Application of techniques for the quantitative analysis of complex surveillance systems to disease and wildlife management

Scenario tree modelling and associated methods provide tools to quantify the combined value of multiple complex surveillance activities over time. The outputs of this analysis are an estimate of the sensitivity of a surveillance system, and the cumulative probability of disease freedom that surveillance provides over time. The ability to quantify the performance of complex surveillance systems provides a number of new opportunities in the design and application of search and detection activities. One of these is the ability to objectively compare alternative detection strategies. The sensitivity of a strategy (the probability that the target biota would be detected, given that they are present at a defined level) may be balanced against cost and practicality considerations to determine the most effective strategy for a given situation. The paper provides an example of the comparison of two surveillance strategies (structured surveys and abattoir surveillance) for disease detection in animal health (Classical Swine Fever). These techniques may also play an important role in the certification of success in pest eradication operations. The ability to use multiple sources of evidence to evaluate success means that a higher level of confidence can often be achieved at lower cost. Examples of the application of scenario tree modelling in plant health and invasive pests are provided to illustrate its use within eradication programs.     

Costing eradications of alien mammals from islands

The ability to estimate costs of alien species eradications is essential for a rigorous assessment of priorities for island restoration. Using a global data file from 41 islands, mostly gleaned from the 'grey' literature, we show that the cost of vertebrate eradications can be satisfactorily predicted if island area and species to be eradicated are known. About 72% of the variation in cost can be explained by island area, whereas, for a given area, rodent eradications are 1.7–3.0 times more expensive than ungulate eradications. Costs per hectare decrease with island size. Restricting the analysis to roughly half the data set, the relatively homogeneous half concerned with New Zealand islands, we identify two further influences on cost: date of eradication and distance to the main airport (an indicator of remoteness). For a given area, costs have declined over time but increase with island remoteness. This information therefore provides conservation planners with a robust, if preliminary, estimate of the cost of any proposed eradication programme.     

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.     

Prioritising islands in the United Kingdom and crown dependencies for the eradication of invasive alien vertebrates and rodent biosecurity

Invasive alien vertebrates (IAVs) pose a significant threat to island biodiversity worldwide, and their removal is an important nature conservation management goal. As methods advance, eradications from larger islands and of multiple species simultaneously are increasingly undertaken. Effective targeting to maximise conservation gain is important given limited resources. We build on existing prioritisation methods and use the islands of the UK and Crown Dependencies (UK) as an example of how vertebrate eradications might be prioritised and invasive-free status maintained through biosecurity. For each of the 9688 UK islands, we assessed ecological importance for native vertebrates and the anticipated impacts of the IAVs present to estimate the benefit of restoration based on the feasibility and sustainability of IAV eradications in relation to island size, human population and risk of unassisted reinvasion by swimming. As reinvasion poses a threat to the long-term benefits of eradication, we incorporated species-specific swimming distances and explored the effects of varying reinvasion probability from risk-averse to higher-risk strategies. The 25 islands that would benefit most from eradications were in Scotland, Northern Ireland and the Channel Islands. Our prioritisation method should be seen as an initial guide to identify islands that might benefit from intervention when faced with a large list of potential sites. Feasibility studies taking account of factors such as interspecific interactions, anthropogenic reinvasion, views of residents or ‘social feasibility’ and cost need to be undertaken before planning any eradication. We prioritised biosecurity for rat-free islands to highlight where comprehensive measures might be most beneficial.     

A review of mammal eradications on Mediterranean islands

1. Impacts of alien invasive species on island communities and ecosystems may be even more detrimental than on the mainland. Therefore, since the 1950s, hundreds of restoration projects have been implemented worldwide, with the aim of controlling or eradicating alien species from islands. To date, no review has been focused on eradication on Mediterranean islands. To fill the gap, I reviewed the available information concerning mammal eradications so far carried out on Mediterranean islands, examining the details of several aspects of project implementation and monitoring.
2. I obtained data for 139 attempted eradications on 107 Mediterranean islands in eight countries, with Greece, Italy, and Spain accounting for the highest number. Eradication projects targeted 13 mammal species. The black rat Rattus rattus was the target of over 75% of the known attempted eradications in the Mediterranean Basin; other species targeted were feral goat Capra hircus, house mouse Mus musculus, European rabbit Oryctolagus cuniculus, and domestic cat Felis catus. The most widely adopted technique was poisoning (77% of all eradications), followed by trapping (15%) and hunting (4%). However, techniques were largely target-specific.
3. The average failure rate was about 11%. However, this percentage varied according to the specific mammalian order, and eradications of Carnivora failed more often than those of other mammals. Among rodents, house mouse eradication attained a very high failure rate (75%). Reinvasion occurred after 15% of successful eradications.
4. A better understanding of the motivations of animal rights activists may improve the chance of success when eradicating charismatic or domesticated species. Furthermore, it is crucial to collect data and case studies about reinvasions, in order to strengthen biosecurity programmes following eradication. As in other parts of the world, the next frontier in alien mammal management on Mediterranean islands concerns the eradication of invasive species from inhabited islands.

