WA Science—Journal of the Royal Society of Western Australia, 97: 65–85, 2014
Relicts, reproduction and reintroductions—a century of marsupial research in Western Australia
N M WARBURTON
School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch WA 6150, Australia and Department of Earth and Planetary Science, Western Australian Museum, Locked Bag 49, Welshpool DC,WA 6986, Australia [email protected]
Marsupials, the quintessential Australian animals, have attracted considerable interest from the scientific community, both at home and abroad. Nowhere is this more evident than in Western Australia. The following review provides an overview of the history of marsupial research in Western Australia, outlining major contributors and findings along the way. Most research can be grouped within one or more of three major study streams; taxonomy and natural history (‘relicts’); reproductive biology and physiology (‘reproduction’) and conservation ecology (‘reintroductions’). Four Australidelphian marsupial orders are represented among the Western Australian fauna: Dasyuromorphia, Peramelemorphia, Diprotodontia and Notoryctemorphia. Many of these species are endemic to Western Australia, some of which represent isolated relicts of ancient phylogenetic lines. Contemporary threatening processes, including habitat change or loss, changes in fire regime and introduced predators, have led to ‘modern’ relicts, many of which exist in very small, disjointed remnants of their former geographical range. The experimental study of Australian marsupials was pioneered by H ‘Harry’ Waring, who saw the potential for the application of classical physiological techniques to the unstudied marsupial fauna. The establishment of the field research station at Rottnest Island led to an array of studies of the ecology and physiology of the quokka (Setonix brachyurus) from the 1950s to the early 1970s. These became a platform for our understanding of marsupial reproductive biology. More recently, research on the ecophysiology, genetics and immunology of Western Australian marsupials has been strongly tied to conservation. A major management tool has been to use these studies to guide threatened species translocations and similar conservation attempts.
KEYWORDS: conservation, diversity, Marsupialia, reproductive biology, Western Australia.
INTRODUCTION widely known. Among the marsupials of Australia and New Guinea (the Australidelphian radiation of Marsupials are recognised throughout the world as the marsupials) there are four recognised groups: quintessential Australian animals (along with dangerous carnivorous marsupials (Order: Dasyuromorphia); spiders and venomous snakes). The term marsupial is omnivorous bandicoots and bilbies (Peramelemorphia); derived from the Latin ‘marsupium’, meaning pouch, principally herbivorous possums, wombats, koalas, and is used to encompass a group of mammals (the kangaroos and their kin (Diprotodontia); and fossorial subclass Marsupialia; formerly Metatheria) that was seen, marsupial moles (Notoryctemorphia). All four historically, to have a reproductive system and strategy Australidelphian marsupial orders are represented that was ‘intermediate’ between the egg-laying among the Western Australian fauna (Appendix 1). In Prototheria (monotremes) and the placenta-bearing his presidential address of 1948 to the Royal Society of Eutheria (eutherian or ‘placental’ mammals). The Western Australia, Glauert (1950) presented a historical Gondwanan distribution of extant marsupials was also account of the early descriptions and development of believed to be reflective of this group having been out- knowledge of the marsupials of Western Australia. There competed on the other continents by eutherian mammals. are numerous species endemic to Western Australia, Thus, since their earliest encounters with Europeans, some of which represent isolated relicts of ancient marsupials were regarded as the ‘poor cousins’ of the phylogenetic lines as a consequence of divergent evolutionarily ‘superior’ eutherian mammals. Research in evolution (e.g. bilbies Macrotis lagotis and numbats Western Australia during the last century has, however, Myrmecobius fasciatus: Archer & Kirsch 1977) and others helped to dramatically change this view. Marsupialia is following past extinction events (i.e. megafaunal now recognised as the evolutionary sister group to the extinctions in which 90% of Australia’s large mammals Eutheria. That research has also provided some went extinct during the Pleistocene: Merrilees 1968; fascinating insight into the ecology and evolution of the Prideaux et al. 2007b). ‘pouched mammals’. The last century has also seen a massive decline in the number, diversity and distribution of marsupials in RELICTS Australia, nowhere more so than in the west. These contemporary threatening processes have led to ‘modern’ While the ‘flying’ kangaroo and koala ‘bears’ are easily relicts, many of which exist in very small, disjointed recognised, the diversity of marsupial fauna is less remnants of their former geographical range. Numerous studies have highlighted the key threatening processes © Royal Society of Western Australia 2014 in this decline, including diversion/reduction in
65 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 resources, vegetation changes in response to exotic Dasyuromorphia comprises three families: Dasyuridae herbivores and dieback disease, changes in fire regime, (dasyurids), the monotypic Myrmecobiidae (numbat), and introduced predators (e.g. foxes and cats) (Archer and Thylacinidae (thyacine). Western Australia is home 1974; Jenkins 1974; Calver & Dell 1999; Fletcher & Morris to a large diversity of small to very small, arid adapted 2003; Friend & Wayne 2003; de Tores et al. 2007). dasyurids, especially dunnarts (Sminthopsis spp.; Figure Burbidge & McKenzie (1989) coined the term ‘critical 1a) which typically range in body mass between 10 and weight range’ (CWR) to define the marsupial species most 40 g, but also Pseudantechinus spp. (15–50 g), the kaluta susceptible to these threats: medium-sized (35–5500 g), (Dasykaluta rosamondae; 25–40 g), Ningaui spp. (6.5–10.5 g: terrestrial animals of the semiarid and arid zones Figure 1b) and Planigale spp. (4–10 g). In contrast, mesic (Johnson & Isaac 2009). Yet, at a time when the extinction genera such as Antechinus and the larger bodied Dasyurus of more marsupial species is a real possibility, we are still are represented by only a few species in Western discovering the true diversity and evolutionary history Australia (e.g. the mardo, Antechinus flavipes; and of Western Australian marsupials. northern and western quolls, Dasyurus hallucatus and D.
Figure 1 Representative marsupials of Western Australia. (a) White-tailed dunnart, Sminthopsis granulipes. (b) Wongai ningaui, Ningaui ridei. (c) Honey possum, Tarsipes rostratus. (d) Spectacled hare-wallaby, Lagorchestes conspicillatus conspicillatus. (e) Golden bandicoot, Isoodon auratus barrowensis. (f) Northern marsupial mole, Notoryctes caurinus. (a–e) courtesy of W Bancroft; (f) courtesy of I Harris.
