Aspects of eradicating disease from wildlife vectors

Bovine tuberculosis (Tb) occurs in cattle and in wildlife, with various species infected in a range of countries. The control or eradication of Tb can be empirically based or based on understanding of disease processes such as described in mathematical models. The eradication of Tb from Australia was largely empirically based, with water buffalo (Bubalus bubalis) apparently being the only significant wildlife disease host. Buffalo populations were apparently greatly reduced to achieve Tb eradication. This paper examines the alternative approach of basing control or eradication on mathematical models, and compares some predictions of one-host (wildlife) and two-host (cattle and wildlife) disease models with empirical data on Tb in both cattle and in wildlife. The one-host and two-host models were based on those published and also derived. For example, reported positive regressions between prevalence’s of Tb in cattle and in brushtail possums in New Zealand and also between prevalence’s of Tb in red deer and in brushtail possums in New Zealand, are consistent with two-host disease models assuming frequency dependent transmission. However most models of Tb in wildlife, e.g. the Barlow models, assume density dependent transmission. The implications for disease eradication are that models assuming density dependent transmission have a threshold host (wildlife) density about zero. Hence, if frequency dependent, not density dependent, transmission actually occurs, then host (wildlife) density would have to be reduced much lower, in order for eradication of Tb from cattle.     

Combining livestock and wildlife surveillance data to assess the likelihood of freedom from bovine tuberculosis in New Zealand

Bovine tuberculosis (Tb) has historically occurred in livestock throughout most of New Zealand, and also in wildlife over about 40% of the country. Using a test-and-cull strategy to eliminate Tb from livestock, intensive control of the major wildlife host (brushtail possums), and surveillance of key spillover hosts (wild ferrets, pigs and deer), the Animal Health Board has reduced the number of infected cattle herds by over 90% since 1994. Many formerly infected areas appear to now be free of the disease, so a key question is whether the disease control programme can be stopped in those places. We have developed a Bayesian framework for combining spatially explicit data derived from livestock testing and surveys of Tb prevalence in key wildlife hosts, and using those data to updating or refine an estimate of the probability of Tb freedom from wildlife provided by a priori prediction derived from a model of how Tb levels in possum are likely to have been affected by the duration and intensity of control. This paper outlines the conceptual framework, and some preliminary “case-study” steps toward implementation.     

Oral vaccination reduces the incidence of tuberculosis in free-living brushtail possums

Bovine tuberculosis (Tb) caused by Mycobacterium bovis has proved refractory to eradication from domestic livestock in countries with wildlife disease reservoirs. Vaccination of wild hosts offers a way of controlling Tb in livestock without wildlife culling. This study was conducted in a Tb-endemic region of New Zealand, where the introduced Australian brushtail possum (Trichosurus vulpecula) is the main wildlife reservoir of Tb. Possums were trapped and vaccinated using a prototype oral-delivery system to deliver the Tb vaccine bacille Calmette–Guerin. Vaccinated and control possums were matched according to age, sex and location, re-trapped bimonthly and assessed for Tb status by palpation and lesion aspiration; the site was depopulated after 2 years and post-mortem examinations were conducted to further identify clinical Tb cases and subclinical infection. Significantly fewer culture-confirmed Tb cases were recorded in vaccinated possums (1/51) compared with control animals (12/71); the transition probability from susceptible to infected was significantly reduced in both males and females by vaccination. Vaccine efficacy was estimated at 95 per cent (87–100%) for females and 96 per cent (82–99%) for males. Hence, this trial demonstrates that orally delivered live bacterial vaccines can significantly protect wildlife against natural disease exposure, indicating that wildlife vaccination, along with existing control methods, could be used to eradicate Tb from domestic animals.     

Persistence of Tb in possums: Insights from a spatially explicit, stochastic model

The majority of models for predicting the dynamics of bovine Tb in brushtail possums in New Zealand owe much to the pioneering work of the late Nigel Barlow. These non-spatial, deterministic models subsumed local disease dynamics by using a heterogeneous mixing term that assumed Tb was confined to a fraction of the population (in patches). However, the underlying mechanism(s) that could result in this heterogeneity of infection risk were obscure. We present a new individual-based, spatial, stochastic simulation model of Tb in possums that provides an explicit mechanism for simulating heterogeneous risk of infection based on a model of individual home range utilisation and disease susceptibility. The manipulation of parameters governing individual utilisation of space also means that processes such as non-linear contact structure can be handled naturally. We use the model to predict the persistence of Tb in possums under scenarios currently implemented for the management of bovine Tb in wildlife and determine conditions under which Tb might be predicted to persist despite control efforts.     

