Daniel M. Tompkins

Distribution and Impacts of Tasmanian Devil Facial Tumor Disease

The Tasmanian devil, Sarcophilus harrisii, is the largest extant marsupial carnivore. In 1996, a debilitating facial tumor was reported. It is now clear that this is an invariably lethal infectious cancer. The disease has now spread across the majority of the range of the species and is likely to occur across the entire range within 5 to 10 years. The disease has lead to continuing declines of up to 90% and virtual disappearance of older age classes. Mark-recapture analysis and a preliminary epidemiological model developed for the population with the best longitudinal data both project local extinction in that area over a timeframe of 10 to 15 years from disease emergence. However, the prediction of extinction from the model is sensitive to the estimate of the latent period, which is poorly known. As transmission appears to occur by biting, much of which happens during sexual encounters, the dynamics of the disease may be typical of sexually transmitted diseases. This means that transmission is likely to be frequency-dependent with no threshold density for disease maintenance. Extinction over the entire current range of the devil is therefore a real possibility and an unacceptable risk.

Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand

Abstract Although the mosquito vector responsible for the epizootic outbreaks of avian malaria in Hawaiian avifauna, Culex quinquefasciatus, has spread rapidly in New Zealand over the past three decades, no survey for malarial parasites has been conducted for more than 50 years. Avian malaria often causes extreme morbidity and mortality in novel hosts, and much of New Zealands native avifauna has likely had no prior exposure, so the impact of this spread on native biodiversity is potentially serious. Wild non‐native birds were surveyed for malarial parasites at multiple locations, to test the hypothesis that the prevalence of malarial infection is associated positively with the known distribution of C. quinquefasciatus. Blood samples collected were analysed using a Polymerase Chain Reaction (PCR) assay. There was a strong pattern of decreasing percentage of samples positive for the blood parasite PCR marker from north to south, closely matching the known distribution of C. quinquefasciatus. A subsample of 10 PCR products were sequenced, and all identified as the malarial parasite Plasmodium relictum. Since historical surveys found no malarial parasites in the New Zealand avifauna, with a few minor exceptions, this suggests that this invasive exotic vector may be one factor driving the emergence of avian malaria. Sampling of wild non‐native birds at Orana Park, Christchurch, where a disease outbreak occurred recently in a captive native bird population, suggested that such outbreaks may spill‐back into local wild bird populations. The high prevalence of malarial infection observed in certain non‐native species, particularly blackbirds, indicates that they may act as reservoirs of infection to native species.

Emerging infectious diseases of wildlife: a critical perspective

We review the literature to distinguish reports of vertebrate wildlife disease emergence with sufficient evidence, enabling a robust assessment of emergence drivers. For potentially emerging agents that cannot be confirmed, sufficient data on prior absence (or a prior difference in disease dynamics) are frequently lacking. Improved surveillance, particularly for neglected host taxa, geographical regions and infectious agents, would enable more effective management should emergence occur. Exposure to domestic sources of infection and human-assisted exposure to wild sources were identified as the two main drivers of emergence across host taxa; the domestic source was primary for fish while the wild source was primary for other taxa. There was generally insufficient evidence for major roles of other hypothesized drivers of emergence.

Climate warming may cause a parasite-induced collapse in coastal amphipod populations

Besides the direct impact on the general performance of individual organisms, the ecological consequences of climate change in terrestrial and marine ecosystems are expected to be determined by complex cascading effects arising from modified trophic interactions and competitive relationships. Recently, the synergistic effect of parasitism and climate change has been emphasised as potentially important to host population dynamics and community structure, but robust empirical evidence is generally lacking. The amphipod Corophium volutator is an ecologically important species in coastal soft-bottom habitats of the temperate North Atlantic, and commonly serves as host to microphallid trematodes that cause intensity-dependent and temperature-dependent mortality in the amphipod population. Using a simulation model parameterised with experimental and field data, we demonstrate that a 3.8°C increase in ambient temperature will likely result in a parasite-induced collapse of the amphipod population. This temperature increase is well within the range predicted to prevail by the year 2075 in the International Wadden Sea region from where the model data are obtained. Due to the amphipods’ ecological importance, their population decline may impact the coastal ecosystem as a whole.

