S. grammiceps) diverged as a group in

the late Miocene to Pliocene, but S. castaniceps has

maintained or regained a wide SE Asian distribution.

Opportunities to date Indochinese–Sundaic vicariance

and dispersal will accrue with more studies. Nevertheless,

doubts about the accuracy of molecular dating without

fossils or geographic evidence for calibration, and the in-

herent vagility of birds, will always plague efforts at

quantification.

The advent of high-latitude glaciation

Starting in the late Pliocene (3.2–2.6 Ma) and continuing

throughout the Quaternary, dramatic increases in the am-

plitude of climatic oscillations caused periods of global

cooling that resulted in long-lasting, high-latitude glacial

events (approx. 40,000–100,000 years each) separated by

relatively short interglacials (approx. 10,000–15,000 years

each), such as the one we are currently experiencing

(Kashiwaya et al. 2001; Zachos et al. 2001; deMenocal

2004; Bintanja et al. 2005). For Sundaland, the conse-

quences of these events were dramatic: lower sea levels as

arctic glaciers tied up oceanic water, a substantially in-

creased lowland area as the Sunda shelf emerged subaeri-

ally, connection of islands with one another and the

mainland, decreased oceanic influence on the interior areas

of Sundaland as the subcontinent enlarged, and increased

areas of montane habitat as mountain forests descended in

elevation with colder temperatures (Hanebuth et al. 2000;

Voris 2000; Wilson et al. 2000; Bird et al. 2005; Cannon

et al. 2009). During interglacials, sea level rose as arctic

glaciers melted, and the Sunda islands became isolated by

ocean waters, as they are today. The overall effect of these

alternating events was not only to isolate and, conversely,

join islands, but to shift the position, size, and types of

habitats covering Sundaland, creating diverse scenarios of

organismal vicariance and colonization.

The biogeography of Sundaland with respect to

Quaternary sea-level changes has been well reviewed

(Whitmore 1981; Heaney 1986; Whitmore 1987; Voris

2000; Woodruff and Turner 2009; Cranbrook 2010; Loh-

man et al. 2011; Morley 2012; de Bruyn et al. 2014;

Wurster and Bird 2014) and is only briefly covered here.

One issue, however, requires special emphasis because it

has been controversial and bears importantly on the evo-

lution of Sundaic birds: whether a drier, open habitat—

originally described as a ‘‘savanna corridor’’ (Heaney

1991; Bird et al. 2005)—occupied the interior of Sundaland

during periods of glacial perturbation. Existence of a dry

Sundaic interior is supported by some lines of evidence, but

disputed by others.

Our molecular phylogeographic studies of rainforest

birds reveal patterns of vicariance and dispersal that are

consistent with alternating periods of drier and wetter

Table 3 Endemic bird genera

of Sundaland

Based on the list of Sundaic

species in Electronic

Supplementary Material 1 and

the classification of Gill and

Donsker (2014)a B, Borneo; J Java; S, Sumatra;

M, Malay Peninsulab Paraphyletic genera (Moyle

et al. 2009; den Tex and

Leonard 2013)

Genus Areaa

Melanoperdix S M B

Rhizothera S M B

Haematortyx B

Hydrochous J S M B

Apalharpactes J S

Rhinoplax S M B

Berenicornis S M B

Reinwardtipicus J S M B

Psilopogonb S M

Caloramphus S M B

Pityriasis B

Urosphena B

Oculocinctab B

Chlorocharisb B

Chlamydochaera B

Platylophus J S M B

Platysmurus S M B

Eupetes S M B

Setornis S B

Tricholestes S M B

Kenopia S M B

Psaltria J

Leucopsar J

J Ornithol

123

Page 14: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

forests in the interior of Sundaland in the Pleistocene. The

area of Sundaland between Borneo, Sumatra, and the

Malay Peninsula was occupied by a dry habitat in the early

to mid-Pleistocene which was sufficiently large to force

rainforest birds into refugia in eastern and western Sun-

daland. During other times (mid-Pleistocene onward?),

drying of Sundaland’s interior was not pervasive enough to

keep rainforest birds in refugia.

Few biogeographers have made the distinction between

the effects of different glacial events when discussing the

‘‘savanna corridor’’ because most arguments have focused

on the Last Glacial Maximum (LGM; approx. 18–21

thousand years ago). Indeed, failure to distinguish between

the effects of different glacial events seems to be the main

cause of disagreement. Only recently has this source of

confusion been emphasized. Morley (2012), and more re-

cently de Bruyn et al. (2014), appreciated the need to

consider the complexity of multiple glacial events, of

which about ten occurred in the last 1 million years and

about 20 (less severe) in the preceding 1 million years

(Augustin et al. 2004; deMenocal 2004). These events

varied in force and, thus, in their effects on habitats.

Sundaland’s forest habitats during glacial events

The data used to identify terrestrial Pleistocene habitats

derive from the fields of geology, palynology, paleon-

tology, and phylogeography. The first three sources usually

provide fairly accurate information on specific sites and

times. Thus, we know, for example, that parts of Sundaland

had a dry, open habitat at certain times and places, such as

in central to eastern Java in the late Pliocene through the

mid-Pleistocene (Cranbrook 2000; van den Bergh et al.

2001; Bettis et al. 2009; Louys and Meijaard 2010; Morley

2012) and on the Malay Peninsula during the LGM

(Wurster et al. 2010). We also know that parts of Sumatra

had wet, closed forest in the late Pleistocene (Louys and

Meijaard 2010). However, these data generally do not bear

on the most important areas for dispersal of rainforest birds

among the main islands, i.e., habitats intervening between

Sumatra, Borneo, and the Malay Peninsula.

The existence of a dry interior in Sundaland is supported

by mid-Pleistocene fossils of the Javan megafauna, includ-

ing extinct proboscideans, rhinos, cattle, buffalo, hog deer,

antelope, and hyenas. A dry habitat in central Sundaland was

required for some of these animals to reach Java from Asia in

the late Pliocene to early Pleistocene (Medway 1972; Hea-

ney 1991; Cranbrook 2000, 2010; Morley 2000; van den

Bergh et al. 2001; Meijaard 2003). Additional circumstantial

evidence is supplied by phylogeographic and distributional

studies of populations of rainforest animals and plants. In

these cases, rainforest populations were clearly divided be-

tween eastern and western Sundaland, apparently by

inhospitable (presumably dry, open) habitat in central Sun-

daland, and this subdivision almost always has been at-

tributed to the early Pleistocene, such as for mammals (Ruedi

1996; Zhi et al. 1996; Brandon-Jones 1998; Fernando et al.

2003; Gorog et al. 2004; Meijaard and Groves 2004; Hirai

et al. 2005; Steiper 2006; Patou et al. 2010; Wilting et al.

2012; Wurster and Bird 2014), reptiles and amphibians

(Wilting et al. 2012), fish (Ryan and Esa 2006), ants (Quek

et al. 2007), termites (Gathorne-Hardy et al. 2002), and trees

(Banfer et al. 2006; Iwanaga et al. 2012; Ohtani et al. 2013).

In contrast to megafaunal and phylogeographic data, only

a few studies dispute the existence of an extensive dry habitat

in central Sundaland. Paleo-habitat modeling and some

geological and organism–distribution studies (Hu et al.

2003; Kershaw et al. 2007; Cannon et al. 2009; Slik et al.

2009; Prentice et al. 2011; Handiani et al. 2013) have found

evidence of substantial rainforest (or at least wet habitats)

across Sundaland in the LGM. Other biogeographers have

presented nuanced perspectives of paleo-environmental

distributions based on thorough reviews of the literature and

sometimes quantitative examinations of fossil data (Mei-

jaard and van der Zon 2003; Louys and Meijaard 2010). Such

studies have uncovered conflicting evidence, especially on

Borneo (e.g., at Niah), where numerous and varying types of

paleo-data are available, and the Malay Peninsula, where

paleo-sites are few and dating uncertain. Such studies indi-

cate the possibility of a mosaic of habitats (in the LGM, but

presumably also during earlier glacial events), which may

have supported movement or isolation of rainforest and dry-

habitat taxa differentially across Sundaland at various times

(Meijaard and van der Zon 2003).

Regardless of the uncertainty about the nature and

timing of habitats at circumscribed sites and times, the

overwhelming weight of evidence indicates a fairly

straightforward outline of Pleistocene habitat geography

(Fig. 7). Late in the Pliocene or early in the Pleistocene,

drier, open forest or savanna must have existed in Sunda-

land, at one or multiple times. The drier habitat provided

the means for elements of the Asian megafauna to reach

Java, and it subdivided Sundaic rainforest into refugia in

eastern and western Sundaland. These refugia most likely

were associated with mountains, coastal areas, and islands,

where the effects of orographic rainfall would be the

greatest (Newsome and Flenley 1988; Stuijts et al. 1988;

Stuijts 1993; Brandon-Jones 1996, 1998; Morley 2000;

Gathorne-Hardy et al. 2002; Gorog et al. 2004; Wilting

et al. 2012). Lower elevation sites associated with moun-

tains would also have benefitted from direct rainfall or

indirect watering from montane runoff. We know from

palynological data that a rainforest refuge existed in eastern

Borneo from the late Miocene to the present (Morley and

Morley 2011; Morley 2012). More recently—almost cer-

tainly in the LGM, when modeling shows extensive

J Ornithol

123

Page 15: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

rainforest across equatorial Sundaland (Cannon et al.

2009), as well as during other glacial events of the last

1 Ma, when the Sundaic interior likely comprised large

sections of kerangas and kerapah (everwet) forests (Morley

2012)—the savanna populations in Java were cut off from

Indochina by perhumid forests, and some refugial rain-

forest populations in eastern and western equatorial Sun-

daland were able to come together.

In the following section, we describe how this rough

approximation of events and timing applies to the birds we

have studied. However, we add the caveat that the differ-

ential effects of glacial events, the likelihood of a mosaic of

habitats, the uncertainty of molecular dating, and the id-

iosyncratic biology of individual bird taxa make our sce-

nario preliminary and almost certainly not universal.

Periodic land and habitat bridges may have allowed some

bird species—but not others—to move from one island to

another. Subsequent glacial events may or may not have

allowed sufficient dispersal to homogenize gene pools.

Small founding sizes of populations, low gene flow, and

unpredictable selection (e.g., sexual selection) would also

have helped drive diversification.

Phylogeography of Sundaic birds

Bornean lowland taxa

Sabah, the Malaysian state in northeast Borneo (Fig. 7),

has an unusually large number of endemic lowland birds

relative to the rest of Borneo, despite continuous rainforest

across the entire island (Sheldon et al. 2001, 2009a; Mann

2008). To investigate the cause of the marked lowland

parapatry in birds, we have conducted molecular phylo-

geographic studies on about 20 passerine species (Moyle

et al. 2005, 2011; Sheldon et al. 2009b; Lim et al. 2010,

2011, 2014; Oliveros and Moyle 2010; Lim and Sheldon

2011; Gawin 2014; Chua et al. 2015). These studies sug-

gest that many of Borneo’s lowland populations were

subdivided early in the Pleistocene into rainforest refugia,

probably when the interior of the Sundaland was drier

(reviewed in Gawin et al. 2014). Subsequently, probably in

the mid-Pleistocene and certainly during more recent gla-

cial events when the interior of Sundaland was wetter

(Cannon et al. 2009), refugial rainforest populations came

together to form a contact zone near the Sabah border

(Fig. 7). This vicariance–dispersal dynamic is illustrated by

the shama species group comprising Copsychus mal-

abaricus and C. stricklandii (Mees 1986, 1996; Lim et al.

2010, 2011, 2014; Gawin 2014; Chua et al. 2015).

Copsychus malabaricus has a black crown. It occurs

from India and southern China to Java, and it inhabits most

of Borneo. C. stricklandii has a white crown and is divided

into two subspecies: C. s. stricklandii in NE Borneo and C.

s. barbouri on Maratua, a small oceanic island ap-

proximately 50 km off Borneo’s east coast (Fig. 7). C.

stricklandii differs from C. malabaricus by a mitochondrial

ND2 gene sequence distance of [3 %. C. stricklandii’s

subspecies differ from each other by an ND2 distance of

2 %. The presence of a genetically divergent white-

crowned population on Maratua Island suggests that in the

early Pleistocene C. stricklandii occurred on Borneo adja-

cent to Maratua, i.e., it provided the stock for the invasion of

Maratua. Hence in Fig. 7, we have located the refugial C.

stricklandii population (in yellow) on Borneo’s east coast

adjacent to Maratua. Rainforest in this area is supported by

palynological and other data (Gathorne-Hardy et al. 2002;

Morley and Morley 2011). Subsequently, C. stricklandii on

mainland Borneo moved or retreated to the region of Sabah.

Its movement would have been in response to a habitat

change because many other Bornean endemics also cur-

rently occupy Sabah. Meanwhile, C. malabaricus must

have inhabited an allopatric refuge in western Sundaland.

This refuge could have been in any of several perhumid

sites in mountains or coastal areas (a few possibilities are

indicated in Fig. 7). Based on genetic similarity among C.

malabaricus populations from Sumatra, the Malay Penin-

sula, and western Borneo, this species must have moved

freely in western Sundaland in the mid to late Pleistocene,

approximately 0.5–1.0 Ma (Lim et al. 2010, 2011). In due

course, probably quite recently, C. malabaricus moved

across Borneo to meet and hybridize (to a limited degree)

with C. stricklandii near the Sabah border (Davison 1999;

Collar 2004; Gawin 2014).

Fig. 7 Map of Sundaland showing the approximate current distribu-

tion of endemic northeastern Bornean bird populations (orange) and

locations of possible Pleistocene rainforest refuges (yellow), including

Maratua Island off eastern Borneo (circle). The phylogeography of

Copsychus, highlighted in the text, concerns C. stricklandii, currently

occurring in the orange region of Borneo and on Maratua Island, and

C. malabaricus, currently occurring throughout the rest of Sundaland

(except Palawan) and across southern mainland Asia

J Ornithol

123

Page 16: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

A similar dynamic occurred in Copsychus saularis, the

Oriental Magpie-Robin (Mees 1986, 1996; Sheldon et al.

2009b; Lim et al. 2010; Gawin 2014). Populations of this

species were also apparently subdivided in the early

Pleistocene. The main difference between magpie-robins

and shamas is that populations of magpie-robins from

western Borneo, Sumatra, and Java have more recently and

thoroughly intermixed, based on their genetic distances and

plumage morphology. Populations of eastern and western

Bornean magpie-robins have also experienced much

greater hybridization in their contact zone than have the

shamas (Gawin 2014), presumably because—as birds of

forest edge—they traversed Borneo more quickly than the

closed forest shamas. Analogous population interactions

also occurred in both Copsychus species on Java (Mees

1986, 1996; Gawin 2014).

To reiterate, the distribution and population genetics of

these Copsychus species strongly suggest vicariance in the

early Pleistocene, presumably by the inhospitable habitat.