66 Warburton: Century of marsupial research in WA geoffroii). Endemic CWR species in the mid-west and consequently are less diverse in Western Australia than southwest such as the dibbler (Parantechinus apicalis), red- in the more heavily forested areas of eastern Australia. tailed phascogale (Phascogale calura) and the numbat have The handful of Western Australian species include the suffered enormously from habitat fragmentation and scaly-tailed possum (Wyulda squamicaudata) endemic to predation by introduced foxes and cats; and are now rocky outcrops of the Kimberley region (Alexander 1918; restricted to tiny pockets of their original distribution Calaby 1957; Runcie 1999); the ubiquitous brush tail (Woolley 1977, 1980; Morcombe 1967; Burbidge & possum (Trichosurus vulpecula), the western ringtail McKenzie 1989). The numbat is unusual among possum (Pseudocheirus occidentalis) found in localised marsupials in being diurnal and feeding exclusively on forest patches of the coastal South West (especially termites. It has long been recognised as distinct from peppermint trees threatened by coastal development) other dasyurids on the basis of dental morphology, and (Wright et al. 2007; Thompson & Thompson 2009), the basicranial skull structure suggested that Myrmecobiidae tropical rock ringtail possum (Petropseudes dahli) and the was an early divergence from the dasyuroid line (Archer western pygmy possum (Cercartetus concinnus) of & Kirsch 1977). The now extinct thylacine, however, southern Australia. The most intensively studied is the represented the youngest form of a previously much honey possum, Tarsipes rostratus (monotypic Family more diverse family (Murray & Megirian, 2000), distinct Tarsipedidae: Figure 1c), which feeds exclusively on from other marsupial carnivores (Archer 1976). nectar and pollen (Glauert 1929; Vose 1973; Wiens et al. 1980) and displays a suite of adaptations to this unusual Bandicoots (family Peramelidae) are medium-sized, diet (Parker 1890; Richardson et al. 1986; Slaven & terrestrial, omnivorous marsupials with a bounding gait Richardson 1988; Bradshaw & Bradshaw 2012). The and forelimbs adapted for digging for food (Gordon & honey possum was used to demonstrate the potential for Hulbert 1989). Approximately 20 species of bandicoots trichromatic vision in marsupials and has adaptations of are known from Australia and New Guinea, eight of the visual system for the detection of mature Banksia which have distributions (at least historically) that attenuata flowers, their favoured food source (Arrese et al. include Western Australia. While Western Australian 2002; Sumner et al. 2005; Cowing et al. 2008). This tiny populations of tropical northern brown bandicoot marsupial (males 7–9 g; females 10–12 g) also has the (Isoodon macrourus) and mesic southern brown bandicoots distinction of having both the largest testes relative to (Isoodon obesulus) are stable (IUCN 2012), only small body mass (4.2%) and the longest sperm among remnant populations remain of western barred mammals (up to 360 μm) (Wooller et al. 1981; Renfree et bandicoots (Perameles bougainville, on the islands of Shark al. 1984). Bay) and golden bandicoot (I. auratus barrowensis, in the Kimberley and islands off the northwest coast: Figure Kangaroos and related taxa (superfamily 1e). Bilbies (Macrotis lagotis; Thylacomyidae), arid- Macropodoidea) represent the largest terrestrial radiation adapted allies of the bandicoots, persist in scattered of the Diprotodontia. Macropodoids of medium to large colonies in the Pilbara and Kimberley (Troughton 1932; body size (>10 kg) especially those of the genus Macropus Jenkins 1974; Friend et al. 2008b), while the lesser bilby are relatively common and often have broad distributions (M. leucura) and pig-footed bandicoot (Chaeropus (IUCN 2012): western grey kangaroo (M. fuliginosus) and ecaudatus; Chaeropodidae) have become extinct during western brush wallaby (M. irma) in the south; red the twentieth century (Burbidge et al. 2008a, c). While kangaroo (M. rufus) and euro (M. robustus) through the bilbies have had significant publicity, most bandicoots semiarid and arid country; and the agile wallaby (M. are unremarkable in appearance; and though the agilis), antilopine wallaroo (M. antilopinus) and northern southern brown bandicoot is often encountered in nailtail wallaby (Onychogalea unguifera) in the tropical gardens in the southwest, little recognition is given to north. A divergent array of rock-wallaby species is also how interesting these marsupials are. The bandicoot found in Western Australia including the monjon skeleton has an unusual combination of a plesiomorphic (Petrogale burbidgei), the smallest of the rock-wallabies polyprotodont dentition with derived syndactylous (Kitchener & Sanson 1978), and the narbarlek (P. hindlimbs, in which the second and third digits of the concinna), which, uniquely among marsupials, has the foot are relatively reduced in size and bound together potential to develop unlimited numbers of supernumary developmentally. Bandicoots also have an ossified molar teeth (Sanson et al. 1985). W D L Ride, Director of patella, uncommon among marsupials, and lack a the Western Australian Museum (1957–1975) contributed clavicle within the pectoral girdle. The syndactylous pes significantly to our understanding of the evolution of was historically thought to reflect a close evolutionary macropodoids (Ride 1957, 1959, 1961, 1962, 1971a, b, relationship with diprotodonts; however, craniodental 1979; Ride & Serventy 1963). morphology (Archer 1976) and molecular studies Small- to medium-sized macropodoids have suffered (Springer et al. 1998) refuted this view, and suggested a heavily through loss of habitat and predation or much more ancient origin for the bandicoot group. The competition by ferals and domestics. Those that have reproductive strategy of bandicoots has been of great managed to persist are found in small remnants of their interest. Bandicoots have among the shortest gestation of former distribution. The burrowing bettong (Bettongia any mammals, as short as 12.5 days, and may produce a lesueur) and rufous hare-wallaby (Lagorchestes hirsutus) litter every 60 days in favourable conditions. This great are now restricted to populations on Barrow Island and efficiency in reproduction is accomplished by the the islands of Shark Bay, and the spectacled hare-wallaby development of a relatively (among marsupials) complex (L. conspicillatus: Figure 1d) is reduced in range, while allantoic placenta and production of very rich milk Gilbert’s potoroo (Potorous gilbertii) on the south coast is (Tyndale-Biscoe 2005). among the most critically endangered of all mammals Diprotodonts are principally arboreal herbivores and (Sinclair et al. 2002). The tammar wallaby (M. eugenii)
