Ongoing unraveling of a continental fauna: Decline and extinction of Australian mammals since European settlement

Significance The island continent of Australia harbors much of the world’s most distinctive biodiversity, but this review describes an extent of recent and ongoing loss of its mammal fauna that is exceptionally high and appreciably greater than previously recognized. The causes of loss are dissimilar to those responsible for most biodiversity decline elsewhere in the world. The highly distinctive and mostly endemic Australian land mammal fauna has suffered an extraordinary rate of extinction (>10% of the 273 endemic terrestrial species) over the last ∼200 y: in comparison, only one native land mammal from continental North America became extinct since European settlement. A further 21% of Australian endemic land mammal species are now assessed to be threatened, indicating that the rate of loss (of one to two extinctions per decade) is likely to continue. Australia’s marine mammals have fared better overall, but status assessment for them is seriously impeded by lack of information. Much of the loss of Australian land mammal fauna (particularly in the vast deserts and tropical savannas) has been in areas that are remote from human population centers and recognized as relatively unmodified at global scale. In contrast to general patterns of extinction on other continents where the main cause is habitat loss, hunting, and impacts of human development, particularly in areas of high and increasing human population pressures, the loss of Australian land mammals is most likely due primarily to predation by introduced species, particularly the feral cat, Felis catus, and European red fox, Vulpes vulpes, and changed fire regimes.

[1]  Corey J. A. Bradshaw,et al.  Little left to lose: deforestation and forest degradation in Australia since European colonization , 2012 .

[2]  Gerard Early Australia's National Environmental Legislation and Human/Wildlife Interactions , 2008 .

[3]  R. Shine,et al.  Conditioned taste aversion enhances the survival of an endangered predator imperilled by a toxic invader , 2010 .

[4]  M. Crowther,et al.  Fire and grazing influence food resources of an endangered rock-wallaby , 2012, Wildlife Research.

[5]  Ian Abbott,et al.  Mammalian faunal collapse in Western Australia, 1875-1925: the hypothesised role of epizootic disease and a conceptual model of its origin, introduction, transmission, and spread , 2006 .

[6]  C. Dickman,et al.  Analysis of factors implicated in the recent decline of Australia's mammal fauna , 2007 .

[7]  N. L. McKenzie,et al.  Patterns in the modern decline of western Australia's vertebrate fauna: Causes and conservation implications , 1989 .

[8]  S. Garnett The Action Plan for Australian Birds , 1992 .

[9]  K. Moseby,et al.  Arid Recovery - A comparison of reptile and small mammal populations inside and outside a large rabbit, cat and fox-proof exclosure in arid South Australia , 2009 .

[10]  D. Lindenmayer,et al.  Ten Commitments Revisited: Securing Australia’s Future Environment , 2015 .

[11]  B. Ward,et al.  Importance of getting the numbers right: quantifying the rapid and substantial decline of an abundant marsupial, Bettongia penicillata , 2013, Wildlife Research.

[12]  C. Dickman,et al.  Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study , 2012, Biological reviews of the Cambridge Philosophical Society.

[13]  Helene Marsh,et al.  Ecology and conservation of the sirenia: dugongs and manatees , 2011 .

[14]  Susanne A. Fritz,et al.  The current decline of tropical marsupials in Australia: Is history repeating? , 2014 .

[15]  M. Palmer,et al.  The extent of extinctions of mammals on islands , 1998 .

[16]  H. Possingham,et al.  Independent review of Western Shield - February 2003 , 2004 .

[17]  H. Hines,et al.  The Black-tailed Antechinus, Antechinus arktos sp. nov.: a new species of carnivorous marsupial from montane regions of the Tweed Volcano caldera, eastern Australia. , 2014, Zootaxa.

[18]  Jessamy Battersby UK Mammals: Species Status and Population Trends. First Report by the Tracking Mammals Partnership , 2005 .

[19]  T. Jefferson,et al.  Taxonomic revision of the humpback dolphins ( Sousa spp.), and description of a new species from Australia , 2014 .

