in

The environmental and ecological determinants of elevated Ross River Virus exposure in koalas residing in urban coastal landscapes

  • 1.

    Gonzalez-Astudillo, V., Allavena, R., McKinnon, A., Larkin, R. & Henning, J. Decline causes of Koalas in South East Queensland, Australia: a 17-year retrospective study of mortality and morbidity. Sci. Rep. 7, 42587 (2017).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 2.

    Ward, M. S. et al. Lots of loss with little scrutiny: The attrition of habitat critical for threatened species in Australia. Conserv. Sci. Pract. 1, e117 (2019).

    Google Scholar 

  • 3.

    Martin, R. & Handasyde, K. The Koala: Natural History, Conservation and Management (University of New South Wales Press Ltd (Hong Kong, Australian Natural History Series, 1999).

    Google Scholar 

  • 4.

    McAlpine, C. et al. Conserving koalas: A review of the contrasting regional trends, outlooks and policy challenges. Biol. Conserv. 192, 226–236 (2015).

    Article  Google Scholar 

  • 5.

    Shumway, N., Lunney, D., Seabrook, L. & McAlpine, C. Saving our national icon: An ecological analysis of the 2011 Australian Senate inquiry into status of the koala. Environ. Sci. Policy 54, 297–303 (2015).

    Article  Google Scholar 

  • 6.

    Adams-Hosking, C., Grantham, H. S., Rhodes, J. R., McAlpine, C. & Moss, P. T. Modelling climate-change-induced shifts in the distribution of the koala. Wildlife Res. 38, 122–130 (2011).

    Article  Google Scholar 

  • 7.

    Rhodes, J. R., Beyer, H., Preece, H. & McAlpine, C. South East Queensland koala population modelling study. UniQuest (2015).

  • 8.

    Dique, D. S., Preece, H. J., Thompson, J. & de Villiers, D. L. Determining the distribution and abundance of a regional koala population in south-east Queensland for conservation management. Wildlife Res. 31, 109–117 (2004).

    Article  Google Scholar 

  • 9.

    Thompson, J. The comparative ecology and population dynamics of koalas in the Koala Coast region of south-east Queensland. PhD Thesis, School of Integrative Biology, University of Queensland (2006).

  • 10.

    Rhodes, J. R. et al. Using integrated population modelling to quantify the implications of multiple threatening processes for a rapidly declining population. Biol. Conserv. 144, 1081–1088 (2011).

    Article  Google Scholar 

  • 11.

    Denner, J. & Young, P. R. Koala retroviruses: Characterization and impact on the life of koalas. Retrovirology 10, 108 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 12.

    Nyari, S. et al. Epidemiology of chlamydial infection and disease in a free-ranging koala (Phascolarctos cinereus) population. PloS One 12 (2017).

  • 13.

    Waugh, C. A. et al. Infection with koala retrovirus subgroup B (KoRV-B), but not KoRV-A, is associated with chlamydial disease in free-ranging koalas (Phascolarctos cinereus). Sci. Rep. 7, 1–11 (2017).

    ADS  CAS  Article  Google Scholar 

  • 14.

    McCallum, H., Kerlin, D. H., Ellis, W. & Carrick, F. Assessing the significance of endemic disease in conservation—koalas, chlamydia, and koala retrovirus as a case study. Conserv. Lett. 11, e12425 (2018).

    Article  Google Scholar 

  • 15.

    Aldred, J., Campbell, J., Mitchell, G., Davis, G. & Elliott, J. Involvement of wildlife in the natural cycle of Ross River and Barmah Forest viruses (Wildlife Disease Association Meeting, Melbourne, Australia, 1991).

    Google Scholar 

  • 16.

    Russell, R. C. Arboviruses and their vectors in Australia: An update on the ecology and epidemiology of some mosquito-borne arboviruses. Rev. Med. Vet. Entomol. 83, 141–158 (1995).

    Google Scholar 

  • 17.

    Harley, D., Sleigh, A. & Ritchie, S. Ross River virus transmission, infection, and disease: A cross-disciplinary review. Clin. Microbiol. Rev. 14, 909–932 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 18.

    Seay, A. R. & Wolinsky, J. S. Ross river virus-induced demyelination: I Pathogenesis and histopathology. Ann. Neurol. 12, 380–389 (1982).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 19.

