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GR focus review
Bearing up well? Understanding the past, present and future of
Australia's koalas
Karen H. Black
a,
⁎, Gilbert J. Price
b
, Michael Archer
a
, Suzanne J. Hand
a
a
School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia
b
Department of Earth Sciences, University of Queensland, St Lucia, Queensland 4072, Australia
abstractarticle info
Article history:
Received 20 October 2013
Received in revised form 17 December 2013
Accepted 22 December 2013
Available online 30 December 2013
Handling Editor: M. Santosh
Keywords:
Phascolarctidae
Cenozoic
Species diversity
Faunal change
Vombatiformes
The modern Koala Phascolarctos cinereus is the last surviving member of a once diverse family Phascolarctidae
(Marsupialia, Phascolarctomorphia). Nine genera and at least 16 species of koala are known. Late Oligocene sed-
iments of central Australiarecord the oldest fossils and highest species diversity.Five species are known from the
early to middle Miocene rainforest assemblages of the Riversleigh World Heritage Area, Queensland. With the
onset of dryer conditions after the middle Miocene climatic optimum (~16 Ma), rainforest habitats contracted
resulting in the apparent extinction of three koala lineages (Litokoala,Nimiokoala,Priscakoala). Phascolarctos
first appears in the fossil record during the Pliocene and the modern species around 350 ka. Despite a dramatic
decline in taxonomic diversity to a single extant species, the fossil record indicates that at most only three koala
species coexisted in any given faunal assemblage throughout their 24 million year history. Within these assem-
blages, the vast majority of extinct koalas are extremely rare (some known from only a single specimen) which
may reflect a general rarity within their palaeohabitats compared with the modern species which is represented
by an estimated400,000 individuals spread over most of eastern mainland Australia. Be that as it may, P.cinereus,
although once geographically more widespread, occurring for example in Western Australia in the Pleistocene,
underwent significant range contractions and localized population extinctions during the stressful climatic con-
ditions of the late Pleistocene and more recently through human-induced habitat destruction. Combined with
threats of disease, reduced genetic diversity and climate change, the survival of this iconic Australian marsupial
is arguably a cause for concern.
© 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
Contents
1. Introduction............................................................. 1187
2. Koalaevolution,diversityandpalaeoecology .............................................. 1188
2.1. Koalaoriginsandevolutionaryrelationships ........................................... 1188
2.2. Thekoalafossilrecord ..................................................... 1188
2.2.1. Koala-likemarsupials ................................................. 1188
2.2.2. Speciesboundariesinfossilkoalas ........................................... 1190
2.2.3. Evolutionofthemodernkoala ............................................. 1191
2.3. Palaeoecology ........................................................ 1192
2.4. Diversitythroughtime..................................................... 1193
3. Discussion ............................................................. 1194
3.1. Koaladiversityinaclimaticallychangingworld ......................................... 1194
3.2. Pleistocenedistributionandpopulationconnectivityofthemodernspecies ............................. 1195
3.3. Historic factors influencingthegeographicrangeofthekoala ................................... 1196
3.4. Thepotentialimpactoffutureclimatechangeonkoalapopulations ................................ 1197
3.5. Currentstatusofkoalapopulations ............................................... 1197
4. Conclusions ............................................................. 1197
Acknowledgements ............................................................ 1198
References ................................................................ 1198
Gondwana Research 25 (2014) 1186–1201
⁎Corresponding author.
E-mail addresses: k.black@unsw.edu.au (K.H. Black), g.price1@uq.edu.au (G.J. Price), m.archer@unsw.edu.au (M. Archer), s.hand@unsw.edu.au (S.J. Hand).
1342-937X/$ –see front matter © 2013 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.gr.2013.12.008
Contents lists available at ScienceDirect
Gondwana Research
journal homepage: www.elsevier.com/locate/gr
Author's personal copy
1. Introduction
The koala family Phascolarctidae (Diprotodontia, Vombatiformes) has
one of the longest fossil records of any of Australia's modern marsupial
families, dating back some 24 million years. Today it is represented by a
single species, Phascolarctos cinereus (Goldfuss, 1817), Australia's largest
extant arboreal folivore. Yet the family was once far more morphological-
ly and ecologically diverse, albeit the number of recognised genera and
species has been the subject of much controversy with anywhere be-
tween eight and ten genera and 13 and 22 species recognised (see
Louys et al., 2007; Pledge, 2010; Black et al., 2012a; Price, 2012; Black
et al., 2013a). This is largely due to the rarity and poorly preserved nature
of fossil koala material. Many taxa are named on the basis of isolated teeth
or at best dentitions (Black, 1999). Only three extinct species are known
from cranial material (Black, and Archer, 1997b; Louys et al., 2007,
2009; Black et al., 2013a) and not one is known from elements of
the postcranial skeleton. Unsurprisingly, accurate assessment of the
palaeodiversity and palaeoecology of phascolarctids is challenging, and
has presented a significant hurdle to understanding the evolution of the
koala lineage and its response to past environmental change.
The modern genus has a fossil record dating back to the late Miocene
or Pliocene (Pledge, 1992) of South Australia and the modern species to
350 ka, with numerous Quaternary records in all states except
Tasmania and the Northern Territory (Price, 2008a). Today, P. cinereus
occupies temperate, sub-tropical and tropical forests and moist to
semi-arid woodlands from northeastern Queensland to the southeast-
ern corner of South Australia (Fig. 1). Over its range, it feeds on the
leaves of more than 70 Eucalyptus species and 30 non-eucalypt species
(Moore and Foley, 2000; Lunney et al., 2009). However, within any spe-
cific area it has a highly selective diet of only a handful of primary food
tree species with individual tree selection dependant on a number of
variables that vary regionally, including leaf chemistry, leaf water con-
tent, and tree structure (Martin and Handasyde, 1999; Lunney et al.,
2009). Because of this, the koala is regarded to be a specialist folivore
and as such, deemed highly susceptible to environmental change (e.g.
Harcourt et al., 2002; IUCN, 2013; Smith et al., 2013).
Here we review current understanding about the evolution and
deep time changes in diversity of phascolarctids, as well as historic
and current challenges facing the living Koala in order to anticipate
how this lineage may respond to future climate change.
Fig. 1. Map of Australia indicatingfossil depositscontaining koalasand the current (including translocation sites) and historic geographical distribution of the modern koala,Phascolarctos
cinereus. Abbreviations: L, lake; LF, Local Fauna; NSW, New SouthWales; NT, Northern Territory; QLD, Queensland; SA, South Australia; TAS, Tasmania; VIC, Victoria; WA, Western
Australia. After Price (2012) and Black et al. (2013a).
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2. Koala evolution, diversity and palaeoecology
2.1. Koala origins and evolutionary relationships
Since the first sighting of the living koala by Europeans in 1798, this
marsupial has been somewhat of an enigma. Originally thought to re-
semble monkeys or sloths (Bladen, 1895), it was tenuously linked to
placental mammals until closer examination revealed numerous fea-
tures shared with marsupials and, in 1886, Richard Owen placed the
genus Phascolarctos in the then marsupial Suborder Diprotodontia.
On the basis of morphology (e.g., forcipate hand in which the first
two digits oppose the other three; and selenodonty, where molars are
characterised by crescent-shaped crests), early authors (e.g., Gill,
1872; Bensley, 1903; Jones, 1923; Simpson, 1945; Ride, 1964) included
the koala asa highly specialised possum in the broadly conceived family
Phalangeridae, noting particular affinities to ringtail possum species of
the genus Pseudocheirus and the Greater Glider Petauroides volans.
These shared features have since been regarded to be convergently de-
veloped (e.g., Kirsch, 1977; Strahan, 1978) or plesiomorphic within
Diprotodontia (Archer, 1978; Weisbeckerand Archer, 2008) and of little
use in determining koala affinities.
Sonntag (1921) suggested a close affinity between koalas and wom-
bats on the basis of more detailed anatomical studies, a relationship that
is now well supported by numerous biological systems including serol-
ogy (e.g., Kirsch, 1968, 1977; Baverstock et al., 1987, 1990), sperm mor-
phology and soft tissue anatomy (e.g., Hughes, 1965; Yadav, 1973;
Harding et al., 1987), nuclear and mitochondrial DNA (Burk et al.,
1999; Amrine-Madsen et al., 2003; Kavanagh et al., 2004; Beck, 2008;
Phillips and Pratt, 2008), and morphology (e.g., Archer, 1976a, 1978;
Szalay, 1982; Horovitz and Sánchez-Villagra, 2003). It is not surprising
that Cardillo et al.'s (2004) analysis, which combined 158 phylogenetic
estimates published since 1980 to build a marsupial phylogenetic
supertree, also saw koalas and wombats forming a monophyletic clade
at the base of the diprotodontian radiation (Fig. 2A).
Modern classifications differ in the precise taxonomic relationship be-
tween koalas and wombats. Archer (1976a, 1978) and Kirsch (1977)
formalised the grouping of Phascolarctidae and Vombatidae within the
superfamily Vombatoidea. Woodburne (1984) established separate su-
perfamilies (Vombatoidea and Phascolarctoidea) within the suborder
Vombatiformes in recognition of a closer relationship between vombatids
and a number of extinct families (e.g., the Ilariidae, Wynyardiidae,
Maradidae, Thylacoleonidae, Palorchestidae and Diprotodontidae) rela-
tive to phascolarctids. Aplin and Archer (1987) continued to use the sub-
order Vombatiformes but erected the infraorders Phascolarctomorphia
(containing Phascolarctidae) and Vombatomorphia (containing
Vombatidae as well as six entirely extinct families) to reflect a greater
degree of separation between the two (Fig. 2B).