Parasites lost - do invaders miss the boat or drown on arrival?

Host species that colonize new regions often lose parasite species. Using population arrival and establishment data for New Zealands introduced bird species and their ectoparasitic chewing lice species, we test the relative importance of different processes and mechanisms in causing parasite species loss. Few lice failed to arrive in New Zealand with their hosts due to being missed by chance in the sample of hosts from the original population (missing the boat). Rather, most lice were absent because their hosts or the parasite themselves failed to establish populations in their new environment. Given they arrived and their host established, parasite persistence was more strongly related to factors associated with transmission efficiency (number of host individuals introduced, host body size, host sociality and parasite suborder) than parasite propagule pressure and aggregation. Such insights into parasite success are invaluable to both understanding and managing their impact.

UNEXPECTED CONSEQUENCES OF VERTEBRATE PEST CONTROL: PREDICTIONS FROM A FOUR-SPECIES COMMUNITY MODEL

Although indirect effects are important structuring forces in ecological communities, they are seldom considered in the design of pest control operations. However, such effects may cause unpredicted and deleterious changes in other populations that could reduce or even negate the benefit to endangered species for which control is undertaken. Furthermore, the complexity and nonlinearities inherent in interacting ecological communities may cause thresholds in the strength of pest control, on either side of which indirect effects could vary greatly in their magnitude and desirability. We constructed a four-species simulation model for a common pest community in New Zealand beech (Nothofagus spp.) forests: house mice, ship rats, stoats, and brushtail possums. When the model was perturbed to simulate common control techniques, marked increases in the abundance of nontarget pest species were observed at the next forest mast. Higher mouse numbers were observed following both toxin (1080) application and rat kill-trapping, and higher rat numbers were observed following stoat kill-trapping, due to a release from predation in all cases. In comparison, a marked decrease in stoat abundance at the next forest mast was observed following simultaneous control of rats and mice, due to the effects of decreased prey abundance on the stoat population. For rat control, the size of the indirect effect on mouse numbers increased monotonically with control strength. Because the curvature of the relationship is slight, the relationship between the direct benefits of control and the indirect costs incurred would remain relatively unchanged regardless of the strength of control employed. For simultaneous mouse and rat control, however, high levels of control (as initially simulated) were predicted to cause decreased peak stoat abundance at the next mast event, whereas intermediate and low levels of control were predicted to cause increased stoat abundance. Hence, this study demonstrates two points of concern for pest managers. First, indirect effects of control operations do have the potential to reduce the planned-for benefit. Second, thresholds in the strength of control employed can potentially occur, across which indirect effects switch from being of conservation benefit to being of conservation concern.

Parasite-induced surfacing in the cockle Austrovenus stuchburyi: adaptation or not?

Parasite manipulation of host behaviour is a compelling example of the extended phenotype. However, in many cases, such manipulation may be incorrectly assumed. Previous work has demonstrated that Austrovenus stuchburyi cockles stranded on mud‐flat surfaces due to an inability to re‐burrow both contain significantly more metacercariae of the trematode Curtuteria australis and are predated by the definitive host of this parasite at a faster rate than burrowed cockles. These results have been interpreted as strong evidence for a manipulation of cockle behaviour by the trematode to facilitate transmission to the definitive host. The model presented here, however, indicates that the selective advantage to the parasite of the altered host behaviour is currently of a negligible level at our study site that is highly unlikely to have been realized as an adaptation over evolutionary time. Hence, there are no grounds on which the more parsimonious explanation, that the altered host behaviour observed is simply an incidental side‐effect of infection, can be rejected. We thus maintain that for any change in the behaviour of infected hosts to be confirmed as potentially a parasite trait that has evolved in response to selection, the adaptive benefit taking into account the entire parasite life cycle may need to be considered.