More recently, these populations have come together be-

cause of continuous perhumid forest intervening in central

Sundaland (Cannon et al. 2009; de Bruyn et al. 2014:

Fig. 2).

Bornean montane taxa

The montane avifauna of Sundaland presents a more baf-

fling array of biogeographic patterns than the lowland

avifauna, making it difficult to reach general conclusions

about its evolutionary history. On Borneo, montane taxa

include widespread species (e.g., Turdus poliocephalus),

Himalayan taxa (Garrulax, Yuhina, Seicercus, Phyllosco-

pus, and Pycnonotus flavescens), ancient monotypic genera

(e.g., Haematortyx and Caloperdix), younger monotypic

genera (e.g., Chlamydochaera, Oculocincta, and Chlor-

ocharis), and many endemic representatives of Sundaic or

widespread SE Asian groups (e.g., Rhizothera dulitensis,

Arborophila hyperythra, Spilornis kinabaluensis, Collo-

calia dodgei, Harpactes whiteheadi, Megalaima eximia, M.

monticola, M. pulcherrima, Calyptomena hosii, Calyp-

tomena whiteheadi, Pitta arquata, etc.). Enigmatic para-

patric distributions also occur between montane taxa and

their lowland congeners. For example, the lowland spi-

derhunter Arachnothera modesta is replaced in the moun-

tains of western Borneo by its close congener, the endemic

A. everetti. In Sabah, however, A. modesta is absent and A.

everetti occupies both the lowlands and mountains (Shel-

don et al. 2001; Moyle et al. 2011). A similar pattern oc-

curs in the leafbirds Chloropsis cochinchinensis and C.

kinabaluensis, but with a twist (Wells et al. 2003; Sheldon

et al. 2009a; Moltesen et al. 2012). C. cochinchinensis

occurs in the lowlands of western Borneo and is replaced in

the western mountains by its close congener, the endemic

C. kinabaluensis. As with the lowland A. modesta, the

lowland C. cochinchinensis is absent in Sabah, but unlike

the ubiquitous Sabahan A. everetti, C. kinabaluensis re-

mains restricted to the mountains of Sabah and is not found

in the lowlands.

Despite its idiosyncrasies, the montane avifauna of Bor-

neo does exhibit a few predictable biogeographic patterns.

One such pattern is that Bornean montane species have

arisen primarily in allopatry, not in parapatry (i.e., not

through ecological speciation on an elevational gradient).

Although elevational parapatry of congeners is common on

Borneo (e.g., between the lowland swiftlet Collocalia es-

culenta and the montane endemic C. dodgei), the parapatric

congeners are not sister taxa. Sister taxa of Bornean montane

endemics have always been found to occur on other islands:

for example, Harpactes whiteheadi (Whitehead’s Trogon)

and H. ardens (Philippine Trogon), Arachnothera juliae

(Whitehead’s Spiderhunter) and A. clarae (Naked Faced

Spiderhunter) of the Philippines; A. everetti (Bornean Spi-

derhunter) and A. affinis (Streaky-breasted Spiderhunter) of

Java; Collocalia dodgei (Bornean Swiftlet) and C. lynchi

(Cave Swiftlet) of Java; Enicurus borneensis (Bornean

Forktail) and E. leschenaulti (White-crowned Forktail) of

Java; Chlamydochaera jefferyi (Fruithunter) and Cochoa

(cochoas) of Sumatra and Java; Chlorocharis emiliae

(Mountain Black-eye) and Zosterops montanus (Mountain

White-eye) of the Philippines, Wallacea, and other Greater

Sunda Islands (Klicka et al. 2005; Moyle et al. 2005, 2008,

2009, 2011; Hosner et al. 2010). When closely related con-

geners are elevationally parapatric, the lowland species ap-

pears to be a recent invader that has restricted the montane

species to higher elevation through competition (although

competition has not been directly demonstrated). This sce-

nario is highly reminiscent of the predictions of taxon cy-

cling (Ricklefs and Cox 1978).

The best studied Bornean montane endemic in terms of

phylogeography is Chlorocharis emiliae, the Mountain

Black-eye (Gawin et al. 2014). This species is a typical

white-eye (Zosteropidae), most closely related to Z. mon-

tanus (Moyle et al. 2009). It has a sky island distribution,

occurring on Borneo’s highest peaks in the central moun-

tain chain, but also on top of two outlying mountains in

western Borneo (Fig. 8). Molecular and morphological

comparisons of Chlorocharis populations indicate that it is

subdivided in the same way (including timing) as many

lowland taxa of Borneo, i.e., the Sabah population is dis-

tinct from that inhabiting the rest of the island (Ramji et al.

2012; Gawin et al. 2014). The pattern and timing of sub-

division suggest that the same Pleistocene forces that cre-

ated lowland subdivision and parapatry on Borneo—

vicariance during dry times and subsequent dispersal dur-

ing wetter times—also created montane subdivision and

parapatry on the island. Some other montane species that

J Ornithol

123

Highlight
Highlight
Highlight
Highlight
Highlight
Page 17: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

are similarly subdivided (based on their subspecific tax-

onomy) are: Garrulax treacheri (Chestnut-hooded Laugh-

ingthrush), Alophoixus ochraceus (Grey-cheeked Bulbul),

and Stachyris nigriceps (Grey-throated Babbler).

Given that orographic precipitation is thought to have

watered lowland rainforest associated with mountains

during dry periods of the Pleistocene, it makes sense that

the wet mountains themselves would have acted as refuges

for montane species. The difficulty then is determining

which mountains served as refuges for subdivided Bornean

montane bird populations. We know from pollen history

that the northeastern mountains (basically in Sabah) of-

fered refuge. The other(s) may have been in one or more

sites across the island (Fig. 7): the Pueh Range, Schwaner

Range (Gorog et al. 2004), or Meratus Range (Gathorne-

Hardy et al. 2002). The Meratus Range seems most likely

from an orographic rainfall standpoint (near the coast,

away from central Sundaland), but in terms of the current

phylogeographic structure of birds, the western or central

mountains of Borneo present a more attractive alternative.

Molecular comparisons of birds from the Meratus Range

should shed light on this issue.

Javan taxa

Because of its young age, Java is home to relatively recent

invaders from Sumatra, Borneo, and Wallacea. Most

interestingly for the reconstruction of Sundaic biogeography,

some of these recent invaders are more closely related to

species in Indochina than to those on other Sunda islands.

Disjunct Javan and Indochinese species include mainly dry-

habitat birds, such as: Dendrocopus analis (Freckle-breasted

Woodpecker), Psittacula alexandri (Red-breasted Parakeet),

Pericrocotus cinnamomeus (Small Minivet), Prinia polychroa

(Brown Prinia), Orthotomus sutorius (Common Tailorbird),

Timalia pileata (Chestnut-capped Babbler); however, some

rainforest species are disjunct as well, such as Tesia

cyaniventer (Grey-bellied Tesia). There are also some closely

related species pairs: Locustella montis (Javan Bush Warbler)

and L. mandelli (Russet Bush Warbler), among others. Only a

few studies have compared these disjunct populations using

molecular methods, e.g., Psittacula alexandri (Kundu et al.

2012), Pericrocotus cinnamomeus (Jønsson et al. 2010c),

Orthotomus sutorius (Sheldon et al. 2012), and Locustella

montis (Alstrom et al. 2011). In each case a close phylogeo-

graphic relationship is evident. In our study of tailorbirds, for

example, we found an uncorrected ND2 sequence divergence

of only 0.8–1.0 % between individuals of Orthotomus sutorius

of Java and Singapore, to which this tailorbird has recently

invaded from the north due to deforestation and drying of the

Malay Peninsula (Medway and Wells 1976). This genetic

distance suggests (but by no means proves) that the tailorbird’s

disjunction occurred in the mid-Pleistocene. As noted earlier,

Reddy (2008) discovered older Javan–Indochinese connec-

tions in shrike-babblers (early Pleistocene and Pliocene).

The ancestors of the disjunct taxa most likely reached

Java across the interior of Sundaland. Rainforest birds, like

Tesia, would also have invaded Sumatra and Borneo and

subsequently been extirpated (perhaps through competi-

tion) on those islands. Dry habitat birds would have

reached Java in the same manner as the Javan megafauna,

through dry interior parts of the Sunda shelf, starting per-

haps in the Pliocene. Judging from the taxic variety (and

presumed genetic variation) between pairs of dryland dis-

juncts, invasion may have occurred in waves, with those

disjunct at the population level arriving most recently. As

with the megafauna, Java’s dry-habitat birds would have

been cut-off from their sister taxa in Indochina during in-

terglacials and during low sea-level events when Sunda-

land’s interior forest was perhumid (Cannon et al. 2009;

Morley 2012). Further molecular comparisons between

Javan and Indochinese populations should yield a rich crop

of biogeographic discovery, especially in dating invasions

and establishing the timing of habitat occurrence.

Conclusions

A major conclusion of this review is that Borneo played the

preeminent role in the evolution of rainforest birds in

Fig. 8 The sky island distribution of Mountain Black-eye (Chlor-

ocharis emiliae) on Borneo. Triangles Known populations, white

circles populations in the two main clades, which are separated by a

mitochondrial ND2 sequence difference of 2.5 %. The northernmost

clade, in Sabah, likely represents the influence of an early Pleistocene

refuge in the vicinity of Mt. Kinabalu. The southwestern clade’s

Pleistocene refuge is unknown, but could be in any site subject to

orographic rainfall during dry periods

J Ornithol

123

Page 18: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Sundaland (de Bruyn et al. 2014). Borneo’s evolutionary

power stems from the long-term existence of its eastern

mountains and their adjacent lowlands, which served as

refuges during the drier, cooler Oligocene, Pliocene, and

Pleistocene and helped foment taxa from the Miocene

through Pleistocene. The island’s refuges probably pre-

served several relicts, including the montane Haematoryx

sanguiniceps (Crimson-headed Partridge) and Caloperdix

oculeus (Ferruginous Partridge), and possibly the lowland

Rollulus roulroul (Crested Partridge) and Calorhamphus

(brown barbets). Bornean mountains probably also were

the center of Miocene bird evolution in Sundaland. In the

Miocene, lowland rainforest extended widely in southern

Asia, but Borneo’s mountains were isolated from those at

higher latitude throughout the epoch (Fig. 3). In contrast to

Borneo, Sumatra or Java did not have substantial land area

until 10 Ma or 5 Ma, respectively, when the wet warmth of

the Miocene was waning. The role of eastern Java, arising

after 5 Ma, would have been very small in terms of the

proliferation of major Sundaic groups, but eastern Java

would have been important in preserving disjunct In-

dochinese taxa.

The Pleistocene brought a different dynamic to Sunda-

land. Starting early in the Pleistocene and continuing

probably until at least 800 ka, glacial events caused enough

habitat drying in central Sundaland to subdivide rainforest

into refugia and to allow dry-habitat birds and mammals to

reach Java from Indochina. Subsequently, glacial events

featured enough perhumid habitat to connect previously

vicariated rainforest populations, creating the parapatry we

see in both the lowlands (e.g., on Borneo, between Sabah

and elsewhere) and mountains (e.g., on Borneo, in Collo-

calia, Enicurus, Chloropsis, Arachnothera, etc.). The dy-

namics between a drier and wetter Sundaic interior was

probably not simply one period of separation and one pe-

riod of connection, but rather a complex interplay of iso-

lation on islands (including islands of habitat) and

colonization events via land or habitat bridges. Also at play

in diversification would have been the influence of

relatively small population sizes, low gene flow, and be-

havioral idiosyncrasies of each species.

Future research needs

Directions of future research are clear. At the population

level, to reconstruct the evolution of Sundaic birds effec-

tively we need extensive sampling from areas for which

there are almost no modern bird specimens: Kalimantan in

southern Borneo, Java, Sumatra, the Malay Peninsula, and

Thailand. For population studies, we also need to move

from Sanger sequencing of mitochondrial DNA and slowly

evolving nuclear genes to next-generation sequencing

methods. The latter will provide more independent nuclear

loci for comparison and, consequently, more precise esti-

mates of phylogeographic parameters, such as population

size, gene flow, and divergence time. For phylogenetic

studies, we need more extensive taxonomic sampling,

which again requires more and better collections. Finally,

we need more information on paleo-habitats that occurred

during early Pleistocene glacial events. Such data will most

likely be provided by increased and improved modeling

methods and continued work on fossil plants and pollen.

Acknowledgments We especially thank Franz Barlein, Erik

Matthysen, David Winkler, and the International Ornithological

Congress for inviting FHS to present a plenary lecture and write this

paper. We also thank Robert Hall for providing his Cenozoic maps

(Fig. 3) and for giving permission to use them, and JC Gonzalez and

Will Stein for sending material from their PhD theses. We are ex-

tremely grateful for input from Ed Braun, Clare Brown, Ryan Burner,

Vivien Chua, Geoff Davison, Dency Gawin, Jake Esselstyn, Kevin

Johnson, Rebecca Kimball, John Mittermeier, Quentin Phillipps, Rick

Prum, Mustafa Abdul Rahman, Mohamad Fizl Sidq Ramji, Roselyn

Remsen, Van Remsen, Frank Rheindt, Subir Shakya, Mike Sorenson,

Katie Stryjewski, and David Wells. This project has been supported

by the Malaysian Chief Minister’s Department and numerous gov-

ernment departments in Sabah and Sarawak. Funding was provided

by NSF DEB-0228688, NSF DEB-1241059, Coypu Foundation of

Louisiana, National Geographic Society, Louisiana State University,

American Museum of Natural History, University of Kansas, Sabah

Parks, Sabah Museum, and the Universiti Malaysia Sarawak.

References

Aggerbeck M, Fjeldsa J, Christidis L, Fabre PH, Jønsson KA (2014)

Resolving deep lineage divergences in core corvoid passerine

birds supports a proto-Papuan island origin. Mol Phylogenet

Evol 70:272–285

Ahlquist JE, Sheldon FH, Sibley CG (1984) The relationships of the

Bornean Bristlehead (Pityriasis gymnocephala) and the Black-

collared Thrush (Chlamydochaera jefferyi). J Ornithol

125:129–140

Aitchison JC, Ali JR, Davis AM (2007) When and where did India

and Asia collide? J Geophys Res 112:B05423

Allen MB, Armstrong HA (2008) Arabia-Eurasia collision and the

forcing of mid-Cenozoic global cooling. Palaeogeogr Palaeocli-

matol Palaeoecol 265:52–58

Alstrom P, Fregin S, Norman JA, Ericson PG, Christidis L, Olsson U

(2011) Multilocus analysis of a taxonomically densely sampled

dataset reveal extensive non-monophyly in the avian family

Locustellidae. Mol Phylogenet Evol 58:513–526

Antoine P-O, Welcomme J-L, Marivaux L, Baloch I, Benammi M,

Tassy P (2003) First record of Paleogene Elephantoidea

(Mammalia, Proboscidea) from the Bugti Hills of Pakistan.

