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Infectious Disease Surveillance in the Woylie (Bettongia penicillata)

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Abstract

Wild populations of the critically endangered woylie (Bettongia penicillata) recently declined by 90% in southwest Western Australia. Increased predation is the leading hypothesis for decline, but disease may be playing a role increasing susceptibility to predation. To explore this possibility, we surveyed woylie populations in the wild, in captivity and in a predator-free sanctuary for exposure to, and infection with, four known pathogens of macropods: herpesviruses, Wallal and Warrego orbiviruses, and Toxoplasma gondii. Our study found two of 68 individuals positive for neutralizing antibodies against known macropodid alphaherpesviruses. Three of 45 individuals were PCR positive for a herpesvirus that was shown to be a novel gammaherpesvirus or a new strain/variant of Potoroid Herpesvirus 1. Further sequence information is required to definitively determine its correct classification. There was no evidence of antibodies to orbivirus Wallal and Warrego serogroups, and all serological samples tested for T. gondii were negative. This is the first report of PCR and serological detection of herpesviruses in the woylie. Positive individuals did not demonstrate clinical signs of herpesviral diseases; therefore, the clinical significance of herpesviruses to wild woylie populations remains unclear. Further monitoring for herpesvirus infections will be important to inform disease risk analysis for this virus and determine temporal trends in herpesvirus activity that may relate to population health and conservation outcomes.

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References

  • Alfaro-Núñez,AM, Gilbert TP (2014) Validation of a sensitive PCR assay for the detection of Chelonid fibropapilloma-associated herpesvirus in latent turtle infections. Journal of Virological Methods 206:38–41

    Article  PubMed  Google Scholar 

  • Amery-Gale J, Vaz PK, Whiteley P, Tatarczuch L, Taggart DA, Charles JA, Schultz D, Ficorilli NP, Devlin JM, Wilks C (2014) Detection and identification of a gammaherpesvirus in Antechinus spp. in Australia. Journal of Wildlife Disease 50(2):334–339.

    Article  CAS  Google Scholar 

  • Attwood HD, Woolley PA, Rickard MD (1975) Toxoplasmosis in dasyurid marsupials. Journal of Wildlife Disease 11:541–543.

    Article  Google Scholar 

  • Averis S, Thompson RCA, Lymbery AJ, Wayne AF, Morris KD, Smith A (2009) The diversity, distribution and host-parasite associations of trypanosomes in Western Australian Wildlife. Parasitology 136:1269–1279.

    Article  CAS  PubMed  Google Scholar 

  • Belaganahalli MN, Maan S, Maan NS, Pritchard I, Kirkland PD, Brownlie J, Attoui H, Mertens PCC (2014) Full Genome Characterization of the Culicoides-Borne Marsupial Orbiviruses: Wallal Virus, Mudjinbarry Virus and Warrego Viruses. PLoS One 9(10): e108379. doi:10.1371/journal.pone.0108379

    Article  PubMed  PubMed Central  Google Scholar 

  • Besier AS, Mahony TJ, Crockford M, Gravel JL, Chapman TF, O’Dea MA (2016) Alphaherpesvirus-associated disease in greater bilbies (Macrotis lagotis). Australian Veterinary Journal. doi:10.1111/avj.12447

    Google Scholar 

  • Botero A, Thompson CK, Peacock CS, Clode PL, Nicholls PK, Wayne AF, Lymbery AJ, Thompson RCA (2013) Trypanosomes genetic diversity, polyparasitism and the population decline of the critically endangered Australian marsupial, the brush tailed bettong or woylie (Bettongia penicillata). International Journal for Parasitology: Parasites and Wildlife 2:77–89.

    PubMed  PubMed Central  Google Scholar 

  • Britt Jr JO, Frost DF, Cockrill JM (1994) Fatal herpesviral hepatitis in a red kangaroo (Macropus rufus). Journal of Zoo and Wildlife Medicine 25:580–584.

    Google Scholar 

  • Callinan RB, Kefford B (1981) Mortalities associated with herpesvirus infection in captive macropods. Journal of Wildlife Disease 17:311–317.