Reliable mop-up of surviving pests: a more cost-effective and fail-safe approach to local extirpation

Achieving very low densities of small mammal pests is routinely attained by expensive, large-scale, broadcast poisoning. There are two strategic responses to maintaining these low pest densities (or attempting to eradicate the survivors) – repeat the poisoning at regular intervals, or attempt to detect and mop- up the survivors. Here we report preliminary trials working toward the latter approach for possums (Trichosurus vulpecula) in a large mainland forest in New Zealand, and show that detection-and-mop-up is not only feasible but also possibly the most economically sensible and reliable way of achieving 100% kills. We use a simple bioeconomic model to predict the optimal surveillance (detection) strategy for possum mop-up, based on the characteristics of the detection device, and the few data available on the aggregation patterns of possums at extreme low density.     

First direct estimate of the detection probability of bovine tuberculosis in possums by possum transmission

We conducted a field trial to determine whether percutaneous challenge of wild brushtail possums (Trichosurus vulpecula) with virulent Mycobacterium bovis, the causative agent of bovine tuberculosis (TB), resulted in subsequent transmission of M. bovis to other possums. We then used our results to make a preliminary first direct estimate of the ‘TB detection probability’ or transmission rate in wild possums. Seven free-living adult possums in the Rimutaka Forest Park, New Zealand, were captured, GPS-collared, experimentally challenged and then released. Possum populations surrounding the challenged individuals were examined for secondary cases 4–8 months post-challenge. Of 37 possums caught within the home ranges of the challenged individuals, one had confirmed TB. As no TB was detected in 355 other possums examined in this study, or 659 possums in a concurrent study in the immediate vicinity, we conclude that this represents the first documented case of onward transmission of M. bovis from an experimentally challenged possum in the wild. This pilot trial therefore gives some confidence that the new percutaneous challenge model for TB in possums can be used to obtain empirical estimates of TB detection probabilities. The calculated probability of onward transmission (‘detection’) here was just 0.027; however, with the possibility that further transmission events would have occurred from the one challenged possum removed from the trial before it had died, or if our trapping missed secondary cases, this value could be an underestimate. The implications of this low preliminary estimate are discussed.     

Are possums important dispersers of large-seeded fruit?

The claim by Dungan et al. (2002) that “in many areas possums may be the only potential dispersal vector for large-seeded native species” is unsubstantiated. There is little evidence possums excrete viable seed of large-seeded fruit greater than 10 mm diameter, and seeds up to this size are dispersed by a suite of bird species. Nowhere in New Zealand are there likely to be possums in the absence of this suite of bird species.     

Assessing Movements of Brushtail Possums (Trichosurus vulpecula) in Relation to Depopulated Buffer Zones for the Management of Wildlife Tuberculosis in New Zealand

In New Zealand, managing the threat of bovine tuberculosis (TB) to livestock includes population reduction of potentially infectious wildlife, primarily the brushtail possum (Trichosurus vulpecula). Population control is often targeted on forested buffer zones adjacent to farmland, in order to limit movements of possums across the buffer and reduce the risk of disease transmission to livestock. To assess the effectiveness of buffers in protecting livestock we analysed GPS telemetry data from possums located in untreated forest adjacent to buffers, and used these data to characterise patterns of movement that could lead to possums reaching farmland during the season when most dispersal occurs. Analyses of movement data showed that the direction of dispersal by sub-adult and adult possums and the extent of long exploratory movements were not biased toward forest buffers, even though these provided vacant habitat as suitable for possums as untreated forest. Instead, dispersal and exploratory movements were uncommon even for sub-adult possums and such events typically lasted <10 days. Dispersing possums settled predominantly in river valleys. A simulation model was developed for the 3-6-month dispersal season; it demonstrated a probability of <0.001 that an infected possum, originating from a low-density population with low disease prevalence in untreated forest, would move across 3 km of recently controlled forest buffer to reach farmland. Our results indicate short-term reduction in the risk of TB transmission from possums to livestock in New Zealand by the use of depopulated buffer zones, while acknowledging that the threat of disease spread from untreated forest is likely to increase over time as possum population density and, potentially, TB prevalence among those possums, increase in the buffer zone.     