J Vertebr Paleontol 23:977–980

Augustin L, Barbante C, Barnes PRF, Barnola JM, Bigler M,

Castellano E, Cattani O, Chappellaz J, DahlJensen D, Delmonte

B, Dreyfus G, Durand G, Falourd S, Fischer H, Fluckiger J,

Hansson ME, Huybrechts P, Jugie R, Johnsen SJ, Jouzel J,

Kaufmann P, Kipfstuhl J, Lambert F, Lipenkov VY, Littot GVC,

Longinelli A, Lorrain R, Maggi V, Masson-Delmotte V, Miller

H, Mulvaney R, Oerlemans J, Oerter H, Orombelli G, Parrenin F,

J Ornithol

123

Page 19: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Peel DA, Petit JR, Raynaud D, Ritz C, Ruth U, Schwander J,

Siegenthaler U, Souchez R, Stauffer B, Steffensen JP, Stenni B,

Stocker TF, Tabacco IE, Udisti R, van de Wal RSW, van den

Broeke M, Weiss J, Wilhelms F, Winther JG, Wolff EW,

Zucchelli M, Members EC (2004) Eight glacial cycles from an

Antarctic ice core. Nature 429:623–628

Banfer G, Moog U, Fiala B, Mohamed M, Weising K, Blattner FR

(2006) A chloroplast genealogy of myrmecophytic Macaranga

species (Euphorbiaceae) in Southeast Asia reveals hybridization,

vicariance and long-distance dispersals. Mol Ecol 15:4409–4424

Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004)

Phylogeny and diversification of the largest avian radiation. Proc

Natl Acad Sci USA 101:11040–11045

Barry JC, Johnson NM, Raza SM, Jacobs LL (1985) Neogene

mammalian faunal change in southern Asia: correlations with

climatic, tectonic, and eustatic events. Geology 13:637–640

Barry JC, Morgan ME, Winkler AJ, Flynn LJ, Lindsay EH, Jacobs

LL, Pilbeam D (1991) Faunal interchange and Miocene terres-

trial vertebrates of southern Asia. Paleobiology 17:231–245

Berggren WA, Prothero DR (1992) Eocene-Oligocene climatic and

biotic evolution: an overview. In: Berggren WA, Prothero DR

(eds) Eocene–Oligocene climatic and biotic evolution. Princeton

University Press, Princeton, pp 1–28

Bettis EA, Milius AK, Carpenter SJ, Larick R, Zaim Y, Rizal Y,

Ciochon RL, Tassier-Surine SA, Murray D, Bronto S (2009)

Way out of Africa: early Pleistocene paleoenvironments inhab-

ited by Homo erectus in Sangiran, Java. J Hum Evol 56:11–24

Bintanja R, van de Wal SW, Oelemans J (2005) Modelled

atmospheric temperatures and global sea levels of the past

million years. Nature 437:125–128

Bird MI, Taylor D, Hunt C (2005) Palaeoenvironments of insular

Southeast Asia during the last glacial period: a savanna corridor

in Sundaland? Quat Sci Rev 24:2228–2242

Blackburn DC, Bickford DP, Diesmos AC, Iskandar DT, Brown RM

(2010) An ancient origin for the enigmatic flat-headed frogs

(Bombinatoridae: Barbourula) from the islands of Southeast

Asia. PLoS One 5:e12090

Brandon-Jones D (1996) The Asian Colobinae (Mammalia: Cer-

copithecidae) as indicators of quaternary climatic change. Biol J

Linn Soc 59:327–350

Brandon-Jones D (1998) Pre-glacial Bornean primate impoverish-

ment and Wallace’s line. In: Hall R, Holloway JD (eds)

Biogeography and geological evolution of SE Asia. Backhuys,

Leiden, pp 393–403

Brown JW, Van Tuinen M (2011) Evolving perceptions on the

antiquity of the modern avian tree. Living Dinosaurs: the

evolutionary history of modern birds. Wiley, New York,

pp 306–324

Brown JW, Rest JS, Garcıa-Moreno J, Sorenson MD, Mindell D

(2008) Strong mitochondrial DNA support for a Cretaceous

origin of modern avian lineages. BMC Biol 6:6. doi:10.1186/

1741-7007-6-6

Cannon CH, Morley RJ, Bush ABG (2009) The current refugial

rainforests of Sundaland are unrepresentative of their biogeo-

graphic past and highly vulnerable to disturbance. Proc Natl

Acad Sci USA 106:11188–11193

Choi DL-T (1996) Geology of Kinabalu. In: Wong, KM, A Phillipps

(eds) Kinabalu, summit of Borneo. Sabah Society and Sabah

Parks, Kota Kinabalu, Sabah, pp 19–29

Chua VL, Phillipps Q, Lim HC, Taylor SS, Gawin DF, Rahman MA,

Moyle RG, Sheldon FH (2015) Phylogeography of three

endemic birds of Maratua Island, a potential archive of Bornean

biogeography. Raffles Bull Zool (in press)

Cibois A, Kalyakin MV, Han LX, Pasquet E (2002) Molecular

phylogenetics of babblers (Timaliidae): Re-evaluation of the

genera Yuhina and Stachyris. J Avian Biol 33:380–390

Cibois A, Thibault J-C, Bonillo C, Filardi CE, Watling D, Pasquet E

(2014) Phylogeny and biogeography of the fruit doves (Aves:

Columbidae). Mol Phylogenet Evol 70:442–453

Clarke JA, Ksepka DT, Smith NA, Norell MA (2009) Combined

phylogenetic analysis of a new North American fossil species

confirms widespread Eocene distribution for stem rollers (Aves,

Coracii). Zool J Linn Soc 157:586–611

Collar NJ (2004) Species limits in some Indonesian thrushes. Forktail

20:71–87

Cottam M, Hall R, Sperber C, Armstrong R (2010) Pulsed emplace-

ment of the Mount Kinabalu granite, northern Borneo. J Geol

Soc 167:49–60

Cracraft J (2014) Avian higher-level relationships and classification:

Passeriformes. In: Dickinson, EC, L Christidis (eds) The Howard

and Moore complete checklist of the birds of the world, 4th edn,

vol 2. Aves Press, Eastbourne, U.K., pp 17–45

Cranbrook E (2000) Northern Borneo environments of the past 40,000

years. Sarawak Mus J 55:61–109

Cranbrook E (2010) Late Quaternary turnover of mammals in Borneo:

the zooarchaeological record. Biodivers Conserv 19:373–391

Crowe TM, Bowie RCK, Bloomer P, Mandiwana TG, Hedderson

TAJ, Randi E, Wakeling J (2006) Phylogenetics, biogeography

and classification of, and character evolution in, gamebirds

(Aves: Galliformes): effects of character exclusion, data parti-

tioning and missing data. Cladistics 22:1–38

Darlington PJ (1957) Zoogeography: the geographical distribution of

animals. Wiley, New York

Davison GWH (1999) Notes on the taxonomy of some Bornean birds.

Sarawak Mus J 54:289–299

de Bruyn M, Stelbrink B, Morley RJ, Hall R, Carvalho GR, Cannon

CH, van den Bergh G, Meijaard E, Metcalfe I, Boitani L,

Maiorano L, Shoup R, von Rintelen K (2014) Borneo and

Indochina are major evolutionary hotspots for Southeast Asian

biodiversity. Syst Biol 63:879–901

deMenocal PB (2004) African climate change and faunal evolution

during the Pliocene–Pleistocene. Earth Planet Sci Lett 220:3–24

den Tex RJ, Leonard JA (2013) A molecular phylogeny of Asian

barbets: Speciation and extinction in the tropics. Mol Phylogenet

Evol 68:1–13

Dinesen L, Lehmberg T, Svendsen TO, Hansen LA, Fjeldsa J (1994)

A new genus and species of perdicine bird (Phasianidae,

Perdicini) from Tanzania; a relict form with Indo-Malayan

affinities. Ibis 136:3–11

Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary

analysis by sampling trees. BMC Evol Biol 7:214

Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed

phylogenetics and dating with confidence. PLoS Biol 4:699–710

Durkee EF (1993) Oil, geology and changing concepts in the

Southwest Philippines (Palawan and the Sulu Sea). Bull Geol

Soc Malays 33:241–262

Ericson PG (2012) Evolution of terrestrial birds in three continents:

biogeography and parallel radiations. J Biogeogr 39:813–824

Ericson PG, Irestedt M, Johansson US (2003) Evolution, biogeogra-

phy, and patterns of diversification in passerine birds. J Avian

Biol 34:3–15

Ericson PGP, Klopstein S, Irestedt M, Nguyen JMT, Nylander JAA

(2014) Dating the divergence of major lineages of Passeriformes.

BMC Evol Biol 14(8):1–15

Esselstyn JA, Oliveros CH, Moyle RG, Peterson AT, McGuire JA,

Brown RM (2010) Integrating phylogenetic and taxonomic

evidence illuminates complex biogeographic patterns along Hux-

ley’s modification of Wallace’s Line. J Biogeogr 37:2054–2066

Fabre PH, Irestedt M, Fjeldsa J, Bristol R, Groombridge JJ, Irham M,

Jønsson KA (2012) Dynamic colonization exchanges between

continents and islands drive diversification in paradise-flycatch-

ers (Terpsiphone, Monarchidae). J Biogeogr 39:1900–1918

J Ornithol

123

Page 20: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Feduccia A (1999) The origin and evolution of birds, 2nd edn. Yale

University Press, New Haven

Feduccia A (2003) ‘Big bang’for tertiary birds? Trends Ecol Evol

18:172–176

Fernando P, Vidya TNC, Payne J, Stuewe M, Davison G, Alfred RJ,

Andau P, Bosi E, Kilbourn A, Melnick DJ (2003) DNA analysis

indicates that Asian elephants are native to Borneo and are

therefore a high priority for conservation. PloS Biol 1:110–115

Fjeldsa J (2013) The global diversification of songbirds (Oscines) and

the build-up of the Sino-Himalayan diversity hotspot. Chin Birds

4:132–143

Fjeldsa J, Bowie RCK (2008) New perspectives on the origin and

diversification of Africa’s forest avifauna. Afr J Ecol

46:235–247

Fuchs J, Fjeldsa J, Bowie RCK, Voelker G, Pasquet E (2006a) The

African warbler genus Hyliota as a lost lineage in the Oscine

songbird tree: molecular support for an African origin of the

Passerida. Mol Phylogenet Evol 39:186–197

Fuchs J, Ohlson JI, Ericson PGP, Pasquet E (2006b) Molecular

phylogeny and biogeographic history of the piculets (Piciformes:

Picumninae). J Avian Biol 37:487–496

Gardner JL, Trueman JW, Ebert D, Joseph L, Magrath RD (2010)

Phylogeny and evolution of the Meliphagoidea, the largest radiation

of Australasian songbirds. Mol Phylogenet Evol 55:1087–1102

Gathorne-Hardy FJ, Syaukani Davies RG, Eggleton P, Jones DT

(2002) Quaternary rainforest refugia in south-east Asia: using

termites (Isoptera) as indicators. Biol J Linn Soc 75:453–466

Gawin DF (2014) Population genetic and hybridization studies of

three Bornean birds species: Mountain Black-eye (Chlorocharis

emiliae), White-rumped Shama (Copsychus malabaricus), and

Oriental Magpie-Robin (Copsychus saularis). In: PhD thesis,

Louisiana State University, Baton Rouge

Gawin DF, Rahman MA, Ramji MFS, Smith BT, Lim HC, Moyle

RG, Sheldon FH (2014) Patterns of avian diversification in

Borneo: the case of the endemic Mountain Black-eye (Chlor-

ocharis emiliae). Auk Adv Ornithol 131:86–99

Gill F, Donsker D (2014) IOC world bird list (v 4.4). Available at:

http://www.worldbirdnames.org/

Gonzalez J-CT (2012) Origin and diversification of hornbills

(Bucerotidae). Oxford University, Oxford

Gonzalez J-CT, Sheldon BC, Collar NJ, Tobias JA (2013) A

comprehensive molecular phylogeny for the hornbills (Aves:

Bucerotidae). Mol Phylogenet Evol 67:468–483

Gorog AJ, Sinaga MH, Engstrom MD (2004) Vicariance or dispersal?

Historical biogeography of three Sunda shelf murine rodents

(Maxomys surifer, Leopoldamys sabanus and Maxomys white-

headi). Biol J Linn Soc 81:91–109

Hall R (1998) The plate tectonics of Cenozoic SE Asia and the

distribution of land and sea. In: Hall R, Holloway JD (eds)

Biogeography and geological evolution of SE Asia. Backhuys,

Leiden, pp 99–131

Hall R (2002) Cenozoic geological and plate tectonic evolution of SE

Asia and the SW Pacific: computer-based reconstructions and

animations. J Asian Earth Sci 20:353–434

Hall R (2009) Southeast Asia’s changing palaeogeography. Blumea

Biodivers Evol Biogeogr Plants 54:1–3

Hall R (2012) Sundaland and Wallacea: geology, plate tectonics and

palaeogeography. In: Gower DJ, Johnson KG, Richardson JE,

Rosen BR, Ruber L, Williams ST (eds) Biotic evolution and

environmental change in Southeast Asia. Cambridge University

Press, Cambridge, pp 32–78

Hall R (2013) The palaeogeography of Sundaland and Wallacea since

the Late Jurassic. J Limnol 72(s2):1–17

Hall R, Nichols G (2002) Cenozoic sedimentation and tectonis in

Borneo: climatic influences on orogenesis. Geol Soc Lond Spec

Publ 191:5–22

Handiani D, Paul A, Prange M, Merkel U, Dupont L, Zhang X (2013)

Tropical vegetation response to Heinrich Event 1 as simulated

with the UVic ESCM and CCSM3. Clim Past 9:1683–1696

Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the

Sunda Shelf: a late-glacial sea-level record. Science 288:1033–1035

Harzhauser M, Kroh A, Mandic O, Piller WE, Gohlich U, Reuter M,

Berning B (2007) Biogeographic responses to geodynamics: a

key study all around the Oligo-Miocene Tethyan Seaway. Zool

Anz 246:241–256

Heaney LR (1986) Biogeography of mammals in SE Asia: estimates

of rates of colonization, extinction and speciation. Biol J Linn

Soc 28:127–165

Heaney LR (1991) A synopsis of climatic and vegetational change in

Southeast Asia. Clim Change 19:53–61

Hirai H, Wijayanto H, Tanaka H, Mootnick AR, Hayano A,

Perwitasari-Farajallah D, Iskandriati D, Sajuthi D (2005) A

whole-arm translocation (WAT8/9) separating Sumatran and

Bornean agile gibbons, and its evolutionary features. Chromo-

some Res 13:123–133

Ho SY, Phillips MJ (2009) Accounting for calibration uncertainty in

phylogenetic estimation of evolutionary divergence times. Syst

Biol 58:367–380

Holt BG, Lessard J-P, Borregaard MK, Fritz SA, Araujo MB,

Dimitrov D, Fabre P-H, Graham CH, Graves GR, Jønsson KA

(2013) An update of Wallace’s zoogeographic regions of the

world. Science 339:74–78

Hosner PA, Sheldon FH, Lim HC, Moyle RG (2010) Phylogeny and

biogeography of the Asian trogons (Aves: Trogoniformes)

inferred from nuclear and mitochondrial DNA sequences. Mol

Phylogenet Evol 57:1219–1225

Hu J, Pa Peng, Fang D, Jia G, Jian Z, Wang P (2003) No aridity in

Sunda Land during the Last Glaciation: evidence from

molecular-isotopic stratigraphy of long-chain n-alkanes. Palaeo-

geogr Palaeoclimatol Palaeoecol 201:269–281

Hughes JB, Round PD, Woodruff DS (2003) The Indochinese-

Sundaic faunal transition at the Isthmus of Kra: an analysis of

resident forest bird species distributions. J Biogeogr 30:569–580

Irestedt M, Johansson US, Parsons TJ, Ericson PGP (2001) Phylogeny

of major lineages of suboscines (Passeriformes) analysed by

nuclear DNA sequence data. J Avian Biol 32:15–25

Iwanaga H, Teshima KM, Khatab IA, Inomata N, Finkeldey R,

Siregar IZ, Siregar UJ, Szmidt AE (2012) Population structure

and demographic history of a tropical lowland rainforest tree

species Shorea parvifolia (Dipterocarpaceae) from Southeastern

Asia. Ecol Evol 2:1663–1675

James HF (2005) Paleogene fossils and the radiation of modern birds.

