Temporal and spatial dynamics of trypanosomes infecting the brush-tailed bettong (Bettongia penicillata): a cautionary note of disease-induced population decline

Abstract

Background: The brush-tailed bettong or woylie (Bettongia penicillata) is on the brink of extinction. Its numbers have declined by 90% since 1999, with their current distribution occupying less than 1% of their former Australian range. Woylies are known to be infected with three different trypanosomes (Trypanosoma vegrandis, Trypanosoma copemani and Trypanosoma sp. H25) and two different strains of T. copemani that vary in virulence. However, the role that these haemoparasites have played during the recent decline of their host is unclear and is part of ongoing investigation.

Methods: Woylies were sampled from five locations in southern Western Australia, including two neighbouring indigenous populations, two enclosed (fenced) populations and a captive colony. PCR was used to individually identify the three different trypanosomes from blood and tissues of the host, and to investigate the temporal and spatial dynamics of trypanosome infections.

Results: The spatial pattern of trypanosome infection varied among the five study sites, with a greater proportion of woylies from the Perup indigenous population being infected with T. copemani than from the neighbouring Kingston indigenous population. For an established infection, T. copemani detection was temporally inconsistent. The more virulent strain of T. copemani appeared to regress at a faster rate than the less virulent strain, with the infection possibly transitioning from the acute to chronic phase. Interspecific competition may also exist between T. copemani and T. vegrandis, where an existing T. vegrandis infection may moderate the sequential establishment of the more virulent T. copemani.

Conclusion: In this study, we provide a possible temporal connection implicating T. copemani as the disease agent linked with the recent decline of the Kingston indigenous woylie population within the Upper Warren region of Western Australia. The chronic association of trypanosomes with the internal organs of its host may be potentially pathogenic and adversely affect their long term fitness and coordination, making the woylie more susceptible to predation.

Figure 1

Sample locations in Western Australia. ‘bold’ denotes an indigenous population and ‘italics’ denotes an enclosed population.

Figure 2

Trypanosome prevalence of infected woylies only (N = 121) from the five study sites (with uninfected woylies not graphically represented). Where a host was recorded as either infected or co-infected if it tested positive to a Trypanosoma sp. or multiple Trypanosoma spp. at least once during the study period.

Figure 3

Prevalence of T. vegrandis and T. copemani from the peripheral blood of the eight infected woylies at NAR during successive seasons. Where each of the eight hosts was tested up to three times per season for both trypanosomes species, and the mean infection state (0(uninfected) and 1(infected)) was calculated for each season (± CI₉₅).

Figure 4

Decline in prevalence of T. copemani P1 and P2 from the peripheral blood of the eight infected woylies at NAR during successive seasons. Where each of the eight hosts was tested up to three times per season for T. copemani, and the mean infection state (0 (uninfected) and 1 (infected)) was calculated for each season (± CI₉₅).

Figure 5

Overall trypanosome prevalence (T. vegrandis and T. copemani) from the peripheral blood of 45 woylies at NAR during successive seasons. Where each of the 45 hosts was tested up to three times per season for both trypanosomes species, and the mean infection state (0 (uninfected) and 1 (infected)) was calculated for each season (± CI₉₅).

Figure 6

Changes in the trypanosome prevalence at the UWR and the changing woylie population status at Warrup, (which is part of the KP). (reproduced with permission from [10]).