Controlling small mammal predators using sodium monofluoroacetate (1080) in bait stations along forestry roads in a New Zealand beech forest

A single five night pulse of sodium monofluroacetate (0.15% 1080) applied in bait stations at two different spacing intervals, 100 and 200 m, along forestry roads in New Zealand beech forest, killed all four of the resident radio-tagged stoats (Mustela erminea) and all three of the resident radio- tagged wild house cats (Felis catus) by secondary poisoning. Gut contents of predators indicated that house mice (Mus musculus), ship rats (Rattus rattus) and bushtail possums (Trichosurus vulpecula) were important sources of the toxin. High kills of predators, possums and rats at both 100 and 200 m spacing regimes suggest that greater efficacy of controlling these pests would be achieved with the latter method. Evidence suggests that routine management of possums and rats using 1080 and brodifacoum has resulted in widespread control of small mammalian carnivores by secondary poisoning in New Zealand forests. However, aerial application of poison can kill large numbers of tomtits (Petroica macrocephala) and robins (Petroica australis) and few other native bird species have been adequately monitored through such operations. Reducing risks to native wildlife is responsible ecological management. Use of bait stations along forestry roads or tracks may be fundamental in mounting cost-effective :Large-scale ground-based protection of native wildlife through safer predator controls.     

A review of the damage caused by invasive wild mammalian herbivores to primary production in New Zealand

ABSTRACT

Wild mammalian herbivores can compete with domestic livestock and damage other types of production systems. We reviewed damage by wild mammalian herbivores, excluding rodents, to primary production in New Zealand and assessed whether primary producers alter stocking rates in response to changes in forage availability following pest control. Given the dearth of information on the damage caused by wild mammalian herbivores to many production systems, we primarily focused on their damage to agriculture. With the exception of the substantial damage that brushtail possums (Trichosurus vulpecula) and European rabbits (Oryctolagus cuniculus) cause, there are no quantitative estimates of pasture depletion by other wild mammalian herbivores on New Zealand farmland. Estimates of dry matter consumption by wild mammalian herbivores, converted to stock unit equivalents, suggest that several species can substantially reduce stocking rates when they occur on farmland. Quantitative data on the damage they cause to horticulture and silviculture are lacking, but damage to coniferous seedlings has been recorded for possums, wallabies (Notamacropus spp.), and some species of deer (Cervus spp., Rusa spp., and Dama dama). The process that primary producers use to decide whether to control wild mammalian herbivores includes complex social and economic factors, but quantitative information is important for weighing up the expected costs and benefits of pest control. However, it is unclear how primary producers manage livestock in response to increases in forage availability following pest control. The paucity of quantitative data on wild mammalian herbivore damage to production assets is a substantial knowledge gap. Key research priorities are (i) understanding how damage varies with pest density (critical information for effective pest management) and (ii) and how primary producers alter stocking rates following reductions in pest density.     

Native plant/herbivore interactions as determinants of the ecological and evolutionary effects of invasive mammalian herbivores: the case of the common brushtail possum

In their native range, mammalian herbivores exist in a suite of direct and indirect ecological and evolutionary relationships with plant populations and communities. Outside their native range these herbivores become embedded in a multitude of new ecological and evolutionary interactions with native plant species in the new range. Sound knowledge of the plant/herbivore interactions in the herbivores’ native range provides an ideal framework to better understand their effects in the introduced range. The example of the common brushtail possum (Trichosurus vulpecula) and its introduction to New Zealand from Australia provides an excellent case study. In Australia, the common brushtail possum is a widespread generalist herbivore and it is thought that this generalist lifestyle has equipped the species well for successful colonisation of New Zealand. In Australia the brushtail possum has co-existed with highly chemically defended foliage since the Oligocene and recent papers have supported the role of possums as agents of selection on eucalypt defences. While the chemical profile of New Zealand foliage is comparatively poorly understood, possums do show clear selectivity between and within populations and some of these interactions may be mediated by the animals ability to ‘cope’ with PSMs, coupled with maintaining its generalist diet. While possums have had less time to effect evolutionary change in New Zealand species, their impacts on plant fitness have been well documented. However, further knowledge on variation and heritability of foliage traits driving possum preferences is needed to elucidate the ecological and evolutionary plant/possum interactions in the invasive range.     

