Avoiding bias in estimates of population size for translocation management.

Mark-recapture surveys are commonly used to monitor translocated populations globally. Data gathered are then used to estimate demographic parameters, such as abundance and survival, using Jolly-Seber (JS) models. However, in translocated populations initial population size is known and failure to account for this may bias parameter estimates, which are important for informing conservation decisions during population establishment. Here, we provide methods to account for known initial population size in JS models by incorporating a separate component likelihood for translocated individuals, using a maximum-likelihood estimation, with models that can be fitted using either R or MATLAB. We use simulated data and a case study of a threatened lizard species with low capture probability to demonstrate that unconstrained JS models may overestimate the size of translocated populations, especially in the early stages of post-release monitoring. Our approach corrects this bias; we use our simulations to demonstrate that overestimates of population size between 78% and 130% can occur in the unconstrained JS models when the detection probability is below 0.3 compared to 1%-8.9% for our constrained model. Our case study did not show an overestimate; however accounting for the initial population size greatly reduced error in all parameter estimates and prevented boundary estimates. Adopting the corrected JS model for translocations will help managers to obtain more robust estimates of the population sizes of translocated animals, better informing future management including reinforcement decisions, and ultimately improving translocation success.

Compensatory recruitment allows amphibian population persistence in anthropogenic habitats.

Habitat anthropization is a major driver of global biodiversity decline. Although most species are negatively affected, some benefit from anthropogenic habitat modifications by showing intriguing life-history responses. For instance, increased recruitment through higher allocation to reproduction or improved performance during early-life stages could compensate for reduced adult survival, corresponding to "compensatory recruitment". To date, evidence of compensatory recruitment in response to habitat modification is restricted to plants, limiting understanding of its importance as a response to global change. We used the yellow-bellied toad (Bombina variegata), an amphibian occupying a broad range of natural and anthropogenic habitats, as a model species to test for and to quantify compensatory recruitment. Using an exceptional capture-recapture dataset composed of 21,714 individuals from 67 populations across Europe, we showed that adult survival was lower, lifespan was shorter, and actuarial senescence was higher in anthropogenic habitats, especially those affected by intense human activities. Increased recruitment in anthropogenic habitats fully offset reductions in adult survival, with the consequence that population growth rate in both habitat types was similar. Our findings indicate that compensatory recruitment allows toad populations to remain viable in human-dominated habitats and might facilitate the persistence of other animal populations in such environments.

Exploring artificial habitat fragmentation to control invasion by infectious wildlife diseases.

One way to reduce the impacts of invading wildlife diseases is setting up fences that would reduce the spread of pathogens by limiting connectivity, similarly to exclusion fences that are commonly used to conserve threatened species against invasive predators. One of the problems with fences is that, while they may have the short-term benefit of impeding the spread of disease, this benefit may be offset by potential long-term ecological costs of fragmentation by fencing. However, managers facing situations where a pathogen has been detected near the habitat of a (highly) vulnerable species may be willing to explore such a trade-off. To aid such exploration quantitatively, we present a series of models trading off the benefits of fragmentation (potential reduction of disease impacts on susceptible individuals) against its costs (both financial and ecological, i.e. reduced viability in the patches created by fragmentation), and exploring the effects of fragmentation on non-target species richness. For all model variants we derive the optimal number of artificial patches. We show that pre-emptive disease fences may have benefits when the risk of disease exceeds the impacts of fragmentation, when fence failure rates are lower than a specific threshold, and when sufficient resources are available to implement optimal solutions. A useful step to initiate planning is to obtain information about the expected number of initial infection events and on the host's extinction threshold with respect to the focal habitat and management duration. Our approach can assist managers to identify whether the trade-offs support the decision to fence and how intensive fragmentation should be.

Why disease ecology needs life-history theory: a host perspective.

