Quantifying the probability of detection of wild ungulates with the Judas technique.

The Judas technique is often used in control or eradication of particular vertebrate pests. The technique exploits the tendency of individuals to form social groups. A radio collar is affixed to an individual and its subsequent monitoring facilitates the detection of other conspecifics. Efficacy of this technique would be improved if managers could estimate the probability that a Judas individual would detect conspecifics. To calculate this probability, we estimated association rates of Judas individuals with other Judas individuals, given the length of time the Judas has been deployed. We developed a simple model of space-use for individual Judas animals and constrained detection probabilities to those specific areas. We then combined estimates for individual Judas animals to infer the probability that a wild individual could be detected in an area of interest via Judas surveillance. We illustrated the method by using data from a feral goat eradication program on Isla Santiago, Galápagos, and a feral pig eradication program on Santa Cruz Island, California. Association probabilities declined as the proximity between individual areas of use of a Judas pair decreased. Unconditional probabilities of detection within individual areas of use averaged 0.09 per month for feral pigs and 0.11 per month for feral goats. Probabilities that eradication had been achieved, given no detections of wild conspecifics, and an uninformative prior probability of eradication were 0.79 (90% CI 0.22-0.99) for feral goats and 0.87 (90% CI 0.44-1.0) for feral pigs. We envisage several additions to the analyses used that could improve estimates of Judas detection probability. Analyses such as these can help managers increase the efficacy of eradication efforts, leading to more effective effects to restore native biodiversity.

La técnica de Judas se usa con frecuencia en el control de ciertas plagas de vertebrados. La técnica se aprovecha de la tendencia a formar grupos sociales que tienen los individuos. Un radio-collar es colocado en uno de los individuos y el monitoreo subsecuente facilita la detección de otros miembros de la misma especie. La eficacia de esta técnica mejoraría si los gestores pudieran estimar la probabilidad que tiene un Judas de detectar a miembros de su especie. Para calcular esta probabilidad, estimamos las tasas de asociación de los Judas con otros Judas, dado el tiempo que el Judas ha sido enviado. Desarrollamos un modelo simple del uso del espacio para animales Judas individuales y limitamos las probabilidades de detección a esas áreas específicas. Después combinamos los estimados de un animal Judas individual para inferir la probabilidad de que un individuo silvestre pudiera ser detectado en un área de interés mediante la vigilancia Judas. Ilustramos el método con los datos de un programa de erradicación de cabras ferales en Isla Santiago, las Galápagos, y uno de cerdos ferales en la Isla de Santa Cruz, California. Las probabilidades de asociación declinaron conforme disminuyó la proximidad entre las áreas individuales de uso de un par de Judas. Las probabilidades incondicionales de detección dentro de las áreas individuales de uso promediaron 0.09 por mes para los cerdos ferales y 0.11 por mes para las cabras ferales. Las probabilidades de que se había logrado la erradicación, dada la ausencia de detecciones de miembros de la misma especie y una mal informada probabilidad previa de erradicación, fueron de 0.79 (90% CI 0.22 - 0.99) para las cabras ferales y 0.87 (90% CI 0.44 - 1.0) para los cerdos ferales. Contemplamos varias adiciones al análisis que usamos que podrían mejorar los estimados de la probabilidad de detección de Judas. Análisis como este pueden ayudar a los gestores a incrementar la efectividad de los esfuerzos de erradicación, lo que resulta en efectos más efectivos para restaurar la biodiversidad nativa.

Field validation of phylodynamic analytical methods for inference on epidemiological processes in wildlife.

Amongst newly developed approaches to analyse molecular data, phylodynamic models are receiving much attention because of their potential to reveal changes to viral populations over short periods. This knowledge can be very important for understanding disease impacts. However, their accuracy needs to be fully understood, especially in relation to wildlife disease epidemiology, where sampling and prior knowledge may be limited. The release of the rabbit haemorrhagic disease virus (RHDV) as biological control in naïve rabbit populations in Australia in 1996 provides a unique data set with which to validate phylodynamic models. By comparing results obtained from RHDV sequence data with our current understanding of RHDV epidemiology in Australia, we evaluated the performances of these recently developed models. In line with our expectations, coalescent analyses detected a sharp increase in the virus population size in the first few months after release, followed by a more gradual increase. Phylodynamic analyses using a birth-death model generated effective reproductive number estimates (the average number of secondary infections per each infectious case, Re ) larger than one for most of the epochs considered. However, the possible range of the initial Re included estimates lower than one despite the known rapid spread of RHDV in Australia. Furthermore, the analyses that accounted for geographical structuring failed to converge. We argue that the difficulties that we encountered most likely stem from the fact that the samples available from 1996 to 2014 were too sparse with respect to both geographic and within outbreak coverage to adequately infer some of the model parameters. In general, while these phylodynamic analyses proved to be greatly informative in some regards, we caution that their interpretation may not be straightforward. We recommend further research to evaluate the robustness of these models to assumption violations and sensitivity to sampling regimes.