67 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 and quokka remain in isolated mainland and island the factors (interactions of climate/hunting/fire) leading populations in the south west (Main 1961; Eldridge et al. to the drastic changes in biodiversity during this period 2004; de Tores et al. 2007) and explanations as to recent (Merrilees 1968; Roberts et al. 2001; Prideaux et al. 2007b; crashes of the formerly recovered populations of the Prideaux et al. 2009). woylie (Bettongia penicillata) have proven elusive (Groom 2010; Pacioni et al. 2011; Rong et al. 2012). The banded hare-wallaby (Lagostrophus fasciatus), extinct on the ECOLOGY, PHYSIOLOGY AND mainland and found only on Bernier and Dorre Islands REPRODUCTION in Shark Bay, provides an interesting case study on the evolution of macropodoid marsupials. It has many Ecology and general physiology unusual features of craniodental (Flannery 1983; The experimental study of Australian marsupials was Prideaux 2004), musculoskeletal (Warburton 2009) and pioneered by H ‘Harry’ Waring, Professor of Zoology at reproductive anatomy (Tyndale-Biscoe 1965) which have the University of Western Australia 1948–1975, who saw made it difficult to place within the kangaroo family tree the potential for the application of classical physiological (Flannery 1983; Westerman et al. 2002; Nilsson 2006). techniques to the unstudied marsupial fauna (Waring Previously hypothesised as the sole survivor of the 1959). Waring sought and achieved the establishment of otherwise extinct group of giant, short-faced sthenurine a field research station on Rottnest Island (off the Perth kangaroos, it has most recently been proposed to be the coast) and, together with graduate students and living relic of a more ancient phylogenetic line, subfamily colleagues, produced significant early advances in Lagostrophinae (Prideaux & Warburton 2010). marsupial physiology using the quokka as a model. Marsupial moles are highly specialised burrowing These studies fell into two main areas, physiological marsupials adapted to life underground. These small ecology and reproductive physiology, and paved the way marsupials (30–70 g) lack eyes and external ears and for the current understanding of marsupial biology and possess short, stout limbs that are highly modified for reproduction. digging. Two species are recognised: the central Ecological studies examined aspects of breeding and marsupial mole (Notoryctes typhlops) and the northern growth of pouch young (Shield & Woolley 1963; Shield marsupial mole (N. caurinus: Figure 1f), the latter 1964, 1968), population studies (Dunnet 1962, 1963; endemic to the Pilbara region of Western Australia Shield & Woolley 1963), and habitat use (Storr 1964; (Thomas 1920; Corbett 1975; Benshemesh & Johnson Nicholls 1971; Kitchener 1972, 1973). An experimental 2003). Relatively little is known about these cryptic approach was taken up to investigate aspects of marsupials, and apart from morphological (Warburton marsupial physiology, including digestive physiology 2006) and physiological (Withers et al. 2000) work based (Moir et al. 1954; Waring et al. 1966), thermoregulation on opportunistic specimen finds, few recent studies (Bartholomew 1956; Kinnear & Shield 1975), and have been undertaken. osmoregulation (Bentley 1955; Barker & Barker 1959; In addition to the extant species, there is a rich, albeit Bentley & Shield 1962; Bakker & Main 1980). These relatively recent, fossil history of marsupials in Western studies on the quokka became a platform for our Australia that has attracted the interest of a number of understanding of marsupial physiology. Conscious of a researchers including Royal Society Western Australia single-species approach, however, Main (1983) examined past presidents L Glauert (1933–1934, 1947–1949), W D L the extent to which studies on the quokka could be Ride (1962–1963) and D Merrilees (1966–1967). extrapolated to marsupials more generally. His review Principally late Pleistocene in age (126–12 ka) the caves drew together the quokka research with studies of other of the Margaret River region (Mammoth Cave, Devil’s macropods, to assimilate aspects of ecophysiology of Lair, Kudjal Yolgah Cave and Tight Entrance Cave) have macropods, as well as to broader theoretical principles. yielded fossils of a number of extinct marsupials Many of the results and interpretations from the study of including the marsupial ‘lion’ (Thylacoleo carnifex), the quokka were shown to be more widely testable and wombats, the large diprotodontid Zygomaturus, and giant applicable for macropod marsupials. Studies of sthenurine (short-faced) kangaroos (Glauert 1910, 1912, marsupial ecophysiology, or how an animal ‘works’ in 1914, 1921, 1926, 1948; Merrilees 1965, 1967, 1970a, b; its environment, have become an important tool in the Archer & Baynes 1972). Additionally these caves have conservation and management of threatened species. yielded evidence of the interaction of Aboriginal people The highly specialised diet and/or behaviour of some with some of these animals (Archer et al. 1980). Caves in marsupials in relation to their diet have been of particular the Nullarbor region range from early Pleistocene interest for physiological studies, and Western Australia (2.6 Ma–781 ka) to Holocene (<12 ka) and have provided has provided numerous oddities in this regard. For unprecedented opportunities to study the diversity and example, tammars on the Abrolhos Islands are able to ecology of extinct species due to the exquisite drink seawater and maintain body weight while eating preservation of semi-articulated specimens (Lundelius poor-quality dry graze (Kinnear et al. 1968). Tammars 1963; Lowry & Lowry 1967; Lowry & Merrilees 1969; survive this extreme water and nutrient deficit by a Lundelius & Turnbull 1973, 1981; Prideaux et al. 2007a). combination of marsupial characteristics and Among these deposits are a large diversity of marsupials, physiological adaptations. All marsupials have a including many species of kangaroos including tree- relatively low basal metabolic rate (BMR) and a kangaroos (Prideaux et al. 2007a; Prideaux & Warburton depressed nitrogen metabolism in comparison to 2008, 2009). The fossil deposits in Western Australia have eutherian mammals, resulting in a relatively lower been key to current understanding of the timing of requirement for these nutrients generally (Fraser & Pleistocene extinctions of the Australian megafauna and Kinnear 1969). But tammars are also able to recycle urea
68 Warburton: Century of marsupial research in WA nitrogen throughout the dry season, by cyclic exchange functionality of the thymus gland (Stanley et al. 1972; of nitrogen between their body tissues and the microbial Yadav et al. 1972; Ashman et al. 1975). community within the pregastric (forestomach) portion of the digestive system, further reducing their nitrogen Reproduction requirements (Kinnear & Main 1975). In order to cope with the salt loading resulting from drinking saltwater, Marsupials are distinguished from eutherian (‘placental’) tammar kidneys have been shown to concentrate urinary mammals primarily on the basis of reproductive biology. electrolytes to a greater degree than highly specialised Marsupial neonates (newborns) are highly altricial at eutherian mammals (Kinnear et al. 1968). birth; that is they are born in an undeveloped state and, thus, require extensive parental care. Most of the The physiological variables most commonly used to development of the young takes place in the pouch, make inferences about the relationship of an animal to its where the joey is provided with milk by the mother for environment are body temperature and metabolic rate (a an extended period of time. All marsupials have fully measure of the total energy used by an animal per unit functioning placentae; they are merely short-lived when time). This has been a dominant theme of Western compared to those of eutherians (Hill 1900; Flynn 1923; Australian research over many decades (Kinnear & McCrady 1938; Enders & Enders 1969). Eutherian Shield 1975; Withers et al. 2000, 2006). As a general rule, mammals, in comparison, tend to give birth to well- marsupials have a lower body temperature and metabolic developed (precocial) young, though the range in rate than eutherian mammals of equivalent size (Hume development is significant if one compares a newborn 1999) which, as with the marsupial reproductive strategy, mouse with a newborn calf, which can walk within has been hypothesised to be a result of the relatively low hours. Reproductive anatomy also differs between productivity of the Australian environment (Tyndale- marsupials and eutherian mammals. The female Biscoe 2001). One particular physiological characteristic reproductive tract of marsupials has two lateral vaginae of a number of marsupials is an ability to enter shallow, which each pass to a separate oviduct (uterine