Recent molecular studies suggest that phascolarctids diverged from
vombatids during the late Eocene around 35–40 Ma (Nilsson et al.,
2004; Beck, 2008; Meredith et al., 2008, 2009a,b). Fossil evidence in sup-
port of these divergence times has not yet been found. The Australian
marsupial fossil record is unknown between 55 and 26 Ma, and there
are no diprotodontians recorded from Australia's oldest marsupial
fossil-bearing deposit, the 55 Ma Tingamarra Local Fauna of southeastern
Queensland (Godthelp et al., 1992). Representatives of all vombatiform
families are known from late Oligocene deposits in Queensland, the
Northern Territory and/or South Australia (Woodburne et al., 1993;
Myers and Archer, 1997; Pledge, 2005; Archer et al., 2006; Murray and
Megirian, 2006; Black, 2007, 2010) including the oldest phascolarctids,
24 million-year-old species of Madakoala,Perikoala,Nimiokoala and
Litokoala from the Etadunna Formation of South Australia (Springer,
1987; Woodburne et al., 1987; Black and Archer, 1997b).
The once ecologically and morphologically diverse vombatiforms
(e.g., marsupial lions, trunked palorchestids, Diprotodon) were repre-
sented by N60 species including carnivorous, herbivorous, terrestrial
and arboreal forms ranging in size from 3 kg to 2.5 tonnes (Black
et al., 2012b), yet only two families represented by four species have
survived into modern times (the koala and three species of wombat).
Understanding the nature of such a decline by analysing deep-time
changes in diversity using the fossil record is critical for conserving
the remaining species within the suborder and is particularly relevant
in the face of current debate over whether the koala should be given en-
dangered species status. Koala selenodont molar morphology has also
been argued by some (e.g., Archer, 1976a) to be close to or indicative
of the ancestral pattern for all other diprotodontian marsupials. As
such, there is further reason for focusing on the evolutionary history
and relationships of this ancient group of Australian mammals which
just may have been the foundation for the subsequent evolution of the
vast majority of Australia's herbivorous marsupials.
2.2. The koala fossil record
Despite theextended fossil record of koalas, their pre-Pleistocenere-
cord, compared with better known vombatomorphian families such as
Diprotodontidae (e.g., Stirton et al., 1967; Black, 1997; Black and
Archer, 1997a; Black and Mackness, 1999; Murray et al., 2000; Black,
2010; Black and Hand, 2010; Black et al., 2012c, 2013b), is very poor
and geographically restricted. This is particularly true for the geological-
ly oldest koalas from South Australia, discovered as early as 1953
(Stirton, 1955). Some fossil koala genera (Table 1)suchasLitokoala,
Nimiokoala and Phascolarctos have a relatively extensive geographic
range, yet most are restricted in distribution, with many species (e.g.,
Invictokoala monticola,Madakoala devisi,Litokoala garyjohnstoni,Koobor
spp.) known from single deposits.
This rarity in fossil assemblages may not necessarily be an artefact of
preservation but may actually reflect a general rarity of koalas in
Australia's ancient forests, with other arboreal folivores such as ringtail
possums (pseudocheirids) displaying greater abundance and diversity
over the entire early Miocene to Holocene interval (see Black et al.,
2012b; table 3). Currently, the fossil record of extinct koala species com-
prises only 163 specimensfrom 58 deposits, with more than one third of
those specimens (n = 55) attributable to a single species; Nimiokoala
greystanesi, from the early to middle Miocene deposits of the Riversleigh
World Heritage Area.
The first fossil koala, Perikoala palankarinnica Stirton, 1957,was
named on the basis of a partial lower jaw from the Ditjimanka Local
Fauna of South Australia. Since that initial discovery, on average one to
two koala species have been described each decade (Table 1). Of
these, ten were named on the basis of a single specimen and four of
those on the basis of a single tooth (Ph. maris,L. kutjamarpensis,
L. thurmerae,K. jimbarratti). The paucity of fossil specimens for so
many taxa has led to problems concerning species identification and
taxonomic inflation within the family (Black et al., 2013a) with the
number of known phascolarctids varying significantly between 13 and
22 species across eight to ten genera. Three major areas of systematic
conflict have been identified and are discussed below: (1) inclusion of
the koala-like Koobor within Phascolarctidae; (2) species boundaries
in koala lineages such as Litokoala; (3) speciation and morphological dif-
ferentiation within the modern genus Phascolarctos.
2.2.1. Koala-like marsupials
Although koalas (modern and fossil) are clearly characterised by as-
pects of their selenodont dentitions, koala-like marsupials referred to
the genus Koobor are not easily pigeon-holed. Controversy regarding the
Fig. 2. Phylogenetic relationships of koalasA, between modernfamilies of the marsupial SuperorderAustralidelphia(based on the nucleargene sequence data of Meredith et al., 2009a); B,
within themostly extinct marsupial Suborder Vombatiformes (based on relationships obtainedby Black et al., 2012a). Phascolarctidaeoccupies a basal position with both Vombatiformes
and the marsupial Order Diprotodontia. Abbreviations: †, extinctfamilies; L.CRET, late Cretaceous; MZ, Mesozoic;Oligo, Oligocene;Paleo, Paleocene; Pl, Pliocene.After Black et al. (2012b).
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placement of the enigmatic Pliocene Koobor within Phascolarctidae and
even Phascolarctomorphia has been long-standing (Black, 1999). Origi-
nally interpreted to be possums (De Vis, 1889) and then reinterpreted
to be koalas (e.g., Archer, 1976b, 1977), subsequent authors have sug-
gested that species of Koobor may either share affinities with Oligo-
Miocene ilariids (a group of terrestrial, selenodont vombatiforms) (e.g.,
Pledge, 1987; Tedford and Woodburne, 1987), or may even be more ap-
propriately placed in a separate family within Vombatomorphia (Myers
and Archer, 1997). The confusion lies in the fact that both species, Koobor
notabilis (De Vis, 1889; Archer, 1976b)andK. jimbarratti Archer, 1977,
from the Queensland Chinchilla and Bluff Downs Local Faunas respective-
ly, are known solely from elements of their upper dentitions. However,
synapomorphies of phascolarctids are confined to features of the lower
dentition with the lower first molar being particularly diagnostic (Black
et al., 2012a). Aplin and Archer (1987) suggested that Koobor should be
regarded as Vombatiformes incertae sedis until more complete fossil ma-
terial is recovered. This classification has been followed by subsequent au-
thors (e.g., Black, 1999; Myers et al., 1999; Long et al., 2002). Despite the
absence of lower dentitions, Black et al. (2012a), in their phylogenetic
analysis of Vombatiformes using cranio-dental material, found that
Koobor consistently grouped within Phascolarctidae. Although that
interpretation was the most parsimonious based on available fossil evi-
dence (i.e., features of the upper dentition), the results are viewed with
caution because the two dental synapomorphies found for
Phascolarctidae are features of the first lower molar which is as yet un-
known for either of the species of Koobor (Black et al., 2012a).
2.2.2. Species boundaries in fossil koalas
The problem of determining species boundaries in fossil lineages has
been a perennial challenge for palaeontological systematists. In
phascolarctids, this problem is exacerbated because of the paucity of
the fossil record. The genus Litokoala is a prime example, with the holo-
types for three species, Litokoala kutjamarpensis,Litokoala kanunkaensis
and Litokoala thurmerae from South Australia, consisting of single, dis-
parate, isolated molars (upper first molar, lower second molar, and
upper third molar, respectively). Although six species of Litokoala have
been described (Table 1), only three are currently considered to be
valid taxa (Black et al., 2013a).
The discovery of partial fossil crania referable to Litokoala
(Fig. 3A–B) from the Riversleigh World Heritage Area, Queensland,
has played a critical role in resolving taxonomic confusion within
the genus (Louys et al., 2007, 2009; Black et al., 2013a). For example,
Table 1
Distribution, age and taxonomic statusof extinct koalas.Koala species considered taxonomically valid in thispaper are listedin bold. Type localities are those listedfirst under Distribution.
Abbreviations: ?, uncertain; E, early; Fm,Formation; FZ, Faunal Zone; L, late; LF,Local Fauna; M, middle;NMV, National Museum of Victoria; QML, Queensland Museum Locality; RV, Riv-
erside; SAM, South Australian Museum; UCR, University of California Riverside; UNSW, University of New South Wales.
Taxon Distribution Age Taxonomic status
Cundokoala yorkensis Pledge, 1992 Corra Lynn Cave, Curramulka LF, S.A.; Wellington
Caves, N.S.W.