Comparative Epidemiology of Rabbit Haemorrhagic Disease Virus Strains from Viral Sequence Data.

Since their introduction in 1859, European rabbits (Oryctolagus cuniculus) have had a devastating impact on agricultural production and biodiversity in Australia, with competition and land degradation by rabbits being one of the key threats to agricultural and biodiversity values in Australia. Biocontrol agents, with the most important being the rabbit haemorrhagic disease virus 1 (RHDV1), constitute the most important landscape-scale control strategies for rabbits in Australia. Monitoring field strain dynamics is complex and labour-intensive. Here, using phylodynamic models to analyse the available RHDV molecular data, we aimed to: investigate the epidemiology of various strains, use molecular data to date the emergence of new variants and evaluate whether different strains are outcompeting one another. We determined that the two main pathogenic lagoviruses variants in Australia (RHDV1 and RHDV2) have had similar dynamics since their release, although over different timeframes (substantially shorter for RHDV2). We also found a strong geographic difference in their activities and evidence of overall competition between the two viruses.

The impact of RHDV-K5 on rabbit populations in Australia: an evaluation of citizen science surveys to monitor rabbit abundance.

The increasing popularity of citizen science in ecological research has created opportunities for data collection from large teams of observers that are widely dispersed. We established a citizen science program to complement the release of a new variant of the rabbit biological control agent, rabbit haemorrhagic disease virus (RHDV), known colloquially as K5, across Australia. We evaluated the impact of K5 on the national rabbit population and compared citizen science and professionally-collected spotlight count data. Of the citizen science sites (n = 219), 93% indicated a decrease in rabbit abundance following the release of K5. The overall finite monthly growth rate in rabbit abundance was estimated as 0.66 (95%CI, 0.26, 1.03), averaging a monthly reduction of 34% at the citizen science sites one month after the release. No such declines were observed at the professionally monitored sites (n = 22). The citizen science data submissions may have been unconsciously biased or the number of professional sites may have been insufficient to detect a change. Citizen science participation also declined by 56% over the post-release period. Future programs should ensure the use of blinded trials to check for unconscious bias and consider how incentives and/or the good will of the participants can be maintained throughout the program.

Baiting and Feeding Revisited: Modeling Factors Influencing Transmission of Tuberculosis Among Deer and to Cattle.

Although tuberculosis caused by Mycobacterium bovis (bTB) is endemic in white-tailed deer (Odocoileus virginianus) in northeastern Michigan, USA, baiting and feeding of deer continue despite a regulatory ban. Previous modeling suggests aggregation at bait sites slows the rates at which harvest and/or vaccination decrease bTB prevalence, prolongs time to eradication, and increases the likelihood that once eradicated, bTB will re-establish following an incursion. However, the extent to which specific factors such as food density, attractiveness to deer, and persistence on the landscape influence bTB transmission is unknown. We used an individual-based, spatially-explicit stochastic simulation model of bTB in deer and cattle to investigate effects of feed density, attractiveness, and spatial and temporal persistence on bTB prevalence in deer and the probability of breakdowns in adjacent cattle herds. Because hunter harvest remains key to controlling bTB in deer, and harvest rates are in long term decline, we modeled these feeding-associated factors at harvest rates prevailing both when the model was developed (2003-2007) and in 2018. Food placement at randomized locations vs. fixed sites had little effect on bTB prevalence in deer, whereas increasing the probability that deer move to food piles (attractiveness) had the greatest effect of factors studied on both prevalence and herd breakdowns. Reducing food pile density reduced prevalence, but decreased herd breakdowns only modestly. Consistent availability of food over longer periods of time, as would occur with supplemental winter feeding or persistent recreational feeding, increased both prevalence in deer and cattle herd breakdowns dramatically. Though perhaps implausible to the public, altering how bait and feed for deer are used can reduce cattle herd breakdowns. Baiting and feeding bans have contributed to declining bTB prevalence, but non-compliance and continued legal sales of feed impede eradication. Requiring hunters to move food piles is unlikely to mitigate effects on transmission and is not a useful management tool. Compared to baiting, winter supplemental feeding or extended recreational feeding is likely to magnify bTB transmission by prolonging temporal availability. Because attractiveness of feed is influenced both by type of feed and deer behavior, research to quantify factors influencing deer movement to food should be a priority.