tube), daily torpor to reduce energy use when food resources rather than two oviducts converging to one uterus, as in are scarce or during adverse environmental conditions. most eutherians. The lateral vaginae function as passages Torpor is indicated physiologically by a significant drop for sperm, while an additional median- or pseudo-vagina in BMR and body temperature. A number of Western forms for the passage of young; in most groups the Australian marsupials enter torpor in order to conserve median vagina must be re-formed each breeding season, energy, including the honey possum (Withers et al. 1990), though in macropods it remains open post-partum numbats (Cooper & Withers 2004) and many dasyurids (Tyndale-Biscoe 2005). In male marsupials, the testes and (Geiser 1994). Cooper & Geiser (2008) reviewed the scrotum lie anterior to (in front of) the penis, rather than relationship between body mass, BMR and posterior (behind) as in eutherian mammals. The thermoregulation and demonstrated that shallow, short- development of other sexual characteristics, such as term (daily) torpor is an adaptive physiological mammary tissue, nipples and pouch in marsupials has a mechanism, rather than an inability to maintain body different genetic signal to that of eutherian mammals, temperature. Investigations of neural control of the heart attributed to a different configuration of the sex in the fat-tailed dunnart (Zosky & O’Shea 2003) and chromosomes in marsupials; male marsupials do not western pygmy possum (Zosky & Larcombe 2003) found possess nipples or a pouch (Tyndale-Biscoe 2005). Other that torpor is regulated by a physiological decrease in differences in anatomy and physiology are apparent heart rate, under the control of the autonomic nervous throughout the body of marsupials, although those of the system. This mechanism is homogeneous with that found reproductive system are perhaps the most obvious. in deep (‘true’) hibernators, such as bats, suggesting a While gestation in marsupials is short, the lactation greater overall similarity between shallow torpor and period is long in comparison to eutherian mammals of deep hibernation than was previously recognised. equivalent size (Tyndale-Biscoe 2001). This has been Two other fields of marsupial physiology have seen interpreted as a strategy to cope with the relatively low significant advancement in Western Australia: productivity or unpredictable availability of resources immunology (the physiological functioning of the within the Australian environment, where the total immune system) and endocrinology (the study of resource requirements for growth are spread over the hormones, their functions and the glands or tissues that extended period of lactation (Tyndale-Biscoe 2001). Other secrete them). Again, the quokka was the subject for aspects of marsupial reproductive biology have similarly much of the early work (Bradshaw 1983a; Stanley 1983). been linked to resource availability. Some marsupials The development of the immune system was of demonstrate embryonic diapause, first described by considerable interest, given the altricial nature of Sharman (1955b) in the quokka, in which the marsupials at birth. Two immunological mechanisms implantation and development of the embryo is were found to help protect marsupial neonates in their suspended until such time as the mother is capable of relatively underdeveloped state. Initially there is a supporting the developing embryo. While not unique to passive transfer of maternal antibodies to the pouch marsupials, this adaptive strategy is found in a number young through the milk (Yadav 1971). However, the of Western Australian species including the honey digestive tract is only able to absorb antibodies during possum and many macropods (Sadleir & Tyndale-Biscoe pouch life and only a proportion of antibodies are able to 1977; Renfree 1980; Tyndale-Biscoe & Hinds 1981). A be transferred in this way. Secondly, there is a relatively more extreme strategy linked to resource availability is rapid maturation of immune competence, as evidenced male die-off (semelparity; breeding only once in a in particular by the early presence of immune cells such lifetime), whereby adult males die after breeding; this as lymphocytes, and a rapid development and strategy has the potential to increase juvenile
69 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 survivorship by reducing competition for food. Male die- receptor assays for progesterone in uterine tissue (Owen off has been observed in many Western Australian et al. 1982). Importantly, the marsupial foetal adrenal dasyurids, the largest being the northern quoll (Woolley gland was shown to secrete cortisol just prior to birth 1991, 2008e; Crowther 2008; Oakwood 2008; Soderquist (Sorokin 1981), and to initiate parturition in the & Rhind 2008). In many species this die-off is obligate marsupial (Shaw et al. 1996) as is the case in eutherian (i.e. all breeding males die, regardless of resource mammals, in which cortisol is the trigger for the cascade availability) as a physiological-stress-related response to of hormonal events leading to birth. Progesterone profiles breeding (Woolley 2008c), while in dibblers and northern throughout pregnancy in the quokka and the tammar quolls it appears to be facultative, and dependent on also revealed that the foeto-placental unit shortened the resource supply (Mills & Bencini 2000; Bradley 2003). life span of the corpus luteum. This was indeed a startling discovery; it is in direct contrast to gestation in Endocrinology became a key tool for the developing most eutheria, in which the foeto-placental unit understanding of marsupial biology, particularly with significantly prolongs the life-span of the corpus luteum regard to the reproductive cycle of marsupials and the (Bradshaw & Bradshaw 2011). hormonal control of pregnancy (Tyndale-Biscoe et al. 1974; Tyndale-Biscoe 1978; Cake et al. 1980; Tyndale- During pregnancy, the placenta also produces Biscoe & Hinds 1981). The early studies of the progesterone, and the amount of progesterone within the reproductive biology of quokkas (Sharman 1955a, b; system has an effect of the rate of embryonic Waring et al. 1955) led to Western Australia becoming a development, and the initiation of parturition (birth) and centre for the study of reproductive endocrinology. The lactation (Bradshaw & Bradshaw 2011). Bradshaw & drive to measure hormonal changes during reproduction Bradshaw (2011) reviewed the role of progesterone in in marsupials came from Sharman’s (1970) claim that marsupials, in comparison with eutherian mammals. In marsupials, unlike eutherians, did not show ‘maternal contrast to historical views, these authors highlighted the recognition of pregnancy’, in other words, that the fact that all of the basic physiological mechanisms of presence of the embryo in the uterus did not bring about progesterone observed in the extended gestation of any changes in the physiology of the mother. Because eutherian mammals are also measurable in the relatively gestation is always contained within a single oestrous short gestation of marsupials. Further, measurable effects cycle in marsupials, and thus pregnancy does not inhibit of progesterone (prior to formation of the corpus luteum) ovulation, the assumption was made that the hormonal on the induction of sexual behaviour, female receptivity changes throughout an oestrous cycle were all that were and ovulation in marsupials were noted. need to sustain a pregnancy. This catalysed the Endocrinology has also provided insight into the development of a specific radioimmunoassay for the control mechanisms of other aspects of marsupial hormone progesterone, one of key hormones responsible reproductive biology including embryonic diapause. for the regulation of the female reproductive cycle and Diapause in macropods is associated