Carnivores of Australia: Past, Present and Future

The Australian continent provides a unique perspective on the evolution and ecology of carnivorous animals. In earlier ages, Australia provided the arena for a spectacular radiation of marsupial and reptilian predators. The causes of their extinctions are still the subject of debate. Since European settlement, Australia has seen the extinction of one large marsupial predator (the thylacine), another (the Tasmanian devil) is in danger of imminent extinction, and still others have suffered dramatic declines. By contrast, two recently-introduced predators, the fox and cat, have been spectacularly successful, with devastating impacts on the Australian fauna.

Carnivores of Australia: Past, Present and Future explores Australia's unique predator communities from pre-historic, historic and current perspectives. It covers mammalian, reptilian and avian carnivores, both native and introduced to Australia. It also examines the debate surrounding how best to manage predators to protect livestock and native biodiversity.

Wildlife managers, academics and postgraduate students will benefit from the most up-to-date synthesis by leading researchers and managers in the field of carnivore biology. By emphasising Australian carnivores as exemplars of flesh-eaters in other parts of the world, this book will be an important reference for researchers, wildlife managers and students worldwide.

Winner of a 2015 Whitley Awards Certificate of Commendation for Zoological Text.

• Language: English
• Publisher: CSIRO PUBLISHING
• Release date: Nov 5, 2014
• ISBN: 9780643103184

Book preview

INTRODUCTION

Alistair S. Glen and Chris R. Dickman

Carnivores play a strong role in the functioning of the world’s ecosystems (Estes et al. 2011), and the carnivores of Australia are no exception. For many millions of years, Australia boasted a spectacular array of fierce predators, including giant marsupials, reptiles and birds, most of which have now disappeared. The causes of their extinctions are still debated. Since European settlement, Australia has seen the extinction of one large marsupial predator (the thylacine), while another (the Tasmanian devil) is in danger of imminent extinction, and still others have suffered dramatic declines.

By contrast, two recently introduced predators, the European red fox and the feral house cat, have been spectacularly successful at exploiting the Australian environment, and continue to have devastating impacts on the native fauna. The dingo* was also brought to Australia by humans, although after more than 4000 years on the continent it is viewed by many as native. Dingoes can have both positive and negative impacts on biodiversity, and on the pastoral industry. While predation of livestock is a problem, dingoes may also help suppress pests such as large herbivores, foxes and feral cats. The issue of how to manage the dingo is further complicated by uncertainty about the purity of remaining dingo populations, many of which are gradually becoming hybridised with domestic dogs.

This volume explores Australia’s unique predator communities from prehistoric, historic and current perspectives, examines the biology of many individual species, and uses the insights gained to suggest future directions in management and research. This book is about ‘carnivores with a small c’. In other words, we do not deal only with mammals in the order Carnivora. Instead, we take a broader approach, defining carnivores as predators of vertebrate prey. This expansive definition allows us to include carnivorous birds, reptiles and mammals. Only by viewing these animals as components in diverse and complex ecosystems will we preserve Australia’s priceless biological heritage and economic prosperity.

References

Crowther MS, Fillios M, Colman N, Letnic M (2014) An updated description of the Australian dingo (Canis dingo Meyer, 1793). Journal of Zoology 293, 192–203.

Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of Planet Earth. Science 333, 301–306.

* The dingo has recently been described as a distinct species (Canis dingo) (Crowther et al. 2014). It was previously considered to be a subspecies of wolf, and was classified as Canis lupus dingo. Nomenclature has been altered throughout the book to reflect this change.

1

The importance of predators

Alistair S. Glen and Chris R. Dickman

Summary

The importance of predators for ecosystem function is being recognised increasingly around the world. Predators can have a strong influence not only on their prey but also on one another, with cascading effects on many species and ecosystem processes. Removal of top-order predators can alter the behaviour and abundance of other species, including herbivores and smaller predators. In turn, this can have profound impacts on vegetation and small vertebrate communities. Here, we briefly outline the importance of predators in shaping the past and present biota of Australia. In prehistoric times, Australia was inhabited by a diverse range of avian, mammalian and reptilian carnivores. Although most of the largest carnivores died out in the Pleistocene or earlier, Australia still supports a vast array of flesh-eaters ranging in size from tiny insectivorous mammals to hulking 7-m crocodiles. These animals vary enormously in their diets, habitat preferences and hunting behaviours. Accordingly, they have very different ecological impacts. Predators have been instrumental in the declines and extinctions of many species, but may also be the saviours of many others. For example, dingoes may help to maintain biodiversity by suppressing large herbivores and smaller predators. Just as predator communities have changed over evolutionary time, they will continue to change in future. The impacts of humans and introduced species are still playing out on the Australian landscape, and many carnivores are threatened with extinction. The shape of things to come will depend largely on the wildlife management practices of today. To maintain or restore functioning ecosystems, wildlife managers must consider the ecological importance of predators.

The importance of predators

The importance of predators for ecosystem function is receiving ever-increasing recognition. For decades, a ‘doomed surplus’ paradigm predominated in ecology; this stated that predators had little influence on prey populations and took only individuals that were surplus to the population while prey abundance was determined by density-dependent processes such as intraspecific competition and density-independent processes such as weather (Errington 1946). Although this may be true in some systems (e.g. Banks 1999), there is no longer any doubt that predators often do limit or even regulate prey populations (Krebs et al. 1995; Pech et al. 1995; Terborgh et al. 1999; Ale and Whelan 2008; Salo et al. 2010). (Limiting factors determine a population’s equilibrium density; regulation is a density-dependent process that forces the population towards equilibrium (Sinclair and Pech 1996)). It is increasingly clear, in addition, that predators can strongly influence not only their prey but also one another (Palomares and Caro 1999; Glen and Dickman 2005; Donadio and Buskirk 2006; Ritchie and Johnson 2009). Through processes of competition and intraguild predation, predators can have a profound influence on each other’s abundance, distribution and resource use. Because the impacts of different predator species on prey populations are not necessarily equivalent, this in turn can have a strong effect on prey species, and ultimately even on the cover, composition and diversity of vegetation. Such interactions, which extend through multiple links in a food web, are called trophic cascades (Paine 1980; Pace et al. 1999; Schmitz et al. 2000).

Some predators facilitate the coexistence of species at lower trophic levels, thereby increasing biodiversity. Such effects were first described by Paine (1966, 1969), who dubbed these influential species ‘keystone predators’. The keystone concept has since been broadened and adapted such that any species (not necessarily a predator) is regarded as a keystone if its ecological influence is disproportionately large relative to its abundance (Heywood 1995; Power et al. 1996). Top-order predators are often keystone species. For example, wolves (Canis lupus lupus) in North America strongly influence the abundance, distribution and behaviour of ungulates (Ripple and Beschta 2003; Frank 2008), as well as smaller predators such as coyotes (C. latrans) (Switalski 2003; Berger and Gese 2007). This in turn has a strong influence on vegetation, small vertebrates and even some invertebrates (Hebblewhite et al. 2005). Thus, the presence of wolves alters the entire ecosystem structure by changing the composition of plant and animal communities. As discussed in later chapters (see Chapters 13 and 18), evidence suggests that Australia too has a keystone predator in the form of the dingo (C. dingo).