?L. Miocene–Pleistocene Referred to Phascolarctos
(Black and Archer, 1997b)
Invictokoala monticola Price,2011 Site QML 1311, Speaking Tube Cave, Mt Etna, Qld M. Pleistocene Valid
Koobor notabilis (DeVis, 1889) Chinchilla Rifle Range, Chinchilla, Darling Downs, Qld Pliocene Valid species. Questionably a phascolarctid
Koobor jimbarratti,Archer, 1976b Bluff Downs, Bluff Downs LF, Qld E. Pliocene Valid species. Questionably a phascolarctid
Litokoala kutjamarpensis Stirton et al., 1967 Leaf Locality, Kutjamarpu LF, Lake Ngapakaldi,
Wipajiri Fm; Kanunka North Site, Lake Kanunka,
Etadunna Fm, S.A.; Jim's Carousel, Henk's Hollow,
Dwornamor, and Gotham Sites, FZC, Riversleigh, Qld
L. Oligocene–M. Miocene Valid
Litokoala kanunkaensis Springer, 1987 Kanunka North Site, Kanunka North LF, Lake
Kanunka, Etadunna Fm, S.A.
L. Oligocene Junior synonym of L. kutjamarpensis
(Louys et al., 2007, 2009; Black et al., 2013a)
Litokoala garyjohnstoni Louys et al., 2007 Outasite Site, Riversleigh FZ B, Qld E. Miocene Valid
Litokoala dicktedfordiPledge, 2010 Jim's Carousel Site, Riversleigh FZ C, Qld M. Miocene Junior synonym of L. kutjamarpensis
(Louys et al., 2007, 2009; Black et al., 2013a)
Litokoala thurmerae Pledge, 2010 Ngama Quarry, Mammalon Hill, Ngama LF, Lake
Palankarinna, Etadunna Fm, S.A.
L. Oligocene Nomen dubium (Black et al., 2013a)
Litokoala dicksmithi Black et al., 2013a Ross Scott Orr Site, FZ B, Riversleigh Qld E. Miocene Valid
Madakoala devisi Woodburne et al., 1987 Lake Pinpa Site D and SiteC, Billero Creek Site3, NMV
Locality North Pinpa, Pinpa Fauna, Namba Fm, S.A.;
Ericmas Quarry, Ericmas Fauna; and Tom O's Quarry,
Tarkarooloo Fauna, Namba Fm, S.A.
L. Oligocene Valid
Madakoala wellsi Woodburne et al., 1987 Ericmas Quarry, Ericmas Fauna, Lake Namba, Namba
Fm, S.A.
L. Oligocene Valid
Madakoala.sp.aff.M. wellsi Woodburne et al., 1987 Tedford Locality; QML SAM Quarry North,Ditjimanka
LF, Lake Palankarinna, Etadunna Fm, S.A.
L. Oligocene Questionably distinct from M. wellsi
(Woodburne et al., 1987)
Madakoala sp. Woodburne et al., 1987 NMV Locality, Wadikali LF, Namba Fm, SA L. Oligocene Questionably distinct from M. wellsi
(Woodburne et al., 1987)
Nimiokoala greystanesi Black and Archer, 1997b Neville's Garden Site, FZ B, Riversleigh, Qld;
Numerous sites from FZ B and FZ C, Riversleigh, Qld
E.–M. Miocene Valid
Nimiokoala sp. Black and Archer, 1997b South Prospect B Locality, Lake Namba, Namba Fm,
S.A.
L. Oligocene Questionably distinct from N. greystanesi
(Black and Archer, 1997b)
Perikoala palankarinnica Stirton, 1957 SAM Quarry North Locality, Tedford Locality, Tedford
Locality East, White Sands Basin Locality; Ditjimanka
LF, Lake Palankarinna, Etadunna Formation, S.A.
L. Oligocene Valid
Perikoala robustus Woodburne et al., 1987 UCR RV-8504,‘Perikoala Max.’(RV-8505) and ‘UNSW
Croc. Pot 8’Localities, Palankarinna South LF, Lake
Palankarinna, Etadunna Formation, S.A.
L. Oligocene Valid
Phascolarctos stirtoni Bartholomai, 1968 Cement Mills, Gore, Qld; Nelson Bay LF, Vic.; Spring
and Fossil Chambers, Victoria Fossil Cave, S.A.; ?
Chinchilla and ?Marmor LFs, Qld.
Pliocene–Pleistocene Questionably distinct from P. cinereus
(Archer and Hand, 1987)
Phascolarctos maris Pledge, 1987 200 m upstream from theSunlands PumpingStation,
Sunlands LF, Loxton-Parilla Sands, S.A.
?E. Pliocene–Pleistocene Questionably distinct from P. cinereus
and P. stirtoni
Phascolarctos yorkensis (Pledge, 1992) Corra Lynn Cave, Curramulka LF, S.A.; Wellington
Caves, N.S.W.
?L. Miocene–Pleistocene Valid, formerly Cundokoala yorkensis
Priscakoala lucyturnbullae Black et al., 2012 Creaser's Ramparts, Camel Sputum, and Cadbury's
Kingdom Sites, FZ B, Riversleigh, Qld
E. Miocene Valid
Encore n. gen. et sp. Encore Site, FZ D, Riversleigh, Qld Early L. Miocene Phascolarctos sp. of (Myers et al., 2001)
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based on the com plete tooth rows preserv ed in a Riversleigh cranium
representing L. kutjamarpensis (Fig. 3A), Louys et al. (2007) demonstrat-
ed that the features originally argued (Springer, 1987) to distinguish
L. kanunkaensis from L. kutjamarpensis were actually intraspecificmeris-
tic differences along the tooth row of the latter. Pledge (2010) erected a
new species for the Riversleigh cranium noted above, L. dicktedfordi.He
also named a new species, L. thurmerae, on the basis of a single well-
worn and abraded upper third molar.
Most recently, Black et al. (2013a) described a new Litokoala species,
L. dicksmithi (Fig. 3B), in conjunction with a general review of the genus
and a detailed analysis of intraspecific morphological and metric variation
in the modern P. cinereus. Their results indicated considerable
intraspecific variation in dental structures of the modern species, some
of which are features previously considered to distinguish one fossil spe-
cies from another. On the basis of their observations, they confirmed
Louys et al.'s (2007) synonomy of L. kanunkaensis with L. kutjamarpensis.
Additionally, Black et al. (2013a) found insufficient evidence to support
the taxonomic distinction of either L. dicktedfordi or L. thurmerae,suggest-
ing that the former was synonymous with L. kutjamarpensis, as originally
proposed by Louys et al. (2007, 2009), and that the latter be regarded as a
nomen dubium.
2.2.3. Evolution of the modern koala
The modern koala genus Phascolarctos appears to have originated
during the late Miocene with two species (P. maris and P. yorkensis)
recorded from late Miocene–early Pliocene deposits of South Australia
(Table 1). Previously, the oldest record of Phascolarctos was a fragmentary
upper molar from the early late Miocene Encore Local Fauna of
Riversleigh (Myers et al., 2001). However, in light of new material from
that deposit, including a complete lower molar and upper premolar, the
Encore koala appears to represent a new genus that is the sister taxon
to Phascolarctos.
Currently, three extinct species of Phascolarctos,Phascolarctos maris,
Phascolarctos stirtoni and Phascolarctos yorkensis (formerly Cundokoala
yorkensis Pledge, 1992), are known. They differ mostly on the basis of
size with dentitions 15%, 15–30%, and 50–65% larger, respectively,
than mean values for modern P. cinereus populations (Black et al.,
2013a). Because of the absence of significant differences in dental mor-
phology between P. yorkensis and species of Phascolarctos,Cundokoala
has since been regarded by Black and Archer (1997b) to be a junior syn-
onym of Phascolarctos.
The specific distinction of P. stirtoni and P. maris from each other, and
from P. cinereus, has been the subject of much debate (e.g., Archer and
Hand, 1987; Pledge, 1987; Black, 1999; Piper, 2005; Price, 2008a). Few
morphological features distinguish the species (Pledge, 1987; Black,
1999; Piper, 2005) and those previously noted (e.g., Bartholomai, 1968;
Pledge, 1987; Price, 2008a; Price et al., 2009) appear to fall within the
range of variation exhibited in the dentitions of the living species (see
Black et al., 2013a). Morphological comparisons between P. stirtoni and
P. maris cannot be made directly because the former is known from its
upper dentition and the latter from an isolated lower molar. Consequent-
ly, Pledge (1987) distinguished P. maris from P. stirtoni on the basis of its
smaller size and much older geological age. However, the degree of tem-
poral separation between the species is unclear and in any case irrelevant
for the purposes of taxonomic distinction. The stratigraphic provenance
of the P. maris holotype within the late Miocene–late Pliocene (~6–
2 Ma; Paine, 2005) Loxton-Parilla Sands, South Australia, is uncertain
(Price, 2008a). Similarly, the exact age of the type locality of P. stirtoni
(Cement Mills, Qld) is unknown with U/Th dates providing only a mini-
mum age of N53 ka for the deposit (Price et al., 2009). Further,
P. stirtoni has since been recognised from deposits spanning the middle
Pliocene to late Pleistocene (Moriarty et al., 2000; Reed and Bourne,
2000; Piper, 2005; Prideaux et al., 2007; Price, 2008a; Price et al., 2009).
Discovery of a partial upper tooth row from the early Pleistocene
Nelson Bay LF of Victoria that is comparable in size to P. maris yet mor-
phologically indistinguishable from P. stirtoni (Piper, 2005; Price,
2008a) suggests that size is not a valid diagnostic feature distinguishing
these species. Piper (2005) tentatively assigned the specimen to P. sp. c f.
P. stirtoni based on morphological similarities, but noted that like
P. maris its molars were 10% smaller than the P. stirtoni holotype. Price
(2008a) subsequently referred the specimento P. stirtoni without ambi-
guity, noting that those differences in size, based on comparison with
size variation in the living species, would fall within the range of mor-
phometric variation expected for P. stirtoni.