with low levels of pregnancy, to monitor changes throughout both pregnant circulating progesterone and an undeveloped corpus and non-pregnant cycles. The publication in 1980 of a luteum (Tyndale-Biscoe & Hinds 1981). While seasonal paper showing the presence of a small but significant photoperiod provides the ultimate control for obligate spike in progesterone early in the pregnant cycle of the diapause (embryos fertilised in late autumn remain in a quokka (Cake et al. 1980) unleashed a torrent of criticism state of diapause until after the summer solstice (Renfree from others in the field and led to the initiation of a & Shaw 2000), facultative diapause is more flexible. In series of studies in the tammar wallaby (Hinds & many species, females mate soon after giving birth and Tyndale-Biscoe 1982), and other species of macropods, the resulting newly fertilised embryo will remain in a all of which showed the presence of a similar spike in the state of diapause while there is a young in the pouch. If pregnant cycle. Hugh Tyndale-Biscoe later described this the pouch young does not survive, for whatever reason, as one of the most important discoveries in marsupial the absence of suckling triggers activation of the corpus reproductive physiology of the last few decades luteum and reactivation of the embryo (Tyndale-Biscoe (Tyndale-Biscoe 1997). 1978). Embryonic diapause in honey possums, similarly, During the reproductive cycle, progesterone is has hormonal controls that respond to lactational cues produced in the ovaries (by the corpus luteum; the and photoperiod, as well as exhibiting their own remains of the follicle after ovulation) and has a number entrained rhythm (Oates et al. 2007). To study hormone of roles including preparing the endometrium (the lining levels in such tiny, and fragile animals, new methods for of the uterus), and helping to support the implantation of examining the hormones present in faeces have been the foetus. The role of the foetus in the process of birth established (Bradshaw et al. 2004; Oates et al. 2004). Such had earlier been indicated by cross-breeding experiments studies have provided significant advances detailing the with grey-kangaroos (Poole 1973) and from the reproductive physiology of the honey possum (Oates et shortening of the life-span of the corpus luteum by the al. 2007) as well as providing important data for foetus in the tammar (Merchant 1979). With the conservation programs including captive breeding demonstration in both the quokka and the tammar that programs (Stead-Richardson et al. 2010) and translocation the placenta is an endocrine organ and capable of attempts (Mills et al. 2012). secreting progesterone (Heller 1973; Bradshaw et al. 1978; Heap et al. 1980), the marsupial foeto-placental unit was suspected of being more than just a passive occupant of REINTRODUCTION the oestrus cycle. It required the advent of improvement By the middle of the twentieth century it was recognised in hormone assays to elaborate the nature of the foeto- that iconic Western Australian species such as the placental effect on the mother and the development of numbat were threatened and that conservation efforts
70 Warburton: Century of marsupial research in WA were needed (Fleay 1952; Calaby 1960; Serventy 1962). mainland range deemed suitable, 10 animals from the As noted in preceding sections, the threatening processes wild population were introduced to Bald Island, a are many and varied, and include habitat loss, feral cats, predator-free island off Cheynes Beach, in 2005–2007 foxes, cane toads, agriculture, fire regimes, logging and (Anon. 2010). The introduction has been successful and a climate change. Attempts to conserve species may breeding population has established on the island. involve the mitigation or minimisation threats, but where Following the success at Bald Island, Gilbert’s potoroos populations are extremely vulnerable this may not be have been subsequently reintroduced to a mainland site enough. A major management tool has been translocation at Waychinicup National Park near Mt Manypeaks (movement by humans) of individuals of threatened (Anon. 2011). species to areas from where they were once known but Where translocation is not practicable, the in situ no longer occur (reintroduction) or to areas outside this management of persisting populations of threatened range but that are considered suitable and secure species (and the threats) can also be an effective habitats, for example offshore islands (introduction). It is conservation strategy. Almost invariably, predation by important to note that, for many species, reliable introduced foxes and cats is one of the most significant estimates of population size are not available, and a pressures threatening the survival of native species recently published study on the decline in woylie (Kinnear et al. 1988; Hayward et al. 2003; Clarke et al. numbers, by Wayne et al. (2013), highlights the 2008; Wayne et al. 2011). In some case, the removal of conservation and management implications of ‘getting introduced predators has led to the successful the numbers right’. management of threatened native species. At the time of The success of a number of translocation attempts of European settlement, quokkas were widespread endangered macropodoids was reviewed by Short et al. throughout the South West, and their subsequent and (1992), including quokka and tammar wallaby to critical decline on the mainland was strongly correlated Jandakot between 1971 and 1988, banded hare-wallaby with the arrival of the red fox (Vulpes vulpes) (White 1952; to Dirk Hartog Island in 1974 and woylie to Perup (1977), Hayward et al. 2003). In 2003 Hayward et al. found that Collie and Nannup (1982–1983). The majority of these three of seven previously recorded mainland populations reintroductions was unsuccessful. Mainland populations had become extinct, and that those remaining were under were under most threat from foxes and cats, though serious threat of extinction. In addition to ongoing habitat degradation and infection may also have been pressure from predation and habitat changes, the large contributing factors (Short et al. 1992). Reintroductions on separation of these populations as a result of habitat islands were significantly more successful than attempts fragmentation was a contributing factor to local on the mainland. Banded hare-wallabies, however, did extinctions. On the basis of metapopulation theory, not manage to establish a viable population on Dirk however, they predicted that appropriate management of Hartog Island. Though Dirk Hartog Island was fox free, local populations through fox control and the restoration it was a pastoral station carrying sheep, with degraded of habitat may result in increased population size habitat, and large numbers of feral goats and cats (Short (Hayward et al. 2003). Seasonal trapping during 2010– et al. 1992). Other documented reintroductions have 2011 demonstrated substantial increases in population included burrowing bettong, rufous hare-wallaby, size correlated with fox baiting. Viable quokka banded hare wallaby and western barred bandicoot as populations were found at six mainland sites, including part of the ‘Return to Dryandra Project’ (Anon. 2012), two previously pronounced locally extinct (Dundas et al. rufous hare-wallaby and banded hare wallaby to Peron 2012). Fox baiting has been successful in the management Peninsula (2001) (Hardman & Moro 2006) and numbats of a number of threatened marsupial species, including into the Arid Recovery Reserve, Roxby Downs, South the numbat and rock wallabies (Kinnear et al. 1988; de Australia in 2005 (Bester & Rusten 2009). Often, however, Tores et al. 2007; Wayne et al. 2011). Cats, however, are the results of these reintroductions are difficult to notoriously difficult to control in open systems (Risbey