[20]  P. Savolainen,et al.  Narrow genetic basis for the Australian dingo confirmed through analysis of paternal ancestry , 2012, Genetica.

[21]  Christopher N. Johnson,et al.  Body mass and extinction risk in Australian marsupials: The ‘Critical Weight Range’ revisited , 2009 .

[22]  Susanne A. Fritz,et al.  An Update of Wallace’s Zoogeographic Regions of the World , 2013, Science.

[23]  A. Baynes,et al.  The original mammal fauna and some information on the original bird fauna of Uluru National Park, Northern Territory. , 1992 .

[24]  P. Fleming,et al.  Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function , 2014 .

[25]  B. Mackey,et al.  Evaluating the status of species using Indigenous knowledge: Novel evidence for major native mammal declines in northern Australia , 2013 .

[26]  M. Cardillo,et al.  A comparison of current and reconstructed historic geographic range sizes as predictors of extinction risk in Australian mammals , 2013 .

[27]  R. Bilney,et al.  Underestimated and severe : small mammal decline from the forests of south-eastern Australia since European settlement, as revealed by a top-order predator , 2010 .

[28]  Andrew P. Smith,et al.  MAMMAL DECLINE AND RECOVERY IN AUSTRALIA , 1994 .

[29]  S. Legge,et al.  The short-term effects of an extensive and high-intensity fire on vertebrates in the tropical savannas of the central Kimberley, northern Australia , 2008 .

[30]  A. P. Smith,et al.  Patterns and causes of extinction and decline in Australian conilurine rodents , 1996 .

[31]  Helene Marsh,et al.  Ecology and Conservation of the Sirenia by Helene Marsh , 2011 .

[32]  H. H. Finlayson On central Australian mammals. Part IV-The distribution and status of central Australian species , 1961 .

[33]  A. Griffiths,et al.  Monitoring indicates greater resilience for birds than for mammals in Kakadu National Park, northern Australia , 2012, Wildlife Research.

[34]  Stuart Cowell,et al.  Conservation planning in a cross‐cultural context: the Wunambal Gaambera Healthy Country Project in the Kimberley, Western Australia , 2012 .

[35]  K. Wilson,et al.  Managing for change: wetland transitions under sea‐level rise and outcomes for threatened species , 2011 .

[36]  M. Crowther,et al.  The impact of the dingo on the thylacine in Holocene Australia , 2012 .

[37]  C. Bradshaw,et al.  Current and future threats from non-indigenous animal species in northern Australia: a spotlight on World Heritage Area Kakadu National Park. , 2007 .

[38]  I. Gordon,et al.  Variation in terrestrial mammal abundance on pastoral and conservation land tenures in north‐eastern Australian tropical savannas , 2012 .

[39]  G. Hardy,et al.  Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia , 2005 .

[40]  R. Bilney Poor historical data drive conservation complacency: The case of mammal decline in south‐eastern Australian forests , 2014 .

[41]  Lauren E. Helgen,et al.  Twentieth century occurrence of the Long-Beaked Echidna Zaglossus bruijnii in the Kimberley region of Australia , 2012, ZooKeys.

[42]  A. Burbidge,et al.  Translocation Of Mala (Lagorchestes Hirsutus) From The Tanami Desert, Northern Territory To Trimouille Island, Western Australia , 2001 .

[43]  H. Berry,et al.  Healthy country, healthy people: the relationship between Indigenous health status and “caring for country” , 2009, The Medical journal of Australia.

[44]  Andrew A. Burbidge,et al.  The Action Plan for Australian Mammals 2012 , 2014 .

[45]  J. Lamarque,et al.  Global Biodiversity: Indicators of Recent Declines , 2010, Science.

[46]  B. Brook,et al.  Determinants of survival for the northern brown bandicoot under a landscape-scale fire experiment , 2003 .

[47]  Damien A. Fordham,et al.  Decline and likely extinction of a northern Australian native rodent, the Brush-tailed Rabbit-rat Conilurus penicillatus , 2010 .

[48]  A. Ash,et al.  Responses of vertebrates to pastoralism, military land use and landscape position in an Australian tropical savanna , 2002 .