Some authors (e.g., Archer and Hand, 1987)havesuggestedthat
P. stirtoni and P. cinereus may be conspecific and the modern species is
the end point of a dwarfing lineage that began between the late Pleisto-
cene and Recent. Price (2008a) challenged this view noting that
Fig. 3. Exceptionally well-preserved fossil koala cranial material from the Riversleigh
World Heritage Area, northwestern Queensland. A, Litokoala kutjamarpensis (QM F
51382, ventral view) from Jim's Carousel Site, Faunal Zone C; B, Comparison of the partial
skull of Litokoala dicksmithi (left) from Ross Scott-Orr Site (Faunal Zone B) with a skull of
the extant koala Phascolarctos ci nereus (right); C, the relatively possum-like skull of
Nimiokoala greystanesi from Boid Site East Site. Estima ted body weights of sp ecies of
Litokoala and Nimiokoala (Table 2)wereonly1/4–1/2 the size of mean values of modern
P. cinereus individuals from Victorian and Queensland populations, respectively. Scale
bars = 1 cm.
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P. stirtoni and P. cinereus potentially occurred sympatrically in middle
Pleistocene deposits within Victoria Fossil Cave in the Naracoorte region
of South Australia. However, it has been suggested by others that these
deposits are likely temporally mixed and sample taxa across several gla-
cial–interglacial cycles (Moriarty et al., 2000)from280to500 ka(Grün
et al., 2001). If that is the case, the species may not have actually
coexisted. A new systematic review of all fossil material referred to
Phascolarctos would help to resolve these uncertainties.
Within the modern species, a latitudinal trend in body size is evi-
dent, with southern (i.e., Victorian) koalas being on average 80% larger
(e.g., mean male body weight 11.8 kg) than their northern (i.e., Queens-
land) counterparts (e.g., mean male body weight 6.5 kg) (Strahan,
2004). There are also obvious variations in body form throughout the
latitudinal cline, including differences in pelage colour and thickness,
and muzzle shape (Lee and Martin, 1988). Although many early taxon-
omists recognised threesubspecies, the distinctions were arbitrarily de-
fined by state borders rather than consistent biological differences
between populations (Lee and Martin, 1988; Sherwin et al., 2000;
Strahan, 2004). Those former subspecies included P. cinereus victor
(Troughton, 1935) from Victoria, P. c. cinereus (Goldfuss, 1817) from
New South Wales, and P. c. adustus (Thomas, 1923) from Queensland.
More recent genetic studies (e.g., Takami et al., 1998; Houlden et al.,
1999) do not support subspecies distinction, rather the morphological
differences between northern and southern populations represent the
limits of a gradual latitudinal cline (Sherwin et al., 2000; Strahan,
2004)reflecting Bergmann's Rule (Mayr, 1956).
2.3. Palaeoecology
Extinct koalas, like the modern species, are characterised by
selenodont dentitions adapted for cutting leaves, and consequently are
interpreted to have been arboreal folivores. A range of body sizes is evi-
dent (Table 2) with many of the oldest and/or most plesiomorphic koalas
(e.g., species of Madakoala,Perikoala,Koobor,Invictokoala and Priscakoala)
falling within the size range of the modern species (4.1–13.5 kg, Strahan,
2004). Some exceptions include the more derived phascolarctids such as
the species P. stirtoni and P. yorkensis that have estimated body weights of
32.9 kg and 40.5 kg, respectively. Conversely, species of Nimiokoala and
Litokoala were comparable in size to the living Common Brushtail Possum
Trichosurus vulpecula (1.5–4.5 kg, Strahan, 2004).
Gigantism in some of the Plio-Pleistocene koalas, as well as in other
browsing marsupial lineages such as the 2.5 tonne Diprotodon, was like-
ly a response to theneed to consume greaterquantities of poorerquality
browse which resulted from the progressive drying of the Australian
continent (Price, 2008b; Price and Piper, 2009; Black et al., 2012b).
Giant koalas have long been thought to have been Australia's largest
marsupial arboreal folivores. Recently, however, it has been demon-
strated that the c. 70 kg diprotodontid Nimbadon lavarackorum was
also an arboreal herbivore (Black et al., 2012c), a species sympatric
with the much smaller N. greystanesi (Fig. 3C) in the middle Miocene
rainforests of Riversleigh.
Species of Litokoala and Nimiokoala represent the smallest-bodied
members (2.4–4.6 kg) of the diprotodontian suborder Vombatiformes.
Black et al. (2013a) suggested that the relatively small and similar
body size (Table 2) of these species may reflect the optimum size for a
koala specialising on nutrient-rich plants in Australia's early–middle
Miocene rainforests. Such koalas possess similar dentitions characterised
by a multitude of cusps and accessory shearing blades that are far more
complex than those of species of Madakoala,Perikoala,Priscakoala and
Invictokoala (Black et al., 2012a). Nimiokoala greystanesi displays the
most complex dentition of all koala species with molars reminiscent of
the complex serrated molars of Australia's extinct ektopodontid pos-
sums. The food preferences of these extinct possums are unclear, but
may have included seeds and fruits as well as leaves (Pledge, 1982). Den-
tal complexity has also been shown to be greater in folivores that special-
ise on fibrous foods (Evans et al., 2007). Consequently, N. greystanesi may
have incorporated a greater proportion of fibrous foliage (e.g., mature
leaves, different tree species) in its diet, relative to species of Litokoala
and Priscakoala. Fossils of N. greystanesi are the most common of all ex-
tinct phascolarctids which may reflect their greater abundance in early
Miocene rainforest palaeoenvironments than sympatric species such as
the much rarer Priscakoala lucyturnbullae and L. garyjohnstoni.
Despite such dental complexity, the cranio-mandibular morphology
of species of Nimiokoala and Litokoala (e.g., unfused mandibular sym-
physis, large pterygoid fossae) indicates a softer, more generalist diet
than the specialist eucalypt diet of P. cinereus (Louys et al., 2009). As a
consequence, Louys et al. (2009) suggested that the association be-
tween Phascolarctos species and eucalypts probably developed after
the divergence (Fig. 4B) of the Litokoala and Phascolarctos lineages.
The earliest probable morphological evidence for koalas specialising
on eucalypts comes from the ?late Miocene–Pliocene species
P. yorkensis and P. ‘maris’(P. stirtoni) which have dentitions morpholog-
ically indistinguishable from that of P. cinereus,hencesuggestingasim-
ilar diet.
It is noteworthy that species of Litokoala and Nimiokoala possesspro-
portionately larger orbits (Fig. 3) relative to the modern species (Black
Table 2
Body massestimates (kg) ofextinct phascolarctids based on thepredictive regression equations(diprotodontian data-set)of Myers (2001; table5) which correlatecranio-dental variables
with body size. To make body estimates more comparable between taxa, calculations were based on upper and lower third molar lengths where available. Body mass for P. stirtoni and
K. jimbarratti were calculated using second upper molar length and first upper molar width, respectively, because third molars are not known for this species. Body mass for extant
P. cinereus was taken from Strahan (2004). Abbreviations: 1UMW, first upper molar width; 2UML, second upper molar length; 3LML, third lower molar length; 3UML, third upper
molar length.
Variable x(mm) Regression Smearing estimate (%) Body mass (kg)
Phascolarctos cinereus N/A N/A N/A 4.1–13.5
Phascolarctos stirtoni 2UML (10.7) log y= 1.039 + 3.340(log x) 9.6 32.9
Phascolarctos yorkensis 3LML (12.9) log y= 1.225 + 3.019(log x) 7.1 40.5
Madakoala devisi 3UML (7.6) log y= 1.348 + 2.890(log x) 6.8 8.4
Madakoala wellsi 3LML (8.0) log y= 1.225 + 3.019(log x) 7.1 9.6
Perikoala robustus 3UML (6.4) log y= 1.348 + 2.890(log x) 6.8 5.1
Perikoala palankarinnica 3LML (6.4) log y= 1.225 + 3.019(log x) 7.1 4.9
Priscakoala lucyturnbullae 3UML (6.4) log y= 1.348 + 2.890(log x) 6.8 5.1
Litokoala kutjamarpensis 3UML (5.4) log y= 1.348 + 2.890(log x) 6.8 3.7
Litokoala garyjohnstoni 3UML (5.1) log y= 1.348 + 2.890(log x) 6.8 2.6
Litokoala dicksmithi 3UML (5.5) log y= 1.348 + 2.890(log x) 6.8 3.3
Nimiokoala greystanesi 3UML (5.7) log y= 1.348 + 2.890(log x) 6.8 3.6
Invictokoala monticola 3UML (7.5) log y= 1.348 + 2.890(log x) 6.8 8.0
Koobor notabilis 3UML (6.9) log y= 1.348 + 2.890(log x) 6.8 6.3
Koobor jimbarratti 1UMW (7.1) log y = 1.109 + 3.470(log x) 13.2 13.1
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et al., 2013a). Large orbits are strongly correlated with nocturnality in
primates (Kay and Cartmill, 1977; Kay and Kirk, 2000) and enhanced vi-
sual acuity (and hence environmental perception) among mammals
(Kiltie, 2000). Combined with their relatively small body size, this sug-
gests that species of Litokoala and Nimiokoala were far more agile than
the relatively sedentary, living species (Black et al., 2013a). Louys et al.
