Ivor Yockney

Unexpected consequences of control: competitive vs. predator release in a four-species assemblage of invasive mammals

Invasive species are frequently the target of eradication or control programmes to mitigate their impacts. However, manipulating single species in isolation can lead to unexpected consequences for other species, with outcomes such as mesopredator release demonstrated both theoretically and empirically in vertebrate assemblages with at least two trophic levels. Less is known about the consequences of species removal in more complex assemblages where a greater number of interacting invaders increases the potential for selective species removal to result in unexpected changes in community structure. Using a replicated Before-After Control-Impact field experiment with a four-species assemblage of invasive mammals we show that species interactions in the community are dominated by competition rather than predation. There was no measurable response of two mesopredators (rats and mice) following control of the top predator (stoats), but there was competitive release of rats following removal of a herbivore (possums), and competitive release of mice following removal of rats.

Comparison of ranging behaviour in a multi-species complex of free-ranging hosts of bovine tuberculosis in relation to their use as disease sentinels

Sentinel species are increasingly used by disease managers to detect and monitor the prevalence of zoonotic diseases in wildlife populations. Characterizing home-range movements of sentinel hosts is thus important for developing improved disease surveillance methods, especially in systems where multiple host species co-exist. We studied ranging activity of major hosts of bovine tuberculosis (TB) in an upland habitat of New Zealand: we compared home-range coverage by ferrets (Mustela furo), wild deer (Cervus elaphus), feral pigs (Sus scrofa), brushtail possums (Trichosurus vulpecula) and free-ranging farmed cattle (Bos taurus). We also report in detail the proportional utilization of a seasonal (4-monthly) range area for the latter four species. Possums covered the smallest home range (<30 ha), ferrets covered ~100 ha, pigs ~4 km(2), deer and cattle both >30 km2. For any given weekly period, cattle, deer and pigs were shown to utilize 37–45% of their estimated 4-month range, while possums utilized 62% during any weekly period and 85% during any monthly period of their estimated 4-month range. We suggest that present means for estimating TB detection kernels, based on long-term range size estimates for possums and sentinel species, probably overstate the true local surveillance coverage per individual.

Reduced spillover transmission of Mycobacterium bovis to feral pigs (Sus scofa) following population control of brushtail possums (Trichosurus vulpecula).

In New Zealand, bovine tuberculosis (bTB) is present in domestic cattle and deer herds primarily as the result of on-going disease transmission from the primary wildlife host, the brushtail possum (Trichosurus vulpecula). However, bTB is also present in other introduced free-ranging mammalian species. Between 1996 and 2007, we conducted a series of studies to determine whether poison control of possum populations would have any effect on the prevalence of Mycobacterium bovis infection in sympatric feral pigs (Sus scrofa). We compared trends in the prevalence of bTB infection in feral pigs in six study areas: possum numbers were reduced in three areas, but not in the other three, effectively providing a thrice-replicated before-after-control-intervention design. Before possum control, the overall prevalence of culture-confirmed M. bovis infection in feral pigs was 16.7-94.4%, depending on area. Infection prevalence varied little between genders but did vary with age, increasing during the first 2-3 years of life but then declining in older pigs. In the areas in which possum control was applied, M. bovis prevalence in feral pigs fell to near zero within 2-3 years, provided control was applied successfully at the whole-landscape scale. In contrast, prevalence changed much less or not at all in the areas with no possum control. We conclude that feral pigs in New Zealand acquire M. bovis infection mainly by inter-species transmission from possums, but then rarely pass the disease on to other pigs and are end hosts. This is in contrast to the purported role of pigs as bTB maintenance hosts in other countries, and we suggest the difference in host status may reflect differences in the relative importance of the oral route of infection in different environments. Despite harbouring M. bovis infection for a number of years, pigs in New Zealand do not sustain bTB independently, but are good sentinels for disease prevalence in possum populations.