Across much of the globe, the removal of apex predators (those at the highest trophic level) has been linked with increased populations of smaller predators, and corresponding declines in small vertebrate prey (Soulé et al. 1988; Crooks and Soulé 1999; Johnson et al. 2007; Ritchie and Johnson 2009; Elmhagen et al. 2010). These effects appear to be pervasive in aquatic as well as in terrestrial systems (Pace et al. 1999; Myers et al. 2007; Heithaus et al. 2008). The absence of top-order predators can also lead to increased abundance of large herbivores such as moose (Alces alces) and elk (Cervus elaphus) in North America (McLaren and Peterson 1994; Ripple and Beschta 2007) or kangaroos (Macropus spp.), feral goats (Capra hircus) and feral pigs (Sus scrofa) in Australia (Caughley et al. 1980; Newsome 1990; Pople et al. 2000). This can have profound impacts on vegetation communities by increasing total grazing pressure, and by changing the spatial pattern of herbivory as prey reduce their vigilance behaviours and begin to forage in areas that were too dangerous when predators were present (Ripple and Beschta 2007; Ale and Whelan 2008; Calcagno et al. 2011). Thus, the impacts of top-order predators can extend down through multiple links in a food chain, potentially influencing the abundance and diversity of species at all trophic levels. Clearly, the role of predators in ecosystems is a vitally important one. In this introductory chapter we briefly outline the importance of predators in shaping the past and present biota of Australia. Throughout the book, the word ‘carnivore’ refers not just to the mammalian order Carnivora, but to vertebrate predators in general, including mammals, reptiles and birds of prey (see Chapters 11 and 12).

The prehistoric fauna of Australia featured myriad carnivorous birds, reptiles and mammals. These varied greatly in body size and predatory habits but some, such as the marsupial lion (Thylacoleo carnifex), sported fierce weaponry that likely allowed them to kill very large prey (Wroe et al. 1999, 2005). Other large prehistoric carnivores included an omnivorous macropod (Propleopus oscillans), a giant monitor lizard (Varanus priscus), a crocodile (Quinkana fortirostrum) that may have been terrestrial, and a large snake (Wonambi naracoortensis) (Flannery 1994; Johnson 2006; see Chapter 3). There was also a giant flightless bird, Bullockornis planei, the ‘demon duck of doom’ with an enormous head and powerful beak suggesting a carnivorous habit (Pain 2000). In addition, two carnivores that survived until modern times only in Tasmania were also widespread on the Australian mainland until the mid to late Holocene. The thylacine (Thylacinus cynocephalus) and Tasmanian devil (Sarcophilus harrisii)¹ occupied the niches of a cursorial predator and bone-cracking scavenger (Johnson 2006). The impacts of these animals on their environment can only be inferred indirectly. For example, there has been some debate as to whether thylacines (Jones and Stoddart 1998; Johnson and Wroe 2003; Wroe et al. 2005, 2007; Attard et al. 2011) and marsupial lions (Flannery 1994; Wroe 2002) were predators of large prey; there is also some contention as to whether reptilian or mammalian predators were dominant (Flannery 1994; Wroe 2002; see Chapters 2 and 3). While the precise ecological roles of these animals are subject to debate, it is clear that Australia provided the arena for a spectacular radiation of avian, marsupial and reptilian predators.

Although most of the largest carnivores died out in the Pleistocene or earlier (Johnson 2006; Wroe 2007; see Chapter 3), Australia still supports a vast array of small to medium-sized flesh-eaters, as well as some formidably large ones. The modern-day carnivore assemblage includes birds, reptiles and mammals, both native and introduced, and spans several orders of magnitude in size from tiny insectivorous mammals to crocodiles reaching 7 m in length. Although insectivorous mammals are enormously important to the ecology of Australia (see Chapter 10), the focus of this book (and therefore this chapter) is primarily on larger, flesh-eating predators. These animals employ various strategies to kill a wide range of prey species, and accordingly have very different impacts on populations of prey and other predators. For example, powerful owls (Ninox strenua) have been observed to prey so heavily upon greater gliders (Petauroides volans) that they drove an abundant local population close to extinction within five years (Kavanagh 1988). Gliders are also important prey for some populations of spotted-tailed quolls (Dasyurus maculatus). This raises the possibility, as yet untested, that owls and quolls might compete for prey (Glen and Dickman 2011), as do letter-winged kites (Elanus scriptus) and introduced mammalian predators in Australia’s arid interior (Pavey et al. 2008). Thus, predators with vastly different hunting modes (aerial and terrestrial) can be direct competitors. In another example, predation by lace monitors (V. varius) and diamond pythons (Morelia spilota spilota) was instrumental in preventing a population of ringtail possums (Pseudocheirus peregrinus) from recovering after bushfire. This was despite the release of translocated animals to supplement the possum population (Russell et al. 2003).

However, perhaps the most dramatic effects are those of introduced predators, which have had greater impacts in Australia than on any other continent (Salo et al. 2007). European red foxes (Vulpes vulpes) have been implicated in the decline and extinction of many native Australian animals (Bur-bidge and McKenzie 1989; Dickman 1996a; Kinnear et al. 2002, 2010; Saunders et al. 2010; see Chapter 5). Because of their impacts on biodiversity and agriculture, foxes are targeted for control across much of Australia (Saunders et al. 1995; see Chapter 6). Foxes can limit populations of native animals through predation (Kinnear et al. 1988, 1998; Banks et al. 2000; Dexter and Murray 2009). They can also affect native predators such as quolls (Dasyurus spp.) (Morris et al. 2003; Glen et al. 2009; Glen and Dickman 2011), goannas (Varanus spp.) (Olsson et al. 2005; Sutherland et al. 2011) and predatory birds (Pavey et al. 2008) through competition and/or intraguild predation. Cats (Felis catus), whether domestic, stray or feral, can also have strong impacts on native prey (Dickman 1996a, b; Risbey et al. 2000; Denny and Dickman 2010; see Chapter 8) and predators (Glen et al. 2009, 2010; Sutherland et al. 2011). For example, following fox control in Shark Bay, Western Australia, predation by feral cats was apparently responsible for an 80% reduction in small mammal captures (Risbey et al. 2000). Also in Shark Bay, eradication of feral cats from Faure Island caused a large increase in sightings of a native predator, the sand goanna (V. gouldii) (Rowles 2008).

Of course, the impacts of introduced predators are not restricted to native species. Predation by foxes and cats can also regulate populations of introduced European rabbits (Oryctolagus cuniculus) (Pech et al. 1992; Banks 2000), and foxes are considered an agricultural pest due to their predation on livestock (Saunders et al. 1995, 2010). Foxes and cats may also have impacts on each other, either through competition for resources or through direct aggression. The two species have strongly overlapping patterns of resource use, indicating potential for competition (Molsher 1999; Glen et al. 2011), and foxes usually dominate cats in direct encounters (Molsher 1999). Several studies have also found cat remains in the diet of foxes, suggesting intraguild predation (Coman 1973; Brunner et al. 1991; Risbey et al. 1999; Paltridge 2002). Perhaps as a result of such interactions, foxes appear to limit the abundance and local distribution of cats. Smith and Quin (1996) showed that the distributions of foxes and cats were inversely related, suggesting exclusion of cats by foxes. Consistent with this, removal of foxes has been associated with increased abundance of cats (Short et al. 1995; Risbey et al. 2000; Davey et al. 2006).