Auk 122:1049–1054

Johansson US, Erickson C (2004) A re-evaluation of basal phyloge-

netic relationships within trogons (Aves: Trogonidae) based on

nuclear DNA sequences. J Zool Syst Evol Res 43:166–173

Johansson US, Alstrom P, Olsson U, Ericson PGR, Sundberg P, Price

TD (2007) Build-up of the Himalayan avifauna through immi-

gration: a biogeographical analysis of the Phylloscopus and

Seicercus warblers. Evolution 61:324–333

Jønsson KA, Fjeldsa J (2006) Determining biogeographical patterns

of dispersal and diversification in oscine passerine birds in

Australia, Southeast Asia and Africa. J Biogeogr 33:1155–1165

Jønsson KA, Fjeldsa J, Ericson PGP, Irestedt M (2007) Systematic

placement of an enigmatic Southeast Asian taxon Eupetes

macrocerus and implications for the biogeography of a main

songbird radiation, the Passerida. Biol Lett 3:323–326

Jønsson KA, Irestedt M, Fuchs J, Ericson PGP, Christidis L, Bowie

RCK, Norman JA, Pasquet E, Fjeldsa J (2008) Explosive avian

radiations and multi-directional dispersal across Wallacea:

evidence from the Campephagidae and other Crown Corvida

(Aves). Mol Phylogenet Evol 47:221–236

J Ornithol

123

Page 21: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Jønsson KA, Bowie RCK, Moyle RG, Christidis L, Norman JA, Benz

BW, Fjeldsa J (2010a) Historical biogeography of an Indo-

Pacific passerine bird family (Pachycephalidae): different

colonization patterns in the Indonesian and Melanesian

archipelagos. J Biogeogr 37:245–257

Jønsson KA, Bowie RCK, Moyle RG, Irestedt M, Christidis L,

Norman JA, Fjeldsa J (2010b) Phylogeny and biogeography of

Oriolidae (Aves: Passeriformes). Ecography 33:232–241

Jønsson KA, Irestedt M, Ericson PGP, Fjeldsa J (2010c) A molecular

phylogeny of minivets (Passeriformes: Campephagidae: Peri-

crocotus): implications for biogeography and convergent plu-

mage evolution. Zool Scr 39:1–8

Jønsson KA, Fabre PH, Ricklefs RE, Fjeldsa J (2011) Major global

radiation of corvoid birds originated in the proto-Papuan

archipelago. Proc Natl Acad Sci USA 108:2328–2333

Jønsson KA, Irestedt M, Christidis L, Clegg SM, Holt BG, Fjeldsa J

(2014) Evidence of taxon cycles in an Indo-Pacific passerine bird

radiation (Aves: Pachycephala). Proc R Soc B Biol Sci

281:20131727

Kashiwaya K, Ochiai S, Sakai H, Kawai T (2001) Orbit-related long-

term climate cycles revealed in a 12-Myr continental record from

Lake Baikal. Nature 410:71–74

Kershaw A, Van Der Kaars S, Flenley J (2007) The Quaternary

history of far eastern rainforests. Tropical rainforest responses to

climatic change. Springer-Praxis, Chichester, pp 77–115

Kimball RT, Braun EL, Ligon JD, Lucchini V, Randi E (2001) A

molecular phylogeny of the peacock-pheasants (Galliformes:

Polyplectron spp.) indicates loss and reduction of ornamental

traits and display behaviours. Biol J Linn Soc 73:187–198

Klicka J, Voelker G, Spellman GM (2005) A molecular phylogenetic

analysis of the ‘‘true thrushes’’. Mol Phylogenet Evol

34:486–500

Koufos GD, Kostopoulos DS, Vlachou TD (2005) Neogene/Quater-

nary mammalian migrations in Eastern Mediterranean. Belg J

Zool 135:181–190

Ksepka DT, Clarke JA (2009) Affinities of Palaeospiza bella and the

phylogeny and biogeography of mousbirds (Coliiformes). Auk

126:245–259

Kumar P, Yuan X, Kumar MR, Kind R, Li X, Chadha R (2007) The

rapid drift of the Indian tectonic plate. Nature 449:894–897

Kundu S, Jones CG, Prys-Jones RP, Groombridge JJ (2012) The

evolution of the Indian Ocean parrots (Psittaciformes): extinc-

tion, adaptive radiation and eustacy. Mol Phylogenet Evol

62:296–305

Li Z, Powell CM (2001) An outline of the palaeogeographic evolution

of the Australasian region since the beginning of the Neopro-

terozoic. Earth Sci Rev 53:237–277

Li XW, Walker D (1986) The plant geography of Yunnan Province,

southwest China. J Biogeogr 13:367–397

Li J-T, Li Y, Klaus S, Rao D-Q, Hillis DM, Zhang Y-P (2013)

Diversification of rhacophorid frogs provides evidence for

accelerated faunal exchange between India and Eurasia during

the Oligocene. Proc Natl Acad Sci USA 110:3441–3446

Lim HC, Sheldon FH (2011) Multilocus analysis of the evolutionary

dynamics of rainforest bird populations in Southeast Asia. Mol

Ecol 20:3414–3438

Lim HC, Zou F, Taylor SS, Marks BD, Moyle RG, Voelker G,

Sheldon FH (2010) Phylogeny of magpie-Robins and shamas

(Aves: Turdidae: Copsychus and Trichixos): implications for

island biogeography in Southeast Asia. J Biogeogr

37:1894–1906

Lim HC, Rahman MA, Lim SLH, Moyle RG, Sheldon FH (2011)

Revisiting Wallace’s haunt: coalescent simulations and com-

parative niche modeling reveal historical mechanisms that

promoted avian population divergence in the Malay Archipela-

go. Evolution 65:321–334

Lim HC, Chua VL, Benham PM, Oliveros CH, Rahman MA, Moyle

RG, Sheldon FH (2014) Divergence history of the Rufous-tailed

Tailorbird (Orthotomus sericeus) of Sundaland: implications for

the biogeography of Palawan and the taxonomy of island species

in general. Auk 131:629–642

Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hal R, Ng PKL,

Shih HT, Carvalho GR, von Rintelen T (2011) Biogeography of

the Indo-Australian Archipelago. Annu Rev Ecol Evol Syst

42:205–226

Louys J, Meijaard E (2010) Palaeoecology of Southeast Asian

megafauna-bearing sites from the Pleistocene and a review of

environmental changes in the region. J Biogeogr 37:1432–1449

MacKinnon JR, Phillipps K (1999) A field guide to the birds of Borneo,

Sumatra, Java and Bali. Oxford University Press, Oxford

Mann CF (2008) The birds of Borneo, an annotated checklist. British

Ornithologists’ Union and British Ornithologists’ Club,

Peterborough

Mayr E (1944) Wallace’s line in light of recent zoogeographic

studies. Q Rev Biol 19:1–14

Mayr G (2005) The Paleogene fossil record of birds in Europe. Biol

Rev 80:515–542

Mayr G (2013) The age of the crown group of passerine birds and its

evolutionary significance–molecular calibrations versus the

fossil record. Syst Biodivers 11:7–13

Mayr G (2014) The origins of crown group birds: molecules and

fossils. Palaeontology 57:231–242

Medway L (1972) The Quaternary mammals of Malesia: a review. In:

Ashton P, Ashton M (eds) Transactions of the second Aberdeen-

Hull symposium on Malesian ecology. University of Hull, Hull,

pp 63–83

Medway L, Wells DR (1976) The birds of the Malay Peninsula, vol 5.

H.F. & G. Witherby, London

Mees GF (1986) A list of birds recorded from Bangka Island,

Indonesia. Zool Verh Leiden 232:1–176

Mees GF (1996) Geographical variation in birds of Java. Publ Nuttall

Ornithol Club 26:1–119

Meijaard E (2003) Mammals of south-east Asian islands and their

Late Pleistocene environments. J Biogeogr 30:1245–1257

Meijaard E, Groves C (2004) The biogeographical evolution and

phylogeny of the genus Presbytis. Primate Rep 68:71–90

Meijaard E, van der Zon APM (2003) Mammals of south-east Asian

islands and their Late Pleistocene environments. J Biogeogr

30:1245–1257

Meijer HJM (2014) The avian fossil record in Insular Southeast Asia

and its implications for avian biogeography and palaeoecology.

PeerJ 2:e295

Meulenkamp JE, Sissingh W (2003) Tertiary palaeogeography and

tectonostratigraphic evolution of the Northern and Southern Peri-

Tethys platforms and the intermediate domains of the African-

Eurasian convergent plate boundary zone. Palaeogeogr Palaeo-

climatol Palaeoecol 196:209–228

Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM,

Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA,

McCain CM, McCune AR, McDade LA, McPeek MA, Near TJ,

Price TD, Ricklefs RE, Roy K, Sax DF, Schluter D, Sobel JM,

Turelli M (2007) Evolution and the latitudinal diversity gradient:

speciation, extinction and biogeography. Ecol Lett 10:315–331

Molengraaff GAF (1921) Modern deep sea research in the East Indian

archipelago. Geogr J 57:95–121

Moltesen M, Irestedt M, Fjeldsa J, Ericson PG, Jønsson KA (2012)

Molecular phylogeny of Chloropseidae and Irenidae–Cryptic

species and biogeography. Mol Phylogenet Evol 65:903–914

Morley RJ (1998a) Palynological evidence for Tertiary plant disper-

sals in the SE Asian region in relation to plate tectonic and

climate. In: Hall R, Holloway JD (eds) Biogeography and

geological evolution of SE Asia. Backhuys, Leiden, pp 211–234

J Ornithol

123

Highlight
Highlight
Page 22: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Morley RJ (1998b) Tertiary history of the Malesian flora: a

palynological perspective. In: Taxonomy: the cornerstone of

biodiversity: Proc 4th Int Flora Malesiana Symp. Kuala Lumpur,

pp 197–210

Morley RJ (2000) Origin and evolution of tropical rain forests. Wiley,

New York

Morley RJ (2003) Interplate dispersal paths for megathermal

angiosperms. Perspect Plant Ecol Evol Syst 6:5–20

Morley RJ (2011) Cretaceous and Tertiary climate change and the

past distribution of megathermal rainforests. In: Bush M, JR

Flenley (eds) Tropical rainforest responses to climatic change.

Springer SBM, Berlin Heidelberg New York, pp 1–34

Morley RJ (2012) A review of the Cenozoic palaeoclimate history of

Southeast Asia. In: Gower DJ, Johnson KG, Richardson JE,

Rosen BR, Ruber L, Williams ST (eds) Biotic evolution and

environmental change in Southeast Asia. Cambridge University

Press, Cambridge, pp 79–114

Morley RJ, Morley HP (2011) Neogene climate history of the

Makassar Straits. In: The Southeast Asian Gateway: history and

tectonics of Australia-Asia collision. Geological Society of

London, London, pp 319–32

Morley RJ, Morley HP (2013) Mid Cenozoic freshwater wetlands of

the Sunda region. J Limnol 72(s2):18–35

Moss SJ, Wilson MEJ (1998) Biogeographic implications of the

Tertiary palaeogeographic evolution of Sulawesi and Borneo. In:

Hall R, Holloway JD (eds) Biogeography and geological

evolution of SE Asia. Backhuys, Leiden, pp 133–155

Moyle RG (2002) Molecular systematics of barbets and trogons:

pantropical biogeography, African speciation, and issues in

phylogenetic inference. In: PhD thesis, Louisiana State Univer-

sity, Baton Rouge

Moyle RG (2004) Phylogenetics of barbets (Aves: Piciformes) based

on nuclear and mitochondrial DNA sequence data. Mol Phylo-

genet Evol 30:187–200

Moyle RG (2005) Phylogeny and biogeographical history of Trogo-

niformes, a pantropical bird order. Biol J Linn Soc 84:725–738

Moyle RG, Schilthuizen M, Rahman MA, Sheldon FH (2005)

Molecular phylogenetic analysis of the white-crowned forktail

Enicurus leschenaulti in Borneo. J Avian Biol 36:96–101

Moyle RG, Chesser RT, Prum RO, Schikler P, Cracraft J (2006a)

Phylogeny and evolutionary history of Old World suboscine

birds (Aves : Eurylaimides). Am Mus Novit 3544:1–22

Moyle RG, Cracraft J, Lakim M, Nais J, Sheldon FH (2006b)

Reconsideration of the phylogenetic relationships of the enig-

matic Bornean Bristlehead (Pityriasis gymnocephala). Mol

Phylogenet Evol 39:893–898

Moyle RG, Hosner PA, Nais J, Lakim M, Sheldon FH (2008)

Taxonomic status of the Kinabalu ‘linchi’ swiftlet. Bull Br

Ornithol Club 128:94–100

Moyle RG, Filardi CE, Smith CE, Diamond J (2009) Explosive

Pleistocene diversification and hemispheric expansion of a

‘‘great speciator’’. Proc Natl Acad Sci USA 106:1863–1868

Moyle RG, Taylor SS, Oliveros CH, Lim HC, Haines CL, Rahman

MA, Sheldon FH (2011) Diversification of an insular Southeast

Asian genus: Phylogenetic relationships of the spiderhunters

(Aves: Nectariniidae). Auk 128:777–788

Moyle RG, Andersen MJ, Oliveros CH, Steinheimer FD, Reddy S

(2012) Phylogeny and Biogeography of the Core Babblers

(Aves: Timaliidae). Syst Biol 61:631–651

Nesbitt SJ, Ksepka DT, Clarke JA (2011) Podargiform affinities of the

enigmatic Fluvioviridavis platyrhamphus and the early diversi-

fication of Strisores (‘‘Caprimulgiformes’’ plus Apodiformes).

