Biosecurity surveillance design: detecting non-indigenous vertebrate introductions using risk and power

Ecosystems can be severely damaged by the introduction, establishment and spread of non-indigenous species (NIS) including vertebrates, invertebrates and plants. Development and use of natural areas poses a biosecurity risk regarding the introduction of increase NIS invasion risks, so biosecurity systems including prevention and detection measures are required. Even with the most rigorous biosecurity efforts, there is potential for NIS to evade quarantine and go on to establish and spread. The cost of such an event can be great, both environmentally and financially (e.g. containment/ management or eradication). We have developed a surveillance design methodology, for an application where increased use of a natural area may result in NIS incursions, even with extensive biosecurity systems. The surveillance design methodology acknowledges heterogeneity of risk in the study area and stratifies the area to optimise surveillance deployment, achieving great efficiencies and improvement in statistical power of detection. Many of the risk decisions require lack data and so the system incorporates expert opinion with available data. The design covers the broad range of potential NIS that may be introduced by using exemplar species and a variety of surveillance system components (SSCs) (such as a combination of formal scientific surveys, trapping methods, and casual observation) distributed optimally over time and space. The mix of SSCs can be manipulated to take into account such factors as their relative financial costs and demands on expertise. The methodology has the flexibility to be applied to various groups of potential NIS (e.g. vertebrates, invertebrates and plants), and the design can evolve as data are collected (adaptive management). Overall, the surveillance design methodology allows for an efficient use of resources, providing sufficient power to detect incursions, resulting in reduced environmental and financial costs from NIS incursions.     

Ecological aspects of biosecurity surveillance design for the detection of multiple invasive animal species

Complex surveillance problems are common in biosecurity, such as prioritizing detection among multiple invasive species, specifying risk over a heterogeneous landscape, combining multiple sources of surveillance data, designing for specified power to detect, resource management, and collateral effects on the environment. Moreover, when designing for multiple target species, inherent biological differences among species result in different ecological models underpinning the individual surveillance systems for each. Species are likely to have different habitat requirements, different introduction mechanisms and locations, require different methods of detection, have different levels of detectability, and vary in rates of movement and spread. Often there is a further challenge of a lack of knowledge, literature, or data, for any number of the above problems. Even so, governments and industry need to proceed with surveillance programs which aim to detect incursions in order to meet environmental, social and political requirements. We present an approach taken to meet these challenges in one comprehensive and statistically powerful surveillance design for non-indigenous terrestrial vertebrates on Barrow Island, a high conservation nature reserve off the Western Australian coast. Here, the possibility of incursions is increased due to construction and expanding industry on the island. The design, which includes mammals, amphibians and reptiles, provides a complete surveillance program for most potential terrestrial vertebrate invaders. Individual surveillance systems were developed for various potential invaders, and then integrated into an overall surveillance system which meets the above challenges using a statistical model and expert elicitation. We discuss the ecological basis for the design, the flexibility of the surveillance scheme, how it meets the above challenges, design limitations, and how it can be updated as data are collected as a basis for adaptive management.     

Many eyes on the ground: citizen science is an effective early detection tool for biosecurity

Early detection of target non-indigenous species is one of the most important determinants of a successful eradication campaign. For early detection to be successful, and provide the highest probability of achieving eradication, intense surveillance is often required that can involve significant resources. Volunteer based monitoring or “citizen science” is one potential tool to address this problem. This study differs from standard citizen science projects because the participants are personnel or contractors of a company working on Barrow Island, Western Australia. We show that personnel can contribute successfully to a surveillance program aimed at detecting a broad taxonomic range of non-indigenous vertebrate and invertebrate species. Using data collected over a five year surveillance period on Barrow Island, we show that eighteen of the nineteen (95%) non-indigenous invertebrate species new to the island were detected by personnel working on the island, and that the number of detections made by these workers was significantly related to the number of personnel on the island at any one time. Most personnel detections (91%) were made inside buildings where the majority of active surveillance tools could not be implemented. For vertebrates, 4 NIS species detections (100% of detections) were made in the built environment by personnel. Although reporting of suspect non-indigenous species is voluntary, personnel are required to attend inductions and toolboxes where reporting of suspect biosecurity risk material is encouraged. These results demonstrate the value of industry led ‘citizen science’ programs, resulting in sustained stewardship and conservation of areas with high environmental value.     

