Using non-invasive sampling methods to determine the prevalence and distribution of Chlamydia pecorum and koala retrovirus in a remnant koala population with conservation importance
Faye Wedrowicz A B C , Jennifer Mosse B , Wendy Wright B and Fiona E. Hogan B
+ Author Affiliations
- Author Affiliations
A Faculty of Science, Monash University, Clayton, Australia. c/o School of Applied and Biomedical Sciences, Federation University Australia, Northways Road, Churchill, Vic. 3842, Australia.
B School of Applied and Biomedical Sciences, Federation University Australia, Churchill, Vic. 3842, Australia.
C Corresponding author. Email: faye.wedrowicz@gmail.com
Wildlife Research 45(4) 366-380 https://doi.org/10.1071/WR17184
Submitted: 27 April 2017 Accepted: 18 May 2018 Published: 11 July 2018
Abstract
Context: Pathogenic infections are an important consideration for the conservation of native species, but obtaining such data from wild populations can be expensive and difficult. Two pathogens have been implicated in the decline of some koala (Phascolarctos cinereus) populations: urogenital infection with Chlamydia pecorum and koala retrovirus subgroup A (KoRV-A). Pathogen data for a wild koala population of conservation importance in South Gippsland, Victoria are essentially absent.
Aims: This study uses non-invasive sampling of koala scats to provide prevalence and genotype data for C. pecorum and KoRV-A in the South Gippsland koala population, and compares pathogen prevalence between wild koalas and koalas in rescue shelters.
Methods: C. pecorum and KoRV-A provirus were detected by PCR of DNA isolated from scats collected in the field. Pathogen genetic variation was investigated using DNA sequencing of the C. pecorum ompA and KoRV-A env genes.
Key results: C. pecorum and KoRV-A were detected in 61% and 27% of wild South Gippsland individuals tested, respectively. KoRV-A infection tended to be higher in shelter koalas compared with wild koalas. In contrast with other Victorian koala populations sampled, greater pathogen diversity was present in South Gippsland.
Conclusions: In the South Gippsland koala population, C. pecorum is widespread and common whereas KoRV appears less prevalent than previously thought. Further work exploring the dynamics of these pathogens in South Gippsland koalas is warranted and may help inform future conservation strategies for this important population.
Implications: Non-invasive genetic sampling from scats is a powerful method for obtaining data regarding pathogen prevalence and diversity in wildlife. The use of non-invasive methods for the study of pathogens may help fill research gaps in a way that would be difficult or expensive to achieve using traditional methods.
Additional keywords: Chlamydia ompA genotyping, KoRV env genotyping, non-invasive sampling, Phascolarctos cinereus, scats.
References
Adams-Hosking, C., Moss, P., Rhodes, J., Grantham, H., and McAlpine, C. (2011). Modelling the potential range of the koala at the Last Glacial Maximum: future conservation implications. Australian Zoologist 35, 983–990.| Modelling the potential range of the koala at the Last Glacial Maximum: future conservation implications.Crossref | GoogleScholarGoogle Scholar |
Allen, C. (2015). Koala distribution, abundance, habitat and Chlamydia prevalence studies in the Strzelecki Ranges. NSW Office of Environment and Heritage, Sydney.
Ávila-Arcos, M. C., Ho, S. Y., Ishida, Y., Nikolaidis, N., Tsangaras, K., Hönig, K., Medina, R., Rasmussen, M., Fordyce, S. L., and Calvignac-Spencer, S. (2013). One hundred twenty years of koala retrovirus evolution determined from museum skins. Molecular Biology and Evolution 30, 299–304.
| One hundred twenty years of koala retrovirus evolution determined from museum skins.Crossref | GoogleScholarGoogle Scholar |
Blanshard, W., and Bodley, K. (2008). Koalas. In ‘Medicine of Australian Mammals’. (Eds L. Vogelnest and R. Woods.) pp. 227–327. (CSIRO Publishing: Melbourne.)
Chappell, K. J., Brealey, J. C., Amarilla, A. A., Watterson, D., Hulse, L., Palmieri, C., Johnston, S. D., Holmes, E. C., Meers, J., and Young, P. R. (2016). Phylogenetic diversity of koala retrovirus within a wild koala population. Journal of Virology 91, 1–11.
| Phylogenetic diversity of koala retrovirus within a wild koala population.Crossref | GoogleScholarGoogle Scholar |
DELWP (2017). Native vegetation – modelled 2005 ecological vegetation classes (with bioregional conservation status). Available at https://www.data.vic.gov.au/data/dataset/native-vegetation-modelled-2005-ecological-vegetation-classes-with-bioregional-conservation-status. Data. Vic, Melbourne.