    Azuolas, J., Wishart, E., Bibby, S. & Ainsworth, C. Isolation of Ross River virus from mosquitoes and from horses with signs of musculoskeletal disease. Aust. Vet. J. 81, 344–347 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Stephenson, E. B., Peel, A. J., Reid, S. A., Jansen, C. C. & McCallum, H. The non-human reservoirs of Ross River virus: A systematic review of the evidence. Parasite. Vector. 11, 188 (2018).

    Article  Google Scholar 

  • 21.

    Skinner, E. B. et al. Associations between Ross River Virus infection in humans and vector-vertebrate community ecology in Brisbane Australia. Vector-borne Zoonot. https://doi.org/10.1089/vbz.2019.2585 (2020).

    Article  Google Scholar 

  • 22.

    Martin, L. B., Weil, Z. M. & Nelson, R. J. Seasonal changes in vertebrate immune activity: Mediation by physiological trade-offs. Philos. T. R. Soc. B. 363, 321–339 (2008).

    Article  Google Scholar 

  • 23.

    Nelson, R. J. & Demas, G. E. Seasonal changes in immune function. Quart. Rev. Biol. 71, 511–548 (1996).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 24.

    Old, J. M. & Deane, E. M. Antibodies to the Ross River virus in captive marsupials in urban areas of eastern New South Wales Australia. J. Wildlife Dis. 41, 611–614 (2005).

    Article  Google Scholar 

  • 25.

    Muhar, A., Dale, P. E., Thalib, L. & Arito, E. The spatial distribution of Ross River virus infections in Brisbane: Significance of residential location and relationships with vegetation types. Environ. Health Prev. 4, 184–189 (2000).

    CAS  Article  Google Scholar 

  • 26.

    Ryan, P., Alsemgeest, D., Gatton, M. & Kay, B. Ross River virus disease clusters and spatial relationship with mosquito biting exposure in Redland Shire, southern Queensland Australia. J. Med. Entomol. 43, 1042–1059 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Davies, N. et al. Movement patterns of an arboreal marsupial at the edge of its range: A case study of the koala. Movement Ecol. 1, 8 (2013).

    Article  Google Scholar 

  • 28.

    Murphy, A. K. et al. Spatial and temporal patterns of Ross River virus in South East Queensland, Australia: Identification of hot spots at the rural-urban interface. Preprint available at Research Square. https://doi.org/10.21203/rs.3.rs-16140/v1 (2020).

  • 29.

    Potter, A., Johansen, C. A., Fenwick, S., Reid, S. A. & Lindsay, M. D. The seroprevalence and factors associated with Ross River virus infection in western grey kangaroos (Macropus fuliginosus) in Western Australia. Vector-borne Zoonot. 14, 740–745 (2014).

    Article  Google Scholar 

  • 30.

    Kay, B. H., Boyd, A. M., Ryan, P. A. & Hall, R. A. Mosquito feeding patterns and natural infection of vertebrates with Ross River and Barmah Forest viruses in Brisbane Australia. Am. J. Trop. Med. Hyg. 76, 417–423 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  • 31.

    Doak, D. F., Marino, P. C. & Kareiva, P. M. Spatial scale mediates the influence of habitat fragmentation on dispersal success: Implications for conservation. Theor. Popul. Biol. 41, 315–336 (1992).

    Article  Google Scholar 

  • 32.

    Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. S. 34, 487–515 (2003).

    Article  Google Scholar 

  • 33.

    Di Giulio, M., Holderegger, R. & Tobias, S. Effects of habitat and landscape fragmentation on humans and biodiversity in densely populated landscapes. J. Environ. Manag. 90, 2959–2968 (2009).

    Article  Google Scholar 

  • 34.

    Saunders, D. A., Hobbs, R. J. & Margules, C. R. Biological consequences of ecosystem fragmentation: A review. Conserv. Biol. 5, 18–32 (1991).

    Article  Google Scholar 

  • 35.

    Allan, B. F., Keesing, F. & Ostfeld, R. S. Effect of forest fragmentation on Lyme disease risk. Conserv. Biol. 17, 267–272 (2003).

    Article  Google Scholar 

  • 36.

    Ostfeld, R. S. Biodiversity loss and the rise of zoonotic pathogens. Clin. Microbiol. Infect. 15, 40–43 (2009).

    PubMed  Article  PubMed Central  Google Scholar 

  • 37.

