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The bare-nosed wombat and its pathogen, Sarcoptes scabiei

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Martin, AM ORCID: 0000-0002-6603-2385 2019 , 'The bare-nosed wombat and its pathogen, Sarcoptes scabiei', PhD thesis, University of Tasmania.

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Abstract

An unintended consequence of the global movement of humans and their domestic animals has, and continues to be, the introduction of pathogens to naïve host species. Such pathogen invasion events have consequences for wildlife ranging from benign to catastrophic. Yet, the specific impacts to affected species – from individuals to populations – and the capacity to mitigate these are often poorly understood. This is perhaps best illustrated in mammals by the parasitic mite, Sarcoptes scabiei (causative agent of sarcoptic mange): among the most successful of known pathogens to benefit from anthropogenic globalisation. The mite now occurs on all continents (except Antarctica) and has been documented infecting >100 mammal species, yet the impacts of this parasite remain enigmatic for most wildlife species it infects.
In Australia, evidence indicates S. scabiei was introduced by European settlers. Over the last 200 years, S. scabiei has been documented in several native and non-native Australian mammals, with most striking impacts observed in the bare-nosed (common) wombat, Vombatus ursinus. Though sarcoptic mange causes conservation, ethical, and welfare concerns to V. ursinus, considerable knowledge gaps have persisted about the effects of the parasite, including the impacts of infection on individuals and at population scales, as well as the capacity to mitigate infection. Furthermore, there is a dearth of fundamental knowledge about the V. ursinus host, despite being a perceived “common” species. The aims of this thesis were therefore four-fold: (i) to identify behavioural and physiological impacts of S. scabiei presence at the individual level, (ii) to quantify the population-scale impact of a sarcoptic mange outbreak in a bare-nosed wombat population, (iii) to evaluate the efficacy of the current suggested treatment protocol administered at a population-scale, and (iv) to understand the genetic structure of V. ursinus across its entire range (encompassing three subspecies).
To understand the impacts of sarcoptic mange at the individual level, I focused on physiological and behavioural changes observed in mange-infected bare-nosed wombats. Specifically, I investigated the effect of sarcoptic mange infection on heat loss, field metabolic rate, resting and foraging behaviour, and fatty acid composition (Chapter 2). I used methods in thermal imagery, doubly labelled water, activity loggers, and fat composition profiles to reveal that as mange severity increased in wombats, (i) heat lost to the environment increased, (ii) field metabolic rates increased, (iii) total time spent foraging decreased while total time spent inactive increased, and (iv) fatty acid composition changed in adipose tissue. I concluded that the compounding effects of physiological and behavioural changes left infected wombats unable to meet the energetic demands of sarcoptic mange disease.
The pattern of disease spread and impact of an outbreak on bare-nosed wombat abundance was assessed at Narawntapu National Park (north-central Tasmania) during a mange epizootic. I used seven years of population data and four years of disease severity data in combination with piece-wise linear regressions and geographic heat maps to understand the consequence of mange outbreak in a semi-isolated wombat population. I found that disease spread through Narawntapu National Park spatiotemporally, in a wave-like pattern from east to west, and caused a >94% decline in wombat abundance from 2010-2016 (Chapter 3). Furthermore, I suggested that sarcoptic mange outbreaks can result in localised extirpation in semi-isolated populations.
During the outbreak event at Narawntapu National Park, I attempted a population scale treatment regime based on the current suggested treatment protocols (Chapter 4). I administered treatment to >200 burrows for 12 consecutive weeks and performed disease severity surveys for 18 months to quantify the efficacy of the treatment regime. I found that current treatment methods provided temporary protection, but were not sufficient to eradicate mange from the park, and reinfection occurred shortly after treatment ceased. Using a novel, purpose-built, state-based model fitted to empirical data from the treatment trial, I explored practical changes to current treatment methods that may influence treatment outcomes. I found that treatment application success was low using current techniques, and that a longer lasting treatment may facilitate capacity for future population scale disease control.
Finally, I sought to develop a baseline understanding of V. ursinus genetic structure across its range, as well as address the currently accepted subspecific claims (mainland V. u. hirsutus, Flinders Island V. u. ursinus, Tasmania V. u. tasmaniensis). Using genome-wide single nucleotide polymorphisms, I identified (i) three genetically distinct groups, consistent with current subspecies classifications, (ii) a second population of the Vulnerable V. u. ursinus on Maria Island (an offshore island of Tasmania), and (iii) isolation by distance across the Tasmanian range (Chapter 5). I concluded that the three subspecies may better be managed as separate units.
The work presented in this thesis has contributed to a greater understanding of: (i) the impacts of sarcoptic mange, at the individual and population level, in bare-nosed wombats, (ii) the efficacy of current treatment methodologies and potential improvements to future management regimes, and (iii) the baseline genetic structure of V. ursinus, identifying three genetically distinct subspecies that may warrant separate management action. The contributions I have made to V. ursinus and S. scabiei research will help to inform future disease management efforts for this species and provides insight to management of evolutionary significant units within the V. ursinus range. Moreover, this thesis contributes to the broader understanding of an invasive, globally significant, and environmentally transmitted pathogen, with conservation implications for other impacted species and similarly transmitted invasive pathogens impacting wildlife.

Item Type: Thesis - PhD
Authors/Creators:Martin, AM
Keywords: Bare-nosed wombat; sarcoptic mange; Sarcoptes scabiei; wildlife disease; disease control; Vombatus ursinus; genetic structure; conservation
DOI / ID Number: 10.25959/100.00031862
Copyright Information:

Copyright 2018 the author

Additional Information:

Chapter 2 appears to be the equivalent of a post-print version of an article published as: Martin, A. M., Fraser, T. A., Lesku, J. A., Simpson, K., Roberts, G. L., Garvey, J., Polkinghorne, A., Burridge, C. P., Carver, S., 2018. The cascading pathogenic consequences of Sarcoptes scabiei infection that manifest in host disease, Royal Society open science (5)4, 1-14. © 2018 The authors. Published by the Royal Society under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited

Chapter 3 appears to be the equivalent of a post-print version of an article published as: Martin, A. M., Burridge, C. P., Ingram, J., Fraser, T. A., Carver, S.2018. Invasive pathogen drives host population collapse: Effects of a travelling wave of sarcoptic mange on bare‐nosed wombats, Journal of applied ecology, 55(21), 331– 341

Chapter 4 appears to be the equivalent of the pre-peer reviewed version of the following article: Martin, A. M., Richards, S. A., Fraser, T. A., Polkinghorne, A., Burridge, C. P., Carver, S., 2019. Population-scale treatment informs solutions for control of environmentally transmitted wildlife disease, Journal of applied ecology, 56(10), which has been published in final form at https://doi.org/10.1111/1365-2664.13467. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions

Chapter 5 appears to be the equivalent of a post-print version of an article published as: Martin, A. M., Carver, S., Proft, K., Fraser, T. A., Polkinghorne, A., Banks, S., Burridge, C. P., 2019. Isolation, marine transgression, and translocation of the bare-nosed wombat (Vombatus ursinus), Evolutionary applications, 1114-1123, © 2019 the authors. Published by John Wiley & Sons, this is an open access article under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) License, https://creativecommons.org/licenses/by/4.0/ which permits use, distribution and reproduction in any medium, provided the original work is properly cited

Appendix 1 appears to be the equivalent of a post-print version of an article published as: Martin, A. M., Carver, S., Proft, K., Fraser, T. A., Polkinghorne, A., Banks, S., Burridge, C. P., 2019. Burrows with resources have greater visitation and may enhance mange transmission among wombats, Australian mammalogy, 41(2), 287–290

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