Mortality rate and gross pathology due to tuberculosis in wild brushtail possums (Trichosurus vulpecula) following low dose subcutaneous injection of Mycobacterium bovis.

Gross pathology due to tuberculosis can be established experimentally in brushtail possums (Trichosurus vulpecula) within 7 weeks of injection of virulent Mycobacterium bovis into subcutaneous connective tissues of the peripheral limbs. This pathology involves lymphadenomegaly and development of gross lesions in peripheral lymph nodes, with subsequent gross lesions in the lungs and reticuloendothelial organs. Using this artificial infection model, we here assessed the mortality rate for possums in the wild, to provide new information on the likely survival period for New Zealands major wildlife host. Possums were trapped and inoculated with <50 CFU of M. bovis, then fitted with mortality signal emitting radio tracking collars, released and re-tracked for 6 months. Possum survival probability was 89% up to 12 weeks post-injection (p.i.), but cumulative mortality was rapid from then on. The median survival period, based on study of 38 possums, was 18 weeks p.i.; this corresponds with a predicted time interval of 11 weeks between first presentation of TB as palpable lymphadenomegaly and death for an average possum, shorter than period values currently used in possum TB epidemiological modelling. We also examined gross pathology in 11 possums by post mortem necropsy, and confirmed lymphadenomegaly and tuberculous lesions at 7 and 12 weeks p.i. Extra-peripheral gross lesions were more frequent among possums at 12 weeks p.i. than at 7 weeks, while the occurrence of lung lesions (the most likely cause of disease-induced mortality) was apparent in animals at 12 weeks but not at 7 weeks p.i. Our results suggest that the time course of TB from development of gross lesions to mortality may be shorter than previously estimated from field studies of naturally tuberculous possums.

Percutaneous Interdigital Injection of Mycobacterium bovis as a Model for Tuberculous Lesion Development in Wild Brushtail Possums (Trichosurus vulpecula)

Brushtail possums (Trichosurus vulpecula) are the major wildlife reservoir of Mycobacterium bovis, the causative agent of bovine tuberculosis (BTB), in New Zealand. Primary diagnosis of BTB in wild possums is by palpation to detect peripheral lymphadenomegaly followed by necropsy examination, which frequently identifies gross tuberculous lesions in the peripheral lymph nodes and lungs. Experimental infection studies were conducted with wild possums in an attempt to emulate field BTB, focussing on percutaneous administration of virulent M. bovis in the paws. In a preliminary study, viable M. bovis bacilli were recovered from lymph nodes draining fore- or hindlimbs 12 days after percutaneous injection. Subsequently, 21 wild possums were injected interdigitally with 500 colony forming units (cfu) of M. bovis, radio-collared and released; 17/18 possums recaptured 8 weeks later had an established M. bovis lymphatic infection, with 16 having culture-positive gross lesions in the superficial and/or deep axillary lymph nodes. A dual-site infection model was established, involving simultaneous interdigital injection of 100 cfu of M. bovis into front and rear paws of 19 wild possums; this identified that the average degree of lymphadenitis involved 30-fold enlargement of the draining lymph node by 7-8 weeks post injection (wpi). A time-course study demonstrated establishment of M. bovis infection in peripheral lymph nodes of 9/11 possums at 3-5 wpi of doses ranging from 60 to 190 cfu, but with no development of gross lesions; by 7 weeks, 8/8 animals injected similarly had both an established infection and gross lesions of peripheral lymph nodes. The incidence and progression of peripheral lesion development, together with indications of sequential infection of the lungs, liver and mesenteric lymph nodes(MLNs), indicates that a low-dose percutaneous M. bovis infection model is likely to emulate natural disease in possums.