    Article  CAS  Google Scholar 

  • Caughley G, Gunn A (1996) Conservation Biology in Theory and Practice. Massachusetts: Blackwell Science.

    Google Scholar 

  • Chmielewicz B, Goltz M, Lahrmann KH, Ehlers B (2003) Approaching virus safety in xenotransplantation: a search for unrecognized herpesviruses in pigs. Xenotransplantation 10:349–356.

    Article  PubMed  Google Scholar 

  • Clopper CJ, Pearson ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26:404–413.

    Article  Google Scholar 

  • Davison JA (2008) Herpesviruses: General features. In: Encyclopedia of Virology, 3rd ed., Mahy BWJ, Van Regenmortel MHV (editors), Oxford: Elsevier, pp. 430–436

    Chapter  Google Scholar 

  • de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecological Letters 8:117–126.

    Article  Google Scholar 

  • Dickens M, Delehanty D, Romero L (2010) Stress: an inevitable component of animal translocation. Biological Conservation 143:1329–1341.

    Article  Google Scholar 

  • Dickson J, Hopkinson WI, Coackley W, Spence T, Fairfax R (1980) Herpesvirus hepatitis in rat kangaroos. Australian Veterinary Journal 56:463–464.

    Article  CAS  PubMed  Google Scholar 

  • Dobson A, Lyles A (2000) Black-footed ferret recovery. Science 288(5468):985–988.

    Article  CAS  PubMed  Google Scholar 

  • Ehlers B (2008) Herpesviruses: Discovery. In: Encyclopedia of Virology, 3rd ed. Mahy BWJ, and Van Regenmortel MHV (editors), Oxford: Elsevier, pp. 420–429.

    Chapter  Google Scholar 

  • Fancourt BA, Nicol, SC, Hawkins CE, Jones ME, Johnson CN (2014) Beyond the disease: Is Toxoplasma gondii infection causing population declines in the eastern quoll (Dasyurus viverrinus)? International Journal for Parasitology: Parasites and Wildlife 3:102–112.

    PubMed  PubMed Central  Google Scholar 

  • Finnie EP, Littlejohns IR, Acland HM (1976) Mortalities in parma wallabies (Macropus parma) associated with probable herpesvirus. Australian Veterinary Journal 52: 294.

    Article  CAS  PubMed  Google Scholar 

  • Finnie EP (1980) A marsupial herpesvirus. In: The Comparative Pathology of Zoo Animals, Montali RJ, Migaki G (editors), Washington, DC: Smithsonian Institution Press, pp 179–182.

    Google Scholar 

  • Guliani S, Smith GA, Young PL, Mattick JS, Mahony TJ (1999) Reactivation of a macropodid herpesvirus from the eastern grey kangaroo (Macropus giganteus) following corticosteroid treatment. Veterinary Microbiology 68:59–69.

    Article  CAS  PubMed  Google Scholar 

  • Harwood J, Hall A (1990) Mass mortality in marine mammals: its implications for population dynamics and genetics. Trends in Ecology and Evolution 5:254–257.

    Article  CAS  PubMed  Google Scholar 

  • Heard M, Smith K, Ripp K,, Berger M, Chen J, Dittmeier J, Goter M, McGarvey ST, Ryan E (2013) The threat of disease increases as species move toward extinction. Conservation Biology 27:1378–1388.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hillman A, Lymbery A, Thompson RCA (2015) Is Toxoplasma gondii a threat to the conservation of free-ranging Australian marsupial populations? International Journal of Parasitology: Parasitology of Wildlife 5(1). doi:10.1016/j.ijppaw.2015.12.002

  • Hooper P (1999) Kangaroo blindness and some other new viral diseases in Australia. Australian Veterinary Journal 77(8):514–515.

    Article  CAS  PubMed  Google Scholar 

  • Hooper PT, Lunt RA, Gould AR, Hyatt AD, Russell GM, Kattenbelt JA, Blacksell SD, Reddacliff, LA, Kirkland PD, Davis RJ, Durham PJ, Bishop AL, Waddington J (1999) Epidemic of blindness in kangaroos–evidence of a viral aetiology. Australian Veterinary Journal 77(8):529–36.