(2009) have argued that the opening up of Australia's forests during
the later Cenozoic would also have impacted on the social behaviour
of koalas, perhaps leading to their distinctive bellowing. Their very
large auditory bullae (Fig. 3A), and increased sensitivity to low frequen-
cy sounds, would have facilitated this means of communicating over in-
creasingly long distances.
2.4. Diversity through time
Potential sampling bias and the limited temporal resolution of the
koala fossil record make it difficult to reliably track changes in
phascolarctid diversity through time. For example, from the late Oligo-
cene through to the Pleistocene, koala species-level diversity appears to
track changes in the number of koala-bearing fossil deposits (Fig. 4A).
Hence, we can predict that during time periods underrepresented in
the fossil record (e.g., late Miocene–Pliocene), koala species diversity
was likely greater than that currently known, whereas more extensively
sampled time periods (e.g.,the Quaternary) are expected to more accu-
rately reflect true koala diversity. Nevertheless, broad-scale changes in
koala diversity (Fig. 4A–B) can be obtained by combining direct evi-
dence from the fossil record with understanding of phylogenetic rela-
tionships within the family (Price, 2008). Here, we recognise 16
species within nine genera (Table 1) based on the following taxonomic
assumptions: three valid species in Litokoala (L. kutjamarpensis,
L. garyjohnstoni,L. dicksmithi) following Black et al. (2013a); three spe-
cies in Phascolarctos (P. cinereus,P. stirtoni, P. yorkensis) with Cundokoala
a junior synonym of Phascolarctos and P. maris a junior synonym of
P. stirtoni, following Black and Archer (1997b),Black (1999) and Price
(2008a, 2012); and the two species of Koobor (K. notabilis,
K. jimbarratti) recognised as phascolarctids, following Black et al.
(2012a). Additional unnamed but potentially distinct taxa (e.g.,
Madakoala sp., Woodburne et al., 1987;Nimiokoala sp., Black and
Fig. 4. Trends in phascolarctiddiversity throughout the Cenozoic. A, comparison of the number of koala-bearing fossildeposits (right y-axis), with changes in known generic and species-
level diversity, and the maximumnumber of koala species within any given faunal assemblage (left y-axis) since the late Oligocene; B, stratocladogram of phascolarctid relationships. In-
tergeneric relationshipsare modified from thosepresented in Blacket al. (2012a). Intraspecific relationships of Litokoalaare based on those of Blacket al. (2013a). Abbreviations: L, late; LF,
Local Fauna; P,Phascolarctos; Oligo., Oligocene; Pleist., Pleistocene.
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Archer, 1997b) are not treated here as distinct speciesbecause of doubts
about their status. However, Nimiokoala sp. in late Oligocene deposits
does provide evidence for theexistence of this highly distinctive lineage
in pre-Miocene deposits (see below).
The most plesiomorphic koala currently known is the early Miocene
Riversleigh species Pr. lucyturnbullae, although it is not geologically the
oldest (Table 1). The relationships of species of Madakoala,Koobor and
Invictokoala to each other and other phascolarctids are unresolved, a con-
sequence of the relatively limited fossil material available for the latter
two. On the basis of dental similarities, Price and Hocknull (2011) sug-
gested the middle Pleistocene I. monticola is the sister taxon to species
of Madakoala. However, the shared features regarded as synapomor-
phies in that paper appear (Black et al., 2012a) to be plesiomorphic with-
in Phascolarctidae and hence not indicative of a clade. The simple,
plesiomorphic dentitions of I. monticola (Price and Hocknull, 2011)and
species of Koobor (Black et al., 2012a) belie their relatively young geolog-
ical ages (middle Pleistocene and Pliocene, respectively) which suggest
these lineages may have actually diverged from other phascolarctids
sometime prior to the Miocene. Alternatively, their plesiomorphic denti-
tions may be secondarily derived rather than a reflection of an early di-
vergence from the koala evolutionary tree, which is in keeping with
the absence of either lineage in pre-Pliocene deposits. Resolution of the
relative positions of I. monticola and species of Koobor to other
phascolarctids requires discovery of additional fossil material, in particu-
lar lower dentitions.
During the late Oligocene six species and four genera are document-
ed in the fossil record (Fig. 4A–B): Madakoala (Madakoala wellsi,
Madakoala devisi), Perikoala (P. palankarinnica,P. robustus), Litokoala
(L. kutjamarpensis), and Nimiokoala (Nimiokoala sp.). Depending on
the resolution of the unresolved polychotomy evident in Fig. 4Bitis
possible that at least nine species and seven generically distinct
phascolarctid lineages were present during the late Oligocene, includ-
ing the hypothesised ancestor of the Priscakoala lineage and the ances-
tors of the Invictokoala and Koobor ghost lineages.
TheearlyMiocene(16.4–23.0 Ma) saw a slight drop in generic
and species level diversity with only three genera and five species
known from fossil deposits of this age. Species of Madakoala and
Perikoala had disappeared from the fossil record, yet Litokoala
apparently diversified with three species (L. kutjamarpensis,
L. garyjohnstoni and L. dicksmithi) recorded from early Miocene de-
positsatRiversleighaswellasN. greystanesi and Pr. lucyturnbullae.
By including the hypothetical ancestors of the Koobor and
Invictokoala lineages at least seven species and five genera may
have been present during the early Miocene.
Only two species recorded from the early Miocene
(L. kutjamarpensis and N. greystanesi) extend into the middle
Miocene (10.4–16.4 Ma). Black et al. (2012a) recorded the presence
of Pr. lucyturnbullae in the Cadbury's Kingdom LF of Riversleigh,
which was previously regarded to be middle Miocene in age. Based
on a reassessment of its lithology and stratigraphic position
(P. Creaser pers. comm., 2012) and the stage of evolution of its
kangaroo fauna (K. Travouillon pers. comm., 2012), this deposit is
now regarded to be early Miocene (Faunal Zone B) in age. Potentially
four genera and four species (Litokoala,Nimiokoala and the hypo-
thetical ancestors of the Koobor and Invictokoala lineages) were pres-
ent during the middle Miocene, with Litokoala and Nimiokoala not
known from post middle-Miocene deposits.
ThelateMiocene(5.3–10.4 Ma) fossil record of Australia is espe-
cially depauperate with only three terrestrial vertebrate-bearing de-
posits known (Black et al., 2012b). Consequently, the single record of
akoalaspecies(Fig. 4) from the early late or very late middle Mio-
cene Encore LF is an obvious underrepresentation of koala diversity
(Black, 1999). This record, along with the hypothetical ancestors of
the Invictokoala and Koobor lineages, suggests that at least three
phascolarctid genera and species may have been present during the
late Miocene.
Pliocene (2.6–5.3 Ma) terrestrial faunal assemblages are more
abundant than those of the late Miocene and are characterised by
the earliest appearance of many modern marsupials such as
macropodine kangaroos (including species of Macropus)andtheex-
tant koala genus Phascolarctos (Black et al., 2012b). Generic level
phascolarctid diversity remains unchanged from that hypothesised
for the late Miocene yet species diversity is greater (Fig. 4)with
levels more consistent with that of early to middle Miocene times
(Price, 2012). Four species are known (K. notabilis,K. jimbarratti,
P. stirtoni,P. yorkensis) as well as, potentially, the hypothetical ances-
tor of the Invictokoala lineage.
Two genera and four species are recorded in Pleistocene deposits:
I. monticola,fromthebca.320 ka rainforest assemblages of Mt Etna,
Queensland; P. yorkensis, from Wellington Caves, NSW; P. stirtoni from
several deposits in Victoria, South Australia and Queensland; and
P. cinereus from numerous deposits across all states except Tasmania
and the Northern Territory. As far as we know, only P. cinereus survived
into the Holocene.
A dramatic decline in generic and species level diversity is evident
from potentially seven genera and nine species during the late Oligo-
cene to a single species today. Yet, as detailed by Black et al. (2012a),
a closer look at the fossil record indicates that at any given time since
the late Oligocene, at most only three (Fig. 4A), and more commonly
only one species, existed in any given palaeoenvironment. For example,
of the 74 late Oligocene to late Pleistocene fossil faunal assemblages
known to contain koalas (Fig. 4A), 82% of these contain a single
phascolarctid species. On this basis, the existence of a single species
in Australia's contemporary forests is consistent with what appears to
be the normal level of diversity displayed by the family in any given
habitat throughout its 24-million year history (Black, 1999; Black
et al., 2012a).
3. Discussion
3.1. Koala diversity in a climatically changing world
The driving forces behind speciation and extinction rates in
phascolarctids and hence diversity is no doubt a complex interplay be-
tween life history (e.g., fecundity, body size), macroevolutionary process-
es (e.g. competition, predation) and environmental factors (geographical
range, habitat) and is by no means clear on the basis of their relatively
scarce fossil record. However, it is clear that koalas, as arboreal folivores,
are inextricably linked to vegetation changes and, consequently, to
climate-induced habitat change (Lunney et al., 2012; Price, 2012; Wroe
et al., 2013).