PloS One 6(11)

Newsome J, Flenley J (1988) Late Quaternary vegetational history of

the Central Highlands of Sumatra. II. Palaeopalynology and

vegetational history. J Biogeogr 15:555–578

Ohtani M, Kondo T, Tani N, Ueno S, Lee LS, Ng KKS, Muhammad

N, Finkeldey R, Na’iem M, Indrioko S, Kamiya K, Harada K,

Diway B, Khoo E, Kawamura K, Tsumura Y (2013) Nuclear and

chloroplast DNA phylogeography reveals Pleistocene diver-

gence and subsequent secondary contact of two genetic lineages

of the tropical rainforest tree species Shorea leprosula (Dipte-

rocarpaceae) in South-East Asia. Mol Ecol 22:2264–2279

Oliveros CH, Moyle RG (2010) Origin and diversification of

Philippine bulbuls. Mol Phylogenet Evol 54:822–832

Olson SL (1973) A classification of the Rallidae. Wilson Bull

85:381–416

Olson SL (1979) Picathartes—another West African forest relict with

probable Asian affinities. Bull Br Ornithol Club 99:112–113

Pacheco MA, Battistuzzi FU, Lentino M, Aguilar RF, Kumar S,

Escalante AA (2011) Evolution of modern birds revealed by

mitogenomics: timing the radiation and origin of major orders.

Mol Biol Evol 28:1927–1942

Packert M, Martens J, Sun YH, Severinghaus LL, Nazarenko AA,

Ting J, Topfer T, Tietze DT (2012) Horizontal and elevational

phylogeographic patterns of Himalayan and Southeast Asian

forest passerines (Aves: Passeriformes). J Biogeogr 39:556–573

Patou ML, Wilting A, Gaubert P, Esselstyn JA, Cruaud C, Jennings

AP, Fickel J, Veron G (2010) Evolutionary history of the

Paradoxurus palm civets–a new model for Asian biogeography.

J Biogeogr 37:2077–2097

Phillipps Q, Phillipps K (2014) Phillipps’ field guide to the birds of

Borneo, 3rd edn. John Beaufoy, Oxford

Pook CE, Joger U, Stumpel N, Wuster W (2009) When continents

collide: Phylogeny, historical biogeography and systematics of

the medically important viper genus Echis (Squamata: Serpen-

tes: Viperidae). Mol Phylogenet Evol 53:792–807

Prentice I, Harrison S, Bartlein P (2011) Global vegetation and

terrestrial carbon cycle changes after the last ice age. New Phytol

189:988–998

Quek SP, Davies SJ, Ashton PS, Itino T, Pierce NE (2007) The

geography of diversification in mutualistic ants: a gene’s-eye

view into the Neogene history of Sundaland rain forests. Mol

Ecol 16:2045–2062

Ramji MFS, Rahman MA, Tuen AA (2012) Morphological variation

of Mountain Blackeye (Chlorocharis emiliae) populations in

Malaysian Borneo. Malays Appl Biol 41:1–10

Reddy S (2008) Systematics and biogeography of the shrike-babblers

(Pteruthius): species limits, molecular phylogenetics, and diver-

sification patterns across southern Asia. Mol Phylogenet Evol

47:54–72

Reddy S, Moyle RG (2011) Systematics of the scimitar babblers

(Pomatorhinus: Timaliidae): phylogeny, biogeography, and

species-limits of four species complexes. Biol J Linn Soc

102:846–869

Richardson JE, Costion CM, Muellner AN (2012) The Malesian

floristic interchange: plant migration patterns across Wallace’s

Line. In: Gower DJ, Richardson JE, Rosen BR, Ruber L, Williams

ST (eds) Biotic evolution and environmental change in Southeast

Asia. Cambridge University Press, Cambridge, pp 138–63

Ricklefs RE, Cox GW (1978) Stage of taxon cycle, habitat

distribution, and population density in the avifauna of the West

Indies. Am Nat 112:875–895

Rogl F (1998) Paleogeographic Considerations for Mediterranean and

Paratethys seaways (Oligocene and Miocene). Ann Naturhist

Mus Wien 99A:279–331

Rogl F (1999) Mediterranean and Paratethys. Facts and hypotheses of

an Oligocene to Miocene paleogeography (short overview). Geol

Carpath 50(4):339–349

Round PD, Hughes JB, Woodruff DS (2003) Latitudinal range limits

of resident forest birds in Thailand and the Indochinese-Sundaic

zoogeographic transition. Nat Hist Bull Siam Soc 51:69–96

J Ornithol

123

Page 23: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Ruedi M (1996) Phylogenetic evolution and biogeography of

Southeast Asian shrews (genus Crocidura: Soricidae). Biol J

Linn Soc 58:197–219

Ryan JRJ, Esa YB (2006) Phylogenetic analysis of Hampala fishes

(Subfamily Cyprininae) in Malaysia inferred from partial

mitochondrial Cytochrome b DNA sequences. Zool Sci

23:893–901

Samonds KE, Godfrey LR, Ali JR, Goodman SM, Vences M,

Sutherland MR, Irwin MT, Krause DW (2012) Spatial and

temporal arrival patterns of Madagascar’s vertebrate fauna

explained by distance, ocean currents, and ancestor type. Proc

Natl Acad Sci USA 109:5352–5357

Schweizer M, Seehausen O, Guntert M, Hertwig ST (2010) The

evolutionary diversification of parrots supports a taxon pulse

model with multiple trans-oceanic dispersal events and local

radiations. Mol Phylogenet Evol 54:984–994

Sheldon FH, Moyle RG, Kennard J (2001) Ornithology of Sabah:

history, gazetteer, annotated checklist, and bibliography. Or-

nithol Monogr 52:1–285

Sheldon FH, Lim HC, Nais J, Lakim M, Tuuga A, Malim P, Majuakim J,

Lo A, Schilthuizen M, Hosner PA, Moyle RG (2009a) Observa-

tions on the ecology, distribution, and biogeography of forest birds

in Sabah, Malaysia. Raffles Bull Zool 57:577–586

Sheldon FH, Lohman DJ, Lim HC, Zou F, Goodman SM, Prawiradi-

laga DM, Winker K, Braile TM, Moyle RG (2009b) Phylogeog-

raphy of the magpie-robin species complex (Aves: Turdidae:

Copsychus) reveals a Philippine species, an interesting isolating

barrier, and unusual dispersal patterns in the Indian Ocean and

Southeast Asia. J Biogeogr 36:1070–1083

Sheldon FH, Oliveros CH, Taylor SS, McKay B, Lim HC, Rahman

MA, Mays H, Moyle RG (2012) Molecular phylogeny and

insular biogeography of the lowland tailorbirds of Southeast Asia

(Cisticolidae: Orthotomus). Mol Phylogenet Evol 65:54–63

Siler CD, Oaks JR, Welton LJ, Linkem CW, Swab JC, Diesmos AC,

Brown RM (2012) Did geckos ride the Palawan raft to the

Philippines? J Biogeogr 39:1217–1234

Slik JWF, Raes N, Aiba SI, Brearley FQ, Cannon CH, Meijaard E,

Nagamasu H, Nilus R, Paoli G, Poulsen AD, Sheil D, Suzuki E,

van Valkenburg J, Webb CO, Wilkie P, Wulffraat S (2009)

Environmental correlates for tropical tree diversity and distribu-

tion patterns in Borneo. Divers Distrib 15:523–532

Smythies BE (1999) The Birds of Borneo, 4th edn. Natural History

Publications (Borneo), Kota Kinabalu

Sorenson MD, Payne RB (2005) A molecular genetic analysis of

cuckoo phylogeny. In: Payne RB (ed) The Cuckoos. Oxford

University Press, Oxford, pp 68–94

Stein RW (2013) Multistage scenerios for the evolution of polymor-

phisms in birds. PhD thesis. Department of Biological Sciences.

Simon Fraser University, Burnaby

Steiper ME (2006) Population history, biogeography, and taxonomy

of orangutans (Genus: Pongo) based on a population genetic

meta-analysis of multiple loci. J Hum Evol 50:509–522

Stelbrink B, Albrecht C, Hall R, von Rintelen T (2012) The

biogeography of Sulawesi revisited: is there evidence for a

vicariant origin of taxa on Wallace’s ‘‘anomalous island’’?

Evolution 66:2252–2271

Stuijts IM (1993) Late Pleistocene and Holocene vegetation of West

Java, Indonesia. Mod Quat Res Southeast Asia Southeast Asia

12:1–173

Stuijts I, Newsome J, Flenley J (1988) Evidence for late Quaternary

vegetational change in the Sumatran and Javan highlands. Rev

Palaeobot Palynol 55:207–216

Sun K, Meiklejohn KA, Faircloth BC, Glenn TC, Braun EL, Kimball

RT (2014) The evolution of peafowl and other taxa with ocelli

(eyespots): a phylogenomic approach. Proc R Soc B Biol Sci

281:20140823

van den Bergh GD, de Vos J, Sondaar PY (2001) The Late Quaternary

palaeogeography of mammal evolution in the Indonesian

Archipelago. Palaeogeogr Palaeoclimatol Palaeoecol

171:385–408

van Steenis C (1950) The delimitation of Malaysia and its main plant

geographical divisions. Flora Malesiana 4:70–75

van Tuinen M (2009) Birds (Aves). In: Hedges SB, Kumar S (eds)

The timetree of life. Oxford University Press, New York,

pp 409–411

Viseshakul N, Charoennitikul W, Kitamura S, Kemp A, Thong-Aree

S, Surapunpitak Y, Poonswad P, Ponglikitmongkol M (2011) A

phylogeny of frugivorous hornbills linked to the evolution of

Indian plants within Asian rainforests. J Evol Biol 24:1533–1545

Voelker G, Penalba JV, Huntley JW, Bowie RC (2014) Diversifica-

tion in an Afro-Asian songbird clade (Erythropygia-Copsychus)

reveals founder-event speciation via trans-oceanic dispersals and

a southern to northern colonization pattern in Africa. Mol

Phylogenet Evol 73:97–105

Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia:

shorelines, river systems and time durations. J Biogeogr

27:1153–1167

Wallace AR (1876) The geographical distribution of animals.

McMillan, London

Wallace AR (1883) The Malay Archipelago. Macmillan, London

Wang N, Kimball RT, Braun EL, Liang B, Zhang Z (2013) Assessing

phylogenetic relationships among Galliformes: a multigene

phylogeny with expanded taxon sampling in Phasianidae. PLoS

One 8(5):e64312

Wells DR (1999) The birds of the Thai-Malay Peninsula, vol 1: Non-

passeries. Academic Press, New York

Wells DR, Dickinson EC, Dekker RWRJ (2003) Systematic notes on

Asian birds. 37. A preliminary review of the Chloropseidae and

Irenidae. Zool Verh Leiden 344:25–42

Whitmore TC (1981) Wallace’s line and plate tectonics. Oxford

University Press, Oxford

Whitmore TC (1987) Biogeographic evolution of the Malay

archipelago. Clarendon Press, Oxford

Whitten T, Soeriaatmadja RE, Afiff SA (1996) The ecology of

Indonesia series, vol II. The Ecology of Java and Bali. Periplus,

Hong Kong

Wilson RCL, Drury SA, Chapman DL (2000) The great Ice age:

climate change and life. Routledge, London

Wilting A, Sollmann R, Meijaard E, Helgen KM, Fickel J (2012)

Mentawai’s endemic, relictual fauna: is it evidence for Pleis-

tocene extinctions on Sumatra? J Biogeogr 39:1608–1620

Witts D, Hall R, Nichols G, Morley R (2012) A new depositional and

provenance model for the Tanjung Formation, Barito Basin, SE

Kalimantan, Indonesia. J Asian Earth Sci 56:77–104

Woodruff DS, Turner LM (2009) The Indochinese-Sundaic zoogeo-

graphic transition: a description and analysis of terrestrial

mammal species distributions. J Biogeogr 36:803–821

Wright TF, Schirtzinger EE, Matsumoto T, Eberhard JR, Graves GR,

Sanchez JJ, Capelli S, Muller H, Scharpegge J, Chambers GK

(2008) A multilocus molecular phylogeny of the parrots

(Psittaciformes): support for a Gondwanan origin during the

Cretaceous. Mol Biol Evol 25:2141–2156

Wurster CM, Bird MI (2014) Barriers and bridges: early human

dispersals in equatorial SE Asia. In: Harff J, Bailey G, Luth F

(eds) Geology and archaeology: submerged landscapes of the

continental shelf. Geological Society, London

Wurster CM, Bird MI, Bull ID, Creed F, Bryant C, Dungait JAJ, Paz

V (2010) Forest contraction in north equatorial Southeast Asia

during the Last Glacial Period. Proc Natl Acad Sci USA

107:15508–15511

Yapp CJ (2004) Fe(CO3)OH in goethite from a mid-latitude North

American Oxisol: estimate of atmospheric CO2 concentration in

J Ornithol

123

Highlight
Page 24: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

the Early Eocene ‘‘climatic optimum’’. Geochim Cosmochim

Acta 68:935–947

Yumul GP, Dimalanta CB, Marquez EJ, Queano KL (2009) Onland

signatures of the Palawan microcontinental block and Philippine

mobile belt collision and crustal growth process: a review.

J Asian Earth Sci 34:610–623

Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends,

rhythms, and aberrations in global climate 65 Ma to present.