[49]  Shelly Lachish,et al.  Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction. , 2009, Ecology.

[50]  F. Jones The Mammals of South Australia , 1926, Nature.

[51]  Carol Palmer,et al.  The disappearing mammal fauna of northern Australia: context, cause, and response , 2011 .

[52]  Christopher N. Johnson Australia's Mammal Extinctions: A 50,000-Year History , 2006 .

[53]  M. Cardillo,et al.  Island mammal extinctions are determined by interactive effects of life history, island biogeography and mesopredator suppression , 2014 .

[54]  D. Grayson,et al.  Climate change frames debate over the extinction of megafauna in Sahul (Pleistocene Australia-New Guinea) , 2013, Proceedings of the National Academy of Sciences.

[55]  Guidelines for Using the IUCN Red List Categories and Criteria , 2005 .

[56]  Jeff Short,et al.  The new guard: the arrival and impacts of cats and foxes , 2014 .

[57]  J. Ling Exploitation of fur seals and sea lions from Australian, New Zealand and adjacent subantarctic islands during the eighteenth, nineteenth and twentieth centuries , 1999 .

[58]  D. J. Milne,et al.  Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia , 2001 .

[59]  N. R. Sumner,et al.  The red fox in Australia—an exotic predator turned biocontrol agent , 2002 .

[60]  Bruce B. Collette,et al.  The Impact of Conservation on the Status of the World’s Vertebrates , 2010, Science.

[61]  Brian D. Smith,et al.  Integrating multiple lines of evidence to better understand the evolutionary divergence of humpback dolphins along their entire distribution range: a new dolphin species in Australian waters? , 2013, Molecular ecology.

[62]  D. Lunney,et al.  Turning the spotlight onto the conservation of Australian bats and the extinction of the Christmas Island Pipistrelle , 2011 .

[63]  A. Kutt Feral cat (Felis catus) prey size and selectivity in north‐eastern Australia: implications for mammal conservation , 2012 .

[64]  H. Grantham,et al.  Modelling climate-change-induced shifts in the distribution of the koala , 2011 .

[65]  M. Hoffmann,et al.  The changing fates of the world's mammals , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  L. Head,et al.  The Spatial and Temporal Patterns of Stick-Nest Rat Middens in Australia , 1999, Radiocarbon.

[67]  A. Burbidge,et al.  Relict Bettongia lesueur warrens in Western Australian deserts , 2007 .

[68]  N. Isaac,et al.  Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny , 2007, PloS one.

[69]  Corey J A Bradshaw,et al.  Synergies among extinction drivers under global change. , 2008, Trends in ecology & evolution.

[70]  N. McKenzie,et al.  A molecular and morphological investigation of species boundaries and phylogenetic relationships in Australian free-tailed bats Mormopterus (Chiroptera : Molossidae) , 2014, Australian Journal of Zoology.

[71]  S. Pearson Late Holocene biological records from the middens of stick-nest rats in the central Australian arid zone , 1999 .

[72]  S. Garnett,et al.  The Action Plan for Australian Birds 2010 , 2011 .

[73]  Bryan F. J. Manly,et al.  Mammal extinctions on Australian islands: causes and conservation implications , 2002 .

[74]  Hugh P. Possingham,et al.  Adapting global biodiversity indicators to the national scale: A Red List Index for Australian birds , 2012 .

[75]  Nick Dexter,et al.  The impact of fox control on the relative abundance of forest mammals in East Gippsland, Victoria , 2009 .

[76]  H. Yamano,et al.  Climate change , sea-level rise , and conservation : keeping island biodiversity afloat , 2014 .

[77]  Jeff Short,et al.  The extinction of rat-kangaroos (Marsupialia:Potoroidae) in New South Wales, Australia , 1998 .

[78]  K. Moseby,et al.  Predation determines the outcome of 10 reintroduction attempts in arid South Australia , 2011 .

[79]  J. Woinarski,et al.  The mammal fauna of the Sir Edward Pellew island group, Northern Territory, Australia: refuge and death-trap , 2011 .