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.     

Potential spread of introduced black rat (Rattus rattus) parasites to endemic deer mice (Peromyscus maniculatus) on the California Channel Islands

Introduced species have the potential to outperform natives in two primary ways: via increased rates of predation and competition, and via the introduction of new parasites against which native species often lack effective immune defences. To assess the extent to which invasive species' parasites spread to native hosts, we compared the composition of helminth parasites found in introduced black rat ( Rattus rattus ) and endemic deer mouse ( Peromyscus maniculatus ) populations on a subset of the California Channel Islands. Results suggest that the whipworm, Trichuris muris , may have spread from introduced black rats to endemic island deer mice and has continued to thrive in one island population where rats were recently eradicated. These results yield two important conservation messages: (1) although the parasites introduced with invasive species may be few, they should not be ignored as they can spread to native species, and (2) introduced parasites have the potential to remain in a system even after their founding host is extirpated. These findings underscore the importance of parasitological surveys in invasive species research and baseline data for ecosystems where exotic species are likely to invade.     

Improved surveillance for early detection of a potential invasive species: the alien Rose-ringed parakeet <Emphasis Type="Italic">Psittacula krameri</Emphasis> in Australia

The Rose-ringed parakeet Psittacula krameri is the most widely introduced parrot in the world, and is an important agricultural pest and competitor with native wildlife. In Australia, it is classified as an ‘extreme threat’, yet captive individuals frequently escape into the wild. The distribution and frequency of incursions are currently unknown, as are the potential impacts of the species in Australia. This lack of critical ecological information greatly limits effective biosecurity surveillance and decision-making efforts. We compiled a unique dataset, which combined passive surveillance sources from government and online resources, for all available information on parakeet detections at-large in Australia. We investigated whether geographic variables successfully predicted parakeet incursions, and used species distribution models to assess the potential distribution and economic impacts on agricultural assets. We recorded 864 incursions for the period 1999–2013; mostly escaped birds reported to missing animal websites. Escapes were reported most frequently within, or around, large cities. Incursions were best predicted by factors related to human presence and activity, such as global human footprint and intensive land uses. We recommend surveillance of high (predicted) establishment areas adjacent to cities where a feral parakeet population could most affect horticultural production. Novel passive surveillance datasets combined with species distribution models can be used to identify the regions where potential invasive species are most likely to establish. Subsequently, active surveillance can be targeted to the areas of highest predicted potential risk. We recommend an integrated approach that includes outreach programs involving local communities, as well as traditional biosecurity surveillance, for detecting new incursions.     

Toward routine,DNA-based detection methods for marine pests

Marine pest incursions can cause significant ongoing damage to aquaculture, biodiversity, fisheries habitat, infrastructure and social amenity. They represent a significant and ongoing economic burden. Marine pests can be introduced by several vectors including aquaculture, aquarium trading, commercial shipping, fishing, floating debris, mining activities and recreational boating. Despite the inherent risks, there is currently relatively little routine surveillance of marine pest species conducted in the majority of countries worldwide. Accurate and rapid identification of marine pest species is central to early detection and management. Traditional techniques (e.g. physical sampling and sorting), have limitations, which has motivated some progress towards the development of molecular diagnostic tools. This review provides a brief account of the techniques traditionally used for detection and describes developments in molecular-based methods for the detection and surveillance of marine pest species. Recent advances provide a platform for the development of practical, specific, sensitive and rapid diagnosis and surveillance tools for marine pests for use in effective prevention and control strategies.     