     

Rodent eradications as ecosystem experiments: a case study from the Mexican tropics

For effective and efficient pest management it is essential to understand the ecology of the target species and recipient ecosystems. The use of rodent eradication as a restoration tool is well established in temperate regions, but less common in the tropics, presenting an opportunity to undertake scientific learning in tandem with rodent eradications. On a dry tropical archipelago, we used a Before-After-Control-Impact framework to document (1) fluctuations in the abundance and demography of invasive Rattus rattus and Mus musculus on three different islands, (2) the trophic niche of all three invasive rodent populations, and (3) changes in the invertebrate community before and after rodent eradication, also comparing with two rodent free islands. While rat density was high and relatively stable throughout the year, the two mouse populations greatly differed in body size and seasonal dynamics, despite their proximity. The rodents in all three populations were generalist and opportunistic feeders, although stable isotope analyses results indicated major differences among them, driven by food availability and rodent species. Seasonal fluctuations in invertebrate communities depended on rodent invasion status, but recovery in the invertebrate communities one year after rodent removal was limited for all islands. Predictions for other tropical ecosystem biomes require long-term research on more tropical islands. Improving our understanding of island and species-specific contexts of rodent eradications can advance island restoration projects and assist the selection of indicator species for ecosystem recovery.     

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.     

A model for long-distance dispersal of boll weevils (Coleoptera: Curculionidae)

The boll weevil, Anthonomus grandis (Boheman), has been a major insect pest of cotton production in the US, accounting for yield losses and control costs on the order of several billion US dollars since the introduction of the pest in 1892. Boll weevil eradication programs have eliminated reproducing populations in nearly 94%, and progressed toward eradication within the remaining 6%, of cotton production areas. However, the ability of weevils to disperse and reinfest eradicated zones threatens to undermine the previous investment toward eradication of this pest. In this study, the HYSPLIT atmospheric dispersion model was used to simulate daily wind-aided dispersal of weevils from the Lower Rio Grande Valley (LRGV) of southern Texas and northeastern Mexico. Simulated weevil dispersal was compared with weekly capture of weevils in pheromone traps along highway trap lines between the LRGV and the South Texas / Winter Garden zone of the Texas Boll Weevil Eradication Program. A logistic regression model was fit to the probability of capturing at least one weevil in individual pheromone traps relative to specific values of simulated weevil dispersal, which resulted in 60.4% concordance, 21.3% discordance, and 18.3% ties in estimating captures and non-captures. During the first full year of active eradication with widespread insecticide applications in 2006, the dispersal model accurately estimated 71.8%, erroneously estimated 12.5%, and tied 15.7% of capture and non-capture events. Model simulations provide a temporal risk assessment over large areas of weevil reinfestation resulting from dispersal by prevailing winds. Eradication program managers can use the model risk assessment information to effectively schedule and target enhanced trapping, crop scouting, and insecticide applications.     

Optimal DNA pooling-based two-stage designs in case-control association studies

Study cost remains the major limiting factor for genome-wide association studies due to the necessity of genotyping a large number of SNPs for a large number of subjects. Both DNA pooling strategies and two-stage designs have been proposed to reduce genotyping costs. In this study, we propose a cost-effective, two-stage approach with a DNA pooling strategy. During stage I, all markers are evaluated on a subset of individuals using DNA pooling. The most promising set of markers is then evaluated with individual genotyping for all individuals during stage II. The goal is to determine the optimal parameters (pi(p)(sample ), the proportion of samples used during stage I with DNA pooling; and pi(p)(marker ), the proportion of markers evaluated during stage II with individual genotyping) that minimize the cost of a two-stage DNA pooling design while maintaining a desired overall significance level and achieving a level of power similar to that of a one-stage individual genotyping design. We considered the effects of three factors on optimal two-stage DNA pooling designs. Our results suggest that, under most scenarios considered, the optimal two-stage DNA pooling design may be much more cost-effective than the optimal two-stage individual genotyping design, which use individual genotyping during both stages.     