Quantifying Short-Term Foraging Movements in a Marsupial Pest to Improve Targeted Lethal Control and Disease Surveillance

In New Zealand, the introduced marsupial brushtail possum (Trichosurus vulpecula) is a pest species subject to control measures, primarily to limit its ability to transmit bovine tuberculosis (TB) to livestock and for conservation protection. To better define parameters for targeted possum control and TB surveillance, we here applied a novel approach to analyzing GPS data obtained from 44 possums fitted with radio-tracking collars, producing estimates of the animals’ short-term nocturnal foraging patterns based on 1-, 3- or 5-nights’ contiguous data. Studies were conducted within two semi-arid montane regions of New Zealand’s South Island High Country: these regions support low-density possum populations (<2 possums/ha) in which the animals’ home ranges are on average larger than in high-density populations in forested habitat. Possum foraging range width (FRW) estimates increased with increasing monitoring periods, from 150-200m based on a single night’s movement data to 300-400m based on 5 nights’ data. The largest average FRW estimates were recorded in winter and spring, and the smallest in summer. The results suggest that traps or poison-bait stations (for lethal control) or monitoring devices (for TB surveillance), set for > 3 consecutive nights at 150m interval spacings, would likely place >95% of the possums in this type of habitat at risk of encountering these devices, year-round. Modelling control efficacy against operational expenditure, based on these estimations, identified the relative cost-effectiveness of various strategies that could be applied to a typical aerial poisoning operation, to reduce the ongoing TB vectorial risk that possums pose in the High Country regions. These habitat-specific findings are likely to be more relevant than the conventional pest control and monitoring methodologies developed for possums in their more typical forested habitat.

Spatial prediction of brushtail possum (Trichosurus vulpecula) distribution using a combination of remotely sensed and field-observed environmental data

Abstract Context. In New Zealand, the introduced brushtail possum, Trichosurus vulpecula, is a reservoir of bovine tuberculosis and as such poses a major threat to the livestock industry. Aerial 1080 poisoning is an important tool for possum control but is expensive, creating an ongoing need for ever more cost-effective ways of using this technique. Aims. To develop geographic information system (GIS) models to better predict spatial variation in the distribution of unmanaged possum populations, to facilitate better targeting of control activities. Methods. Relative abundance of possums and their distribution among habitat types were surveyed in a dry high-country area of the northern South Island. Two GIS-based models were developed to predict the relative abundance of possums on trap lines. The first model used remotely sensed (digital) environmental data; the second complemented the remotely sensed data with fine-scale habitat and topographic data collected on the ground. Key results. Digital environmental factors and habitat features proved to be key predictors of relative possum abundance. In both GIS models, height above valley floor, presence of forest cover and mean annual temperature were the strongest predictors. Conclusions. Predictive maps (projections) of relative possum abundance produced from these models can provide useful decision-support tools for pest-control managers, by enabling possum control to be targeted spatially. Implications. Spatially targeted pest control could allow effective control activities for invasive species or disease vectors to be applied at a lower cost for the same benefit.

Field Trial of an Aerially-Distributed Tuberculosis Vaccine in a Low-Density Wildlife Population of Brushtail Possums (Trichosurus vulpecula).

Oral-delivery Mycobacterium bovis bacillus Calmette-Guérin (BCG) vaccine in a lipid matrix has been shown to confer protection against M. bovis infection and reduce the severity of tuberculosis (TB) when fed to brushtail possums (Trichosurus vulpecula), the major wildlife vector of bovine TB in New Zealand. Here we demonstrate the feasibility of aerial delivery of this live vaccine in bait form to an M. bovis-infected wild possum population, and subsequently assess vaccine uptake and field efficacy. Pre-trial studies indicated a resident possum population at very low density (<0.6 possums/ha) at the field site, with a 5.1% prevalence of macroscopic TB lesions. Pilot studies indicated that flavoured lipid matrix baits in weather-proof sachets could be successfully sown aerially via helicopter and were palatable to, and likely to be consumed by, a majority of wild possums under free-choice conditions. Subsequently, sachet-held lipid baits containing live BCG vaccine were sown at 3 baits/ha over a 1360 ha area, equating to >5 baits available per possum. Blood sampling conducted two months later provided some evidence of vaccine uptake. A necropsy survey conducted one year later identified a lower prevalence of culture-confirmed M. bovis infection and/or gross TB lesions among adult possums in vaccinated areas (1.1% prevalence; 95% CI, 0–3.3%, n = 92) than in unvaccinated areas (5.6%; 0.7–10.5%, n = 89); P = 0.098. Although not statistically different, the 81% efficacy in protecting possums against natural infection calculated from these data is within the range of previous estimates of vaccine efficacy in trials where BCG vaccine was delivered manually. We conclude that, with further straightforward refinement to improve free-choice uptake, aerial delivery of oral BCG vaccine is likely to be effective in controlling TB in wild possums. We briefly discuss contexts in which this could potentially become an important complementary tool in achieving national eradication of TB from New Zealand wildlife.