Integration of non-indigenous species within the interspecific abundance–occupancy relationship

There is a broad consensus that habitat disturbance and introduction of non-indigenous species may dramatically modify community structure, particularly in insular ecosystems. However, it is less clear whether emergent macroecological patterns are similarly affected. The positive interspecific abundance–occupancy relationship (IAOR) is one of the most pervasive macroecological patterns, yet has rarely been analyzed for oceanic island assemblages. We use an extensive dataset for arthropods from six islands within the Azorean archipelago to test: (1) whether indigenous and non-indigenous species are distributed differently within the IAOR; and (2) to the extent that they are, can differences can be attributed to two indices of disturbance. We implemented modeling averaged methods using five of the most common IAOR models to derive an averaged IAOR fit for each island. After testing if species colonization status (indigenous versus non-indigenous) may explain the residuals of the IAOR, we identified true negative and positive outliers and tested the effect of colonization status on the likelihood of a species being a positive or negative outlier. We found that the indigenous and non-indigenous species are randomly distributed on both sides of the overall IAOR. Only for Flores Island, were non-indigenous species more aggregated than indigenous species. We were unable to detect a meaningful relationship between deviation from the IAOR and disturbance, despite the undoubted impact of both severe habitat loss and non-indigenous species on these oceanic islands. Our results show that the non-indigenous species have been integrated alongside indigenous species in the contemporary Azorean arthropod communities such that they are mostly undetectable by the study of the IAOR.     

Watershed Conservation in the Long Run

We studied unanticipated long-run outcomes of conservation activities that occurred in forested watersheds on O`ahu, Hawaii, in the early twentieth century. The initial general impetus for the conservation activities was to improve irrigation surface water flow for the sugar industry. Industry concentration facilitated conservation of entire ecosystems. We investigate the benefits that accrued through dynamic linkages of the hydrological cycle and groundwater aquifer system. This provides a clear example of the need to consider integrated watershed effects, industrial structure, and linkages in determining conservation policy. We incorporated remote-sensing data, expert opinion on current watershed quality, and a spatial economic and hydrological model of O`ahu’s freshwater use with reports of conservation activities from 1910–1960 to assess these benefits. We find a 2.3% annual increase in groundwater recharge levels from these activities, with a lower bound benefit–cost ratio of 7.1–18.2. This lower-bound excludes returns from such high value, yet controversial to measure, amenities as species preservation.     

Detection of a colonizing, aquatic, non-indigenous species

Detecting the presence of rare species has interested ecologists and conservation biologists for many years. A particularly daunting application of this problem pertains to the detection of non-indigenous species (NIS) as they colonize new ecosystems. Ethical issues prevent experimental additions of NIS to most natural systems to explore the relationship between sampling intensity and the detection probability of a colonizing NIS. Here we examine this question using a recently introduced water flea, Cercopagis pengoi , in Lake Ontario. The species has biphasic population development, with sexually-produced 'spring morphs' developing prior to parthenogenetically-produced 'typical' morphs. Thus, this biphasic morphology allows distinction between new colonists (spring morphs) from subsequent generations. We repeatedly sampled Hamilton Harbour, Lake Ontario for the presence of both spring and typical morphs. Probability of detection was positively related to both the number of samples taken and animal density in the lake; however, even highly intensive sampling (100 samples) failed to detect the species in early spring when densities were very low. Spatial variation was greatest when densities of Cercopagis were intermediate to low. Sub-sampling, which increased space between adjacent samples, significantly decreased the number of samples required to reach greater, calculated detection probabilities on these dates. Typical sampling protocols for zooplankton have a low probability (< 0.2) of detecting the species unless population density is high. Results of this study suggest that early detection of colonizing, aquatic NIS may be optimized through use of a risk-based sampling design, combined with high sampling intensity in areas deemed most vulnerable to invasion, rather than less intensive sampling at a wider array of sites.     

Optimal surveillance strategy for invasive species management when surveys stop after detection

Invasive species are a cause for concern in natural and economic systems and require both monitoring and management. There is a trade‐off between the amount of resources spent on surveying for the species and conducting early management of occupied sites, and the resources that are ultimately spent in delayed management at sites where the species was present but undetected. Previous work addressed this optimal resource allocation problem assuming that surveys continue despite detection until the initially planned survey effort is consumed. However, a more realistic scenario is often that surveys stop after detection (i.e., follow a “removal” sampling design) and then management begins. Such an approach will indicate a different optimal survey design and can be expected to be more efficient. We analyze this case and compare the expected efficiency of invasive species management programs under both survey methods. We also evaluate the impact of mis‐specifying the type of sampling approach during the program design phase. We derive analytical expressions that optimize resource allocation between monitoring and management in surveillance programs when surveys stop after detection. We do this under a scenario of unconstrained resources and scenarios where survey budget is constrained. The efficiency of surveillance programs is greater if a “removal survey” design is used, with larger gains obtained when savings from early detection are high, occupancy is high, and survey costs are not much lower than early management costs at a site. Designing a surveillance program disregarding that surveys stop after detection can result in an efficiency loss. Our results help guide the design of future surveillance programs for invasive species. Addressing program design within a decision‐theoretic framework can lead to a better use of available resources. We show how species prevalence, its detectability, and the benefits derived from early detection can be considered.     