In addition to the lethal effects of predation, there is abundant evidence from Australia that predators can alter the behaviour and resource use patterns of other species. Animals must balance the need to obtain essential resources (e.g. food, water, shelter) with the need to avoid being killed by a predator. This can result in a trade-off whereby resources are used less than optimally in order to reduce predation risk (Brown 1988; Lima and Dill 1990; Brown et al. 1999). For example, saltwater crocodiles (Crocodylus porosus) prey on a range of terrestrial mammals (Taylor 1979) including agile wallabies (Macropus agilis), which they ambush near the water’s edge (Doody et al. 2007). In order to reduce their risk of predation, the wallabies have adopted an extraordinary tactic. Rather than drink at the river’s edge, they prefer where possible to dig for subterranean water some distance from the bank. This requires much more time and energy than drinking directly from the river, and therefore carries costs; however, these are presumably outweighed by the benefits of reduced predation risk (Doody et al. 2007). The sublethal effects of predators can be as important for ecosystem function as their lethal effects. For example, spiders can change the behaviour of their grasshopper prey, with flow-on effects for plant diversity, nitrogen mineralisation rate and net primary productivity (Schmitz 2008).

Native species also alter their behaviour in order to reduce their risk of predation from cats and foxes. In the presence of foxes, brushtail possums (Trichosurus vulpecula vulpecula) in central New South Wales are more active in trees, and forage less on the ground (Gresser 1996; Pickett et al. 2005). Similarly, the Western Australian koomal (T. v. hypoleucus) responds to higher densities of predators (foxes, cats and chuditch, Dasyurus geoffroii) by foraging in denser microhabitats (Cruz et al. 2013). This raises the possibility of managing predation risk by manipulating habitat (e.g. Stokes et al. 2004; Arthur et al. 2005). Many other Australian animals modify their foraging behaviour in response to real or perceived risk of predation (e.g. Blumstein et al. 2000; Banks 2001; Strauß et al. 2008). Indeed, evidence is beginning to emerge that some native species can distinguish and avoid cues to the presence of particular predators, suggesting that modifications to behaviour are not simply generic responses to risk. Kovacs et al. (2012) proposed recently that, for survivors of the initial impact of the arrival of foxes and cats, there would have been intense selection to discriminate and avoid the new predator archetypes (see also Carthey and Banks 2012).

Predators can exert ‘fear effects’ not only on prey but also on other predators. Direct aggression is common among carnivores, and often fatal due to their behavioural and morphological adaptations for killing (Dickman 1991; Palomares and Caro 1999; Creel et al. 2001; Donadio and Buskirk 2006; Ritchie and Johnson 2009). Just as prey alter their behaviour for fear of predation, so too subordinate predators are influenced by fear of larger ones. For example, many birds of prey alter their behaviour or habitat use in order to reduce their risk of predation by larger raptors (Sergio et al. 2007; Sergio and Hiraldo 2008). In Australia, wedge-tailed eagles (Aquila audax) prey on a wide range of smaller raptors (Brooker and Ridpath 1980); however, the effects of such intraguild predation on the abundances and behaviour of the smaller victims are unknown. Similar interactions also occur between mammalian predators in Australia. There is abundant evidence to show that larger predators are aggressive towards smaller ones. For example, dingoes (Canis dingo) are aggressive towards foxes (Marsack and Campbell 1990), foxes towards cats (Molsher 1999), and cats towards chuditch (Glen et al. 2010). It has been hypothesised that fear of dingoes deters foxes and cats from using certain areas or resource patches (O’Neill 2002; Brawata and Neeman 2011). This is quite plausible, as recent observations show that dingoes kill but do not eat the smaller introduced predators if they encounter them (Moseby et al. 2012). This exclusion effect may provide indirect protection for small and medium-sized prey, which are vulnerable to cats and foxes. Of course, dingoes themselves also prey upon vulnerable species, but they consume a wide size range of prey and their impacts are thus not focused on smaller species. This is partly due to the behavioural plasticity of dingoes. When small prey becomes scarce, dingoes can switch to hunting in packs, targeting larger prey (Corbett and Newsome 1987). By contrast, foxes and cats prey almost exclusively on small to medium-sized species, which are often the most vulnerable to decline and extinction (Burbidge and McKenzie 1989; Johnson and Isaac 2009). Dingoes also have large home ranges and tend to occur at low population densities. This may reduce the risk of small prey species encountering a dingo. Foxes and cats, on the other hand, have smaller home ranges and can exist at higher densities (Ritchie and Johnson 2009).

The potential biodiversity benefits of dingoes have led to suggestions for their restoration in parts of Australia where they are currently suppressed (Dickman et al. 2009; Bowman 2012). Just as reintroduction of wolves has led to ecosystem restoration in Yellowstone National Park, USA (e.g. Clark et al. 1999; Ripple and Beschta 2007), reinstating the top-order predator in parts of the Australian landscape could reduce overgrazing by large herbivores, minimise the impacts of foxes and cats, and deliver far-reaching ecological benefits (Dickman et al. 2009). However, before any such action could be taken, there are several questions that need to be investigated. First, the purported benefits of dingo restoration must be demonstrated (Glen et al. 2007; Dickman et al. 2009), and any potential threats posed by dingoes evaluated (Allen and Fleming 2012; Fleming et al. 2012). The comparative roles of dingoes, feral dogs and hybrids must also be clarified (see Chapter 7). Just as importantly, effective alternative measures need to be developed to protect livestock from predation by dingoes (Dickman et al. 2009; see Chapter 14).

Conservation of apex predators has also been promoted in other parts of the world as a tool for conserving broader biodiversity (Ritchie et al. 2012). The presence of top-order predators is often associated with high levels of biodiversity (Sergio et al. 2005), either because these predators select such areas, or because their presence actually enhances biodiversity, for example, through keystone predation (Sergio et al. 2006). Thus, apex predators may be useful either as indicator species guiding the placement of reserves and other conservation measures, or as strongly interactive species enhancing biodiversity and ecosystem function (Sergio et al. 2008). Other potential conservation roles for top-order predators include acting as umbrella, sentinel or flagship species (Caro and O’Doherty 1999; Ray 2005; Sergio et al. 2008).

As we have seen from this introductory discussion, predators represent an important component of ecosystems in Australia and globally. Why then is their importance often overlooked? One possibility, alluded to in our opening paragraph, is a tendency for ecologists and wildlife managers to draw a false dichotomy between ecosystems that are driven by top-down or bottom-up processes. We must be mindful that these concepts are not mutually exclusive. Although much has been written on the relative importance of top-down and bottom-up influences on ecosystems, the reality is that both can be important (Polis and Strong 1996; Polis 1999; Terborgh et al. 2001; Sinclair 2003; Elmhagen and Rushton 2007). For example, the Australian arid zone experiences a cycle of boom and bust driven primarily from the bottom up by rainfall (Stafford Smith and Morton 1990; Letnic et al. 2005; Letnic and Dickman 2010; Morton et al. 2011). However, top-down processes such as predation also play an important role in these systems, driving prey populations to low abundance during drought (Letnic and Dickman 2010; Letnic et al. 2011). In the most extreme case, a population depleted by drought may be driven to extinction by predators. Bottom-up forces, however strong, cannot resurrect a species from extinction. In reality, populations are not driven exclusively by top-down or bottom-up processes, but by the interaction of the two (Boyce and Anderson 1999).

The assemblage of Australian carnivores has changed through time as a result of evolution, extinctions and species introductions. Ecosystems are still in a state of flux as they adjust to the relatively recent arrival of foxes and cats, suppression of dingoes, and many other anthropogenic influences. Many of Australia’s carnivores have suffered dramatic range declines, and many are threatened with extinction (see Chapter 9). Their intrinsic value alone makes them a priority for conservation. However, the persistence of other species, and of ecological processes, may also depend on predator conservation.