Detecting rare carnivores using scats: Implications for monitoring a fox incursion into Tasmania.

The ability to detect the incursion of an invasive species or destroy the last individuals during an eradication program are some of the most difficult aspects of invasive species management. The presence of foxes in Tasmania is a contentious issue with recent structured monitoring efforts, involving collection of carnivore scats and testing for fox DNA, failing to detect any evidence of foxes. Understanding the likelihood that monitoring efforts would detect fox presence, given at least one is present, is therefore critical for understanding the role of scat monitoring for informing the response to an incursion. We undertook trials to estimate the probability of fox scat detection through monitoring by scat-detector dogs and person searches and used this information to critically evaluate the power of scat monitoring efforts for detecting foxes in the Tasmanian landscape. The probability of detecting a single scat present in a 1-km2 survey unit was highest for scat-detector dogs searches (0.053) compared with person searches (x¯â‰…0.015) for each 10 km of search effort. Simulation of the power of recent scat monitoring efforts undertaken in Tasmania from 2011 to 2015 suggested that single foxes would have to be present in at least 20 different locations or fox breeding groups present in at least six different locations, in order to be detected with a high level of confidence (>0.80). We have shown that highly structured detection trials can provide managers with the quantitative tools needed to make judgments about the power of large-scale scat monitoring programs. Results suggest that a fox population, if present in Tasmania, could remain undetected by a large-scale, structured scat monitoring program. Therefore, it is likely that other forms of surveillance, in conjunction with scat monitoring, will be necessary to demonstrate that foxes are absent from Tasmania with high confidence.

Management of on-farm risk to livestock from bovine tuberculosis in Michigan, USA, white-tailed deer: Predictions from a spatially-explicit stochastic model.

The eradication of bovine tuberculosis (bTB), caused by Mycobacterium bovis, from cattle in many locations worldwide is complicated by endemic foci of the disease in free-ranging wildlife. Recent simulation modeling of the bTB outbreak in white-tailed deer (WTD) in Michigan, USA, suggests current management is unlikely to eradicate bTB from the core outbreak area (DMU 452) within the next three decades. However, some level of control short of eradication might sufficiently reduce transmission from deer to cattle to a point at which the negative effects of bTB on the cattle industry could be reduced or eliminated, while minimizing the negative consequences of reducing deer numbers. We extended our existing spatially-explicit, individual-based stochastic simulation model of bTB transmission in WTD to incorporate transmission to cattle, to characterize the effects of vaccination and increased harvest of WTD on cattle herd breakdown rates, to examine the effects of localized culling or vaccination of WTD in the vicinity of cattle farms, to assess the effects of concurrent deer baiting, and to determine the effect of progressive restriction of deer/cattle contact on herd breakdowns. A spatially-explicit "cattle layer" was constructed describing the spatial locations, farm size and cattle density of all farms within and directly adjacent to DMU452. Increased hunter harvest or vaccination of deer, or a combination, would likely decrease the number of cattle herd breakdowns to <1 per year in less than 15 years. Concurrent deer baiting variably increased the time necessary to achieve zero breakdowns. The prevalence of bTB in deer needed to fall below ∼0.5% before ≤1 herd breakdown per year could be expected, and below 0.1% before zero breakdowns were likely. Locally applied post-harvest deer culling or vaccination also rapidly reduced herd breakdowns. On farm biosecurity measures needed to reduce deer to cattle contact by >95% in order to reliably reduce herd breakdowns, and did not achieve zero breakdowns in the absence of other deer controls.

Refugia and connectivity sustain amphibian metapopulations afflicted by disease.