Sounding out pests: the potential of hydroacoustics as a surveillance and compliance tool in aquatic biosecurity

Shipping is the main method for goods transportation, accounting for approximately 60% of all global trade. Biofouling of these shipping vessels is a critical pathway for the introduction of non-indigenous species (NIS) across the world’s oceans. In order to reduce the likelihood of NIS introductions, appropriate biosecurity mechanism need to be in place, including maintaining high standards in vessel hygiene, such as zero secondary biofouling. Development of methodologies that can accurately quantify vessel biofouling without impeding maritime operations, while simultaneously providing effective biosecurity for the marine environment and resources, and mitigation of introduced marine pests would be highly advantageous. This study tests such a methodology. We conduct a proof-of-concept study that uses hydroacoustics to quantify the biofouling on a vessel’s hull, using surrogates for a vessel hull and biofouling. Based on a simple off-the-shelf single beam echosounder, the method was able to visually detect and quantify various biofouling mimics (ranging in height from 10 to 200 mm in height) at a slow tow speed (0.5 m/s). The efficacy of the hydroacoustic method was influenced by the movement of the echosounder, with the discriminating capability reduced to the detection of only larger mimics as the speed of movement increased. With further development, the use of hydroacoustics could become a viable biosecurity surveillance option for the mitigation of introduced marine pest incursions.     

Non-indigenous ungulates as a threat to biodiversity

Non-indigenous ungulate species pose a problem for conservation. They can be socially and economically valuable, but are also potentially harmful to biodiversity. Therefore, their introduction requires an explicit assessment of risk relative to benefit. To conduct such risk assessments, information regarding the impacts of non-indigenous ungulates on biodiversity is required. Here, we review the available evidence for the biodiversity impacts of non-indigenous ungulates. Hybridization, exploitation and apparent competition, vegetation impacts, predation, facilitation, trophic cascades and soil system functioning were assessed using a hierarchical set of criteria for the strength of the evidence. Strong evidence was lacking for risks posed by competition. Numerous reports exist of hybridization in captivity between ungulate species that normally do not co-occur, but conclusive evidence for introgression in the wild was restricted to one case. Strong evidence (using exclosure experiments) for the impacts of introduced ungulates on vegetation structure and composition was found and in some cases introduced ungulates caused the extirpation of plant species. Predation by Sus scrofa is a substantial threat to island faunas and systems, and impacts on soil system functioning elsewhere have also been found. Facilitation by ungulates has been shown to be substantial in promoting invasive plant species. By contrast, little evidence exists for apparent competition. The largest impacts from introduced ungulates are likely to be in cases where they perform novel functions in the new environment. However, to determine which types of impacts are likely to be most problematic, further evidence is required, ideally from well-designed field experiments.     

Adult mosquito trap sensitivity for detecting exotic mosquito incursions and eradication: a study using EVS traps and the Australian southern saltmarsh mosquito, Aedes camptorhynchus

Adult mosquito traps are commonly used in biosecurity surveillance for the detection of exotic mosquito incursions or for the demonstration of elimination. However, traps are typically deployed without knowledge of how many are required for detecting differing numbers of the target species. The aim of this study was to determine the sensitivity (i.e., detection probability) provided by carbon dioxide-baited EVS traps for adult female Australian southern saltmarsh mosquitoes, Aedes camptorhynchus, a recent biosecurity problem for New Zealand. A mark-release-recapture study of three concurrently released cohorts (sized 56, 296, and 960), recaptured over four days with a matrix of 20 traps, was conducted in Australia. The detection probability for different numbers of traps and cohorts of different sizes was determined by random sampling of recapture data. Detection probability ranged from approximately 0.3 for a single trap detecting a cohort of 56 mosquitoes to 1.0 (certainty of detection) when seven or more traps were used. For detection of adult Ae. camptorhynchus around a known source, a matrix of traps provides a strong probability of detection. Conversely, the use of single traps deployed over very large areas to detect mosquitoes of unknown entry pathway is unlikely to be successful. These findings have implications for the design of mosquito surveillance for biosecurity.     