et monitor, and detailed studies of survivorship over the al. 1997; Short & Turner 2005). long-term are not always possible due to lack of funding. Obviously, translocations also require in situ A high profile case study of a successful translocation management, and a combination of the above approaches attempt is that of the critically endangered Gilbert’s can improve success. In practice this requires clear potoroo, the most endangered mammal in Australia. objectives to be set and a commitment to long-term Gilbert’s potoroo was rediscovered in 1994 at Two management (Short et al. 1992). An example of the Peoples Bay reserve near Albany, having been successful outcome of well-thought out and well- considered extinct for over one hundred years. Fewer managed reintroduction programs is that of the dibbler. than 50 individuals remained and a management The dibbler had been considered extinct for almost a programme was established in order to conserve the century before being rediscovered near the south coast in population by habitat preservation, predator control and 1967 (Morcombe 1967). It is currently regarded as captive breeding (Courtenay & Friend 2004). Genetic endangered (Friend et al. 2008a). A very successful studies of the population indicated a substantial genetic captive breeding program was established at Perth Zoo bottleneck consistent with significant population decline in 1997 from a colony of wild caught individuals from (Sinclair et al. 2002). Captive-breeding attempts have been Whitlock and Boullanger Islands near Jurien Bay. These unsuccessful and faecal hormonal measurements animals provided study specimens for intensive research demonstrated a lack of reproductive hormonal activity in into the reproductive biology and behaviour of the captive females (Stead-Richardson et al. 2010). In order to dibbler (Lambert & Mills 2006). Subsequently, more than protect the extant population from stochastic events such 80 captive bred individuals were released on Escape as fire, and with no sites within the species’ former Island (Jurien Bay) from 1998 to 2000. Radiotelemetry
71 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 and intensive trapping were used to monitor the Escape populations of woylie, though genetic variation between Island population. Breeding and dispersal of young were populations was evident (Pacioni et al. 2011). In contrast, recorded within the first year and by 2001 a third the genetic diversity of the quokka (measured by generation of wild-born dibblers had been recruited into microsatellites and other molecular techniques) indicated the population (Moro 2003). The success of this project significant genetic differences between island and reflects the combination of detailed reproductive and mainland populations (Alacs et al. 2011), highlighting the ecophysiological research, a clear set of objectives and need for caution when considering the translocation of careful monitoring of reintroduced population. possibly maladapted island individuals to supplement The success of reintroductions is improved with mainland populations of this species; while the Barrow greater knowledge of species and their ecology to guide Island population of black-footed rock wallabies has been conservation attempts. While this is a very broad area of shown to have the lowest level of genetic variation found research, many such studies in Western Australia appear in any mammal (Eldridge et al. 1999). to fall into three discrete fields: ecophysiology, genetics An opportunity to investigate a population response and immunology. in the face of a threatening process, from a conservation That ecophysiological principles could be applied to genetics perspective, has been taken up in the case of the conservation and management strategies was advocated northern quoll. Using a variety of genetic markers, How by Bert Main (Main 1961, 1968; Main & Yadav 1971). et al. (2009) have investigated the population structure of Through his series of papers, intensive ecological studies the northern quoll, which is threatened by the spread of were made of eight macropodoid species on Western the introduced cane toad (Chaunus marinus). Varied Australian offshore islands in order to determine the patterns of gene-flow between island and mainland characteristics of both animals (habitat cover, nutritional populations, and genetic divergence between populations and water requirements) and the islands (size, floral in the Pilbara, Kimberley and offshore islands has diversity including trees) which accounted for the implications for conservation of genetic diversity in this observed diversity of fauna. Following this, he considered keystone marsupial predator (How et al. 2009). the likely implications for the management and The last two decades have seen a rapid increase in the conservation of those systems. Main & Yadav (1971) immunological study of marsupials. Immunological highlighted the importance of Barrow Island as a refuge threats to marsupial populations, and particularly for many species as a result not only of its large size, but captive-bred populations, have led to extensive more importantly by the fact that Barrow Island retains characterisation of viruses, microbes and parasites in the topographic diversity (including stable rocky outcrops) marsupials. Haematological studies may be performed and floral assemblages of the adjacent mainland. In a few for assessments of animal health as an element of instances habitat disturbance has had the opposite effect, management strategies (Bennett et al. 2007). Such a study for example significant population growth of spectacled in the quokka found differences in the blood hare-wallabies on Barrow Island and quokka on Rottnest characteristics of wild versus captive populations, Island. In such cases, careful management is required in potentially reflecting nutritional deficiency in the wild. order to minimise the possible detrimental effects of large The same study also identified a number of population size, especially on islands (Bradshaw 1983b; haemoparasites in wild populations of quokka, Bakker & Bradshaw 1989). highlighting the need for more work in order to More recently, the application of genetic methods and understand the risk such parasites might pose to techniques to conservation problems has become an sympatric species, for example the endangered Gilbert’s important area of research. Population genetics, as a potoroo which overlaps the range of the quokka in the field, measures genetic variation within and between far South West (Clark & Spencer 2006). The ongoing populations in order to understand patterns of gene flow identification and characterisation of parasites has been and evolution of species. It is understood that decreased an important focus and a recent review has demonstrated genetic variation within a population leads to reduced the importance of understanding the conservation fitness in an evolutionary sense. Conservation genetics, implications of parasite diversity, both within species then, seeks to understand genetic variation within and more broadly at the level of ecosystems (Thompson populations in order to conserve genetic diversity. et al. 2010). Further, it is important to establish baseline data of Captive breeding of individuals for reintroduction genetic variation within and between donor and recipient requires a high level of care to ensure that disease is not population prior to mixing populations (Alacs et al. 2011). introduced to wild populations. For example, For example, in order to better understand the effects of Cryptosporidium muris infection detected in captive-bred range reduction on gene flow and genetic variation in bilbies was most likely acquired from mice by faecal the numbat, Fumagalli et al. (1999) analysed contamination of food and water (Warren et al. 2003). mitochondrial DNA (mtDNA) sequences of free-ranging Viral infections, too, have been identified and may be individuals and museum specimens. Though reduced hampering conservation attempts. A bandicoot genetic diversity following population decline was papillomatosis carcinomatosis virus that causes lesions evident, relatively recent connectivity between remnant and may have a severe impact on locomotion, sight or populations was indicated. For management purposes, feeding, has been described in some wild and captive- then, remnant populations could be treated as a single bred populations of the endangered western barred historical lineage and translocation might be a successful bandicoot (Bennett et al. 2008; Woolford et al. 2009). strategy for the maintenance of genetic diversity Often, the impact of parasites and viruses is difficult to (Fumagalli et al. 1999). Historical patterns of determine and it is often unknown to what extent the interconnectedness have also been elucidated between microbes and parasites found may be correlated with