Efficacy of oral BCG vaccination in protecting free-ranging cattle from natural infection by Mycobacterium bovis

Vaccination of cattle against bovine tuberculosis could be a valuable control strategy, particularly in countries faced with intractable ongoing infection from a disease reservoir in wildlife. A field vaccination trial was undertaken in New Zealand. The trial included 1286 effectively free-ranging cattle stocked at low densities in a remote 7600ha area, with 55% of them vaccinated using Mycobacterium bovis BCG (Danish strain 1311). Vaccine was administered orally in all but 34 cases (where it was injected). After inclusion, cattle were exposed to natural sources of M. bovis infection in cattle and wildlife, most notably the brushtail possum (Trichosurus vulpecula). Cattle were slaughtered at 3-5 years of age and were inspected for tuberculous lesions, with mycobacteriological culture of key tissues from almost all animals. The prevalence of M. bovis infection was 4.8% among oral BCG vaccinates, significantly lower than the 11.9% in non-vaccinates. Vaccination appeared to both reduce the incidence of detectable infection, and to slow disease progression. Based on apparent annual incidence, the protective efficacy of oral BCG vaccine was 67.4% for preventing infection, and was higher in cattle slaughtered soon after vaccination. Skin-test reactivity to tuberculin was high in vaccinates re-tested 70days after vaccination but not in non-vaccinates, although reactor animals had minimal response in gamma-interferon blood tests. In re- tests conducted more than 12 months after vaccination, skin-test reactivity among vaccinates was much lower. These results indicate that oral BCG vaccination could be an effective tool for greatly reducing detectable infection in cattle.

Low-dose BCG vaccination protects free-ranging cattle against naturally-acquired bovine tuberculosis

Vaccination of cattle with Mycobacterium bovis BCG has been shown to protect against infection with virulent strains of M. bovis, and against resultant bovine tuberculosis (TB). Here we report on a large-scale trial in New Zealand where free-ranging cattle were vaccinated with 3 x 105 BCG via injection, a lower dose than any previously trialed in cattle against exposure to a natural force of M. bovis infection. In a multi-year enrolment study involving >800 animals, three cohorts of 1-2 year old cattle were randomised to receive vaccine or to serve as non-vaccinated controls. Cattle were slaughtered and subject to standard abattoir post mortem examination for M. bovis culture-positive TB lesions after up to 3.7 years of in-field exposure; additionally, lymph node samples from approximately half of the cattle were examined further to identify infection in the absence of lesions. Overall TB prevalence, as identified by gross lesions detected at slaughter, was low among farmed cattle at the study site (<4% annually). There were two lesioned cases among 520 vaccinated trial cattle (0.38%) compared to eight among 297 non-vaccinated trial cattle (2.69%). Trial vaccine efficacy was 85.7% against abattoir-detectable TB (statistically significant protection), and 86.7% when adjusted for duration of exposure. BCG vaccination did not significantly affect the response rates of cattle to ante mortem skin- or blood-tests in diagnostic tests conducted >7 months post-vaccination. Use of a reduced, yet effective, dose of BCG would increase the cost effectiveness of using this vaccine in a bovine TB control programme.