Acknowledgements

We thank R. Pech and A. Pople for helpful comments on a previous draft. A. Glen was supported by Landcare Research Capability Funding, and C. Dickman by an Australian Research Council Professorial Fellowship.

Endnote

1   DNA from three scats found in Tasmania between 1986 and 2002 have been ascribed to an as-yet undescribed species similar to the Tasmanian devil (Bevers et al. 2011). Confirmation awaits further study.

References

Ale SB, Whelan CJ (2008) Reappraisal of the role of big, fierce predators! Biodiversity and Conservation 17, 685–690.

Allen BL, Fleming PJS (2012) Reintroducing the dingo: the risk of dingo predation to threatened vertebrates of western New South Wales. Wildlife Research 39, 35–50.

Arthur AD, Pech RP, Dickman CR (2005) Effects of predation and habitat structure on the population dynamics of house mice in large outdoor enclosures. Oikos 108, 562–572.

Attard MRG, Chamoli U, Ferrara TL, Rogers TL, Wroe S (2011) Skull mechanics and implications for feeding behaviour in a large marsupial carnivore guild: the thylacine, Tasmanian devil and spotted-tailed quoll. Journal of Zoology 285, 292–300.

Banks PB (1999) Predation by introduced foxes on native bush rats in Australia: do foxes take the doomed surplus? Journal of Applied Ecology 36, 1063–1071.

Banks PB (2000) Can foxes regulate rabbit populations? The Journal of Wildlife Management 64, 401–406.

Banks PB (2001) Predation-sensitive grouping and habitat use by eastern grey kangaroos: a field experiment. Animal Behaviour 61, 1013–1021.

Banks PB, Newsome AE, Dickman CR (2000) Predation by red foxes limits recruitment in populations of eastern grey kangaroos. Austral Ecology 25, 283–291.

Berger KM, Gese EM (2007) Does interference competition with wolves limit the distribution and abundance of coyotes? Journal of Animal Ecology 76, 1075–1085.

Bevers J, Robertson S, Zinck J, Hyde ZD, Ruedas LA (2011) Mitochondrial DNA reveals a new species of carnivorous marsupial in Tasmania. In: ‘Proceedings of the Joint American Society of Mammalogists/Australian Mammal Society Conference.’ p. 14. (American Society of Mammalogists: Portland).

Blumstein DT, Daniel JC, Griffin AS, Evans CS (2000) Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators. Behavioral Ecology 11, 528–535.

Bowman D (2012) Conservation: Bring elephants to Australia? Nature 482, 30.

Boyce MS, Anderson EM (1999) Evaluating the role of carnivores in the Greater Yellowstone Ecosystem. In: ‘Carnivores in Ecosystems: The Yellowstone Experience.’ (Eds TW Clark, AP Curlee, SC Minta and PM Kareiva). pp. 265–283. (Yale University Press: New Haven).

Brawata RL, Neeman T (2011) Is water the key? Dingo management, intraguild interactions and predator distribution around water points in arid Australia. Wildlife Research 38, 426–436.

Brooker MG, Ridpath MG (1980) The diet of the wedge-tailed eagle Aquila audax in Western Australia. Australian Wildlife Research 7, 433–452.

Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology 22, 37–47.

Brown JS, Laundre JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. Journal of Mammalogy 80, 385–399.

Brunner H, Moro D, Wallis R, Andrasek A (1991) Comparison of the diets of foxes, dogs and cats in an urban park. Victorian Naturalist 108, 34–37.

Burbidge AA, McKenzie NL (1989) Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biological Conservation 50, 143–198.

Calcagno V, Sun C, Schmitz OJ, Loreau M (2011) Keystone predation and plant species coexistence: the role of carnivore hunting mode. American Naturalist 177, E1–E13.

Caro TM, O’Doherty G (1999) On the use of surrogate species in conservation biology. Conservation Biology 13, 805–814.

Carthey AJR, Banks PB (2012) When does an alien become a native species? A vulnerable native mammal recognizes and responds to its long-term alien predator. PLoS ONE 7, e31804.

Caughley G, Grigg GC, Caughley J, Hill GJE (1980) Does dingo predation control the densities of kangaroos and emus? Australian Wildlife Research 7, 1–12.

Clark TW, Curlee AP, Minta SC, Kareiva PM (eds) (1999) ‘Carnivores in Ecosystems: the Yellowstone Experience’. (Yale University Press: New Haven).

Coman BJ (1973) The diet of red foxes, Vulpes vulpes L., in Victoria. Australian Journal of Zoology 21, 391–401.

Corbett LK, Newsome AE (1987) The feeding ecology of the dingo. 3. Dietary relationships with widely fluctuating prey populations in arid Australia – an hypothesis of alternation of predation. Oecologia 74, 215–227.

Creel S, Spong G, Creel N (2001) Interspecific competition and the population biology of extinction-prone carnivores. In: ‘Carnivore Conservation.’ (Eds JL Gittleman, SM Funk, DW Macdonald and RK Wayne). pp. 35–60. (Cambridge University Press: Cambridge).

Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400, 563–566.

Cruz J, Sutherland DR, Anderson D, Glen AS, de Tores P, Leung LK-P (2013) Antipredator responses of koomal (Trichosurus vulpecula hypoleucus) against introduced and native predators. Behavioral Ecology and Sociobiology 67, 1329–1338.

Davey C, Sinclair ARE, Pech RP, Arthur AD, Krebs CJ, Newsome AE, Hik D, Molsher R, Allcock K (2006) Do exotic vertebrates structure the biota of Australia? An experimental test in New South Wales. Ecosystems 9, 992–1008.

Denny EA, Dickman CR (2010) ‘Review of Cat Ecology and Management Strategies in Australia’. (Invasive Animals CRC: Canberra).

Dexter N, Murray A (2009) The impact of fox control on the relative abundance of forest mammals in East Gippsland, Victoria. Wildlife Research 36, 252–261.

Dickman CR (1991) Mechanisms of competition among insectivorous mammals. Oecologia 85, 464–471.

Dickman CR (1996a) Impact of exotic generalist predators on the native fauna of Australia. Wildlife Biology 2, 185–195.

Dickman CR (1996b) ‘Overview of the Impacts of Feral Cats on Australian Native Fauna’. (Australian Nature Conservation Agency: Canberra).

Dickman CR, Glen AS, Letnic M (2009) Reintroducing the dingo: can Australia’s conservation wastelands be restored? In: ‘Reintroduction of Top-Order Predators.’ (Eds MW Hayward and MJ Somers). pp. 238–269. (Wiley-Blackwell: Oxford).

Donadio E, Buskirk SW (2006) Diet, morphology, and interspecific killing in Carnivora. American Naturalist 167, 524–536.

Doody JS, Sims RA, Letnic M (2007) Environmental manipulation to avoid a unique predator: drinking hole excavation in the agile wallaby, Macro-pus agilis. Ethology 113, 128–136.

Elmhagen B, Ludwig G, Rushton SP, Helle P, Linden H (2010) Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. Journal of Animal Ecology 79, 785–794.

Elmhagen B, Rushton SP (2007) Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecology Letters 10, 197–206.

Errington PL (1946) Predation and vertebrate populations. The Quarterly Review of Biology 21, 144–177.

Flannery TF (1994) ‘The Future Eaters: An Ecological History of the Australasian Lands and People’. (Reed Books: Port Melbourne).

Fleming PJS, Allen BL, Ballard G-A (2012) Seven considerations about dingoes as biodiversity engineers: the socioecological niches of dogs in Australia. Australian Mammalogy 34, 119–131.