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80 Warburton: Century of marsupial research in WA 2008 2008 et al. et al. Rhind 2008 Soderquist 2008 Dickman 2008 Serena & Soderquist & Reference Dunlop Cooper 2008 Fisher 2008 Oakwood 2008 Bradley McKenzie & Woolley 2008d Valente 2008 Burnett 2008 Woolley 2008f Masters 2008 Crowther 2008 Woolley 2008a Woolley 2008h Carthew & Bos 2008 V, S1[v] E, S1[e] Status E, S1[e] V, S1[v] P4 spinifex sandplain, granite rockpiles sandplains supporting spinifex commonly rocky escarpments; also woodlands. Isolated patches of forest in the south-west. Limestone and sandstone outcrops of the Kimberley. Along drainage lines in spinifex Constructs burrows in sandy swales spinifex Inland red Inland Varied habitats from forests to swamps Spinifex grasslands Great Victoria Desert. Rocky hills, breakaways, red sandplains of Habitat Constructs burrows in desert sand dunes Arboreal specialist; open forest with sparse groundcover. S1[v] hummock grassland. Rocky habitats through Pilbara and western deserts. Open woodland, Open 3.6-9.5 g males 6.5-10.5 g 17-26 g femalesPilbara. the of 60-90 g females grassland; medium to dense cover. 65-120 g femalescover. sparse with 21-52 g females and dry mulga country. 20-40 g femalesdeserts. northern 15-20 g females mean 890 g femalesWA. south-west the of 3.5-17.2 g females Coastal and subcoastal areas of north-west. 30-45 g females 25-40 g males20-30 g females Hummock grasslands of the Pilbara.240-690 g females 60-125 g males40-73 g females Coastal and subcoastal areas.175-311 g males Woolley 2008e 2.6-5.8 g females Blacksoil plains of the tropical north. S1[e] E, Woolley 2008c 3.5-7.5 g females grasslands of the Pilbara. Body mass Body 6-14 g 4-16.3 g males 75-110 g males mean 20 g females 2.8-6.6 g males 340-1120 g males Most 106-212 g females Yellow-footed antechinus, 26-79 g males Crest-tailed mulgara, ampurtamales g 110-185 Brush-tailed mulgara mardo Ningbing false antechinus 20-25 g males Fat-tailed pseudantechinus 25-45 g males Northern quoll Northern Common planigale Western quoll, chuditch mean 1310 g malesWongai ningaui Sclerophyll forest, dry woodland or shrubland Red-tailed phascogale, 39-68 g males Kaluta Pilbara ningaui Dibbler red-tailed wambengerBrush-tailed phascogale, Kultarr, jerboa marsupial 38-48 g females mouse Long-tailed planigale malesg 30 mean Desert plains, grasslands and acacia woodland. Rory’s pseudantechinusWoolley’s pseudantechinus 19-32 g males 35-50 g males Southern ningaui, common wambenger common mallee ningaui Common names End
End
End End
) End
End Marsupials of Western Australia. f leucogaster macdonnellensis Pseudantechinus woolleyae Appendix 1 Taxa Dasyuridae Antechinus flavipes ( A . Dasycercus cristicauda Dasykaluta rosamondae Dasycercus blythi Pseudantechinus ningbing Pseudantechinus Pseudantechinus roryi Dasyurus hallucatus Planigale maculata Dasyurus geoffroii Ningaui ridei Phascogale calura Phascogale tapoatafa Antechinomys laniger Planigale ingrami Ningaui yvonnae Parantechinus apicalis Ningaui timealeyi
81 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 2008 2008 2008b et al. et al. 2008d McKenzie 2008 McKenzie 2008 Dickman Churchill Kitchener 2008 Cole 2008 Burbidge 2008a Pearson & Pearson Johnson & Johnson Pearson & Morton & Morton Morton & Morton Burbidge, Friend & Pearson 2008 Dickman 2008a Reference McKenzie & Gordon 2008b Woolley 2008b Friend 2008b McKenzie & Foulkes 2008 McKenzie Woolley 2008g Dickman 2008 E, S1[e] P4 Ex, S2 Status V, S1[v] V, V, S1[v] V, S1[v] regions grasslands. Desert. north and eastern states. ranges of south-west WA. open woodland; isolated the Great Victoria of the Darling Scarp, mallee-heaths in & Morris woodlands or spinifex grasslands of through arid and semi-arid Australia, tropical woodland on blacksoil/sand ; shrublands of hummock grassslands through rocky country through the Pilbara, Gibson Tussock grasslands, low grasslands, Tussock Semi-arid and arid south-western WA SA. Open low Open Primary mulga shrublands and woodlands with tussock Arid, Widely Open understory, through the Pilbara and central continent. Kulumbaru WA and Tiwi Islands NT Habitat Varied habitats across the southern half of continent. of south-west WA. central and southern wheatbelt. Proteaceous shrublands of semi-arid grassland and tussock grass. particularly shrubland and tussock Pilbara and central Australia. south-central red sandplains Desert to Alice Springs. Tropical savannah woodlands; isolated populations Coastal plain and lateritic ) ) Sandplain or sand-dune spinifex grasslands. I. a. barrowensis I. a. auratus 26-55 g males 10-21 g females 15-30 g Open 500-1700 g females 500-3100 g males Varied habitats through tropical 14-25 g Woodlands 14-20 g females 13-19.5 g Body mass Body 18-34 g females8.5-12.0 g in the Kimberley. 305-647 g females 15-25 g 15-25 g 9-17 g males 8-15 g females 25-42 g femalesin populations 250-600 g ( 10-20 g 10-20 18-37 g 18-37 300-670 g ( 200 g (estimated) Sand dunes and sandplains with hummock 31-58 g males 15-24 g males Fat-tailed dunnart Little long-tailed dunnart 11-20 g males Butler’s dunnart Northern brown bandicoot Grey-bellied dunnart Gilbert’s dunnart White-tailed dunnart Hairy-footed dunnart Lesser hairy-footed dunnart Pig-footed bandicoot Numbat, banded anteater 405-752 g malesGolden bandicoot Open woodlands with abundant termite activity. Stripe-faced dunnart Ooldea dunnart Red-cheeked dunnart Sandhill dunnart Common names End ta Long-tailed dunnart
End :
End ; mainland) Sminthopsis crassicaudata Sminthopsis gilberti Sminthopsis dolichura Taxa Sminthopsis butleri Barrow Island) Isoodon macrourus Sminthopsis griseoventer Sminthopsis granulipes Sminthopsis hirtipes Sminthopsis youngsoni Peramelidae Chaeropus ecaudatus Sminthopsis longicauda Myrmecobiidae Myrmecobius fasciatus Isoodon auratus Sminthopsis macroura ( I. a. auratus ( I. a. barrowensis Sminthopsis ooldea Sminthopsis virginiae Sminthopsis psammophila