    Johnson, B. J. et al. The roles of mosquito and bird communities on the prevalence of West Nile virus in urban wetland and residential habitats. Urban Ecosyst. 15, 513–531 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 38.

    Quigley, B. L., Ong, V. A., Hanger, J. & Timms, P. Molecular dynamics and mode of transmission of koala retrovirus as it invades and spreads through a wild Queensland koala population. J. Virology 92 (2018).

  • 39.

    Woodward, W. et al. Koalas on North Stradbroke Island: diet, tree use and reconstructed landscapes. Wildlife Res. 35, 606–611 (2008).

    Article  Google Scholar 

  • 40.

    De Oliveira, S., Murray, P., De Villiers, D. & Baxter, G. Ecology and movement of urban koalas adjacent to linear infrastructure in coastal south-east Queensland. Aust. Mammal. 36, 45–54 (2014).

    Article  Google Scholar 

  • 41.

    Callaghan, J. et al. Ranking and mapping koala habitat quality for conservation planning on the basis of indirect evidence of tree-species use: A case study of Noosa Shire, south-eastern Queensland. Wildlife Res. 38, 89–102 (2011).

    Article  Google Scholar 

  • 42.

    MBRC. Koala Management Plan: The Mill at Moreton Bay Redevelopment, Moreton Bay Regional Council. www.moretonbay.qld.gov.au/files/assets/public/services/projects/the-mill/the-mill-koala-management-plan.pdf (2016).

  • 43.

    Hanger, J. et al. Final Technical Report: Moreton Bay Rail Koala Management Program (Department of Transport and Main Roads, Queensland, 2017).

    Google Scholar 

  • 44.

    Fabijan, J. et al. Prevalence and clinical significance of koala retrovirus in two South Australian koala (Phascolarctos cinereus) populations. J. Med. Microbiol. 68, 1072–1080 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Whisson, D. A., Zylinski, S., Ferrari, A., Yokochi, K. & Ashman, K. R. Patchy resources and multiple threats: How do koalas navigate an urban landscape?. Landsc. Urban Plan. 201, 103854 (2020).

    Article  Google Scholar 

  • 46.

    Mitchell, P. in Biology of the Koala (eds AK Lee, KA Handasyde, & GD Sanson) 171–187 (1990).

  • 47.

    Jansen, C. C., Zborowski, P., Ritchie, S. A. & Van Den Hurk, A. F. Efficacy of bird-baited traps placed at different heights for collecting ornithophilic mosquitoes in eastern Queensland Australia. Aust. J. Med. Entomol. 48, 53–59 (2009).

    Article  Google Scholar 

  • 48.

    Johnston, E. et al. Mosquito communities with trap height and urban-rural gradient in Adelaide, South Australia: Implications for disease vector surveillance. J. Vect. Ecol. 39, 48–55 (2014).

    Article  Google Scholar 

  • 49.

    Kay, B., Boreham, P. & Fanning, I. Host-feeding patterns of Culex annulirostris and other mosquitoes (Diptera: Culicidae) at Charleville, southwestern Queensland Australia. J. Med. Entomol. 22, 529–535 (1985).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 50.

    Johansen, C., Power, S. & Broom, A. Determination of mosquito (Diptera: Culicidae) bloodmeal sources in Western Australia: Implications for arbovirus transmission. J. Med. Entomol. 46, 1167–1175 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    Kay, B., Fanning, I. & Carley, J. The vector competence of Australian Culex annulirostris with Murray Valley encephalitis and Kunjin viruses. A J. Exp. Biol. Med. 62, 641–650 (1984).

    Article  Google Scholar 

  • 52.

    Jacups, S. P., Whelan, P. I. & Currie, B. J. Ross River virus and Barmah Forest virus infections: A review of history, ecology, and predictive models, with implications for tropical northern Australia. Vector-Borne Zoonot. 8, 283–298 (2008).

    Article  Google Scholar 

  • 53.

    Hassell, J. M., Begon, M., Ward, M. J. & Fèvre, E. M. Urbanization and disease emergence: dynamics at the wildlife–livestock–human interface. Trends Ecol. Evol. 32, 55–67 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 54.

    Kelly, T. R. et al. One Health proof of concept: Bringing a transdisciplinary approach to surveillance for zoonotic viruses at the human-wild animal interface. Prev. Vet. Med. 137, 112–118 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  • 55.