When facing an emerging infectious disease of conservation concern, we often have little information on the nature of the host-parasite interaction to inform management decisions. However, it is becoming increasingly clear that the life-history strategies of host species can be predictive of individual- and population-level responses to infectious disease, even without detailed knowledge on the specifics of the host-parasite interaction. Here, we argue that a deeper integration of life-history theory into disease ecology is timely and necessary to improve our capacity to understand, predict and mitigate the impact of endemic and emerging infectious diseases in wild populations. Using wild vertebrates as an example, we show that host life-history characteristics influence host responses to parasitism at different levels of organisation, from individuals to communities. We also highlight knowledge gaps and future directions for the study of life-history and host responses to parasitism. We conclude by illustrating how this theoretical insight can inform the monitoring and control of infectious diseases in wildlife.

Applying a values-based decision process to facilitate comanagement of threatened species in Aotearoa New Zealand.

Ko koe ki tena, ko ahau ki tenai kiwai o te kete (you at that, and I at this handle of the basket). This Maori (New Zealanders of indigenous descent) saying conveys the principle of cooperation-we achieve more through working together, rather than separately. Despite decades of calls to rectify cultural imbalance in conservation, threatened species management still relies overwhelmingly on ideas from Western science and on top-down implementation. Values-based approaches to decision making can be used to integrate indigenous peoples' values into species conservation in a more meaningful way. We used such a values-based method, structured decision making, to develop comanagement of pekapeka (Mystacina tuberculata) (short-tailed bat) and tara iti (Sternula nereis davisae) (Fairy Tern) between Maori and Pakeha (New Zealanders of European descent). We implemented this framework in a series of workshops in which facilitated discussions were used to gather expert knowledge to predict outcomes and make management recommendations. For both species, stakeholders clearly stated their values as fundamental objectives from the start, which allowed alternative strategies to be devised that naturally addressed their diverse values, including matauranga Maori (Maori knowledge and perspectives). On this shared basis, all partners willingly engaged in the process, and decisions were largely agreed to by all. Most expectations of conflicts between values of Western science and Maori culture were unfounded. Where required, positive compromises were made by jointly developing alternative strategies. The values-based process successfully taha wairua taha tangata (brought both worlds together to achieve the objective) through codeveloped recovery strategies. This approach challenges the traditional model of scientists first preparing management plans focused on biological objectives, then consulting indigenous groups for approval. We recommend values-based approaches, such as structured decision making, as powerful methods for development of comanagement conservation plans between different peoples.

Aplicación de un Proceso de Decisiones Basadas en Valores para Facilitar el Comanejo de Especies Amenazadas en Aotearoa Nueva Zelanda Resumen Ko koe ki tena, ko ahau ki tenai kiwai o te kete (tú en ésa y yo en esta asa de la cesta). Este dicho Maori (neozelandeses con ascendencia indígena) expresa el principio de la cooperación - logramos más trabajando juntos que por separado. A pesar de las décadas de peticiones para rectificar el desbalance ambiental que existe en la conservación, el manejo de especies amenazadas todavía depende abrumadoramente de ideas tomadas de la ciencia occidental y en la implementación de arriba-abajo. Los enfoques para la toma de decisiones basados en valores pueden usarse para integrar de manera más significativa los valores de los pueblos indígenas dentro de la conservación de especies. Usamos un método basado en valores, la toma estructurada de decisiones, para desarrollar una estrategia de comanejo del pekapeka (Mystacina tuberculata) (murciélago de cola corta) y el tara iti (Sternula nereis davisae) (charrancito australiano) entre los Maori y los Pakeha (neozelandeses de ascendencia europea). Implementamos este marco de trabajo en una serie de talleres en los cuales se usaron discusiones facilitadas para recabar el conocimiento de los expertos para pronosticar los resultados y realizar recomendaciones de manejo. Para ambas especies, los actores sociales mencionaron claramente a sus valores como objetivos fundamentales desde el inicio, lo que permitió el diseño de estrategias alternativas que consideraran naturalmente estos diferentes valores, incluyendo el matauranga Maori (conocimiento y perspectivas Maori). Sobre esta base compartida, todos los colaboradores participaron voluntariamente en el proceso y la mayoría estuvo de acuerdo con las decisiones. La mayoría de los conflictos esperados entre la ciencia occidental y la cultura Maori no tuvieron fundamentos. En donde fueron requeridos, se realizaron concesiones positivas mediante el desarrollo conjunto de estrategias alternativas. El proceso basado en valores logró exitosamente taha wairua taha tangata (juntó a ambos mundos para conseguir el objetivo) por medio de estrategias de recuperación desarrolladas en conjunto. Esta estrategia desafía el modelo tradicional de los científicos preparando primero los planes de manejo enfocados en objetivos biológicos para después consultar a los grupos indígenas para que los aprueben. Recomendamos estos enfoques basados en valores, como la toma estructurada de decisiones, como métodos poderosos para el desarrollo de planes de conservación que incluyan el comanejo entre diferentes pueblos y personas.