Science 292:686–693

Zamoros LR, Matsuoka A (2004) Accretion and postaccretion

tectonics of the Calamian Islands, North Palawan block,

Philippines. Island Arc 13:506–619

Zamoros LR, Montes MGA, Queano KL, Marquez EJ, Dimalanta CB,

Gabo JAS, Yumul GP (2008) Buruanga peninsula and Antique

Range: two contrasting terranes in Northwest Panay, Philippines

featuring an arc-continent collision zone. Island Arc 17:443–457

Zhi L, Karesh W, Janczewski D, Frazier-Taylor H, Sajuthi D,

Gombek F, Andau M, Martenson J, O’Brien S (1996) Genomic

differentiation among natural populations of orang-utan (Pongo

pygmaeus). Curr Biol 6:1326–1336

Zhou L, Su YC, Thomas DC, Saunders RM (2012) ‘Out-of-

Africa’dispersal of tropical floras during the Miocene climatic

optimum: evidence from Uvaria (Annonaceae). J Biogeogr

39:322–335

J Ornithol

123

Page 25: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Online Resource 1: List of resident land birds of Sundaland

Article: Return to the Malay Archipelago: the biogeography of Sundaic rainforest birds

Journal: Journal of Ornithology

Authors: Frederick H. Sheldon · Haw Chuan Lim · and Robert G. Moyle

Correspondence: F. H. Sheldon: Museum of Natural Science and Department of Biological Sciences, Louisiana State University,

Baton Rouge, Louisiana, USA; email: [email protected]

Online Resource 1: List of resident land birds of Sundaland, derived from http://avibase.bsc-eoc.org, based on the classification of

Gill and Donsker (2014). Species’ occurrence was also checked using MacKinnon and Phillipps (1999), Phillipps and Phillipps

(2014), Van Marle and Voous (1988), and Wells (1999, 2007). Area abbreviations: B = Borneo, M = Malay Peninsula, S = Sumatra, J

= Java, and P = Palawan; * indicates an island or Malay Peninsula endemic; ** indicates a Sunda endemic

Common Name Scientific Name Area Common Name Scientific Name Area

Megapodes Megapodidae

Drongos Dicruridae

Philippine Megapode Megapodius cumingii B P

Black Drongo Dicrurus macrocercus J

Pheasants & Allies Phasianidae

Ashy Drongo Dicrurus leucophaeus B J M P S

Long-billed Partridge Rhizothera longirostris B M S **

Bronzed Drongo Dicrurus aeneus B M S

Hose's Partridge Rhizothera dulitensis B *

Lesser Racket-tailed Drongo Dicrurus remifer J M S

Black Partridge Melanoperdix niger B M S **

Hair-crested Drongo Dicrurus hottentottus B J P

King Quail Excalfactoria chinensis B J M P S

Sumatran Drongo Dicrurus sumatranus S *

Malaysian Partridge Arborophila campbelli M *

Greater Racket-tailed Drongo Dicrurus paradiseus B J M S

Roll's Partridge Arborophila rolli S *

Fantails Rhipiduridae

Sumatran Partridge Arborophila sumatrana S *

White-throated Fantail Rhipidura albicollis B M S

Grey-breasted Partridge Arborophila orientalis J *

White-bellied Fantail Rhipidura euryura J *

Chestnut-bellied Partridge Arborophila javanica J *

Malaysian Pied Fantail Rhipidura javanica B J M S

Red-billed Partridge Arborophila rubrirostris S *

Philippine Pied Fantail Rhipidura nigritorquis P

Red-breasted Hill Partridge Arborophila hyperythra B *

Spotted Fantail Rhipidura perlata B M S **

Chestnut-necklaced Partridge Arborophila charltonii B M S **

Rufous-tailed Fantail Rhipidura phoenicura J *

Ferruginous Partridge Caloperdix oculeus B M S

Monarchs Monarchidae

Crimson-headed Partridge Haematortyx sanguiniceps B *

Black-naped Monarch Hypothymis azurea B J M P S

Crested Partridge Rollulus rouloul B M S

Asian Paradise Flycatcher Terpsiphone paradisi B J M S

Red Junglefowl Gallus gallus J M S

Japanese Paradise Flycatcher Terpsiphone atrocaudata P

Green Junglefowl Gallus varius J

Blue Paradise Flycatcher Terpsiphone cyanescens P *

Hoogerwerf's Pheasant Lophura hoogerwerfi S *

Crows & Jays Corvidae

Page 26: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Salvadori's Pheasant Lophura inornata S *

Crested Jay Platylophus galericulatus B J M S **

Crestless Fireback Lophura erythrophthalma B M S **

Black Magpie Platysmurus leucopterus B M S **

Crested Fireback Lophura ignita B M S **

Common Green Magpie Cissa chinensis B M S

Bulwer's Pheasant Lophura bulweri B *

Javan Green Magpie Cissa thalassina J *

Bronze-tailed Peacock-Pheasant Polyplectron chalcurum S *

Bornean Green Magpie Cissa jefferyi B *

Mountain Peacock-Pheasant Polyplectron inopinatum M *

Sumatran Treepie Dendrocitta occipitalis S *

Malayan Peacock-Pheasant Polyplectron malacense M *

Bornean Treepie Dendrocitta cinerascens B *

Bornean Peacock-Pheasant Polyplectron schleiermacheri B *

Racket-tailed Treepie Crypsirina temia J M S

Palawan Peacock-Pheasant Polyplectron napoleonis P *

Slender-billed Crow Corvus enca B J M P S

Crested Argus Rheinardia ocellata M

Large-billed Crow Corvus macrorhynchos J M P S

Great Argus Argusianus argus B M S

Rail-babbler Eupetidae

Green Peafowl Pavo muticus J M

Rail-babbler Eupetes macrocerus B M S **

Ospreys Pandionidae

Fairy Flycatchers Stenostiridae

Western Osprey Pandion haliaetus M

Grey-headed Canary-Flycatcher Culicicapa ceylonensis B J M S

Eastern Osprey Pandion cristatus J

Citrine Canary-flycatcher Culicicapa helianthea P

Kites, Hawks & Eagles Accitripidae

Tits Paridae

Black-winged Kite Elanus caeruleus B J M P

Sultan Tit Melanochlora sultanea M S

Crested Honey Buzzard Pernis ptilorhynchus B J M P

Palawan Tit Pardaliparus amabilis P *

Philippine Honey Buzzard Pernis steerei P

Great Tit Parus major B

Jerdon's Baza Aviceda jerdoni B M P

Cinereous Tit Parus cinereus J M S

White-rumped Vulture Gyps bengalensis M

Larks Alaudidae

Red-headed Vulture Sarcogyps calvus M

Horsfield's Bush Lark Mirafra javanica J

Crested Serpent Eagle Spilornis cheela B J M P S

Bulbuls Pycnonotidae

Kinabalu Serpent Eagle Spilornis kinabaluensis B *

Straw-headed Bulbul Pycnonotus zeylanicus B J M S **

Philippine Serpent Eagle Spilornis holospilus P

Cream-striped Bulbul Pycnonotus leucogrammicus S *

Bat Hawk Macheiramphus alcinus B M S

Spot-necked Bulbul Pycnonotus tympanistrigus S *

Changeable Hawk-Eagle Nisaetus cirrhatus B J M P S

Black-and-white Bulbul Pycnonotus melanoleucos B M S **

Mountain Hawk-Eagle Nisaetus nipalensis M

Black-headed Bulbul Pycnonotus atriceps B J M P S

Blyth's Hawk-Eagle Nisaetus alboniger B M S **

Black-crested Bulbul Pycnonotus flaviventris M

Javan Hawk-Eagle Nisaetus bartelsi J *

Ruby-throated Bulbul Pycnonotus dispar J S **

Pinsker's Hawk-Eagle Nisaetus pinskeri P

Bornean Bulbul Pycnonotus montis B *

Wallace's Hawk-Eagle Nisaetus nanus B M S **

Scaly-breasted Bulbul Pycnonotus squamatus B J M S **

Rufous-bellied Hawk-Eagle Lophotriorchis kienerii B J M P S

Grey-bellied Bulbul Pycnonotus cyaniventris B M S **

Indian Black Eagle Ictinaetus malaiensis B J M S

Red-whiskered Bulbul Pycnonotus jocosus M

Greater Spotted Eagle Clanga clanga M S

Sooty-headed Bulbul Pycnonotus aurigaster J *

Crested Goshawk Accipiter trivirgatus B J M P S

Puff-backed Bulbul Pycnonotus eutilotus B M S **

Page 27: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Besra Accipiter virgatus B J

Blue-wattled Bulbul Pycnonotus nieuwenhuisii B S

Brahminy Kite Haliastur indus B J M P S

Orange-spotted Bulbul Pycnonotus bimaculatus J S

White-bellied Sea Eagle Haliaeetus leucogaster B J M P S

Stripe-throated Bulbul Pycnonotus finlaysoni M

Lesser Fish Eagle Haliaeetus humilis B M S

Flavescent Bulbul Pycnonotus flavescens B

Grey-headed Fish Eagle Haliaeetus ichthyaetus B J M P S

Yellow-vented Bulbul Pycnonotus goiavier B J M P S

Rufous-winged Buzzard Butastur liventer J

Olive-winged Bulbul Pycnonotus plumosus B J M S **

Buttonquail Turnicidae

Ashy-fronted Bulbul Pycnonotus cinereifrons P *

Common Buttonquail Turnix sylvaticus J

Streak-eared Bulbul Pycnonotus blanfordi M

Barred Buttonquail Turnix suscitator J M S

Cream-vented Bulbul Pycnonotus simplex B J M S **

Pigeons & Doves Columbidae

Asian Red-eyed Bulbul Pycnonotus brunneus B J M S **

Silvery Pigeon Columba argentina B S

Spectacled Bulbul Pycnonotus erythropthalmos B M S **

Metallic Pigeon Columba vitiensis B P

Finsch's Bulbul Alophoixus finschii B M S **

Island Collared Dove Streptopelia bitorquata J P

Ochraceous Bulbul Alophoixus ochraceus B M S

Spotted Dove Spilopelia chinensis J M P S

Grey-cheeked Bulbul Alophoixus bres B J M S **

Barred Cuckoo-Dove Macropygia unchall J M S

Palawan Bulbul Alophoixus frater P *

Philippine Cuckoo-Dove Macropygia tenuirostris P

Yellow-bellied Bulbul Alophoixus phaeocephalus B M S **

Ruddy Cuckoo-Dove Macropygia emiliana B J S

Hook-billed Bulbul Setornis criniger B S

Little Cuckoo-Dove Macropygia ruficeps B J M S

Hairy-backed Bulbul Tricholestes criniger B M S **

Common Emerald Dove Chalcophaps indica B J M P S

Buff-vented Bulbul Iole olivacea B M S **

Zebra Dove Geopelia striata B J M S

Sulphur-bellied Bulbul Iole palawanensis P *

Nicobar Pigeon Caloenas nicobarica B J M P S

Mountain Bulbul Ixos mcclellandii M

White-eared Brown Dove Phapitreron leucotis P

Streaked Bulbul Ixos malaccensis B M S **

Cinnamon-headed Green Pigeon Treron fulvicollis B M S **

Sunda Bulbul Ixos virescens J S **

Little Green Pigeon Treron olax B J M S ** Cinereous Bulbul Hemixos cinereus B M S

Pink-necked Green Pigeon Treron vernans B J M P S

Swallows & Martins Hirundinidae

Orange-breasted Green Pigeon Treron bicinctus J M S

Pacific Swallow Hirundo tahitica B J M P S

Philippine Green Pigeon Treron axillaris P

Dusky Crag Martin Ptyonoprogne concolor M

Thick-billed Green Pigeon Treron curvirostra B J M P S

Striated Swallow Cecropis striolata J M P

Grey-cheeked Green Pigeon Treron griseicauda J

Wren-babblers Pnoepygidae

Large Green Pigeon Treron capellei B J M S ** Pygmy Wren-babbler Pnoepyga pusilla J M S

Sumatran Green Pigeon Treron oxyurus J S **

Cettia Bush Warblers Cettiidae

Yellow-vented Green Pigeon Treron seimundi M

Yellow-bellied Warbler Abroscopus superciliaris B J M S

Wedge-tailed Green Pigeon Treron sphenurus J M S

Mountain Tailorbird Phyllergates cuculatus B J M P S

Banded Fruit Dove Ptilinopus cinctus J

Sunda Bush Warbler Horornis vulcanius B J P S

Pink-headed Fruit Dove Ptilinopus porphyreus J S

Javan Tesia Tesia superciliaris J *

Yellow-breasted Fruit Dove Ptilinopus occipitalis P

Bornean Stubtail Urosphena whiteheadi B *

Page 28: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Jambu Fruit Dove Ptilinopus jambu B J M S ** Bushtits Aegithalidae

Black-chinned Fruit Dove Ptilinopus leclancheri P

Pygmy Bushtit Psaltria exilis J *

Black-naped Fruit Dove Ptilinopus melanospilus B P

Leaf Warblers & Allies Phylloscopidae

Green Imperial Pigeon Ducula aenea B J M P S

Philippine Leaf Warbler Phylloscopus olivaceus P

Grey Imperial Pigeon Ducula pickeringii B P

Mountain Leaf Warbler Phylloscopus trivirgatus B J M S

Mountain Imperial Pigeon Ducula badia B J M S

Negros Leaf Warbler Phylloscopus nigrorum P

Dark-backed Imperial Pigeon Ducula lacernulata J

Chestnut-crowned Warbler Seicercus castaniceps M S

Pied Imperial Pigeon Ducula bicolor B J M P S

Yellow-breasted Warbler Seicercus montis B M P S

Cuckoos Cuculidae

Sunda Warbler Seicercus grammiceps J S

Short-toed Coucal Centropus rectunguis B M S **

Reed Warblers Acrocephalidae

Sunda Coucal Centropus nigrorufus J *

Oriental Reed Warbler Acrocephalus orientalis J

Greater Coucal Centropus sinensis B J M P S

Clamorous Reed Warbler Acrocephalus stentoreus B J

Lesser Coucal Centropus bengalensis B J M P S

Grassbirds & Allies Locustellidae

Bornean Ground Cuckoo Carpococcyx radiceus B *

Javan Bush Warbler Locustella montis J *

Sumatran Ground Cuckoo Carpococcyx viridis S *

Friendly Bush Warbler Locustella accentor B *

Raffles's Malkoha Rhinortha chlorophaea B M S

Striated Grassbird Megalurus palustris B P

Red-billed Malkoha Zanclostomus javanicus B J M S

Cisticolas & Allies Cisticolidae

Chestnut-breasted Malkoha Phaenicophaeus curvirostris B J M P S

Zitting Cisticola Cisticola juncidis J M P S

Chestnut-bellied Malkoha Phaenicophaeus sumatranus B M S **

Golden-headed Cisticola Cisticola exilis B J P

Black-bellied Malkoha Phaenicophaeus diardi B M S

Brown Prinia Prinia polychroa J

Green-billed Malkoha Phaenicophaeus tristis J M S

Hill Prinia Prinia superciliaris M

Chestnut-winged Cuckoo Clamator coromandus P

Rufescent Prinia Prinia rufescens M

Asian Koel Eudynamys scolopaceus M P S

Bar-winged Prinia Prinia familiaris J S

Asian Emerald Cuckoo Chrysococcyx maculatus S

Yellow-bellied Prinia Prinia flaviventris B J M S

Violet Cuckoo Chrysococcyx xanthorhynchus B J M P S

Plain Prinia Prinia inornata J

Little Bronze Cuckoo Chrysococcyx minutillus B J M S

Common Tailorbird Orthotomus sutorius J M

Banded Bay Cuckoo Cacomantis sonneratii B J M P S

Dark-necked Tailorbird Orthotomus atrogularis B J M S

Plaintive Cuckoo Cacomantis merulinus B J M P S

Rufous-tailed Tailorbird Orthotomus sericeus B M P S **

Rusty-breasted Cuckoo Cacomantis sepulcralis J M P S

Ashy Tailorbird Orthotomus ruficeps B J M S

Square-tailed Drongo-Cuckoo Surniculus lugubris B J M P S

Olive-backed Tailorbird Orthotomus sepium J

Moustached Hawk-Cuckoo Hierococcyx vagans B M S

Babblers Timaliidae

Dark Hawk-Cuckoo Hierococcyx bocki B M S **

Large Scimitar Babbler Pomatorhinus hypoleucos M

Philippine Hawk-Cuckoo Hierococcyx pectoralis P

Chestnut-backed Scimitar Babbler Pomatorhinus montanus B J M S **

Malaysian Hawk-Cuckoo Hierococcyx fugax J M S

White-breasted Babbler Stachyris grammiceps J *

Indian Cuckoo Cuculus micropterus B J M S

Grey-throated Babbler Stachyris nigriceps B M S

Sunda Cuckoo Cuculus lepidus J M S

Grey-headed Babbler Stachyris poliocephala B M S **

Page 29: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Barn Owls Tytonidae

Spot-necked Babbler Stachyris strialata S

Western Barn Owl Tyto alba J M S

Chestnut-rumped Babbler Stachyris maculata B M S **

Grass Owl Tyto capensis B

White-necked Babbler Stachyris leucotis B M S **

Eastern Grass Owl Tyto longimembris P

Black-throated Babbler Stachyris nigricollis B M S **

Oriental Bay Owl Phodilus badius B J M S

White-bibbed Babbler Stachyris thoracica J *

Owls Strigidae

Chestnut-winged Babbler Stachyris erythroptera B M S **

White-fronted Scops Owl Otus sagittatus M

Crescent-chested Babbler Stachyris melanothorax J *

Reddish Scops Owl Otus rufescens B J M S ** Rufous-fronted Babbler Stachyridopsis rufifrons B M S