82 Warburton: Century of marsupial research in WA 2008 2008 et al. et al. Aplin 2008 Templesmith 2008 Webb 2008 Webb Suckling 2008 Benshemesh 2008 Carthew Johnson 2008b Taggart & Renfree 2008 Johnson 2008a Gordon 2008a Friend 2008c ) ) P. b. myosuros P. b. bougainville P3 P5 Paull 2008 ( Ex ( E, S1 [e] S1 E, V, S1[v] Ex, S2 E, S1[e] and heath communities. Kimberley. and dunes fields, hummock low heath or hummock grasslands. containing tree hollows and varied food sources. containing tree hollows and woodland and closed forests of the rugged, P3 Burbidge & Mallee woodlands, heathlands, shrubland and producing Proteaceae and Myrtaceae. Rocky outcrops of the Kimberley and tropical northern Australia. Sand-dune deserts of central Australia. Semi-arid grasslands of southern Australia. Sand-dune deserts of north-western Australia. E, S1[e] Benshemesh & Varied, though prefers dry eucalypt forestsrocky country of the Kerle & How 2008 Gibson desert. dry sclerophyll of southern Australia. Coastal sandplain heaths with abundant nectar- Sandplain and sand-ridge desert with spinifex grassland. Ex, S2 g females 8-16 g females 95-135 g females 1280-2000 g 500-1850 g malesshrub woodland, Forest, 168-280 g malesscrub, Dense 40-70 g 17.5-36 kg females 8-21 g 30-50 g 700-1300 g males750-1200 g females Jarrah, wandoo, marri and especially coastal peppermint forest and woodland. 1300-4500 g males 1200-3500 g females900-2000 gwoodlands. and S1[v] V, Open 2008b Tores de 311 g female 1000-2500 g males800-1100 g females360-435 g males sandplains Desert grasslands and acacia shrubland. 165-379 g females 400-1200 115-160 g males Forest unknown 7-11 g males g 7-11 Sugar glider Sugar Rock ringtail possum Southern brown bandicoot, quenda Western barred bandicoot Southern marsupial mole, Western pygmy possum Northern marsupial mole, kakarratul possum Honey Western ringtail possum Common brushtail possum Scaly-tailed possum Desert bandicoot Lesser bilby Bilby, rabbit-eared bandicoot itjaritjari Southern hairy-nosed wombat 19-36 kg males End
End
End
; End ; Shark Bay)
End
; mainland Petauridae Petaurus breviceps Pseudocheiridae Petropseudes dahli Pseudocheirus occidentalis ( I. o. fusciventer Isoodon obesulus Western Australia) Perameles bougainville ( P. b. bougainville Notoryctes typhlops Burramyidae Cercartetus concinnus Phalangeridae Trichosurus vulpecula Wyulda squamicaudata Notoryctidae Notoryctes caurinus ( P. b. myosuros Western Australia) Perameles eremiana Macrotis leucura Thylacomyidae Macrotis lagotis Vombatidae Lasiorhinus latifrons Tarsipedidae Tarsipes rostratus
83 WA Science—Journal of the Royal Society of Western Australia, 97(1), June 2014 2008b et al. 2008 Friend 2000 Christensen 2008 Start Short 2008 Burbidge Morris & Morris de Tores & Burbidge & Burbidge Kitchener & Johnson & Clancy & Croft 2008 Burbidge & Burbidge Reference Burbidge 2008a Merchant 2008 Hinds 2008 Coulson 2008 ) Johnson 2008 ) ) Burbidge 2008b ) L. h. M. r. L. h. ) L. c. leichardti P4 V, S1[v] V, Ex SW mainland E, S1[e] NTM U2430 V, S1[v] ( bernieri Ritchie 2008 Ex, S2 isabellinus V, S1[v] ( L. c. conspicillatus P3 ( Status Ex, S2 Ex, S2 E, S1[e] ( S1[e] E, spp.; distribution. Gastrolobium dunes of Gibson Desert arid and semiarid with dense sedge understory or CE, S1[ce] Friend 2008a Dense low scrub with adjacent grassy areas for feeding. P5 Riperian vegitation in open forest and adjacent Open forest or woodland with low grass and open thickets. open and or rocky hills. Unknown. Coastal heath with limestone cap-rock, Habitat though formerly more widespread. Scattered to dense vegetation with grass-dominated Tropical grasslands and open shrublands. Varied habitats across southern Australia; consumes ) ); L. h. bernieri 6-10 kg males unknown; similar toand sandplains Arid 6.25-28 kg females Australia usually containing steep escarpments 16-27 kg males unknown 980-1850 g malescontaining thickets Wheatbelt 17-39 kg females principally graze but also some browse. 4-6 kg females ( L. h. NTM U2430 mean 1310 g females 9-15 kg females grasslands of the tropic north. 14-24.5 kg females understory of monsoonal tropical woodlands. 708-1205 g femaleswoodland. closed adjacent 845-1200 g malesheath Melaleuca burrowing bettong1600-4750 g and surrounding areas. ( Body mass Body mean 1220 g males 750-1500 g femalesbroad historically mean 1740 g females shrublands of arid and semi-arid areas. 18.6-51 kg males mean 680 g Burrowing bettong Burrowing Woylie Western grey kangaroogrey Western 18-72 kg males Agile wallaby Antilopine kangaroo Tammar wallaby Broad-faced potoroo Central hare-wallaby Euro, common wallaroo 7.25-60 kg males Varied habitats across arid, semi-arid and tropical( S1[v] V, Gilbert’s potoroo Western brush wallaby, 7-9 kg Spectacled hare-wallaby Rufous hare-wallaby, mala mean 1580 g males Spinifex hummock, tussock grasslands and black gloved wallaby Nullarbor dwarf bettong Common names ; Barrow ; ; mainland) ; Barrow End ; mainland
; mainland) ; End ; Bernier End End
; mainland) End
; Western ; ( M. e. derbianus Potoroidae Bettongia lesueur Bettongia penicillata Taxa Macropus irma Western Australia) Macropus fuliginosus Macropus agilis Macropus antilopinus ( L. h. NTM U2430 Macropus eugenii and Dorre Islands) Island) ( M. r. woodwardi Kimberley) ( M. r. isabellinus Potorous platyops Macropodidae Lagorchestes asomatus ( L. h. bernieri Macropus robustus ( M. r. erubescens Lagorchestes conspicillatus ( L. c. conspicillatus Island) ( L. c. leichardti Lagorchestes hirsutus ( B. p. olgibyi Potorous gilbertii Australia) Bettongia pusilla
84 Warburton: Century of marsupial research in WA 2008 et al. Richards 2008 Pearson 2008 Churchill 2008 Telfer 2008 Eldridge 2008 Gordon 2008 Pearson & Pearson Sanson & Sanson Ingleby & Eldridge & Eldridge Burbidge 2008b Eldridge & Eldridge de Tores 2008a ) Prince & L. f. L. f. albipilis V, S1[v] V, S1[v] ( fasciatus) Ex ( Ex, S2 V, S1[v] with rocky shelter. spp. Acacia woodland and vine thickets with P4 Pearson vegetation including floodplain, vine thickets, Open woodlands with tussock grass or grasslands Dense thickets of Varied habitats in arid and semi-arid Australia. Rocky environments with surrounding spinifex rocky outcrops. Ashburton regions. 1.0-2.3 kg 1.6-3.5 kg females riparian vegetation. 17-39 kg females Archipelago 960-1430 gopen Low 2.6-3.9 kg Dampier grasslands and shrublands of the Pilbara 1070-1700 g femalesgrassland and rainforest, 4.5-7 kg females scattered trees or shrubs of northern Australia. 2.2-4.7 kg females woodland in the Kimberley and NT. 2.7-4.2 kg males Shrub thickets and sedges on Rottnest Island; Banded hare-wallaby, merrnine Red kangaroo 22-92 kg males Open plains of arid and semi-arid Australia. Croft & Clancy 2008 Crescent nail-tail wallaby ~3.5 kg Monjon Rothschild’s rock-wallaby 3.7-6.6 kg mainland Quokka Nabarlek, little rock wallaby 1050-1500 g malesBlack-flanked rock-wallaby, 4.1-5.3 kg males Varied Varied and discontinuous rocky habitats. Northern nail-tail wallabyShort-eared rock-wallaby 6-9 kg males 3.2-5.6 kg males Rocky hills, gorges and escarpments with savannah ; Black-footed rock-wallabyfemales kg 3.1-3.8 End ; West End E End
End End
; Bernier End ; mainland) ; mainland) ; south coast hacketti fasciatus
indicates taxa endemic to Western Australia. Ex, extinct (taxa not definitely located in the wild during past 50 years) CE, critically endangered (taxa facing an extremely high risk of extinction in the wild immediate future E, endangered (taxa facing a very high risk of extinction in the wild near future) V, vulnerable (taxa facing a high risk of extinction in the wild medium-term future) S1, Schedule 1 (threatened fauna; fauna that is rare or likely to become extinct) with rankings shown in square parentheses: [ce], critically endangered; [e], [v], vulnerable. S2, Schedule 2 (fauna that is presumed to be extinct) P1, Priority 1 (poorly known species on threatened lands) P2, Priority 2 (poorly known species on conservation lands) P3, Priority 3 (poorly known species, some on conservation lands) P4, Priority 4 (rare, near threatened and other species in need of monitoring) P5, Priority 5 (conservation dependent species) Lagostrophus fasciatus ( L. f. albipilis ( L. f. Environment Protection and Biodiversity Conservation Act 1999 status codes: Western Australian Wildlife Conservation Act 1950 status codes: Western Australian Department of Environment and Conservation (DEC) priority species status codes: Macropus rufus Onychogalea lunata and Dorre Islands) End MacDonnell Ranges) (P. l. islands) ( P. l. lateralis ( P. l. WAM M15135 Kimberley) Petrogale rothschildi Setonix brachyurus Petrogale concinna Petrogale lateralis ( P. l. ANWC CM15314 Onychogalea unguifera Petrogale brachyoti Petrogale burbidgei
85