Active responses to outbreaks of infectious wildlife diseases: objectives, strategies and constraints determine feasibility and success.

Emerging wildlife diseases are taking a heavy toll on animal and plant species worldwide. Mitigation, particularly in the initial epidemic phase, is hindered by uncertainty about the epidemiology and management of emerging diseases, but also by vague or poorly defined objectives. Here, we use a quantitative analysis to assess how the decision context of mitigation objectives, available strategies and practical constraints influences the decision of whether and how to respond to epidemics in wildlife. To illustrate our approach, we parametrized the model for European fire salamanders affected by Batrachochytrium salamandrivorans, and explored different combinations of conservation, containment and budgetary objectives. We found that in approximately half of those scenarios, host removal strategies perform equal to or worse than no management at all during a local outbreak, particularly where removal cannot exclusively target infected individuals. Moreover, the window for intervention shrinks rapidly if an outbreak is detected late or if a response is delayed. Clearly defining the decision context is, therefore, vital to plan meaningful responses to novel outbreaks. Explicitly stating objectives, strategies and constraints, if possible before an outbreak occurs, avoids wasting precious resources and creating false expectations about what can and cannot be achieved during the epidemic phase.

Presence of low virulence chytrid fungi could protect European amphibians from more deadly strains.

Wildlife diseases are contributing to the current Earth's sixth mass extinction; one disease, chytridiomycosis, has caused mass amphibian die-offs. While global spread of a hypervirulent lineage of the fungus Batrachochytrium dendrobatidis (BdGPL) causes unprecedented loss of vertebrate diversity by decimating amphibian populations, its impact on amphibian communities is highly variable across regions. Here, we combine field data with in vitro and in vivo trials that demonstrate the presence of a markedly diverse variety of low virulence isolates of BdGPL in northern European amphibian communities. Pre-exposure to some of these low virulence isolates protects against disease following subsequent exposure to highly virulent BdGPL in midwife toads (Alytes obstetricans) and alters infection dynamics of its sister species B. salamandrivorans in newts (Triturus marmoratus), but not in salamanders (Salamandra salamandra). The key role of pathogen virulence in the complex host-pathogen-environment interaction supports efforts to limit pathogen pollution in a globalized world.

Response to Comment on "Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity".

Lambert et al question our retrospective and holistic epidemiological assessment of the role of chytridiomycosis in amphibian declines. Their alternative assessment is narrow and provides an incomplete evaluation of evidence. Adopting this approach limits understanding of infectious disease impacts and hampers conservation efforts. We reaffirm that our study provides unambiguous evidence that chytridiomycosis has affected at least 501 amphibian species.

Realising the potential of Natura 2000 to achieve EU conservation goals as 2020 approaches.