Assessing species’ habitat associations from occurrence records,standardised monitoring data and expert opinion: A test with British butterflies

Accurate knowledge of species’ habitat associations is important for conservation planning and policy. Assessing habitat associations is a vital precursor to selecting appropriate indicator species for prioritising sites for conservation or assessing trends in habitat quality. However, much existing knowledge is based on qualitative expert opinion or local scale studies, and may not remain accurate across different spatial scales or geographic locations. Data from biological recording schemes have the potential to provide objective measures of habitat association, with the ability to account for spatial variation. We used data on 50 British butterfly species as a test case to investigate the correspondence of data-derived measures of habitat association with expert opinion, from two different butterfly recording schemes. One scheme collected large quantities of occurrence data (c. 3 million records) and the other, lower quantities of standardised monitoring data (c. 1400 sites). We used general linear mixed effects models to derive scores of association with broad-leaf woodland for both datasets and compared them with scores canvassed from experts.Scores derived from occurrence and abundance data both showed strongly positive correlations with expert opinion. However, only for occurrence data did these fell within the range of correlations between experts. Data-derived scores showed regional spatial variation in the strength of butterfly associations with broad-leaf woodland, with a significant latitudinal trend in 26% of species. Sub-sampling of the data suggested a mean sample size of 5000 occurrence records per species to gain an accurate estimation of habitat association, although habitat specialists are likely to be readily detected using several hundred records. Occurrence data from recording schemes can thus provide easily obtained, objective, quantitative measures of habitat association.     

A Characterization of the Non-indigenous Flora of the Azores Archipelago

The 9 Azores islands are located in the North Atlantic Ocean, about 1500 km from Europe. The vascular plant flora, consisting of 1002 taxa, was characterized using a database. Biogeographic and historic criteria were used to categorize the taxa as indigenous (31%) and non-indigenous (69%). The proportion of non-indigenous vascular plant taxa is higher than in other island ecosystems. This might have resulted from the removal of native vegetation and the introduction of many cultivated and ornamental plants, and from the relatively large extension of the agricultural landscape. The introduced plants were largely subcosmopolitan therophytes and hemicryptophytes, mainly Dicotyledoneae and Monocotyledoneae. The families with highest absolute contributions were similar to those in other areas of the world (Poaceae, Asteraceae, Fabaceae, Brassicaceae, Scrophulariaceae), but not all contributed as expected by their species richness worldwide. Many were introduced as ornamental or crop plants, but there were also many accidental introductions of weeds (about 55% of non-indigenous taxa). Considering the 9 islands, the percentage of introductions was positively correlated with human population density and island surface below 300 m, and negatively correlated with island surface allocated to natural areas.     

Insect Biocontrol with Non-endemic Entomopathogenic Nematodes (Steinernema and Heterorhabditis spp.): Conclusions and Recommendations of a Combined OECD and COST Workshop on Scientific and Regulatory Policy Issues

Fifteen invited experts from 10 Organisation for Economic Cooperation and Development (OECD) and European countries participating in the European Commission's Cooperation in the Field of Science and Technical Research (COST) Action 819, along with 12 other participants, met to review and debate the potential problems associated with the introduction and commercial use of non-indigenous nematodes for insect biological control. The consensus view of the participants was that entomopathogenic nematodes (EPNs) possess specific biological and ecological features, which make their use in biological control exceptionally safe. All the scientific evidence available supports the conclusion that EPNs are safe to the environment, as well as to production and application personnel, the general public and the consumers of agricultural products treated with them. Only a few potential, but very remote, risks could be identified. Therefore, it was recommended that EPNs should not be subject to any kind of registration. The introduction of non-indigenous nematode species, however, should be regulated. Species should be accurately identified, and details of the origin, known distribution, probable host range and safety to the user must be provided. In addition, an expert opinion, based on available information, of the possible impact on non-target organisms must be available.     