Frank DA (2008) Evidence for top predator control of a grazing ecosystem. Oikos 117, 1718–1724.

Glen AS, Berry O, Sutherland DR, Garretson S, Robinson T, de Tores PJ (2010) Forensic DNA confirms intraguild killing of a chuditch (Dasyurus geoffroii) by a feral cat (Felis catus). Conservation Genetics 11, 1099–1101.

Glen AS, de Tores PJ, Sutherland DR, Morris KD (2009) Interactions between chuditch (Dasyurus geoffroii) and introduced predators: a review. Australian Journal of Zoology 57, 347–356.

Glen AS, Dickman CR (2005) Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biological Reviews of the Cambridge Philosophical Society 80, 387–401.

Glen AS, Dickman CR (2011) Why are there so many spotted-tailed quolls Dasyurus maculatus in parts of north-eastern New South Wales? Australian Zoologist 35, 711–718.

Glen AS, Dickman CR, Soulé ME, Mackey BG (2007) Evaluating the role of the dingo as a trophic regulator in Australian ecosystems. Austral Ecology 32, 492–501.

Glen AS, Pennay M, Dickman CR, Wintle BA, Firestone KB (2011) Diets of sympatric native and introduced carnivores in the Barrington Tops, eastern Australia. Austral Ecology 36, 290–296.

Gresser S (1996) ‘Anti-predator behaviour of the common brushtail possum (Trichosurus vulpecula) at Burrendong Dam, NSW’. BSc(Hons) Thesis. (University of Sydney: Sydney).

Hebblewhite M, White CA, Nietvelt CG, McKenzie JA, Hurd TE, Fryxell JM, Bayley SE, Paquet PC (2005) Human activity mediates a trophic cascade caused by wolves. Ecology 86, 2135–2144.

Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends in Ecology & Evolution 23, 202–210.

Heywood VH (1995) ‘Global Biodiversity Assessment’. (Cambridge University Press: Cambridge).

Johnson C (2006) ‘Australia’s Mammal Extinctions: a 50,000 Year History’. (Cambridge University Press: Cambridge).

Johnson CN, Isaac JL (2009) Body mass and extinction risk in Australian marsupials: The ‘Critical Weight Range’ revisited. Austral Ecology 34, 35–40.

Johnson CN, Isaac JL, Fisher DO (2007) Rarity of a top predator triggers continent-wide collapse of mammal prey: dingoes and marsupials in Australia. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 341–346.

Johnson CN, Wroe S (2003) Causes of extinction of vertebrates during the holocene of mainland Australia: arrival of the dingo, or human impact? The Holocene 13, 941–948.

Jones ME, Stoddart DM (1998) Reconstruction of the predatory behaviour of the extinct marsupial thylacine (Thylacinus cynocephalus). Journal of Zoology 246, 239–246.

Kavanagh RP (1988) The impact of predation by the powerful owl Ninox strenua on a population of the greater glider Petauroides volans. Australian Journal of Ecology 13, 445–450.

Kinnear JE, Krebs CJ, Pentland C, Orell P, Holme C, Karvinen R (2010) Predator-baiting experiments for the conservation of rock-wallabies in Western Australia: a 25-year review with recent advances. Wildlife Research 37, 57–67.

Kinnear JE, Onus ML, Bromilow RN (1988) Fox control and rock-wallaby population dynamics. Australian Wildlife Research 15, 435–450.

Kinnear JE, Onus ML, Sumner NR (1998) Fox control and rock-wallaby population dynamics: II. An update. Wildlife Research 25, 81–88.

Kinnear JE, Sumner NR, Onus ML (2002) The red fox in Australia: an exotic predator turned bio-control agent. Biological Conservation 108, 335–359.

Kovacs EK, Crowther MS, Webb JK, Dickman CR (2012) Population and behavioural responses of native prey to alien predation. Oecologia 168, 947–957.

Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, Dale MRT, Martin K, Turkington R (1995) Impact of food and predation on the snowshoe hare cycle. Science 269, 1112–1115.

Letnic M, Dickman CR (2010) Resource pulses and mammalian dynamics: conceptual models for hummock grasslands and other Australian desert habitats. Biological Reviews of the Cambridge Philosophical Society 85, 501–521.

Letnic M, Story P, Story G, Field J, Brown O, Dickman CR (2011) Resource pulses, switching trophic control, and the dynamics of small mammal assemblages in arid Australia. Journal of Mammalogy 92, 1210–1222.

Letnic M, Tamayo B, Dickman CR (2005) The responses of mammals to la Niña (el Niño southern oscillation)-associated rainfall, predation, and wildfire in central Australia. Journal of Mammalogy 86, 689–703.

Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.

Marsack P, Campbell G (1990) Feeding behaviour and diet of dingoes in the Nullarbor region, Western Australia. Australian Wildlife Research 17, 349–358.

McLaren BE, Peterson RO (1994) Wolves, moose and tree rings on Isle Royale. Science 266, 1555–1558.

Molsher RL (1999) ‘The ecology of feral cats (Felis catus) in open forest in New South Wales: interactions with food resources and foxes’. PhD Thesis. (University of Sydney: Sydney).

Morris K, Johnson B, Orell P, Gaikhorst G, Wayne A, Moro D (2003) Recovery of the threatened chuditch (Dasyurus geoffroii): a case study. In: ‘Predators with Pouches: the Biology of Carnivorous Marsupials.’ (Eds M Jones, C Dickman and M Archer). pp. 435–451. (CSIRO Publishing: Collingwood).

Morton SR, Smith DMS, Dickman CR, Dunkerley DL, Friedel MH, McAllister RRJ, Reid JRW, Roshier DA, Smith MA, Walsh FJ, Wardle GM, Watson IW, Westoby M (2011) A fresh framework for the ecology of arid Australia. Journal of Arid Environments 75, 313–329.

Moseby KE, Neilly H, Read JL, Crisp HA (2012) Interactions between a top predator and exotic mesopredators in the Australian rangelands. International Journal of Ecology 2012, 250352.

Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850.

Newsome A (1990) The control of vertebrate pests by vertebrate predators. Trends in Ecology & Evolution 5, 187–191.

Olsson M, Wapstra E, Swan G, Snaith E, Clarke R, Madsen T (2005) Effects of long-term fox baiting on species composition and abundance in an Australian lizard community. Austral Ecology 30, 899–905.

O’Neill A (2002) ‘Living with the Dingo’. (Enviro-book: Annandale).

Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends in Ecology & Evolution 14, 483–488.

Pain S (2000) The demon duck of doom. New Scientist 166, 36–39.

Paine RT (1966) Food web complexity and species diversity. American Naturalist 100, 65–75.

Paine RT (1969) A note on trophic complexity and community stability. American Naturalist 103, 91–93.

Paine RT (1980) Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology 49, 667–685.

Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. American Naturalist 153, 492–508.

Paltridge R (2002) The diets of cats, foxes and dingoes in relation to prey availability in the Tanami Desert, Northern Territory. Wildlife Research 29, 389–403.

Pavey CR, Eldridge SR, Heywood M (2008) Population dynamics and prey selection of native and introduced predators during a rodent outbreak in arid Australia. Journal of Mammalogy 89, 674–683.

Pech RP, Sinclair ARE, Newsome AE (1995) Predation models for primary and secondary prey species. Wildlife Research 22, 55–64.

Pech RP, Sinclair ARE, Newsome AE, Catling PC (1992) Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments. Oecologia 89, 102–112.

Pickett KN, Hik DS, Newsome AE, Pech RP (2005) The influence of predation risk on foraging behaviour of brushtail possums in Australian woodlands. Wildlife Research 32, 121–130.