Metapopulation persistence in fragmented landscapes depends on habitat patches that can support resilient local populations and sufficient connectivity between patches. Yet epidemiological theory for metapopulations has largely overlooked the capacity of particular patches to act as refuges from disease, and has suggested that connectivity can undermine persistence. Here, we show that relatively warm and saline wetlands are environmental refuges from chytridiomycosis for an endangered Australian frog, and act jointly with connectivity to sustain frog metapopulations. We coupled models of microclimate and infection probability to map chytrid prevalence, and demonstrate a strong negative relationship between chytrid prevalence and the persistence of frog populations. Simulations confirm that frog metapopulations are likely to go extinct when they lack environmental refuges from disease and lose connectivity between patches. This study demonstrates that environmental heterogeneity can mediate host-pathogen interactions in fragmented landscapes, and provides evidence that connectivity principally supports host metapopulations afflicted by facultative pathogens.

Inferring the distribution and demography of an invasive species from sighting data: the red fox incursion into Tasmania.

A recent study has inferred that the red fox (Vulpes vulpes) is now widespread in Tasmania as of 2010, based on the extraction of fox DNA from predator scats. Heuristically, this inference appears at first glance to be at odds with the lack of recent confirmed discoveries of either road-killed foxes--the last of which occurred in 2006, or hunter killed foxes--the most recent in 2001. This paper demonstrates a method to codify this heuristic analysis and produce inferences consistent with assumptions and data. It does this by formalising the analysis in a transparent and repeatable manner to make inference on the past, present and future distribution of an invasive species. It utilizes Approximate Bayesian Computation to make inferences. Importantly, the method is able to inform management of invasive species within realistic time frames, and can be applied widely. We illustrate the technique using the Tasmanian fox data. Based on the pattern of carcass discoveries of foxes in Tasmania, we infer that the population of foxes in Tasmania is most likely extinct, or restricted in distribution and demographically weak as of 2013. It is possible, though unlikely, that that population is widespread and/or demographically robust. This inference is largely at odds with the inference from the predator scat survey data. Our results suggest the chances of successfully eradicating the introduced red fox population in Tasmania may be significantly higher than previously thought.

Wetland characteristics influence disease risk for a threatened amphibian.

Identifying determinants of the probability and intensity of infections is important for understanding the epidemiology of wildlife diseases, and for managing their impact on threatened species. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, has decimated populations of some amphibians. However, recent studies have identified important environmental constraints on the disease, related to the pathogen's physiological tolerances. In this study, we identified several intrinsic and extrinsic determinants of the probability and intensity of chytrid infections for the threatened growling grass frog (Litoria raniformis) in southeastern Australia, and used mark-recapture to estimate the effect of chytrid infections on the probability of survival of these frogs. Water temperature and salinity had negative effects on both the probability and intensity of chytrid infections. We coupled models of the infection process with a model of the effect of chytrid infections on the probability of survival to assess variation in the impact of chytridiomycosis between wetlands with differing temperature and salinity profiles. Our results suggest that warm, saline wetlands may be refuges from chytridiomycosis for L. raniformis, and should be priorities for protection. Our results also suggest that management actions that increase water temperature (e.g., reducing canopy shading) and salinity (e.g., complementing inflows with groundwater) could be trialed to reduce the impacts of chytridiomycosis on this species. This and other recent studies highlight the value of research on environmental risk factors for chytridiomycosis.

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.

Quantifying eradication success: the removal of feral pigs from Santa Cruz Island, California.

A major challenge facing pest-eradication efforts is determining when eradication has been achieved. When the pest can no longer be detected, managers have to decide whether the pest has actually been eliminated and hence to decide when to terminate the eradication program. For most eradication programs, this decision entails considerable risk and is the largest single issue facing managers of such programs. We addressed this issue for an eradication program of feral pigs (Sus scrofa) from Santa Cruz Island, California. Using a Bayesian approach, we estimated the degree of confidence in the success of the eradication program at the point when monitoring failed to detect any more pigs. Catch-effort modeling of the hunting effort required to dispatch pigs during the eradication program was used to determine the relationship between detection probability and searching effort for different hunting methods. We then used these relationships to estimate the amount of monitoring effort required to declare eradication successful with criteria that either set a threshold for the probability that pigs remained undetected (type I error) or minimized the net expected costs of the eradication program (cost of type I and II errors). For aerial and ground-based monitoring techniques, the amount of search effort required to declare eradication successful on the basis of either criterion was highly dependent on the prior belief in the success of the program unless monitoring intensities exceeded 30 km of searching effort per square kilometer of search area for aerial monitoring and, equivalently, 38 km for ground monitoring. Calculation of these criteria to gauge the success of eradication should form an essential component of any eradication program as it allows for a transparent assessment of the risks inherent in the decision to terminate the program.