    Article  Google Scholar 

  • Johnson MA, Whalley JM, Littlejohns IR, Dickson J, Smith VW, Wilks CR, Reisner AH (1985) Macropodid herpesviruses 1 and 2: Two herpesviruses from Australian marsupials differentiated by restriction endonucleases, DNA composition and hybridization. Archives of Virology 85:313–319.

    Article  CAS  PubMed  Google Scholar 

  • Johnson AM, Roberts H, Statham P, Munday BL (1988) Serodiagnosis of acute toxoplasmosis in macropods. Veterinary Parasitology 34:24–33.

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kerr A, Whalley JM, Poole WE (1981) Herpesvirus neutralizing antibody in grey kangaroos. Australian Veterinary Journal 57(7):347–348.

    Article  CAS  PubMed  Google Scholar 

  • Kock R, Woodford M, Rossiter P (2010) Disease risks associated with the translocation of wildlife. Scientific and Technical Review of the Office International des Epizooties 29(2):329.

    Article  CAS  Google Scholar 

  • Ladds P (2009) Pathology of Australian native wildlife. Collingwood: CSIRO Publishing, p. 640

    Google Scholar 

  • Marlow NJ, Thomas ND, Williams AAE, Macmahon B, Lawson J, Hitchen Y, Angus J, Berry O (2015) Cats (Felis catus) are more abundant and are the dominant predator of woylies (Bettongia penicillata) after sustained fox (Vulpes vulpes) control. Australian Journal of Zoology 63(1):18–27.

    Article  Google Scholar 

  • MacLauchlan NJ, Dubovi EJ (2011) Fenner’s Veterinary Virology, 4th ed. London: Academic Press, Elsevier, pp. 181–200.

    Google Scholar 

  • Mathews F, Moro D, Strachan R, Gelling M, Buller N (2006) Health surveillance in wildlife reintroductions. Biological Conservation 131(2):338–347. doi:10.1016/j.biocon.2006.04.011

    Article  Google Scholar 

  • Melville L (2000) Wallal serogroup viruses in black wallaroos. Veterinary Pathology Reports 16:19.

    Google Scholar 

  • O’Brien C, van Riper III C, Myers D (2009) Making reliable decisions in the study of wildlife diseases: using hypothesis tests, statistical power, and observed effects. Journal of Wildlife Disease 45(3):700–712.

    Article  Google Scholar 

  • Pacioni C (2010) The population and epidemiological dynamics associated with recent decline of woylies (Bettongia penicillata) in Australia. Ph.D. thesis, Murdoch University.

  • Pacioni C (2014) Modelling woylie (Bettongia penicillata) population genetics to inform management strategies. World Wildlife Fund, Perth, Australia.

    Google Scholar 

  • Pacioni C, Johansen CA, Mahony TJ, O’Dea MA, Robertson ID, Wayne AF, Ellis T (2013a) A virological investigation into declining woylie populations. Australia Journal of Zoology 61:446–453

  • Pacioni C, Wayne AF, Spencer PBS (2013b) Genetic outcomes from the translocations of the critically endangered woylie. Current Zoology 59:294–310

  • Pacioni C, Eden P, Reiss A, Ellis T, Knowles G, Wayne AF (2015) Disease hazard identification and assessment associated with wildlife population declines. Ecological Management and Restoration 16:142–152.

    Article  Google Scholar 

  • Pan S, Thompson RCA, Grigg ME, Sundar N, Smith A, Lymbery AJ (2012) Western Australian marsupials are multiply co-infected with genetically diverse strains of Toxoplasma gondii. International Journal of Parasitology 7:1–6.

    Google Scholar 

  • Parameswaran N (2008) Toxoplasma gondii in Australian Marsupials. Ph.D. Thesis, Veterinary Parasitology and Conservation Medicine Murdoch University, Perth, Western Australia, p 139.