Denner, J., and Young, P. R. (2013). Koala retroviruses: characterization and impact on the life of koalas. Retrovirology 10, 108–113.
| Koala retroviruses: characterization and impact on the life of koalas.Crossref | GoogleScholarGoogle Scholar |
Department of the Environment (2015). Phascolarctos cinereus (combined populations of Qld, NSW and the ACT) in Species Profile and Threats Database. Available at: https://www.environment.gov.au/cgi-bin/sprat/public/publicspecies.pl?taxon_id=85104 [accessed 23 December 2015]
EaCRC (2011a). The koala – saving our national icon. Available at: https://www.aph.gov.au/Parliamentary_Business/Committees/Senate/Environment_and_Communications/Completed_inquiries/2010-13/koalas/report/index [accessed 4 March 2016]. The Senate Printing Unit, Parliament House, Canberra.
EaCRC (2011b). Official Committee Hansard – Status, health and sustainability of Australia’s koala population. Available at: https://www.aph.gov.au/Parliamentary_Business/Committees/Senate/Environment_and_Communications/Completed_inquiries/2010-13/koalas/hearings/index [accessed 4 March 2016].
EaCRC (2012). Koala protected under national environment law. The Senate Environment and Communications Reference Committee. Sustainability, Environment, Water, Population and Communities, Canberra.
Eiden, M. V., and Taliaferro, D. L. (2011). Emerging retroviruses and cancer. In ‘Retroviruses and Insights into Cancer’. (Ed. J. Dudley.) pp. 307–333. (Springer New York: New York.)
Emmins, J. J. (1996). The Victorian koala: genetic heterogeneity, immune responsiveness and epizootiology of chlamydiosis. Ph.D. thesis, Monash University, Melbourne.
Gavel, Y., and Heijne, G. v. (1990). Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Engineering, Design & Selection 3, 433–442.
| Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering.Crossref | GoogleScholarGoogle Scholar |
Gerber, L. R., McCallum, H., Lafferty, K. D., Sabo, J. L., and Dobson, A. (2005). Exposing extinction risk analysis to pathogens: Is disease just another form of density dependence? Ecological Applications 15, 1402–1414.
| Exposing extinction risk analysis to pathogens: Is disease just another form of density dependence?Crossref | GoogleScholarGoogle Scholar |
González-Orozco, C. E., Pollock, L. J., Thornhill, A. H., Mishler, B. D., Knerr, N., Laffan, S. W., Miller, J. T., Rosauer, D. F., Faith, D. P., and Nipperess, D. A. (2016). Phylogenetic approaches reveal biodiversity threats under climate change. Nature Climate Change 6, 1110–1114.
| Phylogenetic approaches reveal biodiversity threats under climate change.Crossref | GoogleScholarGoogle Scholar |
Grogan, L. F., Ellis, W., Jones, D., Hero, J.-M., Kerlin, D. H., and McCallum, H. (2017). Current trends and future directions in koala chlamydial disease research. Biological Conservation 215, 179–188.
| Current trends and future directions in koala chlamydial disease research.Crossref | GoogleScholarGoogle Scholar |
Guy, A. J., and Banks, P. (2012). A survey of current rehabilitation practices for native mammals in eastern Australia. Australian Mammalogy 34, 108–118.
| A survey of current rehabilitation practices for native mammals in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Hanger, J. J., Bromham, L. D., McKee, J. J., O’Brien, T. M., and Robinson, W. F. (2000). The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus. Journal of Virology 74, 4264–4272.
| The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus.Crossref | GoogleScholarGoogle Scholar |
Hartmann, K. (2012). Clinical aspects of feline retroviruses: a review. Viruses 4, 2684–2710.
| Clinical aspects of feline retroviruses: a review.Crossref | GoogleScholarGoogle Scholar |
Higgins, D., Beninati, T., Meek, M., Irish, J., and Griffith, J. (2012). Within-population diversity of koala Chlamydophila pecorum at ompA VD1–VD3 and the ORF663 hypothetical gene. Veterinary Microbiology 156, 353–358.