Periods of high koala diversity appear to coincide with warm, wet
climates (e.g., early–middle Miocene) or palaeoenvironments with a
mosaic of vegetation types (e.g., late Oligocene, early Pliocene). A
warming trend, beginning in the late Oligocene (approx. 26 Ma) and
peaking with the mid-Miocene climatic optimum (approx. 16 Ma),
saw a transition from cool, seasonal climates to warm, wet greenhouse
conditions (McGowran and Li, 1994; Zachos et al., 2001; Shevenell et al.,
2004; Billups and Scheiderich, 2010). Palynological evidence from the
late Oligocene and early Miocene of central Australia indicates the pres-
ence of open forest palaeoenvironments dominated by sclerophyll com-
munities (Eucalyptus,Acacia,Casuarina) but with rarer rainforest taxa
present in refugial wetter habitats (McGowran et al., 2000; Martin,
2006). This mosaic of vegetation types sustained a greater diversity of
koalas (at least six species in four genera known from central
Australia) than at any other period in their known history.
Continued warming during the early–middle Miocene resulted in
widespread rainforest across southern, northern and eastern Australia
(Greenwood and Christophel, 2005). The early Miocene rainforest as-
semblagesof Riversleigh sustained the highestnumber of sympatric ko-
alas with as many as three species (Pr. lucyturnbullae,N. greystanesi,
L. dicksmithi) recorded from a single deposit (Black et al., 2012a).
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Rainforest habitats appear to have benefited small-bodied forms such as
Litokoala and Nimiokoala, with speciation evident in the Litokoala line-
age and potentially moderate levels of abundance evident for
N. greystanesi. Higher numbers of sympatric koalas may correlate with
greater plant diversity in Riversleigh's rainforest assemblages.
Following the mid-Miocene climatic optimum, the expansion of ice
sheets on Antartica (c. 15–13 Ma) saw palaeotemperatures drop by
up to 7 °C (Shevenell et a l., 2004; Bil lups and Scheiderich, 2010). The re-
sultant progressive cooling and drying of the Australian continent
(McGowran and Li, 1994) saw a regional contraction of rainforests ac-
companied by the expansion of Eucalyptus and casuarinaceous
sclerophyll vegetation, setting the scene, by late Miocene times, for
Australia's current climatic and vegetation patterns (Martin, 2006;
Billups and Scheiderich, 2010). The late Miocene (10.4–5.2 Ma) was
characterised by significant faunal turnover with the extinction of entire
mammalian families (e.g. balbarid kangaroos, pilkipildrid and mirilinid
possums) unable to adapt to Australia's progressive aridity (Archer
et al., 1997; Black et al., 2012b). A corresponding trend is evident within
Phascolarctidae with the extinction of some apparent rainforest-
adapted lineages (Nimiokoala,Litokoala,Priscakoala) and the subse-
quent origin and diversification of the modern genus. Although the
broader interpretation of a decline in biological diversity may partly
be an artefact of the scarcity of Australian late Miocene fossil deposits
(Fig. 4A), faunal turnover at this timehas been extensively documented
globally in other mammalian lineages (e.g., Badgley et al., 2008). Among
phascolarctids, an apparent trade-off is evident between a diverse
array of less abundant species in early–middle Miocene rainforest as-
semblages, with a greater abundance of taxonomically and ecological-
ly less-diverse species (e.g., Phascolarctos spp.) that capitalised on the
expanding sclerophyll forests of the late Miocene onwards (see
below).
The Australian Pliocene climate fluctuated markedly with warm wet
conditions evident in the early Pliocene followed by continued
aridification into the Pleistocene (Martin, 2006). Significant climate
and vegetation gradients were established across the continent
(McGowran et al., 2000) with wet sclerophyll forests along eastern
and southeastern coastal margins and drier sclerophyll forests and
grasslands in central Australia (Martin, 2006). Reconstruction of the Pli-
ocene palaeoenvironment of Chinchilla in southeastern Queensland
through stable isotope geochemistry of fossil tooth enamel, indicates a
mosaic of wet tropical sclerophyll forest, wetlands and tropical grass-
lands (Montanari et al., 2013). This vegetation mosaic supported two
species of koala, K. notabilis and P. stirtoni, the dentitions of which differ
significantly in morphology, suggesting ecological partitioning on the
basis of both diet and size (Table 2). A third potential species,
Phascolarctidae gen. et sp. indet., was also identified from the Chinchilla
LF on the basis of an edentulous lower jaw (Price et al., 2009). This spec-
imen is too incomplete to assign to a new or existing koala species, yet
appears to fall within the size range of P. stirtoni. The presence of the
giant koala P. stirtoni in the Chinchilla LF, which possesses a dentition
very similar to the eucalypt-specialist living species, suggests a direct
association between Phascolarctos and Eucalyptus from at least the
Pliocene.
Nevertheless, koalas appear to have persisted in rainforest environ-
ments up until the middle Pleistocene (c. 320 ka or younger) as evi-
denced by the presence of I. monticola in a rainforest-adapted faunal
assemblage from Mt Etna, central eastern Queensland (Price and
Hocknull, 2011). Hocknull et al. (2007) indicated that the rainforest as-
semblages of the region were relatively stable between 500 ka and
280 ka, enduring several glacial cycles, but sometime between 205
and 280 ka it was replaced by more xeric-adapted taxa. This faunal
turnover was attributed to a Mid-Brunhes Climatic Event that resulted
in increased climatic variability and progressive aridity in northern
Australia (Hocknull et al., 2007). The extinction of I. monticola potential-
ly represents the end of a 24 million-year association between koalas
and rainforest habitats.
3.2. Pleistocene distribution and population connectivity of the modern
species
The modern koala has a fossil record dating back at least to 350 ka
(Price, 2008a). Pleistocene deposits containing P. cinereus are known
from all Australian states except Tasmania and the Northern Territory
(Fig. 1). Although once geographically widespread, the extreme climatic
conditions of the late Pleistocene (i.e., glacial and interglacial cyclicity)
resulted in severe range contractions and localized population extinc-
tions, most notably along the southwestern and southern extent of its
range. Phascolarctos cinereus is recorded in numerous mid-late Pleisto-
cene deposits in the Leeuwin-Naturaliste Region of southwestern West-
ern Australia (e.g., Archer, 1972) including Labyrinth Cave (Merrilees,
1969), Mammoth Cave (46–84 ka; Glauert, 1910; Archer et al., 1980;
Roberts et al., 2001) and Tight Entrance Cave (143–70 ka, Prideaux
et al., 2010) with the youngest record from Devil's Lair dated at around
31–43 ka (Balme et al., 197 8).The apparent disappearance of P. cinereus
from the region after that time coincides with a change in fire regimes
accompanied by significant changes in vegetation. Prideaux et al.
(2010) documented faunal succession and changes in stable carbon
and oxygen isotopes throughout the main fossil-bearing deposit at
Tight Entrance Cave that are consistent with a progressive opening up
of the forests from closed canopied at 100 ka to a more open vegetation
type by 30 ka. The last appearance of P. cinereus at Tight Entrance Cave
(c. 70 ka) corresponds to a significant increase in charcoal suggestive of
a marked increase in fire activity within the region at this time, with the
largest peaks occurring between 37 and 29 ka (Prideaux et al., 2010).
Palynological evidence from offshore sediment cores across south-
ern Australia indicates similar continent-wide losses in potential koala
habitat during the late Pleistocene (Harle, 1997; Van der Kaars et al.,
2007; Price, 2012). In the Nullarbor region of southern Australia, euca-
lypts were widespread around 130 ka but progressively declined and
by 74 ka were replaced with a mosaic of open habitats including semi-
arid woodland and shrubland (Prideauxet al., 2007; Van der Kaars et al.,
2007; Warburton and Prideau x, 2010). Also at this time in southwestern
Victoria, dry sclerophyll forest was replaced by open heath and mallee
communities with continued declines in effective precipitation leading
to the expansion of grasslands during the Last Glacial Maximum
(LGM) (Harle, 1997).
The apparent geographic range contraction of koalas during the late
Pleistocene is further supported by independent bioclimatic modelling.
Adams-Hosking et al. (2011b) developed a climate envelope model to
predict the potential geographic range of P. cinereus during climatic con-
ditions reminiscent of the LGM including a decrease in temperature of
6 °C and a 20% (Fig. 5B) and 40% (Fig. 5C) reduction in rainfall, relative
to today (Fig. 5A). The resulting model suggested that a reduction in
temperature by 6 °C and rainfall by 20% had the potential to cause the
retraction of suitable koala habitat to geographically restricted areas of
northern NSW and Queensland and small areas of coastal Western
Australia, South Australia and Victoria. A further reduction in rainfall
(Fig. 5C) had the potential to lead to an even greater range contraction
to the eastern states with the loss of suitable habitat from WA, SA and
coastal Victoria (Adams-Hosking et al., 2011b).
Of note is a late Pleistocene population of a small form of P. cinereus
known from Madura Cave on the Western Australian Nullarbor Plain
(N24–b101 ka, Lundelius and Turnbull, 1982). Molar lengths are 10–
15% smaller than the sample means of modern Victorian and Queens-
land populations of P. cinereus (Black et al., 2013a). It is possible that
the small size of this material may be the result of insular dwarfing
and reflect a geographically isolated, refugial population with limited
resource availability.