  • Parameswaran N, O’Handley R, Grigg M, Fenwick S, Thompson R (2009) Seroprevalence of Toxoplasma gondii in wild kangaroos using an ELISA. Parasitology International 58:161–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parameswaran N, Thompson RCA, Sundar N, Pan M, Johnson NC, Smith Grigg ME (2010) Nonarchetypal type II-like and atypical strains of Toxoplasma gondii infecting marsupials of Australia. International Journal of Parasitology 40:635–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Portas TJ (2010) Toxoplasmosis in Macropodids: A review. Journal of Zoo and Wildlife Medicine 41:1–6.

    Article  PubMed  Google Scholar 

  • Portas T, Fletcher D, Spratt D, Reiss A, Holz P, Stalder K, Devlin J, Taylor D, Dobroszczyk D, Manning AD (2014) Health evaluation of free-ranging eastern bettongs (Bettongia gaimardi) during translocation for reintroduction in Australia. Journal of Wildlife Disease 50:210–23

    Article  CAS  Google Scholar 

  • Preston CM (2008) Herpesviruses: Latency. In: Encyclopedia of Virology, 3rd ed. Mahy BWJ, Van Regenmortel MHV (editors), Oxford: Elsevier, pp. 436–442.

    Chapter  Google Scholar 

  • Reddacliff L, Kirkland P, Philbey A, Davis R, Vogelnest L, Hulst F, Blyde D, Deykin A, Smith J, Hooper P, Gould A, Hyatt, A (1999) Experimental reproduction of viral chorioretinitis in kangaroos. Australian Veterinary Journal 77:522–528.

    Article  CAS  PubMed  Google Scholar 

  • Reiss A, Jackson B, Gillespie G, Stokeld D, Warren K (2015) Investigation of potential diseases associated with Northern Territory mammal declines. Darwin: Charles Darwin University, p 132.

  • Roizman B, Pellet PE (2007) The Family of Herpesviridae: a brief introduction. In: Field Virology, 4th ed. Knipe DM, Howley PM (editors), Philadelphia: Lippincott Williams and Wilkins, pp. 2381–2397.

    Google Scholar 

  • Rong J, Bunce M, Wayne A, Pacioni C, Ryan U, Irwin PJ (2012) High prevalence of Theileria penicillata in woylies (Bettongia penicillata). Experimental Parasitology 131(2):157–161.

    Article  PubMed  Google Scholar 

  • Rose K (1999) Common diseases of urban wildlife. In: Wildlife in Australia, Healthcare and management. Proceedings 327, 13–17 September, University of Sydney: Post Graduate Foundation of Veterinary Medicine. Western Plains Zoo, Dubbo Australia.

  • Sainsbury A, Vaughan-Higgins R (2012) Analyzing disease risks associated with translocations. Conservation Biology 26(3): 442–452.

    Article  PubMed  Google Scholar 

  • Sergeant ESG (2017) Epitools epidemiological calculators. Ausvet Pty Ltd. Available at: http://epitools.ausvet.com.au

  • Smith JA, Wellehan Jr JFX, Pogranichniy RM, Childress AL, Landolfi JA, Terio KA (2008) Identification and isolation of a novel herpesvirus in a captive mob of eastern grey kangaroos (Macropus giganteus). Veterinary Microbiology 129:236–245.

    Article  CAS  PubMed  Google Scholar 

  • Staker L (2006) The complete guide to the care of macropods. Panorama Print, Australia, p. 437.

    Google Scholar 

  • Stalder K, Vaz PK, Gilkerson JR, Baker R, Whiteley P, Ficorilli N, Tatarczuch L, Portas T, Skogvold K, Anderson G, Devlin JM (2015) The prevalence and clinical significance of herpesvirus infection in populations of Australian maruspials. PLoS ONE 10(7): e0133807. doi:10.1371/journal.pone.0133807.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson CK, Wayne AF, Godfrey SS, Thompson RCA (2014) Temporal and spatial dynamics of trypanosomes infecting the brush-tailed bettong (Bettongia penicillata): a cautionary note of disease-induced population decline. Parasites and Vectors 7:169.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vaz PK, Motha J, McCowan, C, Ficorilli N, Whiteley PL, Wilks CR, Hartley CA, Gilkerson JR, Browning GF, Devlin JM (2013) Isolation and characterization of a novel herpesvirus from a free-ranging eastern grey kangaroo (Macropus giganteus). Journal of Wildlife Disease 49:143–151.