Spatially-explicit wildlife surveillance to prove freedom from diseases or pests

Surveillance undertaken to prove freedom from a disease has traditionally focussed on sampling a specified proportion of the population to determine the presence of the infective agent. Based on a sample of individuals testing negative for disease, standard probability theory using the binomial or hypergeometric distribution can be used to make inference about the probability of disease being absent. However, if the disease agent involves a wildlife host, then determining what proportion of the population was sampled becomes problematic as it requires an estimate of population abundance, which may be difficult and expensive to obtain. Surveillance during the eradication of pests such as feral ungulates often make use of the Judas technique, whereby radio-collared individuals are released and followed in the hope that the sociality of the individuals will betray the locations of conspecifics, which can then be dispatched. Data collected during such surveillance is explicitly spatial, containing information about the ‘search area’ of the Judas animal. However, there has been no attempt to use such data to make inference about the probability of the area being free of the pest, given Judas animals fail to detect any conspecifics. We present a framework for making specific use of the spatial nature of such wildlife surveillance data to make inference about the probability of freedom from the disease or pest. Underlying the sampling framework is a model of the detection process by sampled individuals. Estimates of individual detection probability are spatially smoothed using the extent of individual movements to produce a spatially- explicit detection surface. Bayes theorem is then used to combine this 2-dimensional surface with prior information on the probability of pest or disease presence, prior to sampling, to estimate the probability that the area is free from the disease or pest, given surveillance fails to detect evidence of their presence. We illustrate the method with examples of the detection of bovine Tb in wildlife in New Zealand and the detection of pigs (Sus scrofa) using the Judas technique during the feral pig eradication programme on Santa Cruz Island, California.     

Responses of kukupa (

The kukupa or New Zealand pigeon (Hemiphaga novaeseelandiae) is gradually declining on the New Zealand mainland, due mostly to predation by introduced pest mammals including ship rats (Rattus rattus) and brushtail possums (Trichosurus vulpecula). We report on a co-operative project between Maori landowners, the Department of Conservation, and Manaaki Whenua–Landcare Research researchers to restore a Northland kukupa population and to examine kukupa nesting success in relation to pest abundance. Ship rats and possums were targeted by trapping and poisoning throughout Motatau Forest (350 ha) from 1997 to 1999; only possums were targeted in 2000. All 13 kukupa nests located before pest control started in late 1997 failed at the egg stage, but all seven nests located in 1998–99 successfully fledged young when trapping and tracking indices of possums and ship rats were less than 4%. After pest control, counts of kukupa and some other bird species increased at Motatau compared with counts in a nearby non-treatment block, suggesting numbers of adult kukupa can be increased in small forest areas by intensive pest control. This increase is due at least partly to increased nest success. Evidence from time-lapse video cameras, sign remaining at nests, and nest success rates under different pest control regimes suggest both ship rats and possums are important predators at kukupa nests.     

Identifying eradication units in an invasive mammalian pest species

Eradication of invasive species is an important component for species conservation and ecosystem restoration. Success of eradications is dependent on knowledge of population connectivity in order to determine reinvasion pathways, and hence populations requiring simultaneous eradication (eradication units). The common brushtail possum (Trichosurus vulpecula) was introduced into New Zealand from Australia and Tasmania, and now occupies a wide range of habitats across the majority of New Zealand. Possums are one of the most destructive invaders within New Zealand, with extensive control operations occurring throughout the country. Understanding the population connectivity of possums on mainland New Zealand (North and South Islands) will enhance the success of planned eradications. We examined the genetic population structure of invasive possums to identify gene flow, thus reinvasion pathways, between seven populations around Dunedin and on the Otago Peninsula where eradication of possums is occurring. Genetic variation at 12 microsatellite loci was comparable between all sampled populations and exhibited a significant isolation by distance pattern. Bayesian clustering methods supported the existence of two population clusters, indicating the presence of a reinvasion pathway onto the Otago Peninsula from urban areas at the Southern end of the Peninsula. To avoid recolonisation, all possums on the Otago Peninsula should be eradicated simultaneously, with the implementation and ongoing maintenance and monitoring of an urban buffer zone. We recommend pre-eradication genetic analyses be adopted by all pest managers to define appropriate eradication units, thereby maximising eradication success and avoiding costly failures.     

Bovine tuberculosis in brushtail possums: models, dogma and data

Three different models of bovine tuberculosis (Tb) in brushtail possums were evaluated against their stated purpose, and testable assumptions and predictions evaluated against available data where possible. Not surprisingly, two of the models may be falsified based on currently available data with respect to either important model assumptions or predictions, and the third may suffer from being right for the wrong reason. This does not mean that these models are not useful. To the contrary, I argue that all models, especially those published in the scientific literature have largely addressed their stated purpose, and have contributed to our understanding of and ability to manage bovine tuberculosis infection in brushtail possum populations. No model, however, satisfactorily explains the pronounced spatial clustering of possum Tb, and the models critiqued have provided little strong inference as to the routes of transmission of Tb among possums. This situation is not helped by the scarcity of datasets on Tb in uncontrolled possum populations that are readily available to confront competing possum/Tb models with. As time passes, there is a very real risk that these data sets will be lost. This is of particular concern, as the expansion in the area of New Zealand under active possum management means the future opportunity to collect further data on Tb in uncontrolled possum populations is severely limited.     

