Investigation of Potential Diseases Associated with Northern Territory Mammal Declines
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Investigation of Potential Diseases Associated with Northern Territory Mammal Declines Final report for NERP Project 4.1: June 2015 Andrea Reiss1, Bethany Jackson1, Graeme Gillespie2, Danielle Stokeld2 and Kris Warren1 1. Conservation Medicine Program, College of Veterinary Medicine, Murdoch University 2. Northern Territory Department of Land Resource Management 2 This page has been left intentionally blank National Environmental Research Program - Small Mammal Disease Investigation: Final Report June 2015 3 EXECUTIVE SUMMARY There is compelling evidence of broad-scale declines in populations of small terrestrial native mammals in northern Australia, including the Top End of the Northern Territory (NT) over the past 20 years. Causes under consideration include changed fire regimes, introduced fauna (including predators) and disease. To date information on health and disease in northern Australian mammals has been limited. Disease is increasingly recognised as a primary driver of some wildlife population declines and extinctions e.g., Tasmanian devil facial tumour disease, white nose syndrome in bats and chytrid fungus in amphibians. Disease has been identified as a risk factor for extinction in declining and fragmented wildlife populations globally, particularly in situations of increased environmental stressors, changing ecosystems, arrival of new vertebrate threats or climate change. Unless wild populations are studied in detail over long periods of time, the effects of disease are easily overlooked and may be difficult to determine. This study is the largest and most comprehensive study of health and disease in small mammals in northern Australia and is one of a small number of studies worldwide to have approached investigation of wildlife populations in this comprehensive manner. A total of 281 individuals from four target species were examined and sampled under anaesthesia across five main sites in the Top End of the NT, from June 2013 to Nov 2014. Non-invasive samples (ticks and faeces) were collected from a further 113 animals. Nine prioritised pathogen groups were investigated by diagnostic testing: o encephalomyocarditis virus (EMCV) o mammalian herpesvirus o Coxiella burnetii (disease agent causing Q fever) o Leptospira spp. o enteric Salmonella spp. o enteric protozoa (Cryptosporidium spp. and Giardia spp.) o protozoal haemoparasites (trypanosomes, Babesia spp. and Hepatozoon spp.) o Toxoplasma gondii o gastrointestinal helminths (worms) Additional investigation was undertaken under collaborative agreements for pathogens of significance to human health: Ross River virus and Barmah Forest virus. Results were analysed for associations with locations, species, seasons, body condition, sex, blood parameters and other potential health indicators such as level of ectoparasite burden. The majority of individuals examined were assessed to be in good health and body condition. The presence of several pathogens which are known to be associated with disease in wildlife populations was identified, including mammalian herpesvirus, enteric Salmonella spp., protozoal haemoparasites (trypanosomes, Babesia spp., Hepatozoon spp.), enteric protozoa (Cryptosporidium spp. and Giardia spp.), microfilaria and Toxoplasma. Of these, several were previously unreported in target species in the NT. De novo molecular pathogen discovery studies on the northern brown bandicoot (Isoodon macrourus) used cutting-edge metagenomic techniques to look for unrecognised pathogens. National Environmental Research Program - Small Mammal Disease Investigation: Final Report June 2015 4 Analysis is still underway; however there is evidence of several potentially significant pathogens including viruses from the Retroviridae family. A number of ectoparasite taxa that may act as vectors for infectious disease were identified. The study found evidence that several pathogens, capable of impacting population health, are circulating in Top End small mammal populations, but did not find compelling evidence that a single pathogen is responsible for, or a risk factor in, the decline of small mammals in the Top End of the NT. The study found no serological evidence of infection with encephalomyocarditis virus, Leptospira spp. or Coxiella burnetii; however it is possible that these pathogens are present in populations (at levels below detection limits due to sample sizes), with resultant morbidity or mortality. Limitations of this study include a short temporal span, a lack of longitudinal and survivorship studies, difficulties in collecting specimens from small species and an inability to study populations in the absence of feral cats and other predators. In combination these factors limit the ability to investigate the potentially complex interactions between disease and other pressures on mammal populations. Top End mammal populations are assessed to be at risk of increased levels of environmental and host stresses and are vulnerable to the likely future impacts of infectious disease. The current situation in the Top End fulfils many of the criteria necessary for an emerging infectious disease and novel disease agents should be considered as risk factors for populations. It is recommended that disease investigation continues in mammal populations of concern in the Top End in the medium to long term (five to 20 years) to increase knowledge; improve data sets; maintain and build capacity; and maximise opportunities for detection and response to new disease threats. It is recommended that future studies include, as priorities: o longitudinal and survivorship studies to determine the impact of nominated pathogens on host survival and fitness (e.g., using cortisol and anti-oxidant capacity), and detect pathogen trends in individuals (e.g. whether certain pathogens are shed intermittently and whether infections persist or resolve). o a particular focus on Toxoplasma gondii (due to its strong epidemiological link to presence of cats in the environment and as the only identified pathogen likely to impact a broad taxonomic range of mammals) and any potentially significant pathogens emerging from de novo molecular work. This should include a focus on sites where feral cats have been excluded, to investigate potential interactions between pathogen presence and predation as well as differences in prevalence of T. gondii in areas where the definitive host (the cat) is present/absent o extension of serological studies to a wider host species range (including macropods) to determine the presence and prevalence of priority pathogens such as T. gondii in the landscape. Ongoing collaborative efforts between NT Department of Land Resource Management and the Conservation Medicine Program (School of Veterinary and Life Sciences), Murdoch University may facilitate research and enable continued opportunities for work funded through competitive grants or industry sponsorship. National Environmental Research Program - Small Mammal Disease Investigation: Final Report June 2015 5 CONTENTS EXECUTIVE SUMMARY ............................................................................................................................ 3 ACKNOWLEDGEMENTS ........................................................................................................................... 9 GLOSSARY and ABBREVIATIONS used in this report ............................................................................. 11 1 INTRODUCTION ............................................................................................................................. 14 1.1 Declining small mammal populations in the Top End of the Northern Territory ................. 14 1.2 The importance of disease in wildlife and declining populations ......................................... 15 1.2.1 Emerging infectious diseases ........................................................................................ 17 1.2.2 Challenges in investigating disease in free-ranging wildlife populations ..................... 17 1.3 Understanding disease processes ......................................................................................... 19 1.4 General indicators of health and disease ............................................................................. 20 1.4.1 Macroparasites ............................................................................................................. 20 1.5 Disease in small mammal species in Australia (with a focus on the tropical north) ............ 21 1.6 Aims of this project ............................................................................................................... 22 2 MATERIALS AND METHODS .......................................................................................................... 23 2.1 Selection of species and sites................................................................................................ 23 2.2 Development of protocols .................................................................................................... 23 2.3 Review of information on disease in target species and in the Top End .............................. 23 2.4 Hazard identification and assessment .................................................................................. 24 2.4.1 Hazard scoring and prioritisation .................................................................................. 24 2.5 Field processes .....................................................................................................................