Mountain Scops Owl Otus spilocephalus B M S

Golden Babbler Stachyridopsis chrysaea M S

Rajah Scops Owl Otus brookii B S

Pin-striped Tit-Babbler Macronus gularis B M P S

Javan Scops Owl Otus angelinae J *

Bold-striped Tit-Babbler Macronus bornensis J M

Mentawai Scops Owl Otus mentawi S *

Grey-cheeked Tit-Babbler Macronus flavicollis J *

Collared Scops Owl Otus bakkamoena B

Fluffy-backed Tit-Babbler Macronus ptilosus B M S **

Sunda Scops Owl Otus lempiji J M S

Chestnut-capped Babbler Timalia pileata J

Palawan Scops Owl Otus fuliginosus P *

Fulvettas & Ground Babblers Pellorneidae

Oriental Scops Owl Otus sunia B M

Rufous-winged Fulvetta Alcippe castaneceps M

Mantanani Scops Owl Otus mantananensis B P **

Brown Fulvetta Alcippe brunneicauda B M S **

Simeulue Scops Owl Otus umbra S *

Javan Fulvetta Alcippe pyrrhoptera J *

Enggano Scops Owl Otus enganensis S *

Mountain Fulvetta Alcippe peracensis M

Barred Eagle-Owl Bubo sumatranus B J M S

Bornean Wren-Babbler Ptilocichla leucogrammica B *

Brown Fish Owl Ketupa zeylonensis M

Falcated Wren-Babbler Ptilocichla falcata P

Buffy Fish Owl Ketupa ketupu B J M S

Rusty-breasted Wren-Babbler Napothera rufipectus S *

Spotted Wood Owl Strix seloputo J M P S

Black-throated Wren-Babbler Napothera atrigularis B *

Brown Wood Owl Strix leptogrammica B J M S

Large Wren-Babbler Napothera macrodactyla J M S **

Collared Owlet Glaucidium brodiei B M S

Marbled Wren-Babbler Napothera marmorata M S **

Javan Owlet Glaucidium castanopterum J *

Streaked Wren-Babbler Napothera brevicaudata M

Brown Hawk-Owl Ninox scutulata B J M P S

Mountain Wren-Babbler Napothera crassa B *

Frogmouths Podargidae

Eyebrowed Wren-Babbler Napothera epilepidota B J M S

Large Frogmouth Batrachostomus auritus B M S **

Collared Babbler Gampsorhynchus torquatus M

Dulit Frogmouth Batrachostomus harterti B *

Sumatran Wren-Babbler Rimator albostriatus S *

Gould's Frogmouth Batrachostomus stellatus B M S **

Abbott's Babbler Malacocincla abbotti B J M S

Short-tailed Frogmouth Batrachostomus poliolophus S *

Horsfield's Babbler Malacocincla sepiaria B J M S **

Bornean Frogmouth Batrachostomus mixtus B *

Black-browed Babbler Malacocincla perspicillata B *

Javan Frogmouth Batrachostomus javensis J *

Short-tailed Babbler Malacocincla malaccensis B M S **

Blyth's Frogmouth Batrachostomus affinis B J M S

Ashy-headed Babbler Malacocincla cinereiceps P *

Palawan Frogmouth Batrachostomus chaseni B P

Moustached Babbler Malacopteron magnirostre B M S **

Page 30: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Sunda Frogmouth Batrachostomus cornutus B M S

Sooty-capped Babbler Malacopteron affine B M S **

Nightjars Caprimulgidae

Scaly-crowned Babbler Malacopteron cinereum B J M S

Malaysian Eared Nightjar Lyncornis temminckii B M S **

Rufous-crowned Babbler Malacopteron magnum B M S **

Great Eared Nightjar Lyncornis macrotis M S

Melodious Babbler Malacopteron palawanense P *

Large-tailed Nightjar Caprimulgus macrurus B J M P S

Grey-breasted Babbler Malacopteron albogulare B M S **

Philippine Nightjar Caprimulgus manillensis P

White-chested Babbler Trichastoma rostratum B M S **

Savanna Nightjar Caprimulgus affinis B J M S

Ferruginous Babbler Trichastoma bicolor B M S **

Bonaparte's Nightjar Caprimulgus concretus B S

Striped Wren-Babbler Kenopia striata B M S **

Salvadori's Nightjar Caprimulgus pulchellus J S

Puff-throated Babbler Pellorneum ruficeps M

Treeswifts Hemiprocnidae

Buff-breasted Babbler Pellorneum tickelli M

Grey-rumped Treeswift Hemiprocne longipennis B J M S

Sumatran Babbler Pellorneum buettikoferi S *

Whiskered Treeswift Hemiprocne comata B M S

Temminck's Babbler Pellorneum pyrrogenys B J S

Swifts Apodidae

Black-capped Babbler Pellorneum capistratum B J M S **

Giant Swiftlet Hydrochous gigas J M S **

Laughingthrushes Leiothrichidae

Glossy Swiftlet Collocalia esculenta B J M S

Sumatran Laughingthrush Garrulax bicolor S *

Cave Swiftlet Collocalia linchi J S

Sunda Laughingthrush Garrulax palliatus B S **

Bornean Swiftlet Collocalia dodgei B *

Rufous-fronted Laughingthrush Garrulax rufifrons J *

Pygmy Swiftlet Collocalia troglodytes P

Chestnut-capped Laughingthrush Garrulax mitratus M S **

Philippine Swiftlet Aerodramus mearnsi P

Chestnut-hooded Laughingthrush Garrulax treacheri B *

Volcano Swiftlet Aerodramus vulcanorum J *

Black Laughingthrush Garrulax lugubris M S **

Mossy-nest Swiftlet Aerodramus salangana B J S

Bare-headed Laughingthrush Garrulax calvus B *

Uniform Swiftlet Aerodramus vanikorensis B P

Malayan Laughingthrush Trochalopteron peninsulae M

Black-nest Swiftlet Aerodramus maximus B J M S

Himalayan Cutia Cutia nipalensis M

Edible-nest Swiftlet Aerodramus fuciphagus B J M

Blue-winged Minla Minla cyanouroptera M

Germain's Swiftlet Aerodramus germani M P

Bar-throated Minla Minla strigula M

Silver-rumped Spinetail Rhaphidura leucopygialis B J M S ** Silver-eared Mesia Leiothrix argentauris M S

White-throated Needletail Hirundapus caudacutus M

Spotted Crocias Crocias albonotatus J *

Brown-backed Needletail Hirundapus giganteus B J M P S

Long-tailed Sibia Heterophasia picaoides M S

Asian Palm Swift Cypsiurus balasiensis B J M P S

White-eyes Zosteropidae

Pacific Swift Apus pacificus J M P

Chestnut-crested Yuhina Yuhina everetti B *

House Swift Apus nipalensis B J M S

Palawan Striped Babbler Zosterornis hypogrammicus P

Trogons Trogonidae

Mees's White-eye Lophozosterops javanicus J *

Javan Trogon Apalharpactes reinwardtii J *

Pygmy White-eye Oculocincta squamifrons B *

Sumatran Trogon Apalharpactes mackloti S *

Mountain Black-eye Chlorocharis emiliae B *

Red-naped Trogon Harpactes kasumba B M S **

Oriental White-eye Zosterops palpebrosus B J M S

Diard's Trogon Harpactes diardii B M S **

Enggano White-eye Zosterops salvadorii S *

Page 31: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Whitehead's Trogon Harpactes whiteheadi B *

Black-capped White-eye Zosterops atricapilla B S

Cinnamon-rumped Trogon Harpactes orrhophaeus B M S **

Everett's White-eye Zosterops everetti B M

Scarlet-rumped Trogon Harpactes duvaucelii B M S **

Yellowish White-eye Zosterops nigrorum P

Orange-breasted Trogon Harpactes oreskios B J M S

Mountain White-eye Zosterops montanus J P S

Red-headed Trogon Harpactes erythrocephalus M S

Javan White-eye Zosterops flavus B J

Rollers Coraciidae

Lemon-bellied White-eye Zosterops chloris J

Indian Roller Coracias benghalensis M

Fairy-bluebirds Irenidae

Oriental Dollarbird Eurystomus orientalis B J M P S

Asian Fairy-bluebird Irena puella B J M P S

Kingfishers Alcedinidae

Nuthatches Sittidae

Rufous-collared Kingfisher Actenoides concretus B M S **

Velvet-fronted Nuthatch Sitta frontalis B J M P S

Banded Kingfisher Lacedo pulchella B J M S

Blue Nuthatch Sitta azurea J M S * *

Stork-billed Kingfisher Pelargopsis capensis B J M P S

Starling Sturnidae

Brown-winged Kingfisher Pelargopsis amauroptera M

Asian Glossy Starling Aplonis panayensis B J M P S

Ruddy Kingfisher Halcyon coromanda B J M P

Short-tailed Starling Aplonis minor J

White-throated Kingfisher Halcyon smyrnensis M P

Coleto Sarcops calvus P

Javan Kingfisher Halcyon cyanoventris J *

Golden-crested Myna Ampeliceps coronatus M

Collared Kingfisher Todiramphus chloris B J M P S

Common Hill Myna Gracula religiosa B J M P S

Cerulean Kingfisher Alcedo coerulescens J S

Nias Hill Myna Gracula robusta S *

Blue-banded Kingfisher Alcedo euryzona B J M S

Enggano Hill Myna Gracula enganensis S *

Blue-eared Kingfisher Alcedo meninting B J M P S

Javan Myna Acridotheres javanicus J *

Common Kingfisher Alcedo atthis J M

Jungle Myna Acridotheres fuscus M

Oriental Dwarf Kingfisher Ceyx erithaca B J M P S

Common Myna Acridotheres tristis M

Bee-eaters Meropidae

Black-winged Starling Acridotheres melanopterus J *

Red-bearded Bee-eater Nyctyornis amictus B M S

Pied Myna Gracupica contra J S

Blue-tailed Bee-eater Merops philippinus J M P S

Daurian Starling Agropsar sturninus J M

Blue-throated Bee-eater Merops viridis B J M P S

Chestnut-cheeked Starling Agropsar philippensis P

Chestnut-headed Bee-eater Merops leschenaulti J M S

White-shouldered Starling Sturnia sinensis M

Hoopoes Upupidae

Bali Myna Leucopsar rothschildi J *

Eurasian Hoopoe Upupa epops M

Thrushes Turdidae

Hornbills Bucerotidae

Chestnut-capped Thrush Geokichla interpres B J M S

White-crowned Hornbill Berenicornis comatus B M S

Enggano Thrush Geokichla leucolaema S *

Rhinoceros Hornbill Buceros rhinoceros B J M S ** Orange-headed Thrush Geokichla citrina B J M S

Great Hornbill Buceros bicornis M S

Siberian Thrush Geokichla sibirica M

Helmeted Hornbill Rhinoplax vigil B M S **

Everett's Thrush Zoothera everetti B *

Palawan Hornbill Anthracoceros marchei P *

Sunda Thrush Zoothera andromedae J S

Oriental Pied Hornbill Anthracoceros albirostris B J M S

Scaly Thrush Zoothera dauma J S

Page 32: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Black Hornbill Anthracoceros malayanus B M S **

Island Thrush Turdus poliocephalus B J S

Bushy-crested Hornbill Anorrhinus galeritus B M S **

Eyebrowed Thrush Turdus obscurus M

Wreathed Hornbill Rhyticeros undulatus B J M S

Sumatran Cochoa Cochoa beccarii S *

Plain-pouched Hornbill Rhyticeros subruficollis M S

Javan Cochoa Cochoa azurea J *

Wrinkled Hornbill Rhabdotorrhinus corrugatus B M S **

Fruithunter Chlamydochaera jefferyi B *

Asian Barbets Megalaimidae

Oriental Magpie-Robin Copsychus saularis B J M S

Fire-tufted Barbet Psilopogon pyrolophus M S **

Rufous-tailed Shama Copsychus pyrropygus B M S **

Lineated Barbet Megalaima lineata J M

Philippine Magpie-Robin Copsychus mindanensis P

Brown-throated Barbet Megalaima corvina J *

White-rumped Shama Copsychus malabaricus J M S

Golden-whiskered Barbet Megalaima chrysopogon B M S **

White-crowned Shama Copsychus stricklandii B *

Red-crowned Barbet Megalaima rafflesii B M S **

White-vented Shama Copsychus niger P *

Red-throated Barbet Megalaima mystacophanos B M S

Old World Flycatchers Muscicapidae

Black-banded Barbet Megalaima javensis J *

Grey-streaked Flycatcher Muscicapa griseisticta B S

Golden-throated Barbet Megalaima franklinii M

Asian Brown Flycatcher Muscicapa latirostris B J

Black-browed Barbet Megalaima oorti M S

Brown-streaked Flycatcher Muscicapa williamsoni M S

Mountain Barbet Megalaima monticola B *

Rufous-browed Flycatcher Anthipes solitaris M S

Yellow-crowned Barbet Megalaima henricii B M S **

Pale Blue Flycatcher Cyornis unicolor B J M S

Flame-fronted Barbet Megalaima armillaris J *

Rück's Blue Flycatcher Cyornis ruckii S *

Golden-naped Barbet Megalaima pulcherrima B *

Hill Blue Flycatcher Cyornis banyumas B J M S

Blue-eared Barbet Megalaima australis B J M S

Large Blue Flycatcher Cyornis magnirostris M

Bornean Barbet Megalaima eximia B *

Palawan Blue Flycatcher Cyornis lemprieri P *

Coppersmith Barbet Megalaima haemacephala J M P S

Tickell's Blue Flycatcher Cyornis tickelliae M S

Brown Barbet Caloramphus fuliginosus B *

Sunda Blue Flycatcher Cyornis caerulatus B S

Sooty Barbet Caloramphus hayii M S **

Bornean Blue Flycatcher Cyornis superbus B *

Honeyguides Indicatoridae

Chinese Blue Flycatcher Cyornis glaucicomans M

Malaysian Honeyguide Indicator archipelagicus B M S

Malaysian Blue Flycatcher Cyornis turcosus B M S **

Woodpeckers Picidae

Mangrove Blue Flycatcher Cyornis rufigastra B J M P S

Speckled Piculet Picumnus innominatus B M S

White-tailed Flycatcher Cyornis concretus B M S

Rufous Piculet Sasia abnormis B J M S ** Fulvous-chested Jungle Flycatcher Cyornis olivaceus B J S