    Article  CAS  Google Scholar 

  • Wayne A (2008) Progress report of the Woylie Conservation Research Project: Diagnosis of recent woylie declines in southwestern Australia. Department of Environment and Conservation, Perth, Western Australia

  • Wayne A, Friend T, Burbidge A, Morris K, van Weenen, J (2008) Bettongia penicillata. The IUCN Red List of Threatened Species 2008: e.T2785A9480872. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T2785A9480872.en. (Online, 1 June 2016)

  • Wayne AF, Maxwell M, Nicholls P, Pacioni C, Reiss A, Smith A, Thompson RCA, Vellios C, Ward C, Wayne JC, Wilson I, Williams MR (2011) The woylie conservation research project: investigating the cause(s) of woylie declines in the Upper Warren region. Progress Report. In. Department of Environment and Conservation, Manjimup, Western Australia, p. 73.

  • Wayne AF, Maxwell MA, Ward CG, Vellios CV, Ward BG, Liddelow GL, Wilson I, Wayne JC, Williams MR (2013a) Importance of getting the numbers right: quantifying the rapid and substantial decline of an abundant marsupial, Bettongia penicillata. Wildlife Research 40:169–183.

    Article  Google Scholar 

  • Wayne, A.F, Maxwell MA, Ward CG, Vellios, CV, Wilson IJ, Dawson K (2013b) Woylie Conservation and Research Project: Progress Report 2010–2013, Department of Parks and Wildlife, Perth. Available: https://www.researchgate.net/profile/Adrian_Wayne/publications

  • Wayne AF, Maxwell MA, Ward CG, Vellios CV, Wilson I, Wayne JC, Williams MR (2015) Sudden and rapid decline of the abundant marsupial Bettongia penicillata in Australia. Oryx 49:175–185

    Article  Google Scholar 

  • Webber CE, Whalley JM (1978) Widespread occurrence in Australian marsupials of neutralizing antibodies to a herpesvirus from a parma wallaby. Australian Journal of Experimental Biology and Medical Science 56:351–357.

    Article  CAS  PubMed  Google Scholar 

  • Wilcox RS, Vaz P, Ficorilli NP, Whiteley PL, Wilks CR, Devlin JM (2011) Gammaherpesvirus infection in a free-ranging eastern grey kangaroo (Macropus giganteus). Australian Veterinary Journal 89:55–57.

    Article  CAS  PubMed  Google Scholar 

  • Wilks CR, Kefford B, Callinan RB (1981) Herpesvirus as a cause of fatal disease in Australian wallabies. Journal of Comparative Pathology 91:461–465.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The staff of the Perth Zoo Veterinary Department and the Native Species Breeding Program are to be thanked for their assistance in clinical examination, sample collection, and processing of results. Department of Parks and Wildlife Manjimup field staff and volunteers are also acknowledged for their hard work and dedication to woylie conservation. We thank Nino Ficorilli for providing expert and technical advice in regard to laboratory methods. This work was supported by the following grants: Caring for Our Country, National Resource Management; Wildlife Conservation in Action, Perth Zoo; Science Division, Department of Parks and Wildlife (DPaW), WA, Student Project Stipend; and Wildlife Disease Association, Australasian Section, Student Award. K. Skogvold was supported by The Murdoch University Veterinary Trust.

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Correspondence to Rebecca J. Vaughan-Higgins.

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Skogvold, K., Warren, K.S., Jackson, B. et al. Infectious Disease Surveillance in the Woylie (Bettongia penicillata). EcoHealth 14, 518–529 (2017). https://doi.org/10.1007/s10393-017-1254-9

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  • DOI: https://doi.org/10.1007/s10393-017-1254-9

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