In the last decades the EU has made substantial efforts implementing conservation strategies to halt biodiversity loss. However, little improvement has been reported. Given the proximity of the 2020 landmark set by the EU Biodiversity Strategy and the Convention for Biological Diversity, alternatives to reduce this conservation gap and prospect future strategies must be assessed urgently. Here, we explore how the current Natura 2000 could be used to enhance management of terrestrial and freshwater threatened vertebrates. We identified Natura 2000 sites to increase the coverage of threatened species as target species under two alternative scenarios: a policy-driven approach including only threatened vertebrates listed in the Directives; and a conservation-driven approach, including all the remaining threatened vertebrates. We show that representation of threatened vertebrates in Natura 2000 could be improved by updating lists of target species in less than 1% and 3% of sites in the policy-driven and conservation-driven scenarios, respectively. We highlight the strength of Natura 2000, with sites that complement each other and could contribute to achieving more ambitious conservation targets under future strategies. Prioritisation exercises like this could help realise the potential of this network and enhance the management of threatened species and improve current gaps.

Reducing Campylobacter jejuni colonization in broiler chickens by in-feed supplementation with hyperimmune egg yolk antibodies.

Campylobacter infections sourced mainly to poultry products, are the most important bacterial foodborne zoonoses worldwide. No effective measures to control these infections in broiler production exist to date. Here, we used passive immunization with hyperimmune egg yolks to confer broad protection of broilers against Campylobacter infection. Two novel vaccines, a bacterin of thirteen Campylobacter jejuni (C. jejuni) and C. coli strains and a subunit vaccine of six immunodominant Campylobacter antigens, were used for the immunization of layers, resulting in high and prolonged levels of specific immunoglobulin Y (IgY) in the hens' yolks. In the first in vivo trial, yolks (sham, bacterin or subunit vaccine derived) were administered prophylactically in the broiler feed. Both the bacterin- and subunit vaccine-induced IgY significantly reduced the number of Campylobacter-colonized broilers. In the second in vivo trial, the yolks were administered therapeutically during three days before euthanasia. The bacterin IgY resulted in a significant decrease in C. jejuni counts per infected bird. The hyperimmune yolks showed strong reactivity to a broad representation of C. jejuni and C. coli clonal complexes. These results indicate that passive immunization with hyperimmune yolks, especially bacterin derived, offers possibilities to control Campylobacter colonization in poultry.

Quantifying the burden of managing wildlife diseases in multiple host species.

Mitigation of infectious wildlife diseases is especially challenging where pathogens affect communities of multiple host species. Although most ecological studies recognize the challenge posed by multiple-species pathogens, the implications for management are typically assessed only qualitatively. Translating the intuitive understanding that multiple host species are important into practice requires a quantitative assessment of whether and how secondary host species should also be targeted by management and the effort this will require. Using a multiple-species compartmental model, we determined analytically whether and how intensively secondary host species should be managed to prevent outbreaks in focal hosts based on the reproduction number of individual host species and between-species transmission rates. We applied the model to the invasive pathogenic fungus Batrachochytrium salamandrivorans in a 2-host system in northern Europe. Avoiding a disease outbreak in the focal host (fire salamanders [Salamandra salamandra]) was impossible unless management also heavily targeted the secondary host (alpine newts [Ichthyosaura alpestris]). Preventing an outbreak in the community required targeted removal of at least 80% of each species. This proportion increased to 90% in the presence of an environmental reservoir of B. salamandrivorans and when the proportion of individuals removed could not be adjusted for different host species (e.g., when using traps that are not species specific). We recommend the focus of disease-mitigation plans should shift from focal species to the community level and calculate explicitly the management efforts required on secondary host species to move beyond the simple intuitive understanding that multiple host species may all influence the system. Failure to do so may lead to underestimating the magnitude of the effort required and ultimately to suboptimal or futile management attempts.