Climatic refugia appear to have played a significant role in the sur-
vival of P. cinereus through the extreme climatic conditions of the LGM
(Adams-Hosking et al., 2011b). Evidence from recent analyses of koala
genetic diversity (Lee et al., 2012; Tsangaras et al., 2012) suggested
that koala populations have undergone significant bottlenecks prior to
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the dramatic declines in populations associated with the fur trade (see
Section 3.3) in the late 1800s and early 1900s. Tsangaras et al. (2012)
analysed mitochondrial DNA haplotypes of P. cinereus taken from muse-
um samples collected as early as 1870. Surprisingly, they found the mi-
tochondrial DNA haplotypes present in the historical koala samples
were the same as those in modern populations and did not contain
any novel haplotypes. Consequently, modern koala genetic diversity
was already low prior to the declines associated with the fur trade and
most likely attributed to the geographic range retractions of the late
Pleistocene and potentially the maintenance of low population levels
(see below) through Aboriginal hunting during the late Pleistocene
and Holocene (Tsangaras et al., 2012).
Interestingly, Lee et al. (2013) suggest the expansion of rainforest in
Queensland during interglacial periods of the Pleistocene may also have
acted as barriers to gene flow in the modern koala. However, consider-
ing the strong behavioural tendency for koalas to disperse (Lee and
Martin, 1988), their relative mobility and transient home range, and ca-
pacity to forage on N100 tree species (Moore and Foley, 2000), as well
as the current and prehistoric distribution of Phascolarctos spp. in trop-
ical, subtropical and wet forest habitats since at least the Pliocene
(Montanari et al., 2013), it is unlikely that rainforestwould have provid-
ed a significant barrier to gene flow during the Pleistocene. Dispersal by
subadult koalas (especially males) is considered the primary source of
gene flow between modern koala populations in Queensland (Tucker
et al., 2008). Forest considered ‘marginal’koala habitat has been
shown to playan important role in such dispersals and the maintenance
of connectivity between koala populations (McAlpine et al., 2006b).
Hence gene flow is dependent on the connectivityof any forest habitats,
not just ‘suitable’forest habitats. Certainly, the retraction of forest and
woodlands and the expansion of shrublands and grasslands during gla-
cial periods of the Pleistocene would have impeded such connectivity.
However, based on the ecology and palaeoecology of Phascolarctos
spp., it is less likely that the expansion of forest during interglacial pe-
riods would have had a similar effect.
3.3. Historic factors influencing the geographic range of the koala
Few references to koala populations occur before 1850 providing
further support to the genetic evidence of Tsangaras et al. (2012) that
population levels were relatively low. In fact, the first record of a
European sighting of a koala occurred in 1798 (Bladen, 1895), more
than 10 years after European settlement in Australia. However, rapid
population growth in the decades following was frequently document-
ed, and was presumed to be associated with relaxation of Aboriginal
hunting and the widespread poisoning of a potential predator, the
Dingo (Canis lupus dingo;Warneke, 1978).
Ironically, greater settlement led to a critical decline in geographic
range (Fig. 1) duringthe latter part of the 19th century primarily as a re-
sult of habitat clearing associated with bushfires, agriculture and urban
expansion (Phillips, 1990). Epidemics of some form of ophthalmic dis-
ease, pneumonia and periostitis of the skull during the late 1800s and
early 1900s, 1920s and 1930s, with symptoms similar to those found
in Chlamydia-infected Koalas today (Eberhard, 1972; Brown and
Carrick, 1985), drastically reduced Koala populations, as did the conten-
tious practice of commercial hunting. Warneke (1978) noted that South
Australian populations became extinct by 1925, with the same fate po-
tentially threatening Koala populations in other states. By 1920 the
Victorian Koala population was estimated to be as low as 500–1000 in-
dividuals yet some of this decline was attributed to extensive bushfires
(Lewis, 1934). A similar figure was estimated for the New South Wales
population (Phillips, 1990). Nevertheless, the national Koala population
was significantly reduced by several million as a result of commercial
hunting. Two million skins were exported in 1924 alone, from Queens-
land, Victoria and NSW (Eberhard, 1972). The fur trade was finally
abolished with the introduction of protective legislation by State Gov-
ernments, and the imposition of export controls by the Commonwealth
Government in 1921 (Phillips, 1990).
The recovery of mainland populations may, in part, be attributed to
the successful introduction during the 1870s and 1890s of koalas onto
the islands of Westernport Bay (Victoria). The rapid proliferation of ko-
alas on Phillip, French and Quail Islands made translocations to the
mainland essential after 1944 to avoid overbrowsing and population
decline (Warneke, 1978). By 2006, approximately 25,000 koalas had
been removed from these islands and used to re-establish populations
in Victoria (Menkhorst, 2008), South Australia and Western Australia
(Phillips, 1997) and had also been used to re-establish populations in
NSW (Martin and Handasyde, 1990). Similarly, koalas introduced to
Kangaroo Island off South Australia, have thrived and are now consid-
ered a pest species (Masters et al., 2004). In addition to translocation,
population control methods such as contraception (including surgical
sterilisation of males and hormone implants in females) (Duka and
Masters, 2005) have been implemented and even culling has been con-
sidered (Ross and Pollett, 2007).
Today, P. cinereus occupies temperate, sub-tropical and tropical for-
ests, woodland and semi-arid communities dominated by species of Eu-
calyptus (Martin and Handasyde, 1999), generally east of the Great
Dividing Range, from north Queensland to the southeast corner of
South Australia (Fig. 1). In the colder temperate climates Koalas are
rarely found at altitudes greater than 700 m above sea-level (Phillips,
Fig. 5. Bioclimatic models of the predicted range of Phascolarctos cinereus:A, modern potential range based on theclimatic envelope of the extant species; B, Last Glacial Maximum (LGM)
predictedrange modelled on a reduction in temperature by 6 °C and rainfall by 20%(with respect to today); C, LGMpredicted range modelled on a reduction in temperature by 6 °C and
rainfall by 40% (with respect to today). After Adams-Hosking et al. (2011b).
1196 K.H. Black et al. / Gondwana Research 25 (2014) 1186–1201
Author's personal copy
1990). Similarly, a line of 50 cm isohyet appears to delimit the western
range of the Koala (Smith, 1987; Menkhorst, 1996).
Across this range, an association is evident between koalas and tree
species restricted to high nutrient soils (Crowther et al., 2009)ofwater-
courses and alluvial flats. Food tree choice was further determined on
the basis of foliage nutrient quality and chemistry (Martin and
Handasyde, 1999; Lunney et al., 2000; Moore and Foley, 2005; Moore
et al., 2010; Callaghan et al., 2011), foliar water availability (Ellis et al.,
2002, 2010), and spatial structure (Moore et al., 2010). Consequently,
the koala carrying capacity of a given area is not simply governed by
the density of preferred browse trees but also by the number of palat-
able individual trees of those preferred species. Additionally, in hotter
climates, the presence of non-food shelter and shade trees (for behav-
ioural thermoregulation) has been suggested to play a significant a
role in koala survivorship and habitat quality, as the presence of palat-
able food-trees (Ellis et al., 2010).
A significant southward and eastward contraction in the modern
(contra historic) distribution of the koala (Fig. 1) is evident with the
loss of some inland and northern Queensland populations, primarily as
a result of habitat loss and fragmentation from anthropogenic factors in-
cluding urbanisation and agriculture and their associated threats of vehi-
cle collisions, dog predation, and disease (ANZECC, 1998; Dique et al.,
2003; McAlpine et al., 2006a; Lunney et al., 2009). A similar contraction
and fragmentation of range is evident in SE Queensland and northern
NSW. Some parts of the northern koala region of NSW, where Koalas
have previously been reported as most abundant (e.g., Reed et al.,
1990), have suffered intensive urbanisation and tourist development
and as a result, many koala populations are now locally extinct
(Lunney et al., 2002) or in decline (Lunney et al., 2007; Matthews et al.,
2007) with further reductions in populations predicted (Lunney et al.,
2009).
Clearly, the current patchy distribution of P. cinereus is the result of a
complex interplay between historical and environmental factors which
may account for why many areas of apparently ‘suitable’habitat (e.g.,
areas in Tasmania, central and Western Australia and alpine areas of
Victoria; see Adams-Hosking et al., 2011a, 2011b) do not currently sup-
port koala populations.
3.4. The potential impact of future climate change on koala populations
Evidencefrom the phascolarctid fossil record clearly indicates thein-
fluence of past climate change, specifically the progressive aridification
of the Australian continent accompanied by increased seasonality and
unpredictable climatic conditions on changes in koala species diversity
and geographic range (Price, 2012). The predicted effects of future cli-
mate change include a hotter and more variable climate for Australia
with an increase in the frequency and severity of drought, heatwaves,
floods and bushfires (IPCC, 2007; Dunlop and Brown, 2008; McAlpine
et al., 2009). The sensitivity of koalas to such extreme climatic events
are well documented, foreshadowing thepotential impactsof future cli-
mate change (Lunney et al., 2012). For example, in response to severe
drought and heatwave conditions, Gordon et al. (1988) and Seabrook
et al. (2011) observed mortality rates of 63% and 80%, respectively, in
Koala populations in semi-arid and arid environments. Individuals
that survived were those occupying riparian habitat along permanent
watercourses which were less likely to be affected by leaf drop during
drought conditions (Gordon et al., 1990). Koala mortality resulting
from bushfires is also well-documented with deaths resulting directly
from incineration or intense heat but also indirectly through enhanced
habitat loss and fragmentation and associated changes in vegetation
composition, all leading to a reduction in available food resources for
surviving populations (Melzer et al., 2000; NPWS, 2003).