| Within-population diversity of koala Chlamydophila pecorum at ompA VD1–VD3 and the ORF663 hypothetical gene.Crossref | GoogleScholarGoogle Scholar |
Houlden, B. A., Costello, B. H., Sharkey, D., Fowler, E. V., Melzer, A., Ellis, W., Carrick, F., Baverstock, P. R., and Elphinstone, M. S. (1999). Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817). Molecular Ecology 8, 999–1011.
| Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817).Crossref | GoogleScholarGoogle Scholar |
Jackson, M., Giffard, P., and Timms, P. (1997). Outer membrane protein A gene sequencing demonstrates the polyphyletic nature of koala Chlamydia pecorum isolates. Systematic and Applied Microbiology 20, 187–200.
| Outer membrane protein A gene sequencing demonstrates the polyphyletic nature of koala Chlamydia pecorum isolates.Crossref | GoogleScholarGoogle Scholar |
Jelocnik, M., Frentiu, F. D., Timms, P., and Polkinghorne, A. (2013). Multilocus sequence analysis provides insights into molecular epidemiology of Chlamydia pecorum infections in Australian sheep, cattle, and koalas. Journal of Clinical Microbiology 51, 2625–2632.
| Multilocus sequence analysis provides insights into molecular epidemiology of Chlamydia pecorum infections in Australian sheep, cattle, and koalas.Crossref | GoogleScholarGoogle Scholar |
Kollipara, A., Polkinghorne, A., Wan, C., Kanyoka, P., Hanger, J., Loader, J., Callaghan, J., Bell, A., Ellis, W., and Fitzgibbon, S. (2013). Genetic diversity of Chlamydia pecorum strains in wild koala locations across Australia and the implications for a recombinant C. pecorum major outer membrane protein based vaccine. Veterinary Microbiology 167, 513–522.
| Genetic diversity of Chlamydia pecorum strains in wild koala locations across Australia and the implications for a recombinant C. pecorum major outer membrane protein based vaccine.Crossref | GoogleScholarGoogle Scholar |
Lee, T., Zenger, K. R., Close, R. L., and Phalen, D. N. (2012). Genetic analysis reveals a distinct and highly diverse koala (Phascolarctos cinereus) population in South Gippsland, Victoria, Australia. Australian Mammalogy 34, 68–74.
| Genetic analysis reveals a distinct and highly diverse koala (Phascolarctos cinereus) population in South Gippsland, Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Legione, A. R., Amery-Gale, J., Lynch, M., Haynes, L., Gilkerson, J. R., Sansom, F. M., and Devlin, J. M. (2016a). Chlamydia pecorum infection in free-ranging koalas (Phascolarctos cinereus) on French Island, Victoria, Australia. Journal of Wildlife Diseases 52, 426–429.
| Chlamydia pecorum infection in free-ranging koalas (Phascolarctos cinereus) on French Island, Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Legione, A. R., Patterson, J. L., Whiteley, P. L., Amery-Gale, J., Lynch, M., Haynes, L., Gilkerson, J. R., Polkinghorne, A., Devlin, J. M., and Sansom, F. M. (2016b). Identification of unusual Chlamydia pecorum genotypes in Victorian koalas (Phascolarctos cinereus) and clinical variables associated with infection. Journal of Medical Microbiology , .
| Identification of unusual Chlamydia pecorum genotypes in Victorian koalas (Phascolarctos cinereus) and clinical variables associated with infection.Crossref | GoogleScholarGoogle Scholar |
Legione, A. R., Patterson, J. L., Whiteley, P., Firestone, S. M., Curnick, M., Bodley, K., Lynch, M., Gilkerson, J. R., Sansom, F. M., and Devlin, J. M. (2017). Koala retrovirus (KoRV) genotyping analyses reveal a low prevalence of KoRV-A in Victorian koalas and an association with clinical disease. Journal of Medical Microbiology 66, 236–244.
| Koala retrovirus (KoRV) genotyping analyses reveal a low prevalence of KoRV-A in Victorian koalas and an association with clinical disease.Crossref | GoogleScholarGoogle Scholar |
Lewis, F. (1954). The rehabilitation of the koala in Victoria. Victorian Naturalist 70, 197–200.