A sensitive environmental DNA (eDNA) assay leads to new insights on Ruffe (<Emphasis Type="Italic">Gymnocephalus cernua</Emphasis>) spread in North America

Detection of invasive species before or soon after they establish in novel environments is critical to prevent widespread ecological and economic impacts. Environmental DNA (eDNA) surveillance and monitoring is an approach to improve early detection efforts. Here we describe a large-scale conservation application of a quantitative polymerase chain reaction assay with a case study for surveillance of a federally listed nuisance species (Ruffe, Gymnocephalus cernua) in the Laurentian Great Lakes. Using current Ruffe distribution data and predictions of future Ruffe spread derived from a recently developed model of ballast-mediated dispersal in US waters of the Great Lakes, we designed an eDNA surveillance study to target Ruffe at the putative leading edge of the invasion. We report a much more advanced invasion front for Ruffe than has been indicated by conventional surveillance methods and we quantify rates of false negative detections (i.e. failure to detect DNA when it is present in a sample). Our results highlight the important role of eDNA surveillance as a sensitive tool to improve early detection efforts for aquatic invasive species and draw attention to the need for an improved understanding of detection errors. Based on axes that reflect the weight of eDNA evidence of species presence and the likelihood of secondary spread, we suggest a two-dimensional conceptual model that management agencies might find useful in considering responses to eDNA detections.     

Translating Predictions of Zoonotic Viruses for Policymakers

Recent outbreaks of Ebola virus disease and Zika virus disease highlight the need for disseminating accurate predictions of emerging zoonotic viruses to national governments for disease surveillance and response. Although there are published maps for many emerging zoonotic viruses, it is unknown if there is agreement among different models or if they are concordant with national expert opinion. Therefore, we reviewed existing predictions for five high priority emerging zoonotic viruses with national experts in Cameroon to investigate these issues and determine how to make predictions more useful for national policymakers. Predictive maps relied primarily on environmental parameters and species distribution models. Rift Valley fever virus and Crimean-Congo hemorrhagic fever virus predictions differed from national expert opinion, potentially because of local livestock movements. Our findings reveal that involving national experts could elicit additional data to improve predictions of emerging pathogens as well as help repackage predictions for policymakers.     

The DIOS framework for optimizing infectious disease surveillance: Numerical methods for simulation and multi-objective optimization of surveillance network architectures

Infectious disease surveillance systems provide vital data for guiding disease prevention and control policies, yet the formalization of methods to optimize surveillance networks has largely been overlooked. Decisions surrounding surveillance design parameters—such as the number and placement of surveillance sites, target populations, and case definitions—are often determined by expert opinion or deference to operational considerations, without formal analysis of the influence of design parameters on surveillance objectives. Here we propose a simulation framework to guide evidence-based surveillance network design to better achieve specific surveillance goals with limited resources. We define evidence-based surveillance design as an optimization problem, acknowledging the many operational constraints under which surveillance systems operate, the many dimensions of surveillance system design, the multiple and competing goals of surveillance, and the complex and dynamic nature of disease systems. We describe an analytical framework—the Disease Surveillance Informatics Optimization and Simulation (DIOS) framework—for the identification of optimal surveillance designs through mathematical representations of disease and surveillance processes, definition of objective functions, and numerical optimization. We then apply the framework to the problem of selecting candidate sites to expand an existing surveillance network under alternative objectives of: (1) improving spatial prediction of disease prevalence at unmonitored sites; or (2) estimating the observed effect of a risk factor on disease. Results of this demonstration illustrate how optimal designs are sensitive to both surveillance goals and the underlying spatial pattern of the target disease. The findings affirm the value of designing surveillance systems through quantitative and adaptive analysis of network characteristics and performance. The framework can be applied to the design of surveillance systems tailored to setting-specific disease transmission dynamics and surveillance needs, and can yield improved understanding of tradeoffs between network architectures.