Polis GA (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86, 3–15.

Polis GA, Strong DR (1996) Food web complexity and community dynamics. American Naturalist 147, 813–846.

Pople AR, Grigg GC, Cairns SC, Beard LA, Alexander P (2000) Trends in the numbers of red kangaroos and emus on either side of the South Australian dingo fence: evidence for predator regulation? Wildlife Research 27, 269–276.

Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46, 609–620.

Ray JC (2005) Large carnivorous animals as tools for conserving biodiversity: assumptions and uncertainties. In: ‘Large Carnivores and the Conservation of Biodiversity.’ (Eds JC Ray, KH Redford, RS Steneck and J Berger). pp. 34–56. (Island Press: Washington).

Ripple WJ, Beschta RL (2003) Wolf reintroduction, predation risk, and cottonwood recovery in Yellowstone National Park. Forest Ecology and Management 184, 299–313.

Ripple WJ, Beschta RL (2007) Restoring Yellowstone’s aspen with wolves. Biological Conservation 138, 514–519.

Risbey DA, Calver MC, Short J (1999) The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. I. Exploring potential impact using diet analysis. Wildlife Research 26, 621–630.

Risbey DA, Calver MC, Short J, Bradley JS, Wright IW (2000) The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. II. A field experiment. Wildlife Research 27, 223–235.

Ritchie EG, Elmhagen B, Glen AS, Letnic M, Ludwig G, McDonald RA (2012) Ecosystem restoration with teeth: what role for predators? Trends in Ecology & Evolution 27, 265–271.

Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecology Letters 12, 982–998.

Rowles C (2008) ‘The diet of the Gould’s monitor Varanus gouldii and its potential impact on the translocated mammals of Faure Island, Shark Bay, Western Australia’. Honours Thesis. (Curtin University: Perth).

Russell BG, Smith B, Augee ML (2003) Changes to a population of common ringtail possums (Pseudocheirus peregrinus) after bushfire. Wildlife Research 30, 389–396.

Salo P, Banks PB, Dickman CR, Korpimäki E (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecological Monographs 80, 531–546.

Salo P, Korpimäki E, Banks PB, Nordström M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 1237–1243.

Saunders G, Coman B, Kinnear J, Braysher M (1995) ‘Managing Vertebrate Pests: Foxes’. (Australian Government Publishing Service: Canberra).

Saunders GR, Gentle MN, Dickman CR (2010) The impacts and management of foxes Vulpes vulpes in Australia. Mammal Review 40, 181–211.

Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319, 952–954.

Schmitz OJ, Hambäck PA, Beckerman AP (2000) Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. American Naturalist 155, 141–153.

Sergio F, Caro T, Brown D, Clucas B, Hunter J, Ketchum J, McHugh K, Hiraldo F (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annual Review of Ecology Evolution and Systematics 39, 1–19.

Sergio F, Hiraldo F (2008) Intraguild predation in raptor assemblages: a review. The Ibis 150 (Suppl. 1), 132–145.

Sergio F, Newton I, Marchesi L (2005) Top predators and biodiversity. Nature 436, 192.

Sergio F, Newton I, Marchesi L, Pedrini P (2006) Ecologically justified charisma: preservation of top predators delivers biodiversity conservation. Journal of Applied Ecology 43, 1049–1055.

Sergio F, Marchesi L, Pedrini P, Penteriani V (2007) Coexistence of a generalist owl with its intraguild predator: distance-sensitive or habitat-mediated avoidance? Animal Behaviour 74, 1607–1616.

Short J, Turner B, Parker S, Twiss J (1995) Reintroduction of endangered mammals to mainland Shark Bay: a progress report. In: ‘Reintroduction Biology of Australian and New Zealand Fauna.’ (Ed. M Serena). pp. 183–188. (Surrey Beatty and Sons: Chipping Norton).

Sinclair ARE (2003) Mammal population regulation, keystone processes and ecosystem dynamics. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 358, 1729–1740.

Sinclair ARE, Pech RP (1996) Density dependence, stochasticity, compensation and predator regulation. Oikos 75, 164–173.

Smith AP, Quin DG (1996) Patterns and causes of extinction and decline in Australian conilurine rodents. Biological Conservation 77, 243–267.

Soulé ME, Bolger DT, Alberts AC, Sauvajot R, Wright J, Sorice M, Hill S (1988) Reconstructed dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conservation Biology 2, 75–92.

Stafford Smith DM, Morton SR (1990) A framework for the ecology of arid Australia. Journal of Arid Environments 18, 255–278.

Stokes VL, Pech RP, Banks PB, Arthur AD (2004) Foraging behaviour and habitat use by Antechinus flavipes and Sminthopsis murina (Marsupialia: Dasyuridae) in response to predation risk in eucalypt woodland. Biological Conservation 117, 331–342.

Strauß A, Solmsdorff KY, Pech RP, Jacob J (2008) Rats on the run: removal of alien terrestrial predators affects bush rat behaviour. Behavioral Ecology and Sociobiology 62, 1551–1558.

Sutherland DR, Glen AS, de Tores PJ (2011) Could controlling mammalian carnivores lead to mesopredator release of carnivorous reptiles? Proceedings of the Royal Society of London. Series B, Biological Sciences 278, 641–648.

Switalski TA (2003) Coyote foraging ecology and vigilance in response to gray wolf reintroduction in Yellowstone National Park. Canadian Journal of Zoology 81, 985–993.

Taylor JA (1979) Foods and feeding habits of sub-adult Crocodylus porosus Schneider in northern Australia. Australian Wildlife Research 6, 347–359.

Terborgh J, Estes JA, Paquet P, Ralls K, Boyd-Heger D, Miller BJ, Noss RF (1999) The role of top carnivores in regulating terrestrial ecosystems. In: ‘Continental conservation: scientific foundations of regional reserve networks.’ (Eds J Terborgh and ME Soulé). pp. 39–64. (Island Press: Washington DC).

Terborgh J, Lopez L, Nuñez PV, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294, 1923–1926.

Wroe S (2002) A review of terrestrial mammalian and reptilian carnivore ecology in Australian fossil faunas, and factors influencing their diversity: the myth of reptilian domination and its broader ramifications. Australian Journal of Zoology 50, 1–24.

Wroe S (2007) A review of the evidence for a human role in the extinction of Australian megafauna and an alternative interpretation. In: ‘Climate change or human impact? Australia’s megafaunal extinction. Selwyn Symposium of the GSA Victoria Division, September 2007.’ (Eds ML

Cupper and SJ Gallagher). pp. 5–10. (Geological Society of Australia: Melbourne).

Wroe S, Clausen P, McHenry C, Moreno K, Cunningham E (2007) Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap. Proceedings of the Royal Society of London. Series B, Biological Sciences 274, 2819–2828.

Wroe S, McHenry C, Thomason J (2005) Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society of London. Series B, Biological Sciences 272, 619–625.

Wroe S, Myers TJ, Wells RT, Gillespie A (1999) Estimating the weight of the Pleistocene marsupial lion, Thylacoleo carnifex (Thylacoleonidae: Marsupialia): implications for the ecomorphology of a marsupial super-predator and hypotheses of impoverishment of Australian marsupial carnivore faunas. Australian Journal of Zoology 47, 489–498.