Estimating realistic costs for strategic management planning of invasive species eradications on islands

Environmental managers regularly face decisions about how to counteract threats. These decisions require an understanding of both the conservation benefits and economic costs of candidate actions. However, transparent frameworks for how to accurately calculate costs for management are rare. We worked with island managers in Australia to develop eradication protocols for six invasive species- four mammals and two weeds. We used the protocols to create an accounting framework for invasive species eradications to produce realistic cost estimates for eradications across multiple locations. We also used our models to test common cost assumptions: (1) that costs scale linearly with area, (2) that terrain does not influence costs, and (3) that eradication costs stay constant through time. By explicating testing assumptions, we found that costs largely scaled linearly with area, that terrain influences costs, and that costs decline as populations decline in response to ongoing management. Estimated mammal eradication costs were driven in large part by the area of an island and the cost of transport. However, when area alone was used as a proxy for costs, the calculated costs deviated from our modelled costs by 40–56%. Weed eradication cost estimates were driven by the size and density of an infestation as well as the terrain of the island, with the effect of terrain becoming more pronounced as area to be treated increased. We provide a method to calculate realistic costs across several sites, which can be used to guide strategic management decision-making, including prioritisation, and on-ground management actions.     

Alterations in marginal zone macrophages and marginal zone B cells in old mice

Marginal zones (MZs) are architecturally organized for clearance of and rapid response against blood-borne Ags entering the spleen. MZ macrophages (MZMs) and MZ B cells are particularly important in host defense against T-independent pathogens and may be crucial for the prevention of diseases, such as streptococcal pneumonia, that are devastating in older patients. Our objective was to determine whether there are changes in the cellular components of the MZ between old and young mice. Using immunocytochemistry and a blinded scoring system, we observed gross architectural changes in the MZs of old mice, including reduction in the abundance of MZMs surrounding the MZ sinus as well as disruptions in positioning of mucosal addressin cell adhesion molecule 1 (MAdCAM-1)(+) sinus lining cells and metallophilic macrophages. Loss of frequency of MZMs was corroborated by flow cytometry. A majority of old mice also showed reduced frequency of MZ B cells, which correlated with decreased abundance of MZM in individual old mice. The spleens of old mice showed less deposition of intravenously injected dextran particles within the MZ, likely because of the decreased frequency in MZMs, because SIGN-R1 expression was not reduced on MZM from old mice. The phagocytic ability of individual MZMs was examined using Staphylococcus aureus bioparticles, and no differences in phagocytosis were found between macrophages from young or old spleens. In summary, an anatomical breakdown of the MZ occurs in advanced age, and a reduction in frequency of MZM may affect the ability of the MZM compartment to clear blood-borne Ags and mount proper T-independent immune responses.     

Bio-Economics of Large-Scale Eradication of Feral Goats From Santiago Island,Galápagos

ABSTRACT Invasive mammals are premier drivers of extinction and ecosystem change, particularly on islands. In the 1960s, conservation practitioners started developing techniques to eradicate invasive mammal populations from islands. Larger and more biologically complex islands are being targeted for restoration worldwide. We conducted a feral goat (Capra hircus) eradication campaign on Santiago Island in the Galápagos archipelago, which was an unprecedented advance in the ability to reverse biodiversity impacts by invasive species. We removed >79,000 goats from Santiago Island (58,465 ha) in <4.5 years, at an approximate cost of US$6.1 million. An eradication ethic combined with a suite of techniques and technologies made eradication possible. A field-based Geographic Information System facilitated an adaptive management strategy, including adjustment and integration of hunting methods. Specialized ground hunting techniques with dogs removed most of the goat population. Aerial hunting by helicopter and Judas goat techniques were also critical. Mata Hari goats, sterilized female Judas goats induced into a long-term estrus, removed males from the remnant feral population at an elevated rate, which likely decreased the length and cost of the eradication campaign. The last 1,000 goats cost US$2.0 million to remove; we spent an additional US$467,064 on monitoring to confirm eradication. Aerial hunting is cost-effective even in countries where labor is inexpensive. Local sociopolitical environments and best practices emerging from large-scale, fast-paced eradications should drive future strategies. For nonnative ungulate eradications, island size is arguably no longer the limiting factor. Future challenges will involve removing invasive mammals from large inhabited islands while increasing cost-effectiveness of removing low-density populations and confirming eradication. Those challenges will require leveraging technology and applying theory from other disciplines, along with conservation practitioners working alongside sociologists and educators.     