Cuantificación de la Carga que Representa el Manejo de Enfermedades de Fauna Silvestre en Múltiples Especies Hospederas Resumen La mitigación de enfermedades infecciosas en fauna silvestre representa un reto especial cuando los patógenos afectan a comunidades de múltiples especies hospederas. Aunque la mayoría de los estudios ecológicos reconocen el reto que plantean los patógenos de múltiples especies, las implicaciones para el manejo comúnmente sólo se evalúan en el aspecto cualitativo. La traducción del entendimiento intuitivo hacia la práctica de que las múltiples especies hospederas son importantes requiere una valoración cuantitativa sobre si y cuán intensivamente se deberían considerar en el manejo las especies hospederas secundarias y los esfuerzos que esto requerirá. Determinamos analíticamente con un modelo compartimentado de múltiples especies si y cuán intensivamente se deberían manejar las especies hospederas secundarias para prevenir brotes en los hospederos focales con base en el número de reproducción de las especies hospederas individuales y en las tasas de transmisión entre especies. Aplicamos el modelo al hongo patógeno invasivo Batrachochytrium salamandrivorans en un sistema de dos hospederos al norte de Europa. Fue imposible evitar un brote de enfermedad en el hospedero focal (la salamandra de fuego [Salamandra salamandra]) a menos que el manejo también se enfocara considerablemente en el hospedero secundario (el tritón alpino [Ichthyosaura alpestris]). Para prevenir un brote dentro de la comunidad se requirió de la extirpación de al menos el 80% de cada especie. Esta proporción incrementó al 90% con la presencia de un reservorio ambiental de B. salamandrivorans y cuando la proporción de individuos removidos no pudo ajustarse para diferentes especies (p. ej.: el uso de trampas que nos son específicas para una especie) Recomendamos que el foco de los planes para la mitigación de enfermedades cambie de una especie focal al nivel de comunidad y que calculen explícitamente los esfuerzos de manejo requeridos sobre las especies hospederas secundarias para avanzar más allá del simple entendimiento intuitivo de que múltiples especies hospederas pueden todas influir sobre el sistema. Si se falla en esto, se podría subestimar la magnitud del esfuerzo requerido y finalmente podría resultar en intentos de manejo sub-óptimos o inútiles.

Hygiene and biosecurity protocols reduce infection prevalence but do not improve fledging success in an endangered parrot.

Emerging Infectious Diseases (EIDs) are recognised as global extinction drivers of threatened species. Unfortunately, biodiversity managers have few tested solutions to manage them when often the desperate need for solutions necessitates a response. Here we test in situ biosecurity protocols to assess the efficacy of managing Psittacine beak and feather disease (PBFD), one of the most common and emergent viral diseases in wild parrots (Psittaciformes) that is currently affecting numerous threatened species globally. In response to an outbreak of PBFD in Mauritius "echo" parakeets (Psittacula eques), managers implemented a set of biosecurity protocols to limit transmission and impact of Beak and feather disease virus (BFDV). Here we used a reciprocal design experiment on the wild population to test whether BFDV management reduced viral prevalence and viral load, and improved nestling body condition and fledge success. Whilst management reduced the probability of nestling infection by approximately 11% there was no observed impact on BFDV load and nestling body condition. In contrast to expectations there was lower fledge success in nests with added BFDV biosecurity (83% in untreated vs. 79% in treated nests). Our results clearly illustrate that management for wildlife conservation should be critically evaluated through targeted monitoring and experimental manipulation, and this evaluation should always focus on the fundamental objective of conservation.

Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity.

Anthropogenic trade and development have broken down dispersal barriers, facilitating the spread of diseases that threaten Earth's biodiversity. We present a global, quantitative assessment of the amphibian chytridiomycosis panzootic, one of the most impactful examples of disease spread, and demonstrate its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. The effects of chytridiomycosis have been greatest in large-bodied, range-restricted anurans in wet climates in the Americas and Australia. Declines peaked in the 1980s, and only 12% of declined species show signs of recovery, whereas 39% are experiencing ongoing decline. There is risk of further chytridiomycosis outbreaks in new areas. The chytridiomycosis panzootic represents the greatest recorded loss of biodiversity attributable to a disease.

Post-epizootic salamander persistence in a disease-free refugium suggests poor dispersal ability of Batrachochytrium salamandrivorans.