    Jansen, C. C. et al. Epidemiologic, entomologic, and virologic factors of the 2014–15 Ross River Virus outbreak, Queensland Australia. Emerg. Infect. Dis. 25, 2243 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Woodruff, R. E. et al. Predicting Ross River virus epidemics from regional weather data. Epidemiology 1, 384–393 (2002).

    Article  Google Scholar 

  • 57.

    Kelly-Hope, L. A., Purdie, D. M. & Kay, B. H. Ross River virus disease in Australia, 1886–1998, with analysis of risk factors associated with outbreaks. J. Med. Entomol. 41, 133–150 (2004).

    PubMed  Article  PubMed Central  Google Scholar 

  • 58.

    Flies, E. J., Flies, A. S., Fricker, S. R., Weinstein, P. & Williams, C. R. Regional comparison of mosquito bloodmeals in South Australia: Implications for Ross River virus ecology. J. Med. Entomol. 53, 902–910 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 59.

    Stephenson, E. B., Murphy, A. K., Jansen, C. C., Peel, A. J. & McCallum, H. Interpreting mosquito feeding patterns in Australia through an ecological lens: An analysis of blood meal studies. Parasite. Vector. 12, 156 (2019).

    Article  Google Scholar 

  • 60.

    Gordon, G. Estimation of the age of the Koala, Phascolarctos cinereus (Marsupialia: Phascolarctidae), from tooth wear and growth. Aust. Mammal. 14, 5–12 (1991).

    Google Scholar 

  • 61.

    Robbins, A., Loader, J., Timms, P. & Hanger, J. Optimising the short and long-term clinical outcomes for koalas (Phascolarctos cinereus) during treatment for chlamydial infection and disease. PLoS ONE 13(12), e0209673. https://doi.org/10.1371/journal.pone.0209679 (2018).

    Article  Google Scholar 

  • 62.

    Calenge, C. Home range estimation in R: the adehabitatHR package (Saint Benoist, Auffargis, France, Office national de la classe et de la faune sauvage, 2011).

    Google Scholar 

  • 63.

    Quantum, G. QGIS geographic information system. Open source geospatial foundation project. https://qgis.osgeo.org (2015).

  • 64.

    Doherty, R., Whitehead, R. & Gorman, B. The isolation of a third group A arbovirus in Australia, with preliminary observations on its relationship to epidemic polyarthritis. Aust. J. Sci. 26, 183–184 (1963).

    Google Scholar 

  • 65.

    Gyawali, N., Taylor-Robinson, A. W., Bradbury, R. S., Potter, A. & Aaskov, J. G. Infection of Western Gray Kangaroos (Macropus fuliginosus) with Australian arboviruses associated with human infection. Vector-Born Zoonotic Dis. 20, 33–39 (2020).

    Article  Google Scholar 

  • 66.

    Togami, E. et al. First evidence of concurrent enzootic and endemic transmission of Ross River virus in the absence of marsupial reservoirs in Fiji. Int. J. Infect. Dis. 96, 94–96 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 67.

    Gyawali, N., Murphy, A. K., Hugo, L. E. & Devine, G. J. A micro-PRNT for the detection of Ross River virus antibodies in mosquito blood meals: A useful tool for inferring transmission pathways. PLoS ONE 15, e0229314. https://doi.org/10.1371/journal.pone.0229314 (2020).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • 68.

    Gatton, M. L., Kay, B. H. & Ryan, P. A. Environmental predictors of Ross River virus disease outbreaks in Queensland Australia. Am. J. Trop. Med. Hyg. 72, 792–799 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  • 69.

    McGrath, J. C., Drummond, G. B., McLachlan, E. M., Kilkenny, C. & Wainwright, C. L. Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br. J. Pharmacol. 160(7), 1573–1576 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 70.

    QDES. Queensland Department of Environment and Science, Wetland data – version 5 – Queensland series. https://www.des.qld.gov.au (2015).

  • 71.

    QDES. Queensland Department of Environment and Science, Matters of state environmental significance—wildlife habitat—koala habitat areas—core. https://www.des.qld.gov.au (2020).

  • 72.

    ESRI. Environmental Systems Research Institute. ArcGIS Desktop. Release 10.4 ed. Redlands, CA, USA. https://esri.com (2020).


  • Source: Ecology - nature.com

    Q&A: Clare Balboni on environmental economics

    Researchers improve efficiency of next-generation solar cell material