The Great Lake Pest Summit: Anticipated issues and outcomes

Abstract

This “Pest Summit” could not be more timely. Public concern about the ecological, economic, and social impacts of pests such as possums and rabbits have never been higher. A new era of pest management in New Zealand is under way, and the Biosecurity Bill, the Resource Management Act, and the Animal Health Board's 5-year strategy to reduce bovine Tb are just three of many important elements in it.     

Is Avian Malaria Playing a Role in Native Bird Declines in New Zealand? Testing Hypotheses along an Elevational Gradient

The mosquito-borne disease avian malaria (Plasmodium spp.) has impacted both captive populations and wild individuals of native New Zealand bird species. However, whether or not it is a cause of concern to their wild populations is still unclear. In Hawaii, the disease has been a major factor in the population declines of some native forest bird species, often limiting their elevational distribution due to an inverse relationship between force of infection and elevation. While studies have investigated latitudinal patterns of infection in New Zealand, elevational patterns are unexplored. To address this, a survey was conducted in Nelson Lakes National Park, a site experiencing native bird declines in which disease has been suggested as playing a role, to investigate whether there is a similar inverse relationship in New Zealand. Results from blood samples (n = 436) collected over three seasons across a broad elevational range (650–1400 m) support there being such a relationship. In addition, an overall higher prevalence in non-native (14.1%) versus native birds (1.7%) may indicate differential impacts on these two groups, while particularly high prevalence in non-native Turdus spp. supports previous suggestions that they are key reservoir hosts for the disease. Overall, these findings add weight to the hypothesis that avian malaria is playing a role in ongoing declines of native New Zealand birds.     

Combining Aspirin with Cholecalciferol (Vitamin D3) – A Potential New Tool for Controlling Possum Populations

The introduced Australian brushtail possum is a major vertebrate pest in New Zealand, with impacts on conservation and agriculture being managed largely through poisoning operations. Cholecalciferol (vitamin D₃) is registered for use in controlling possums and despite its many advantages it is expensive and relatively inhumane. Combination of a high proportion of aspirin with a low proportion of cholecalciferol was effective in killing high proportions of groups of acclimatised, caged possums: this is attributed to both an unexpectedly high toxicity of the type of cholecalciferol used, and a proposed synergistic mechanism between the two compounds. Death was caused by localised damage to heart ventricles by aspirin, and inhibition of tissue repair by both aspirin and cholecalciferol. The observed toxicosis had lower impact on the welfare of possums than either compound administered alone, particularly aspirin alone. Residue analyses of bait remains in the GI tract suggested a low risk of secondary poisoning by either compound. The combination of cholecalciferol and aspirin has the potential to meet key requirements of cost-effectiveness and humaneness in controlling possum populations, but the effect of the combination in non-target species has yet to be tested.     

Creating new evolutionary pathways through bioinvasion: the population genetics of brushtail possums in New Zealand

Rapid increases in global trade and human movement have created novel mixtures of organisms bringing with them the potential to rapidly accelerate the evolution of new forms. The common brushtail possum (Trichosurus vulpecula), introduced into New Zealand from Australia in the 19th century, is one such species having been sourced from multiple populations in its native range. Here, we combine microsatellite DNA‐ and GIS‐based spatial data to show that T. vulpecula originating from at least two different Australian locations exhibit a population structure that is commensurate with their introduction history and which cannot be explained by landscape features alone. Most importantly, we identify a hybrid zone between the two subspecies which appears to function as a barrier to dispersal. When combined with previous genetic, morphological and captive studies, our data suggest that assortative mating between the two subspecies may operate at a behavioural or species recognition level rather than through fertilization, genetic incompatibility or developmental inhibition. Nevertheless, hybridization between the two subspecies of possum clearly occurs, creating the opportunity for novel genetic combinations that would not occur in their natural ranges and which is especially likely given that multiple contact zones occur in New Zealand. This discovery has implications for wildlife management in New Zealand because multiple contact zones are likely to influence the dispersal patterns of possums and because differential susceptibility to baiting with sodium fluoroacetate between possums of different origins may promote novel genetic forms.     

Seasonally pulsed resources and non-interactive plant–herbivore models

[First paragraph]A strong argument for consumer–resource models over single–species population models is that they are consistent with actual ecological processes, and that this mechanistic realism leads to greater predictive power. These benefits depend wholly on the accuracy with which a model captures the dynamics of the resource. We review the key food resources used by brushtail possums in New Zealand and find that their dynamics are poorly represented in “interactive” models of the dynamics of possums and their plant foods. More realistic models that we develop lead to direct density dependence of approximately è-logistic form (Barlow and Clout, 1983), where è depends on observable characteristics of the system.