Grey-and-buff Woodpecker Hemicircus concretus B J M S ** Grey-chested Jungle Flycatcher Cyornis umbratilis B J M S **

Sunda Pygmy Woodpecker Dendrocopos moluccensis B J M S

Rufous-tailed Jungle Flycatcher Cyornis ruficauda B

Grey-capped Pygmy Woodpecker Dendrocopos canicapillus B M S

Rufous-vented Niltava Niltava sumatrana M S **

Freckle-breasted Woodpecker Dendrocopos analis J S

Large Niltava Niltava grandis M S

White-bellied Woodpecker Dryocopus javensis B J M P S

Verditer Flycatcher Eumyias thalassinus B M S

Banded Woodpecker Chrysophlegma miniaceum B J M S

Indigo Flycatcher Eumyias indigo B J S

Checker-throated Woodpecker Chrysophlegma mentale B J M S ** Lesser Shortwing Brachypteryx leucophris J M S

Page 33: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Greater Yellownape Chrysophlegma flavinucha M S

White-browed Shortwing Brachypteryx montana B J M P S

Lesser Yellownape Picus chlorolophus M S

Eyebrowed Jungle Flycatcher Vauriella gularis B *

Crimson-winged Woodpecker Picus puniceus B J M S

Siberian Blue Robin Larvivora cyane M

Streak-breasted Woodpecker Picus viridanus M

White-tailed Robin Myiomela leucura M

Laced Woodpecker Picus vittatus J M S

Sunda Robin Myiomela diana J S

Grey-headed Woodpecker Picus canus M S

Sunda Forktail Enicurus velatus J S

Olive-backed Woodpecker Dinopium rafflesii B M S

Chestnut-naped Forktail Enicurus ruficapillus B M S **

Common Flameback Dinopium javanense B J M S

Slaty-backed Forktail Enicurus schistaceus M

Spot-throated Flameback Dinopium everetti P

White-crowned Forktail Enicurus leschenaulti B J M S

Greater Flame-backed Woodpecker Chrysocolaptes lucidus B

Bornean Forktail Enicurus borneensis B *

Red-headed Flameback Chrysocolaptes

erythrocephalus P

Shiny Whistling Thrush Myophonus melanurus S *

Javan Flameback Chrysocolaptes strictus J *

Javan Whistling Thrush Myophonus glaucinus J *

Greater Flameback Chrysocolaptes guttacristatus J M S

Bornean Whistling Thrush Myophonus borneensis B *

Bamboo Woodpecker Gecinulus viridis M

Brown-winged Whistling Thrush Myophonus castaneus S *

Maroon Woodpecker Blythipicus rubiginosus B M S **

Malayan Whistling Thrush Myophonus robinsoni M *

Orange-backed Woodpecker Reinwardtipicus validus B J M S ** Blue Whistling Thrush Myophonus caeruleus J M S

Rufous Woodpecker Micropternus brachyurus B J M S

Rufous-chested Flycatcher Ficedula dumetoria B J M S

Buff-rumped Woodpecker Meiglyptes tristis B J M S

Taiga Flycatcher Ficedula albicilla M

Buff-necked Woodpecker Meiglyptes tukki B M S **

Snowy-browed Flycatcher Ficedula hyperythra B J M P S

Great Slaty Woodpecker Mulleripicus pulverulentus B J M P S

Palawan Flycatcher Ficedula platenae P *

Falcons Falconidae

Little Pied Flycatcher Ficedula westermanni B J M P S

Black-thighed Falconet Microhierax fringillarius B J M S

Pygmy Flycatcher Muscicapella hodgsoni B M S

White-fronted Falconet Microhierax latifrons B *

Blue Rock Thrush Monticola solitarius M P S

Spotted Kestrel Falco moluccensis J

Pied Bush Chat Saxicola caprata J

Peregrine Falcon Falco peregrinus B J M S

Leafbirds Chloropseidae

Cockatoos Cacatuidae

Yellow-throated Leafbird Chloropsis palawanensis P *

Red-vented Cockatoo Cacatua haematuropygia P

Greater Green Leafbird Chloropsis sonnerati B J M S

Parrots Psittacidae

Lesser Green Leafbird Chloropsis cyanopogon B M S **

Blue-crowned Hanging Parrot Loriculus galgulus B J M S ** Blue-winged Leafbird Chloropsis cochinchinensis B J M S

Yellow-throated Hanging Parrot Loriculus pusillus J

Bornean Leafbird Chloropsis kinabaluensis B *

Blue-rumped Parrot Psittinus cyanurus B M S

Sumatran Leafbird Chloropsis media S *

Blue-headed Racket-tail Prioniturus platenae P *

Orange-bellied Leafbird Chloropsis hardwickii M

Blue-naped Parrot Tanygnathus lucionensis B P

Blue-masked Leafbird Chloropsis venusta S *

Red-breasted Parakeet Psittacula alexandri J S

Flowerpeckers Dicaeidae

Long-tailed Parakeet Psittacula longicauda B M S **

Yellow-breasted Flowerpecker Prionochilus maculatus B M S **

Broadbills Eurylaimidae

Crimson-breasted Flowerpecker Prionochilus percussus B J M S **

Page 34: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Green Broadbill Calyptomena viridis B M S

Palawan Flowerpecker Prionochilus plateni P *

Hose's Broadbill Calyptomena hosii B *

Yellow-rumped Flowerpecker Prionochilus xanthopygius B *

Whitehead's Broadbill Calyptomena whiteheadi B *

Scarlet-breasted Flowerpecker Prionochilus thoracicus B M S

Black-and-red Broadbill Cymbirhynchus macrorhynchos B M S

Thick-billed Flowerpecker Dicaeum agile B J M S

Long-tailed Broadbill Psarisomus dalhousiae B M S

Striped Flowerpecker Dicaeum aeruginosum P

Silver-breasted Broadbill Serilophus lunatus M S

Brown-backed Flowerpecker Dicaeum everetti B M **

Banded Broadbill Eurylaimus javanicus B J M S

Yellow-vented Flowerpecker Dicaeum chrysorrheum B J M S

Black-and-yellow Broadbill Eurylaimus ochromalus B M S

Orange-bellied Flowerpecker Dicaeum trigonostigma B J M P S

Dusky Broadbill Corydon sumatranus B M S

Plain Flowerpecker Dicaeum minullum B J M S

Pittas Pittidae

Pygmy Flowerpecker Dicaeum pygmaeum P

Rusty-naped Pitta Hydrornis oatesi M

Blue-cheeked Flowerpecker Dicaeum maugei J

Schneider's Pitta Hydrornis schneideri S *

Black-sided Flowerpecker Dicaeum monticolum B *

Giant Pitta Hydrornis caeruleus B M S

Fire-breasted Flowerpecker Dicaeum ignipectus M S

Blue-headed Pitta Hydrornis baudii B *

Blood-breasted Flowerpecker Dicaeum sanguinolentum J

Javan Banded Pitta Hydrornis guajanus J *

Scarlet-backed Flowerpecker Dicaeum cruentatum B M S

Malayan Banded Pitta Hydrornis irena M S **

Scarlet-headed Flowerpecker Dicaeum trochileum J

Bornean Banded Pitta Hydrornis schwaneri B *

Sunbirds Nectariniidae

Red-bellied Pitta Erythropitta erythrogaster P

Ruby-cheeked Sunbird Chalcoparia singalensis B J M S

Blue-banded Pitta Erythropitta arquata B *

Plain Sunbird Anthreptes simplex B M S

Garnet Pitta Erythropitta granatina B M S **

Brown-throated Sunbird Anthreptes malacensis B J M P S

Graceful Pitta Erythropitta venusta S *

Red-throated Sunbird Anthreptes rhodolaemus B M S **

Black-crowned Pitta Erythropitta ussheri B *

Purple-naped Sunbird Hypogramma hypogrammicum B M S

Hooded Pitta Pitta sordida B J M P S

Purple-throated Sunbird Leptocoma sperata B P

Blue-winged Pitta Pitta moluccensis M

Van Hasselt's Sunbird Leptocoma brasiliana J M S

Mangrove Pitta Pitta megarhyncha M S

Copper-throated Sunbird Leptocoma calcostetha B J M P S

Australasian Warblers Acanthizidae

Olive-backed Sunbird Cinnyris jugularis B J M P S

Golden-bellied Gerygone Gerygone sulphurea B J M P S

Lovely Sunbird Aethopyga shelleyi P

Woodshrikes & Allies Tephrodornithidae

Handsome Sunbird Aethopyga bella P

Bar-winged Flycatcher-shrike Hemipus picatus B M S

White-flanked Sunbird Aethopyga eximia J *

Black-winged Flycatcher-shrike Hemipus hirundinaceus B J M S

**

Black-throated Sunbird Aethopyga saturata M

Large Woodshrike Tephrodornis virgatus B J M S

Crimson Sunbird Aethopyga siparaja B J M S

Rufous-winged Philentoma Philentoma pyrhoptera B M S **

Javan Sunbird Aethopyga mystacalis J *

Maroon-breasted Philentoma Philentoma velata B J M S ** Temminck's Sunbird Aethopyga temminckii B M S **

Bristlehead Pityriaseidae

Little Spiderhunter Arachnothera longirostra B J M S

Bristlehead Pityriasis gymnocephala B *

Pale Spiderhunter Arachnothera dilutior P *

Woodswallows and Allies Artamidae

Thick-billed Spiderhunter Arachnothera crassirostris B M S **

Page 35: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

White-breasted Woodswallow Artamus leucorynchus B J M P S

Long-billed Spiderhunter Arachnothera robusta B J M S **

Ioras Aegithinidae

Spectacled Spiderhunter Arachnothera flavigaster B M S

Common Iora Aegithina tiphia B J M P S

Yellow-eared Spiderhunter Arachnothera chrysogenys B J M S **

Green Iora Aegithina viridissima B M S **

Grey-breasted Spiderhunter Arachnothera modesta M S

Great Iora Aegithina lafresnayei M

Streaky-breasted Spiderhunter Arachnothera affinis J *

Cuckooshrikes Campephagidae

Bornean Spiderhunter Arachnothera everetti B *

Large Cuckooshrike Coracina macei M

Streaked Spiderhunter Arachnothera magna M

Javan Cuckooshrike Coracina javensis J

Whitehead's Spiderhunter Arachnothera juliae B *

Sunda Cuckooshrike Coracina larvata B J S

Old World Sparrows Passeridae

Bar-bellied Cuckooshrike Coracina striata B J M P S

Plain-backed Sparrow Passer flaveolus M

Lesser Cuckooshrike Coracina fimbriata B J M S *

Eurasian Tree Sparrow Passer montanus J M P S

Pied Triller Lalage nigra B J M P S

Weavers Ploceidae

White-shouldered Triller Lalage sueurii J

Asian Golden Weaver Ploceus hypoxanthus J

Small Minivet Pericrocotus cinnamomeus J

Streaked Weaver Ploceus manyar J

Fiery Minivet Pericrocotus igneus B M P S ** Baya Weaver Ploceus philippinus J M S

Grey-chinned Minivet Pericrocotus solaris B M S

Waxbills Estrildidae

Sunda Minivet Pericrocotus miniatus J S

Red Avadavat Amandava amandava J

Scarlet Minivet Pericrocotus speciosus B J M S

Tawny-breasted Parrotfinch Erythrura hyperythra B J M S

Whistlers Pachycephalidae

Pin-tailed Parrotfinch Erythrura prasina B J M S

Mangrove Whistler Pachycephala cinerea B J M P S

White-rumped Munia Lonchura striata M S

White-vented Whistler Pachycephala homeyeri B

Javan Munia Lonchura leucogastroides J S **

Bornean Whistler Pachycephala hypoxantha B *

Dusky Munia Lonchura fuscans B *

Rusty-breasted Whistler Pachycephala fulvotincta J

Black-faced Munia Lonchura molucca J

Shrikes Laniidae

Scaly-breasted Munia Lonchura punctulata J M P S

Long-tailed Shrike Lanius schach B J M P S

White-bellied Munia Lonchura leucogastra B J M P S

**

Vireos & Greenlets Vireonidae

Black-headed Munia Lonchura malacca B

White-bellied Erpornis Erpornis zantholeuca B M S

White-capped Munia Lonchura ferruginosa J *

Pied Shrike-babbler Pteruthius flaviscapis J *

Chestnut Munia Lonchura atricapilla J M P S

Blyth's Shrike-babbler Pteruthius aeralatus M S

White-headed Munia Lonchura maja J M S

Black-eared Shrike-babbler Pteruthius melanotis M

Java Sparrow Lonchura oryzivora J *

Trilling Shrike-babbler Pteruthius aenobarbus J *

Wagtails & Pipits Motacillidae

Orioles Oriolidae

Paddyfield Pipit Anthus rufulus J M P S

Dark-throated Oriole Oriolus xanthonotus B J M P S

Finches Fringillidae

Black-naped Oriole Oriolus chinensis B J M P S

Brown Bullfinch Pyrrhula nipalensis M

Black-hooded Oriole Oriolus xanthornus B M S

Mountain Serin Chrysocorythus estherae J S

Black Oriole Oriolus hosii B *

Page 36: Return to the Malay Archipelago: the biogeography of Su ndaic …lithornis.nmsu.edu/~phoude/Sheldon et al 2015 Return to... · 2019-01-10 · Return to the Malay Archipelago: the

Black-and-crimson Oriole Oriolus cruentus B J M S **

Gill F, Donsker D)2014) IOC World Bird List (v 4.4). URL http://www.worldbirdnames.org/

MacKinnon JR, Phillipps K (1999) A field guide to the birds of Borneo, Sumatra, Java and Bali. Oxford University Press

Phillipps Q, Phillipps K (2014) Phillipps' Field Guide to the Birds of Borneo, Third Edition. John Beaufoy, Oxford

Van Marle JG, Voous KH (1988) The birds of Sumatra. British Ornithologists' Union, Tring, Herts, United Kingdom

Wells DR (1999) The Birds of the Thai-Malay Peninsula. Vol. 1. Non-passeries. Academic Press, New York

Wells DR (2007) The Birds of the Thai-Malay Peninsula, Volume 2, Passerines. Christopher Helm, London, 800 pp

View publication statsView publication stats