[80]  D. Lindenmayer,et al.  How to make a common species rare: A case against conservation complacency , 2011 .

[81]  Ben Collen,et al.  Monitoring Change in Vertebrate Abundance: the Living Planet Index , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[82]  H. H. Finlayson On Central Australian mammals lwith notice of related species from adjacent tractsrp Part IIIp The Potoroinae , 1958 .

[83]  B. Murphy,et al.  There is a critical weight range for Australia's declining tropical mammals , 2014 .

[84]  A. Kutt,et al.  The effects of grazing and fire on vegetation and the vertebrate assemblage in a tropical savanna woodland in north-eastern Australia , 2007, Journal of Tropical Ecology.

[85]  Christopher N. Johnson,et al.  Experimental evidence that feral cats cause local extirpation of small mammals in Australia's tropical savannas , 2014 .

[86]  S. Hocknull,et al.  New Quaternary records of Conilurus (Rodentia: Muridae) from eastern and northern Australia with the description of a new species , 2010 .

[87]  E. Sanderson,et al.  The Human Footprint and the Last of the Wild , 2002 .

[88]  Christopher N. Johnson,et al.  Lack of chronological support for stepwise prehuman extinctions of Australian megafauna , 2013, Proceedings of the National Academy of Sciences.

[89]  The loss of Banks’s legacy , 1994 .

[90]  D. Lindenmayer,et al.  Cross-sectional vs. longitudinal research: a case study of trees with hollows and marsupials in Australian forests , 2011 .

[91]  Natalie A. Rossiter-Rachor,et al.  Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna. , 2009, Ecological applications : a publication of the Ecological Society of America.

[92]  N. McKenzie,et al.  The status of non-volant mammals along a rainfall gradient in the south-west Kimberley, Western Australia , 2012 .

[93]  Kate E. Jones,et al.  Multiple Causes of High Extinction Risk in Large Mammal Species , 2005, Science.

[94]  F. Jones,et al.  The red centre : man and beast in the heart of Australia , 1937 .

[95]  I. Abbott,et al.  Mammals of Australian islands: factors influencing species richness , 2003 .

[96]  Liana N. Joseph,et al.  Trends and biases in the listing and recovery planning for threatened species: an Australian case study , 2012, Oryx.

[97]  R. Southgate,et al.  Aboriginal knowledge of the mammals of the central deserts of Australia , 1988 .

[98]  S. Williams,et al.  Climate change in Australian tropical rainforests: an impending environmental catastrophe , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[99]  Thomas A A Prowse,et al.  An ecological regime shift resulting from disrupted predator-prey interactions in Holocene Australia. , 2014, Ecology.

[100]  J. Atchison,et al.  Human impacts on Persoonia falcata. Perspectives on post-contact vegetation change in the Keep River region, Australia, from contemporary vegetation surveys , 2009 .

[101]  I. Abbott,et al.  The spread of the cat, Felis catus, in Australia: re-examination of the current conceptual model with additional information. , 2008 .

[102]  D. Algar,et al.  Increasing the target-specificity of ERADICAT® for feral cat (Felis catus) control by encapsulating a toxicant , 2007 .

[103]  Carol Palmer,et al.  Monitoring indicates rapid and severe decline of native small mammals in Kakadu National Park, northern Australia , 2010 .

[104]  S. Legge,et al.  Rapid recovery of mammal fauna in the central Kimberley, northern Australia, following the removal of introduced herbivores. , 2011 .

[105]  Rob DeSalle,et al.  Historical Mammal Extinction on Christmas Island (Indian Ocean) Correlates with Introduced Infectious Disease , 2008, PloS one.

[106]  Jeremy Russell-Smith,et al.  Fire ecology and Aboriginal land management in central Arnhem Land, northern Australia: a tradition of ecosystem management , 2001 .

[107]  Christopher N. Johnson,et al.  Landscape Management of Fire and Grazing Regimes Alters the Fine-Scale Habitat Utilisation by Feral Cats , 2014, PloS one.