Evaluation of weed eradication programs: the delimitation of extent

Eradication is a management strategy that can provide substantial ecological and economic benefits by eliminating incursions of pest organisms. In contrast to eradication efforts that target other pests, weed eradication programs can be very protracted owing to the presence of persistent seed banks and difficulties in detecting the target. Hence there is a need to develop criteria to assist in the evaluation of progress towards eradication. Knowledge of the extent of a weed incursion (the ‘delimitation’ criterion) is considered fundamental for eradication success, as an incursion will progress from any infestations that remain undetected and thus uncontrolled. This criterion is examined with regard to eradication programs targeting Bassia scoparia L. A.J. Scott [= Kochia scoparia L. Schrader], Chondrilla juncea L. (both in Western Australia) and Orobanche ramosa L. in South Australia. The B. scoparia incursion, which has been eradicated, was largely delimited within 12 months of the inception of its eradication program. In contrast, the Western Australian C. juncea incursion has never been delimited, owing to insufficient investment in surveillance during an eradication program spanning 30 years. An exponential decrease in the detection ratio (infested area detected/area searched) over time suggests that delimitation has been approached within 6 years of the inception of the eradication program for O. ramosa. An effective surveillance program is essential for achieving delimitation of a weed incursion.     

Eradication of populations of an invasive ant in northern Australia: successes, failures and lessons for management

Eradication is the most difficult management goal for exotic species, and successes are rare and even more rarely published. The lack of publication of the methodology and outcomes of eradication programs severely limits the transfer of knowledge to programs elsewhere that target the same or similar species. Here I detail the successes and failures of eradication efforts on six populations of African big headed ant Pheidole megacephala in northern Australia, covering a combined area of almost 9 ha. Two years post-treatment, assessment criteria for successful eradication were met for four of the six populations, whereas eradication failed in the remaining two, resulting in the need for ongoing management. Positive outcomes are attributed to eight criteria being met: (1) a single line of project management authority; (2) over-arching legal authority; (3) susceptibility of the target organism to control procedures; (4) sufficient resources; (5) detectibility of the target organism at low densities; (6) early intervention; (7) prevention of reinvasion; and (8) prevention of invasive succession. Reasons for one of the failures remain unclear, but eradication failed in the other because a part of the population was not treated. In both cases, the eradication failures could have been detected and managed much earlier than was the case. The successes and lessons documented here, coupled with the now large number of small-scale eradications of this ant, warrant the implementation of larger and more ambitious management programs against this significant invader, especially within areas of high conservation value.     

Network theory as a method for developing biosecurity preparedness: Netweork topology of Paratrechina longicornis in the Pacific and within New Zealand

One of the greatest challenges in eradicating pest species is determining when no further individuals remain: terminating the control programme too early means failure to eradicate, whereas continuing for too long can add considerable expense. Since monitoring tools are usually only qualitative and invariably imperfect, there may be considerable uncertainty about when and if eradication has been achieved. However, it is possible to quantify the efficacy of monitoring tools and to use this together with knowledge of the basic ecology of the target pest to robustly quantify the probability of successful eradication over time. Here, I describe one such approach and demonstrate its use in the large-scale eradication of painted apple moth (Teia anartoides) from Auckland, New Zealand. A population model for the production of male moths was used in conjunction with spatially-explicit pheromone trap locations and attraction radii to determine the daily probability of detecting a hypothetical wild population at a particular location. Over time, these probabilities compounded to decrease the likelihood of painted apple moth presence given an ongoing lack of detection. In this way, spatio-temporal risk maps were produced to inform managers and to suggest when eradication had been achieved to a predetermined level of certainty. The model suggested that eradication was likely to have been successful in the main infestation areas by mid 2005, with subsequent catches likely to represent further small incursions, as corroborated by evidence from mitochondrial DNA and stable isotope markers. While it was plausible that a wild population was present in the Otahuhu area in 2005, it was very unlikely that it remained by the end of 2006. Population probability models have potential for much wider use in border biosecurity and establishment of area freedom, particularly in combination with future automated trapping systems.     