PRESENCE AND SEASONAL PREVALENCE OF PLASMODIUM SPP. IN A RARE ENDEMIC NEW ZEALAND PASSERINE (TIEKE OR SADDLEBACK, PHILESTURNUS CARUNCULATUS)

The conservation and management of Saddlebacks (Philesturnus carunculatus) and other New Zealand birds, currently relies on the translocation of individuals to predator-free sites. Avian malaria has been identified as one of the diseases to be tested for prior to translocations in New Zealand, with the aim of translocating disease-free individuals. We describe avian malaria lineages and their seasonal prevalence in 2007–2008 in Saddlebacks from Mokoia Island, a source of birds for translocations, and investigate their pathogenicity. Three lineages of avian malaria were found at low prevalence (≥10.6%) and parasitemia (all but one infection were below 1/10,000 erythrocytes), typical of chronic infections. Two lineages clustered with previously identified lineages of Plasmodium relictum and one with a lineage of Plasmodium (Huffia) elongatum. Prevalence of malaria infection was higher in the spring with no significant difference in prevalence between juvenile and adult birds. We found no effect of stress on infections or any indication of pathogenicity.

Epidemiology of an avian malaria outbreak in a native bird species (Mohoua ochrocephala) in New Zealand

Abstract Emerging infectious diseases pose a considerable threat to wildlife globally. One such disease that has apparently emerged in recent years in New Zealand is avian malaria, with Plasmodium infections being detected in numerous species for the first time. Although the overall significance of this apparent emergence is not yet known, infection by Plasmodium has been diagnosed as a cause of mortality in several native species in captivity. Here we investigate the epidemiology of the most recently confirmed case, with our results having potentially important implications for native bird management. Avian malaria caused the death of five mohua or yellowheads (Mohoua ochrocephala) at Orana Wildlife Park in Canterbury during 2003–05, after their translocation from the Blue Mountains (Otago) in 2003. A lack of detectable Plasmodium infection in wild mohua in both the Blue Mountains and the nearby Catlins region, in contrast to an unusually high prevalence in wild bird populations at Orana Park at the time of the outbreak, indicates that infection was most likely acquired by the birds after translocation. This evidence, although not conclusive, strongly argues for assessment of the risk of greater (and potentially deleterious) exposure to malarial parasites to be undertaken prior to native bird translocation. A mosquito investigation carried out at Orana Wildlife Park identified the ubiquitous indigenous mosquito Culex pervigilans as the likely disease vector. Hence, management of this mosquito species (in addition to the exotic Cx. quinquefasciatus, a known vector of avian malaria in other countries) is a potentially useful preventative measure against disease outbreaks in native bird populations of conservation value in New Zealand.

Sustained protection against tuberculosis conferred to a wildlife host by single dose oral vaccination

BACKGROUND Vaccination of wildlife against bovine tuberculosis (TB) is being considered by several countries to reduce the transmission of Mycobacterium bovis infection to livestock. In New Zealand, where introduced brushtail possums (Trichosurus vulpecula) are the major wildlife hosts, we have previously shown that repeat applications of a lipid-encapsulated oral bacille Calmette-Guerin (BCG) vaccine reduce the incidence of naturally acquired TB in wild possums. Here we extend this conceptual demonstration to an operational level, assessing long-term protection against TB conferred to free-living possums by a single oral immunisation. METHODS Possums in a non-TB area were randomly allocated to receive lipid-formulated BCG vaccine or remained unvaccinated. After initial trials to assess vaccine immunogenicity and establishment of protection within the first year post-vaccination, 13 individuals of each treatment group were relocated to a biosecurity facility and challenged (at 28 months post-vaccination) by subcutaneous injection of virulent M. bovis. RESULTS Vaccine immunogenicity and short-term protection were confirmed at 2 months and 12 months post-vaccination, respectively. In the long-term assessment, vaccinated possums had significantly reduced bacterial counts in peripheral lymph nodes compared to controls, with 0.6-2.3 log(10)-fold reductions in M. bovis burdens. DISCUSSION The magnitude of protective response by possums to experimental challenge at 28 months post-vaccination is known to equate to a high degree of protection against natural infection in this species. With techniques for oral bait delivery well advanced, the longevity of protection demonstrated here shows that an operable wildlife vaccine against TB is feasible.