A. Smith

Parasites, emerging disease and wildlife conservation

In this review some emerging issues of parasite infections in wildlife, particularly in Australia, are considered. We discuss the importance of understanding parasite biodiversity in wildlife in terms of conservation, the role of wildlife as reservoirs of parasite infection, and the role of parasites within the broader context of the ecosystem. Using a number of parasite species, the value of undertaking longitudinal surveillance in natural systems using non-invasive sampling and molecular tools to characterise infectious agents is illustrated in terms of wildlife health, parasite biodiversity and ecology.

Zoonotic enteric protozoa

A growing number of enteric protozoan species are considered to have zoonotic potential. Their clinical impact varies and in many cases is poorly defined. Similarly, the epidemiology of infections, particularly the role of non-human hosts, requires further study. In this review, new information on the life cycles and transmission of Giardia, Cryptosporidium, Entamoeba, Blastocystis and Balantidium are examined in the context of zoonotic potential, as well as polyparasitism and clinical significance.

Trypanosomes in a declining species of threatened Australian marsupial, the brush-tailed bettong Bettongia penicillata (Marsupialia: Potoroidae)

The brush-tailed bettong (Bettongia penicillata), or woylie, is a medium-sized macropod marsupial that has undergone a rapid and substantial decline throughout its home range in the Upper Warren region of Western Australia over a period of approximately 5 years. As part of an investigation into possible causes of the decline a morphologically distinct Trypanosoma sp. was discovered by light microscopy in the declining population but was absent in a stable population within the Karakamia Wildlife Sanctuary. Further investigations employing molecular methods targeting variations in the 18s rRNA gene determined that the trypanosome was novel and was also present within the Karakamia population albeit at a much lower overall prevalence and individual parasitaemia levels. Phylogenetic analysis suggests the novel Trypanosoma sp. to be closely related to other trypanosomes isolated from native Australian wildlife species. Although it appears unlikely that the parasite is solely responsible for the decline in woylie population size, it may (singularly or in conjunction with other infectious agents) predispose woylies to increased mortality.

Parasite zoonoses and wildlife: emerging issues.

The role of wildlife as important sources, reservoirs and amplifiers of emerging human and domestic livestock pathogens, in addition to well recognized zoonoses of public health significance, has gained considerable attention in recent years. However, there has been little attention given to the transmission and impacts of pathogens of human origin, particularly protozoan, helminth and arthropod parasites, on wildlife. Substantial advances in molecular technologies are greatly improving our ability to follow parasite flow among host species and populations and revealing valuable insights about the interactions between cycles of transmission. Here we present several case studies of parasite emergence, or risk of emergence, in wildlife, as a result of contact with humans or anthropogenic activities. For some of these parasites, there is growing evidence of the serious consequences of infection on wildlife survival, whereas for others, there is a paucity of information about their impact.

Giardia in Western Australian wildlife

Giardia has been found in numerous species of mammalian wildlife but very little information is available on the species and strains/genotypes that occur naturally in mammals in the wild. Recently, a novel genotype of Giardia was described in Western Australia, in the Southern brown bandicoot, or quenda (Isoodon obesulus). In order to determine the host range, distribution and prevalence of this novel quenda genotype of Giardia, a comprehensive survey of this marsupial and cohabiting mammalian species was undertaken throughout the mainland and some off-shore islands of Western Australia, including urban areas. The overall prevalence of Giardia in 351 wildlife samples was low, with only 4.8% (17) samples testing positive. Amongst the 51 quenda samples, 11.8% (6) were positive for the quenda genotype, 5.9% (3) for assemblage C/D and 2% (1) for assemblages A and E. This study has demonstrated that Giardia is a remarkably rare parasite in native wildlife in Western Australia, raising questions about the ecology of Giardia infections in wildlife.

The diversity, distribution and host-parasite associations of trypanosomes in Western Australian wildlife

Little is known regarding the diversity, distribution or host-parasite associations of Trypanosoma spp. in Australian wildlife. Here we report on an investigation based on divergence of the 18S rRNA gene of trypanosomes isolated from a range of hosts and varied geographical locations. A total of 371 individuals representing 19 species of native animals from 14 different locations were screened. In total, 32 individuals from 9 different species tested positive for the parasite. Phylogenetic analysis revealed considerable parasite diversity with no clear geographical distribution and no evidence of host specificity. In general, it appears that Australian Trypanosoma spp. are widespread, with several genotypes appearing in multiple host species and in varied locations including both mainland areas and offshore islands. Some host species were found to be susceptible to multiple genotypes, but no individuals were infected with more than a single isolate.

Tuberculosis (Mycobacterium microti) in wild field vole populations

Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5.2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10.78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13.15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.

Trypanosomes, fleas and field voles : ecological dynamics of a host-vector-parasite interaction

To investigate the prevalence of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in its field vole (Microtus agrestis) host, we monitored over a 2-year period a range of intrinsic and extrinsic parameters pertaining to host demographics, infection status and vector (flea) prevalence. Generalized Linear Mixed Modelling was used to analyse patterns of both flea and trypanosome occurrence. Overall, males of all sizes and ages were more likely to be infested with fleas than their female counterparts. Flea prevalence also showed direct density dependence during the winter, but patterns of density dependence varied amongst body mass (age) classes during the summer. Trypanosome prevalence did not vary between the sexes but was positively related to past flea prevalence with a lag of 3 months, with the highest levels occurring during the autumn season. A convex age-prevalence distribution was observed, suggesting that individuals develop a degree of immunity to trypanosome infection with age and exposure. An interaction between age and whether the individual was new or recaptured suggested that infected animals are less likely to become territory holders than their uninfected counterparts.

Western Australian Marsupials Are Multiply Infected with Genetically Diverse Strains of Toxoplasma gondii

Five different organs from 16 asymptomatic free-ranging marsupial macropods (Macropus rufus, M. fuliginosus, and M. robustus) from inland Western Australia were tested for infection with Toxoplasma gondii by multi-locus PCR-DNA sequencing. All macropods were infected with T. gondii, and 13 had parasite DNA in at least 2 organs. In total, 45 distinct T. gondii genotypes were detected. Fourteen of the 16 macropods were multiply infected with genetically distinct T. gondii genotypes that often partitioned between different organs. The presence of multiple T. gondii infections in macropods suggests that native mammals have the potential to promote regular cycles of sexual reproduction in the definitive felid host in this environment.

Infection prevalence and vector-borne transmission: are vectors always to blame?

The potential for vector-independent transmission of pathogens to occur in what is generally considered to be a vector-borne system is a subject that has received little direct attention. The circumstances under which such a process might take place could conceivably be described as occasional under natural conditions and accidental under unnatural conditions. A more immediate concern is the ability to detect the presence of vector-independent transmission in action and, where possible, to quantify its contribution to overall infection prevalence. As intrinsically difficult as this process might be, careful observation and the use of laboratory and field-scale experiments have indicated that alternative, vector-independent routes of transmission do exist and might contribute significantly to overall prevalence in some host-vector-pathogen systems.