Lunney, D., Crowther, M. S., Wallis, I., Foley, W. J., Lemon, J., Wheeler, R., Madani, G., Orscheg, C., Griffith, J. E., and Krockenberger, M. (2012). Koalas and climate change: a case study on the Liverpool Plains, north-west New South Wales. In ‘Wildlife and Climate Change: towards robust conservation strategies for Australian Fauna’. (Eds D. Lunney and P. Hutchings.) pp. 150–168. (Royal Zoological Society of NSW: Sydney.)
Markey, B., Wan, C., Hanger, J., Phillips, C., and Timms, P. (2007). Use of quantitative real-time PCR to monitor the shedding and treatment of chlamydiae in the koala (Phascolarctos cinereus). Veterinary Microbiology 120, 334–342.
| Use of quantitative real-time PCR to monitor the shedding and treatment of chlamydiae in the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Martin, R. W. (1989). Draft management plan for the conservation of the koala (Phascolarctos cinereus) in Victoria: a report to the Department of Conservation, Forests, and Lands, Victoria. Department of Conservation, Forests, and Lands, Melbourne.
Martin, R., and Handasyde, K. (1990). Population dynamics of the koala (Phascolarctos cinereus) in southeastern Australia. In ‘Biology of the Koala’. (Eds A. K. Lee, K. A. Handasyde and G. D. Sanson.) pp. 75–84. (Surrey Beatty and Sons: Sydney.)
Martin, R., and Handasyde, K. (1999) ‘The Koala: Natural History, Conservation and Management.’ (University of New South Wales: Sydney.)
May, R. M., and Anderson, R. M. (1979). Population biology of infectious diseases: Part II. Nature 280, 455.
| Population biology of infectious diseases: Part II.Crossref | GoogleScholarGoogle Scholar |
McAlpine, C., Brearley, G., Rhodes, J., Bradley, A., Baxter, G., Seabrook, L., Lunney, D., Liu, Y., Cottin, M., Smith, A. G., and Timms, P. (2017). Time-delayed influence of urban landscape change on the susceptibility of koalas to chlamydiosis. Landscape Ecology 32, 663–679.
| Time-delayed influence of urban landscape change on the susceptibility of koalas to chlamydiosis.Crossref | GoogleScholarGoogle Scholar |
McCallum, H. (2012). Disease and the dynamics of extinction. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 2828–2839.
| Disease and the dynamics of extinction.Crossref | GoogleScholarGoogle Scholar |
McCallum, H., Kerlin, D. H., Ellis, W., and Carrick, F. (2017). Assessing the significance of endemic disease in conservation—koalas, chlamydia, and koala retrovirus as a case study. Conservation Letters 2017, e12425.
| Assessing the significance of endemic disease in conservation—koalas, chlamydia, and koala retrovirus as a case study.Crossref | GoogleScholarGoogle Scholar |
Menkhorst, P. (2008). Hunted, marooned, re-introduced, contracepted: A history of koala management in Victoria. In ‘Too Close for Comfort: Contentious Issues in Human–Wildlife Encounters’. (Eds D. Lunney, A. Munn and W. Meikle.) pp. 73–92. (Royal Zoological Society of New South Wales: Sydney.)
Mohamad, K. Y., Roche, S. M., Myers, G., Bavoil, P. M., Laroucau, K., Magnino, S., Laurent, S., Rasschaert, D., and Rodolakis, A. (2008). Preliminary phylogenetic identification of virulent Chlamydophila pecorum strains. Infection, Genetics and Evolution 8, 764–771.
| Preliminary phylogenetic identification of virulent Chlamydophila pecorum strains.Crossref | GoogleScholarGoogle Scholar |
Mohamad, K. Y., Kaltenboeck, B., Rahman, K. S., Magnino, S., Sachse, K., and Rodolakis, A. (2014). Host adaptation of Chlamydia pecorum towards low virulence evident in co-evolution of the ompA, incA, and ORF663 loci. PLoS One 9, e103615.
| Host adaptation of Chlamydia pecorum towards low virulence evident in co-evolution of the ompA, incA, and ORF663 loci.Crossref | GoogleScholarGoogle Scholar |
Narayan, E. J., Webster, K., Nicolson, V., Mucci, A., and Hero, J.-M. (2013). Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the koala (Phascolarctos cinereus). General and Comparative Endocrinology 187, 39–47.
| Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Nyari, S., Waugh, C. A., Dong, J., Quigley, B. L., Hanger, J., Loader, J., Polkinghorne, A., and Timms, P. (2017). Epidemiology of chlamydial infection and disease in a free-ranging koala (Phascolarctos cinereus) population. PLoS One 12, e0190114.
| Epidemiology of chlamydial infection and disease in a free-ranging koala (Phascolarctos cinereus) population.Crossref | GoogleScholarGoogle Scholar |
Obendorf, D. L., and Handasyde, K. A. (1990). Pathology of chlamydial infection in the reproductive tract of the female koala (Phascolarctos cinereus). In ‘Biology of the Koala’. (Eds A. K. Lee, K. A. Handasyde and G. D. Sanson.) pp. 255–259. (Surrey Beatty & Sons: Sydney.)
Pantchev, A., Sting, R., Bauerfeind, R., Tyczka, J., and Sachse, K. (2010). Detection of all Chlamydophila and Chlamydia spp. of veterinary interest using species-specific real-time PCR assays. Comparative Immunology, Microbiology and Infectious Diseases 33, 473–484.
| Detection of all Chlamydophila and Chlamydia spp. of veterinary interest using species-specific real-time PCR assays.Crossref | GoogleScholarGoogle Scholar |
Phillips, S. (2011). Development of a lightweight, portable trap for capturing free-ranging koalas Phascolarctos cinereus. Australian Zoologist 35, 747–749.
| Development of a lightweight, portable trap for capturing free-ranging koalas Phascolarctos cinereus.Crossref | GoogleScholarGoogle Scholar |
Polkinghorne, A., Hanger, J., and Timms, P. (2013). Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas. Veterinary Microbiology 165, 214–223.
| Recent advances in understanding the biology, epidemiology and control of chlamydial infections in koalas.Crossref | GoogleScholarGoogle Scholar |
Quigley, B. L., Ong, V. A., Hanger, J., and Timms, P. (2018). Molecular dynamics and mode of transmission of koala retrovirus as it invades and spreads through a wild Queensland koala population. Journal of Virology 92, e01871-17.
| Molecular dynamics and mode of transmission of koala retrovirus as it invades and spreads through a wild Queensland koala population.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
Radford, S. L., McKee, J., Goldingay, R. L., and Kavanagh, R. P. (2006). The protocols for koala research using radio-collars: a review based on its application in a tall coastal forest in New South Wales and the implications for future research. Australian Mammalogy 28, 187–200.
| The protocols for koala research using radio-collars: a review based on its application in a tall coastal forest in New South Wales and the implications for future research.Crossref | GoogleScholarGoogle Scholar |
Rank, R. G., and Yeruva, L. (2014). Hidden in plain sight: chlamydial gastrointestinal infection and its relevance to persistence in human genital infection. Infection and Immunity 82, 1362–1371.
| Hidden in plain sight: chlamydial gastrointestinal infection and its relevance to persistence in human genital infection.Crossref | GoogleScholarGoogle Scholar |
Santamaria, F., and Schlagloth, R. (2016). The effect of Chlamydia on translocated Chlamydia-naïve koalas: a case study. Australian Zoologist 38, 192–202.
| The effect of Chlamydia on translocated Chlamydia-naïve koalas: a case study.Crossref | GoogleScholarGoogle Scholar |
Simmons, G., Young, P., Hanger, J., Jones, K., Clarke, D., McKee, J., and Meers, J. (2012). Prevalence of koala retrovirus in geographically diverse populations in Australia. Australian Veterinary Journal 90, 404–409.
| Prevalence of koala retrovirus in geographically diverse populations in Australia.Crossref | GoogleScholarGoogle Scholar |
Speight, K. N., Polkinghorne, A., Penn, R., Boardman, W., Timms, P., Fraser, T., Johnson, K., Faull, R., Bate, S., and Woolford, L. (2016). Prevalence and pathological features of Chlamydia pecorum infections in South Australian koalas (Phascolarctos cinereus). Journal of Wildlife Diseases 52, 301–306.
| Prevalence and pathological features of Chlamydia pecorum infections in South Australian koalas (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.Crossref | GoogleScholarGoogle Scholar |
Tarlinton, R., Meers, J., Hanger, J., and Young, P. (2005). Real-time reverse transcriptase PCR for the endogenous koala retrovirus reveals an association between plasma viral load and neoplastic disease in koalas. The Journal of General Virology 86, 783–787.
| Real-time reverse transcriptase PCR for the endogenous koala retrovirus reveals an association between plasma viral load and neoplastic disease in koalas.Crossref | GoogleScholarGoogle Scholar |
Timms, P. (2005). Chlamydial infection and disease in the koala. Microbiology Australia 26, 65–68.