Trophic niche changes associated with the eradication of invasive mammals in an insular lizard: an assessment using isotopes

Invasive species are a major threat to island biodiversity, and their eradications have substantially contributed to the conservation of island endemics. However, the consequences of eradications on the trophic ecology of native taxa are largely unexplored. Here, we used the eradication of invasive black rats Rattus rattus and European rabbits Oryctolagus cuniculus from the Berlenga Island, in the western coast of Portugal, as a whole-ecosystem experiment to investigate the effects of the eradication of invasive mammals on the trophic niche and body dimensions of the island-restricted Berlenga wall lizard Podarcis carbonelli berlengensis over a 2-year period. Our results suggest an expansion of the isotopic niche and an intensification of the sexual dimorphism of the lizard following mammal eradication. Additionally, we found considerable variability in isotopic niche across the island and detected evidence of sex-specific and season-modulated nutritional requirements of this threatened reptile. Our findings support that the eradication of 2 of the planet’s most problematic invasive vertebrates led to changes in the lizard trophic niche and sexual dimorphism in just 2 years. This suggests that the ecological pressures—for example, prey availability and habitat structure—to which lizards are exposed have substantially changed post-eradication. Our study emphasizes the scientific value of island eradications as experiments to address a wide range of ecological questions and adds to the increasing body of evidence supporting substantial conservation gains associated with these restoration interventions.     

Population probability models for insect eradication

One of the greatest challenges in eradicating pest species is determining when no further individuals remain: terminating the control programme too early means failure to eradicate, whereas continuing for too long can add considerable expense. Since monitoring tools are usually only qualitative and invariably imperfect, there may be considerable uncertainty about when and if eradication has been achieved. However, it is possible to quantify the efficacy of monitoring tools and to use this together with knowledge of the basic ecology of the target pest to robustly quantify the probability of successful eradication over time. Here, I describe one such approach and demonstrate its use in the large-scale eradication of painted apple moth (Teia anartoides) from Auckland, New Zealand. A population model for the production of male moths was used in conjunction with spatially-explicit pheromone trap locations and attraction radii to determine the daily probability of detecting a hypothetical wild population at a particular location. Over time, these probabilities compounded to decrease the likelihood of painted apple moth presence given an ongoing lack of detection. In this way, spatio-temporal risk maps were produced to inform managers and to suggest when eradication had been achieved to a predetermined level of certainty. The model suggested that eradication was likely to have been successful in the main infestation areas by mid 2005, with subsequent catches likely to represent further small incursions, as corroborated by evidence from mitochondrial DNA and stable isotope markers. While it was plausible that a wild population was present in the Otahuhu area in 2005, it was very unlikely that it remained by the end of 2006. Population probability models have potential for much wider use in border biosecurity and establishment of area freedom, particularly in combination with future automated trapping systems.     

Clenbuterol (planipart(trade mark)) for the postponement of parturition in cattle

Clenbuterol is a highly specific, long-acting (four to eight hours) beta-two sympathomimetic which causes bronchodilation and tocolysis (myometrial paralysis). The tocolytic effect was explored as a means to control parturition and reduce dystocia. Forty-six heifers were injected i.m. with either Clenbuterol or saline placebo in a randomly controlled experiment. Animals were treated when a cervical dilation of five centimeters or more was detected by vaginal examination. Length of first, second and third stages of parturition, ease of parturition, maternal pelvic area and calf viability were compared between treatment groups. Treatment with Clenbuterol increased (P<0.025; 119 vs 468 mins) the time heifers were in Stage I. However, the lengths of Stages II and III, pelvic area at birth and calf viability were not influenced by treatment. Diameter of the cervix at treatment was negatively related to the length of Stage I delay. Pelvic area also significantly affected the length of Stage II. Clenbuterol effectively delays Stage I of parturition with no adverse effects on the fetus or dam.     

A Two-stage Procedure with Controlled Error Probabilities for Testing Bioequivalence

The procedures currently used for testing the bioequivalence of two drug formulations achieve control over the error probability of erroneously accepting bioequivalence or over the probability of erroneous rejection, but not over both error probabilities. A two-stage procedure that rectifies this drawback is presented, assuming that the performance of the drug is characterized by a normally distributed variate.     

Quantitative evaluation of complex surveillance systems for pest and disease detection

Surveillance for disease detection is used primarily for early detection of incursions and to support assertions of freedom from disease.Analytical techniques used to evaluate the efficacy of such surveillance are equally applicable across the domains of invasive species (both plant and animal), diseases and pests of agriculture crops, livestock, and of wildlife. Scenario tree models of surveillance activities may be used to estimate their diagnostic sensitivities, or the probability that the target organism will be detected given that it is present at a defined level. This paper will outline techniques for estimating the sensitivity of both targeted and general surveillance activities, and for the surveillance system as a whole. Probability of freedom from the target organism may be estimated from the surveillance sensitivity, and this Bayesian approach may be extended to estimate current probability of freedom from appropriate use of historical and ongoing surveillance evidence.