Lack of disease spill-over between adjacent populations has been associated with habitat fragmentation and the absence of population connectivity. We here present a case which describes the absence of the spill-over of the chytrid fungus Batrachochytrium salamandrivorans (Bsal) between two connected subpopulations of fire salamanders (Salamandra salamandra). Based on neutrally evolving microsatellite loci, both subpopulations were shown to form a single genetic cluster, suggesting a shared origin and/or recent gene flow. Alpine newts (Ichthyosaura alpestris) and fire salamanders were found in the landscape matrix between the two sites, which are also connected by a stream and separated by no obvious physical barriers. Performing a laboratory trial using alpine newts, we confirmed that Bsal is unable to disperse autonomously. Vector-mediated dispersal may have been impeded by a combination of sub-optimal connectivity, limited dispersal ability of infected hosts and a lack of suitable dispersers following the rapid, Bsal-driven collapse of susceptible hosts at the source site. Although the exact cause remains unclear, the aggregate evidence suggests that Bsal may be a poorer disperser than previously hypothesized. The lack of Bsal dispersal between neighbouring salamander populations opens perspectives for disease management and stresses the necessity of implementing biosecurity measures preventing human-mediated spread.

Fragile coexistence of a global chytrid pathogen with amphibian populations is mediated by environment and demography.

Unravelling the multiple interacting drivers of host-pathogen coexistence is crucial in understanding how an apparently stable state of endemism may shift towards an epidemic and lead to biodiversity loss. Here, we investigate the apparent coexistence of the global amphibian pathogen Batrachochytrium dendrobatidis (Bd) with Bombina variegata populations in The Netherlands over a 7-year period. We used a multi-season mark-recapture dataset and assessed potential drivers of coexistence (individual condition, environmental mediation and demographic compensation) at the individual and population levels. We show that even in a situation with a clear cost incurred by endemic Bd, population sizes remain largely stable. Current environmental conditions and an over-dispersed pathogen load probably stabilize disease dynamics, but as higher temperatures increase infection probability, changing environmental conditions, for example a climate-change-driven rise in temperature, could unbalance the current fragile host-pathogen equilibrium. Understanding the proximate mechanisms of such environmental mediation and of site-specific differences in infection dynamics can provide vital information for mitigation actions.

An avirulent Brachyspira hyodysenteriae strain elicits intestinal IgA and slows down spread of swine dysentery.

Swine dysentery caused by Brachyspira hyodysenteriae, results in substantial economic losses in swine producing countries worldwide. Although a number of different vaccine approaches have been explored with regard to this disease, they show limitations and none of them have reached the market. We here determine the vaccine potential of a weakly haemolytic B. hyodysenteriae strain. The virulence of this strain was assessed in experimental infection trials and its protection against swine dysentery was quantified in a vaccination-challenge experiment using a seeder infection model. Systemic IgG production and local IgA production were monitored in serum and faeces respectively. Across all trials, pigs that were colonized by virulent, strongly haemolytic B. hyodysenteriae strains consistently developed swine dysentery, in contrast to none of the pigs colonized by the weakly haemolytic B. hyodysenteriae vaccine strain. In the seeder vaccination trial nearly all immunised animals developed swine dysentery on subsequent challenge with a virulent strain, but the speed of spread of swine dysentery and faecal score were significantly reduced in animals immunised with the weakly haemolytic strain compared to sham-immunised animals. The IgA response of immunised animals upon challenge with a virulent B. hyodysenteriae strain significantly correlated to a later onset of disease. The correlation between local IgA production and protection induced by a weakly haemolytic B. hyodysenteriae strain provides leads for future vaccine development against swine dysentery.

Is Reintroduction Biology an Effective Applied Science?

Reintroduction biology is a field of scientific research that aims to inform translocations of endangered species. We review two decades of published literature to evaluate whether reintroduction science is evolving in its decision-support role, as called for by advocates of evidence-based conservation. Reintroduction research increasingly addresses a priori hypotheses, but remains largely focused on short-term population establishment. Similarly, studies that directly assist decisions by explicitly comparing alternative management actions remain a minority. A small set of case studies demonstrate full integration of research in the reintroduction decision process. We encourage the use of tools that embed research in decision-making, particularly the explicit consideration of multiple management alternatives because this is the crux of any management decisions.