Significant shifts in the climate envelope of the koala throughout its
natural distribution are predicted under a future hotter, drier climate.
The climate envelope of a species is defined as its potential geographic
range predicted using climatic variables (e.g., temperature and rainfall
maxima and minima) under which the species currently exists
(Adams-Hosking et al., 2011b). Using bioclimatic modelling, Adams-
Hosking et al. (2011a) predicted the current range of the koala would
contract eastwards and southwards into areas where koala populations
are currently under pressure from threats imposed by urbanisation
(e.g., habitat loss, vehicle collisions, dog attacks). When the distribution
of five key eucalypt food trees were modelled using identical climate
change scenarios, significant range contractions were predicted for
each of the eucalypts studied. However each species was found to con-
tract differently resulting in increasingly fragmented overlap between
koalas and their preferred tree species (Adams-Hosking et al., 2012).
In addition, the viability of some eucalypt species to support koala
populations will also be significantly impacted by future climate change
with rises in CO
2
levels predicted to alter vegetation quality. Lawler et al.
(1996) found eucalypts grown under elevated CO
2
levels produced
higher concentrations of anti-herbivore compounds in leaf foliage
while the nitrogen content(and hence available protein and nutritional
content) of leaves decreased.
3.5. Current status of koala populations
Predicting koala population numbers in the wild has proven difficult
with many areas across its extensive range remaining unsurveyed. Cur-
rent estimates vary between 43,000 (Australian Koala Foundation,
2010) to over 400,000 individuals (TSSC, 2011). In November 2011,
the federal Threatened Species Scientific Committee (TSSC), in their re-
view of koala populations for amendments to the Environment Protec-
tion and Biodiversity Conservation (EPBC) Act 1999, estimated the
national koala population (excludingACT) to comprise 407,500 individ-
uals; a decline of 29% over 1990 population estimates (573,400). On a
national scale, this value marginally precluded the koala’s eligibility to
be listed as vulnerable under the EPBC Act list of threatened species,
which requires a loss of 30% of total population size over three genera-
tions (approx. 20 years in the koala's case) (TSSC, 2011).
Currently, while koalas are protected in all Australian states, their
conservation status varies nationally with different states affording dif-
ferent levels of protection that may vary regionally depending on the
perceived threats. For example, NSW and Queensland populations have
declined by N30% since 1990 (TSSC, 2011), having been significantly im-
pacted by habitat loss and fragmentation, and are listed as vulnerable
and endangered in parts of their range. In contrast mismanagement of
some populations, particularly in southern Australia, has resulted in un-
sustainable densities leading to overbrowsing (Warneke, 1978; Masters
et al., 2004; Cristescu et al., 2009; Lee et al., 2010) and the subsequent
need for active population control (TSSC, 2011). Because of their com-
mon status in some parts of their range, koalas are classified as ‘Least
Concern’in the International Union for Conservation of Nature (IUCN)
Red List of Threatened Species (IUCN Version 2013.2), albeit potentially
vulnerable to climate change.
4. Conclusions
The modern koala P. cinereus is one of the most iconic Australian an-
imals. It has had a complex history having suffered broad-scale range re-
tractions over the past 100 ka as a result of climate change and
associated habitat changes during the Pleistocene. Since European arriv-
al in Australia, there have been regional extinctions, range retractions,
translocations, reintroductions, and consequent overpopulation in
some parts of its range (Menkhorst, 2008).
Nevertheless, it has not only survived but in many respects has
thrived. Evidence from recolonisation programmes in Victoria and
South Australia (Martin and Handasyde, 1999) and population growth
and geographic expansion in newly available suitable habitats in north-
ern NSW (e.g., Lee et al., 2012) indicate the relatively short timescale in
which koala populationscan be established. They were also successfully
1197K.H. Black et al. / Gondwana Research 25 (2014) 1186–1201
Author's personal copy
re-established in parts of their prehistoric range in Yanchep National
Park, Western Australia (Adams-Hosking et al., 2011b).
However, evidence from the koala fossil record indicates that
phascolarctids, like all specialist folivores, are particularly sensitive to
climate change with the family undergoing a considerable loss in gener-
ic and species-level diversity and ecological diversity with the extinc-
tion of koalas from rainforest habitats sometime during the middle
Pleistocene (Price and Hocknull, 2011). On this basis, and in light of
the responses of modern koala populations to historic climatic ex-
tremes, the likely impact of Australia's predicted future hotter, drier cli-
mates on koalas, include continued broad scale shifts in habitat
distribution, habitat loss, changes in vegetation suitability, and, in at
least some cases, concomitant population declines.
Habitat loss, fragmentation and degradation are contributing to ex-
tinction of species at rates not seen in the last 65 million years or possi-
bly ever (Blois and Hadly, 2009). Recognition of the need for the
identification and conservation of suitable habitat including potential
future habitat refugia (Adams-Hosking et al., 2012) is a priority for
optimising the future survival of the species.
Of particular importance will be optimising the connectivity of koala
populations through establishment of adequate habitat corridors as well
as forced translocations to maintain genetic diversity and hence the ca-
pacity of the species to survive selective forces such as disease which
might otherwise threaten local populations. Recently, a national frame-
work for the conservation and management of koala populations has
been developed in conjunction with the drafting and implementation
of the National Koala Conservation Management Strategy 2009–2014
by the Natural Resource Management Ministerial Council. Priorities of
the strategy include anticipation of the effects of climate change and de-
velopment planning on koala habitat throughout the range of this last
surviving phascolarctid.
Today, with 20% of Australia's mammal fauna listed as threatened
(Chapman, 2009), understanding the nature and rate of change in past
palaeocommunities (Archer et al., 1991; Louys, 2012) is increasingly
important for understanding future challenges related to ongoing cli-
mate change. Without this deep-time understanding of the conse-
quences of climate change on the Australian biota, it will be difficult if
not impossible to know how to prioritise conservation efforts to opti-
mise the future of the currently fragile fauna.
Acknowledgements
Support for Riversleigh research has been provided by the Australian
Research Council grants to M. Archer, S. Hand and K. Black
(DE130100467, DP043262, DP0881279, DP1094569, LP0453664,
LP0989969, LP100200486), Xstrata Community Partnership Program
North Queensland, Queensland Parks and Wildlife Service, Environment
Australia, the Queensland and Australian Museums, the University of
New South Wales, P. Creaser and the CREATE Fund at UNSW, Ken and
Margaret Pettit, Outback at Isa, Mount Isa City Council and the Waanyi
people of northwestern Queensland. Research funding for G. Price has
been provided by the Australian Research Council (DE120101533 and
DP120101752). We thank A. Gillespie and T. Myers for their expert prep-
aration of Riversleigh fossil material, and E. Lundelius Jr and J. Louys for
their thoughtful comments which greatly improved this manuscript.
Vital assistance in the field has come from H. Godthelp,C. (Lizard) Cannell,
C.LarkinandS.Williamsandmanyhundredsofvolunteersaswellasstaff
and postgraduate students of the University of New South Wales.
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Karen H. Blackis an Australian Research Council Postdoctoral
Fellow in the School of Biological, Earth and Environmental Sci-
ences at the University of New South Wales. She has published
in the fields of marsupial evolution, taxonomy, morphology,
phylogeny, ontogeny and biocorrelation, and has named many
new fossil species. Karen has 12 years experience extracting,
curating and analysing the rich fossil vertebrate faunas of the
limestone deposits of the Riversleigh World Heritage Area in
northwestern Queensland. Her current projects are focused
on understanding faunal change, behaviour, development,
species interactions and community structure in Australian
ecosystems to provide new understanding about current and
future climate-driven changes in biodiversity.
Gilbert J. Price is a Postdoctoral Research Fellow at The Uni-
versity of Queensland in Australia. He obtained his Ph.D. in
Palaeoecology from Queensland University of Technology
in 2006. His Ph.D. an d subsequent post-doctoral projects
have spanned a wide breadth of distinctive research fields
that include palaeoecology, geochronology, zoolo gy and
modern conservation. He is especially focused on developing
key datasets with which to test hypotheses concerning the
extinction of Australia's Pleistocene megafauna.
Michael Archer is a Professor of Biological, Earth & Environ-
mental Sciences at the University of New South Wales. Born
in Australia,he graduated from Princeton University (BAGe-
ology/Biology), and the University of Western Australia (PhD
Zoology). He was a Curator of Mammals in the Queensland
Museum (1972–78), Director of the Australian Museum
(1999–2003), Dean of Science at UNSW (2004–2009) and
Lecturer/Professor at UNSW (since 1978). A member of the
Australian Acad emy of Science, Fellow of many societies
and medalist, he has produced over 350 pub lications in a
range of fields including palaeontology (e.g. Riversleigh
World Heritage area), mammalogy, innovative conservation
and deExtinction.
SuzanneJ. Hand (BSc Hons UNSW,Ph.D.Macquarie)isanAs-
sociate Professor in Biological, Earth and Environmental Sci-
ences at the University of New Sou th Wales, Sydney. A
vertebrate palaeontologist for 30 years, she has published
widely on the origins, systematics and evolutionary history
of Australia's native fauna,the implications of continuing cli-
matic and environmental change in Australia and the south
Pacific, biocorrelation, and the global relationships, evolu-
tionary ecology and biogeography of mammals, especially
bats.
1201K.H. Black et al. / Gondwana Research 25 (2014) 1186–1201