Úbeda, F., and Jansen, V. A. A. (2016). The evolution of sex-specific virulence in infectious diseases. Nature Communications 7, 13849.
| The evolution of sex-specific virulence in infectious diseases.Crossref | GoogleScholarGoogle Scholar |
Vigerust, D. J., and Shepherd, V. L. (2007). Virus glycosylation: role in virulence and immune interactions. Trends in Microbiology 15, 211–218.
| Virus glycosylation: role in virulence and immune interactions.Crossref | GoogleScholarGoogle Scholar |
Waugh, C., Hanger, J., Timms, P., and Polkinghorne, A. (2016). Koala translocations and Chlamydia: managing risk in the effort to conserve native species. Biological Conservation 197, 247–253.
| Koala translocations and Chlamydia: managing risk in the effort to conserve native species.Crossref | GoogleScholarGoogle Scholar |
Wedrowicz, F., Karsa, M., Mosse, J., and Hogan, F. E. (2013). Reliable genotyping of the koala (Phascolarctos cinereus) using DNA isolated from a single faecal pellet. Molecular Ecology Resources 13, 634–641.
| Reliable genotyping of the koala (Phascolarctos cinereus) using DNA isolated from a single faecal pellet.Crossref | GoogleScholarGoogle Scholar |
Wedrowicz, F., Saxton, T., Mosse, J., Wright, W., and Hogan, F. E. (2016). A non-invasive tool for assessing pathogen prevalence in koala (Phascolarctos cinereus) populations: detection of Chlamydia pecorum and koala retrovirus (KoRV) DNA in genetic material sourced from scats. Conservation Genetics Resources 8, 511–521.
| A non-invasive tool for assessing pathogen prevalence in koala (Phascolarctos cinereus) populations: detection of Chlamydia pecorum and koala retrovirus (KoRV) DNA in genetic material sourced from scats.Crossref | GoogleScholarGoogle Scholar |
Wedrowicz, F., Wright, W., Schlagloth, R., Santamaria, F., and Cahir, F. (2017). Landscape, koalas and people: A historical account of koala populations and their environment in South Gippsland. Australian Zoologist 38, 518–536.
| Landscape, koalas and people: A historical account of koala populations and their environment in South Gippsland.Crossref | GoogleScholarGoogle Scholar |
Wedrowicz, F., Mosse, J., Wright, W., and Hogan, F. E. (2018a). Genetic structure and diversity of the koala population in South Gippsland, Victoria: a remnant population of high conservation significance. Conservation Genetics 19, 713–728.
| Genetic structure and diversity of the koala population in South Gippsland, Victoria: a remnant population of high conservation significance.Crossref | GoogleScholarGoogle Scholar |
Wedrowicz, F., Mosse, J., Wright, W., and Hogan, F. E. (2018b). Isolating DNA sourced non-invasively from koala scats: a comparison of four commercial DNA stool kits. Conservation Genetics Resources , .
| Isolating DNA sourced non-invasively from koala scats: a comparison of four commercial DNA stool kits.Crossref | GoogleScholarGoogle Scholar |
Whisson, D. A., Dixon, V., Taylor, M. L., and Melzer, A. (2016). Failure to respond to food resource decline has catastrophic consequences for koalas in a high-density population in southern Australia. PLoS One 11, e0144348.
| Failure to respond to food resource decline has catastrophic consequences for koalas in a high-density population in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Xu, W., Stadler, C. K., Gorman, K., Jensen, N., Kim, D., Zheng, H., Tang, S., Switzer, W. M., Pye, G. W., and Eiden, M. V. (2013). An exogenous retrovirus isolated from koalas with malignant neoplasias in a US zoo. Proceedings of the National Academy of Sciences of the United States of America 110, 11547–11552.
| An exogenous retrovirus isolated from koalas with malignant neoplasias in a US zoo.Crossref | GoogleScholarGoogle Scholar |