2

The rise and fall of large marsupial carnivores

Chris N. Johnson

Summary

Australia currently has few large mammalian carnivores, and the largest and most widespread of these are recently arrived placental species. However, the carnivorous marsupials of Australia have a glorious past. Specialised carnivory evolved in four marsupial families, and over the last 30 million years marsupial carnivores became steadily more specialised, larger and (probably) more diverse in species. They included some powerful, large predators, comparable to the most specialised predators among placental mammals on other continents. The fall of marsupial carnivores began with the extinction of the largest species around 45 000 years ago, when all large vertebrates disappeared. The cause of this extinction has been much debated, but most recent evidence suggests that human hunting was responsible. More recently, the thylacine and devil disappeared from mainland Australia, and the thylacine ultimately went extinct from Tasmania as well. The causes of these extinctions are also controversial.

Introduction

When Europeans first came to Australia, they found a place unusual among the continents for its lack of large, specialised mammalian carnivores. On mainland Australia, the largest carnivorous mammal is the dingo. While the dingo is a formidable predator, at a modest 15–20 kg it is considerably smaller than the largest predators on other continents, and it is a versatile species that eats invertebrate prey and carrion as well as hunting large vertebrates. In any case, it is a recent arrival to Australia (see Chapter 4). Marsupials dominate Australia’s mammal fauna, but few marsupials are predominantly flesh-eaters. Of these the thylacine and devil are the most specialised, but both are restricted to Tasmania, and the thylacine is now extinct. Among other marsupials, the spotted-tailed quoll (Dasyurus maculatus) feeds predominantly on vertebrates, but the other quoll species eat large volumes of invertebrate as well as vertebrate prey. The remaining dasyurid marsupials are mostly insectivores (see Chapter 10). The omnivorous bandicoots occasionally feed on small vertebrates, but with the possible exception of the recently extinct lesser bilby (Macrotis leucura) (Finlayson 1935), vertebrate flesh is (or was) a small fraction only of their diets.

Because of this remarkable shortage of large carnivorous marsupials, Australian biologists have tended to assume that predation is a less significant factor in Australian ecosystems than elsewhere. However, a look into the past reveals a different picture. Before ~3500 years ago, both the thylacine and devil were widespread on mainland Australia. Step back another 40 000 years or so and the marsupial lion (Thylacoleo carnifex) – a species rivalling the extinct sabre-toothed lions and their marsupial counterpart, the South American Thylacosmilus, in its extreme specialisation for predation – was widespread over the continent. Also alive at that time were giant carnivorous rat-kangaroos. These large carnivores formed part of Australia’s Pleistocene megafauna, a complex assemblage of perhaps 60–70 species of large vertebrates dominated by extra-large marsupials, along with some equally remarkable giant monotremes, reptiles and birds (Rich and van Tets 1985; Murray 1991; Flannery 1994; Johnson 2006).

Just as the big predators in this assemblage were comparable in their specialisation for carnivory with large predators elsewhere in the world, the body-size range of Australia’s Pleistocene megafauna, and the place of top predators in that size distribution, were also not unusual. In their review of the maximal body sizes of mammals worldwide, Smith et al. (2010) demonstrate a strong relationship between land-mass area and the size of the largest mammals on each land mass. That relationship predicts a value of 4168 kg for the largest land mammal in an area the size of Australia. The largest marsupial ever to have lived was Diprotodon optatum, which was one of the Australian megafaunal species that went extinct around 40 000 years ago. The mass of D. optatum, estimated from the thickness of its leg bones, was between 2200 and 3400 kg (Wroe et al. 2004b). This is less than predicted from Australia’s land area, but not radically so. Smith et al. (2010) also found a consistent value of the ratio of the size of the largest carnivorous mammal to that of the largest coeval herbivore: typically, the largest carnivore is between 10 and 20 times smaller than the largest herbivore. Given the estimate of 2700 kg for the mass of Australia’s largest herbivore, the largest carnivore in Pleistocene Australia should have weighed between 135 and 270 kg. The mass of T. carnifex, estimated using the same methodology as for D. optatum, was probably between 100 and 150 kg (Wroe et al. 1999). This estimate overlaps with the expected range for large predators given the size range of potential prey, albeit at the low end of that range.

So, in the late Pleistocene, just before Australia’s ecosystems were radically changed by extinction of all vertebrates above a body mass of 40 kg, large carnivorous marsupials were a significant component of Australia’s terrestrial vertebrate fauna. Further, the brief review of their evolution that follows will show that carnivorous marsupials have been a prominent part of the fauna for at least the last 20 million years.

A brief history of carnivorous marsupials

Carnivory, defined as feeding on the flesh of vertebrate animals, has evolved in four families of Australian marsupials: the Thylacinidae, Dasyuridae, Thylacoleonidae and Hypsiprymnodontidae (Long et al. 2002; Wroe 2003). The Thylacinidae and Dasyuridae are allied to one another in the order Dasyuromorphia. This large order includes many invertebrate-feeding marsupials as well as carnivores, and also contains a third family represented by a single specialised anteater (Myrmecobiidae, the numbat Myrmecobius fasciatus). The families Thylacoleonidae and Hypsiprymnodontidae are in the order Diprotodontia, which is made up predominantly of herbivores. The family Thylacoleonidae is in the superfamily Vombatoidea (wombats, koala and diprotodons), while the Hypsiprymnodontidae is related to the Macropodoidea (kangaroos and rat-kangaroos). The carnivorous representatives of these four families are summarised in turn below.

Thylacinidae

Only one species of thylacinid, the ‘Tasmanian tiger’ or thylacine (Thylacinus cynocephalus), survived into recent times, and is now sadly extinct, but another 11 are known from the fossil record (Long et al. 2002). All were dog-like or fox-like marsupials, and all were carnivorous. Most known thylacinid fossils come from one series of deposits, sampling the Late Oligocene-Miocene (26–5.3 million years ago) of the Riversleigh area in northwestern Queensland (Wroe and Musser 2001). Given that the fossil record for this period, the Oligocene especially, is poor over most of Australia, it is highly probable that thylacinid diversity around 20 million years ago and earlier was much greater than currently known. Molecular evidence supports a divergence of thylacinids from their common ancestor with dasyurids in the late Oligo-cene (Krajewski and Westerman 2003; Beck 2008), around 25 million years ago or earlier. The thylacinids evidently underwent a rapid diversification early in their evolutionary history. The Riversleigh deposits show that during the Miocene several species may have been sympatric at any one time, presumably occupying niches differentiated by habitat and prey type (Long et al. 2002).

The earliest thylacinids were relatively small creatures, probably about quoll size, with dentition that suggests they preyed on insects as well as small vertebrates, much as quolls do. The main evolutionary trends in the family were for increased body mass and dental specialisation for carnivory in the form of extreme modification of the molars for vertical shearing. Two genera, Wabulacinus (one species, of early Miocene age) and Thylacinus, were specialised carnivores (Wroe & Musser 2001); this may also have been true of the two species of Nimbacinus. Thylacinus was the most species-rich genus, with at least four species from early Miocene to recent times. The largest species of thylacines are thought to have been T. potens and T. megiriani, both of which were larger and more robust than the recent T. cynocephalus. Wroe et al. (2004a) estimated weights of 39 kg and 57 kg respectively for these two species, compared with 30 kg for recent thylacines. Both species are known from the late Miocene Alcoota faunas of central Australia, where they coexisted with a still larger marsupial lion (Wakaleo alacootaensis) and at least one smaller thylacinid, Tyarrpecinus rothi (Long et al. 2002). Thylacinid diversity evidently peaked in the Miocene, and then declined in the late Miocene with the disappearance of smaller species. During the Pliocene and Pleistocene, only T. cynocephalus was extant.

Dasyuridae

The dasyurid radiation complemented that of the thylacinids. Dasyurids evidently diversified later than thylacinids, so that as thylacinid diversity was in decline in the late Miocene, the dasyurid radiation was taking off. Molecular evidence suggests that the subfamilies of the Dasyuridae diverged during the Miocene, and that modern genera appeared during the late Miocene (Krajewski and Westerman 2003; Beck 2008; Meredith et al. 2008). Few dasyurid species are known from the Miocene, but the diversity of fossil species increases steadily through the Pliocene, Pleistocene and Holocene. Most dasyurids are small and medium-sized species, and it is likely that the middle-sized dasyurids were ecological replacers of the smaller thylacinids. Unlike thylacinids, in which evolutionary change was mainly characterised by specialisation of the dentition, dental morphology of dasyurids remained conservative; instead, there was rapid evolution in skull morphology, especially in the middle ear region. Wroe (1997) and Wroe and Musser (2001) argue that the effect of these changes was to heighten sensitivity of hearing. This may have increased the efficiency with which dasyurids were able to hunt small prey, and helps explain their success as nocturnal predators of small vertebrates and invertebrates. The diversification of dasyurids coincided with a general drying of the Australian climate during the late Miocene. As a result of this, the desert regions of Australia now have exceptionally high diversity of small insectivorous mammals (Morton 1993; Morton et al. 1994).

The devil (Sarcophilus harrisii) is larger than any other dasyurid (the late Pleistocene form, S. laniarius, may have been up to twice as heavy as the living devil but it is not clear whether it was a distinct species or the larger ancestor of the living animal) and it possesses the most specialised cranial and dental adaptations for carnivory of any dasyurid. One smaller species, S. moornaensis, is known from the early Pleistocene. An earlier dasyurid from Miocene deposits at Riversleigh was devil-like: Ganbulanyi djadjinguli had very large premolars with blunt conical cusps, ideal for fracturing brittle material and similar to the teeth of bone-cracking mammals like devils and hyaenas. Ganbulanyi is not only the oldest bone-cracking marsupial; with an estimated weight of only ~4 kg (Wroe et al. 2004a) it also holds the record as the world’s smallest bone-cracking mammal (Wroe 1998; Long et al. 2002).

Apart from the devils, the most carnivorous fossil dasyurid appears to be the Pliocene Glaucodon ballaretensis, a species known only from fragmentary dental material but thought to have been intermediate between the quolls and devils in size and specialisation for carnivory (Long et al. 2002).

Thylacoleonidae

The thylacoleonids were a group of highly specialised carnivores characterised by development of the third premolars as elongated cutting blades, with reduction of the other molar teeth. The earliest species are of late Oligocene age, and during the Oligo-Miocene there was a moderate diversity of species in the genera Wakaleo (four species), Lekaneleo (two species) and Microleo, which had a single species (Gillespie 2007). Thylacoleonids from the early Miocene were mostly relatively small species with less specialised dentition than in Thyalcoleo, and many were probably arboreal. Later species were larger, and two species are thought to have exceeded 100 kg (the late Miocene W. alacootaensis and the Pleistocene T. carnifex). Three species are currently recognised in Thylacoleo: the small T. hilli of Miocene to Pliocene age, the intermediate T. crassidentatus from the Pliocene, and the Pleistocene-age T. carnifex, which is the culmination of the evolutionary trend towards increased size and specialisation in the genus (Long et al. 2002).

Both the thylacinids and thylacoleonids show a trend for increased body size and specialisation for carnivory along with reduced species richness from the mid-Miocene onwards. This may be linked to the expansion of open, dry habitats from the late Miocene as the climate of Australia became drier. Such habitats would have provided increased ecological opportunity for large predators, as medium to large herbivores, kangaroos especially, diversified to exploit expanding grasslands, savannahs and shrublands (Prideaux 2004; Johnson 2006). Smaller species in these families declined with the contraction of complex forest habitat and, perhaps, competitive pressure from the vigorous radiation of the Dasyuridae.

Hypsiprymnodontidae

The one living survivor of this family is the musky rat-kangaroo, a tiny omnivorous, rainforest-restricted animal weighing only half a kilogram. Estimates of the weight of extinct hypsiprymnodontids range up to 70 kg for the largest species, the Pleistocene Propleopus oscillans. This species was a long-faced animal with molar teeth adapted for shearing as well as crushing, but not grinding of fibrous plant material as in kangaroos. Ride et al. (1997) interpret the dentition of P. oscillans as being distinctly canid-like, and suggest that it was an opportunistic predator analogous to dogs. Fossil material of P. oscillans is rare, and there is little post-cranial material available for study, but what there is suggests that the species was quadrupedal (rather than bipedal, like its kangaroo relatives) and terrestrial, not fast but probably a capable endurance runner, being possibly similar in this respect to the wolverine (Gulo gulo). The analogy with the wolverine is interesting, given that wolverines typically occur at low population densities and have huge home ranges (Landa et al. 1998); if that were true of P. oscillans, it could explain the rarity of the species in the fossil record.

There were two other somewhat smaller species of Propleopus (chillagoensis of Plio-Pleistocene and wellingtonensis of Pleistocene age), one species of Jackmahoneya (early Pliocene), and two species of Ekaltadeta (Miocene). The older Ekaltadeta appears to have been more omnivorous than Propleopus, and Jackmahoneya had an intermediate morphology.

The marsupial hypercarnivores

‘Hypercarnivores’ are species whose diet consists of more than 70% meat (Van Valkenburgh 1989). Hypercarnivory is associated with relatively large body size, pronounced dental specialisation – typically consisting of development of large shearing surfaces on the molars and elongation of canines for puncturing and grasping prey – and a range of other morphological adaptations that confer power, speed or endurance. Hypercarnivores must be efficient hunters and killers of their prey. This is true even of those species like hyaenas and devils that are also well adapted as scavengers.

Among recently extant Australian marsupials, there are three hypercarnivores: the thylacine, Tasmanian devil, and spotted-tailed quoll (Jones and Barmuta 1998). Identification of hypercarnivory is often less certain in fossil species. However, a workable criterion is to consider marsupial species with clear dental specialisation for carnivory and estimated body weight greater than 3 kg (equivalent to a large spotted-tailed quoll) as being probable hypercarnivores. Wroe et al. (2004a) list 25 fossil species that qualify as hypercarnivores on these grounds.

The distribution of hypercarnivore species through time is shown in Fig. 2.1. Species richness en was low in the late Oligocene, with only one species. This could be an artefact of the poor fossil record from that interval, but probably does signal a true lack of differentiation of specialised carnivores in the generally small-bodied mammal fauna of the time. Then, there are about equal numbers of hypercarnivore species known from each of the Early Miocene, Late Miocene, Pliocene and Pleistocene. These periods are of unequal length, however. Expressing species richness as number of species per million years, to allow for the fact that longer periods of time should encompass more species because of greater turnover through origination and extinction, reveals a striking pattern of increase towards the present in the time-density of species. Again, this could at least partly reflect a sampling bias due to better knowledge of geologically recent fossil deposits, but the fact that the increase is matched by increasing specialisation and a general trend for increased body size (Wroe et al. 2004a) suggests that Australia’s communities of marsupial carnivores really did increase in diversity towards the present.

Fig. 2.1. Standardised species richness (number of species per million years) of large (> 3 kg) marsupial carnivores in geological epochs from the late oligocene to the recent. Total numbers of species in each interval are shown above the bars. Time divisions and placement of species follow Long