Using comparative extinction risk analysis to prioritize the IUCN Red List reassessments of amphibians.

Assessing the extinction risk of species based on the International Union for Conservation of Nature (IUCN) Red List (RL) is key to guiding conservation policies and reducing biodiversity loss. This process is resource demanding, however, and requires continuous updating, which becomes increasingly difficult as new species are added to the RL. Automatic methods, such as comparative analyses used to predict species RL category, can be an efficient alternative to keep assessments up to date. Using amphibians as a study group, we predicted which species are more likely to change their RL category and thus should be prioritized for reassessment. We used species biological traits, environmental variables, and proxies of climate and land-use change as predictors of RL category. We produced an ensemble prediction of IUCN RL category for each species by combining 4 different model algorithms: cumulative link models, phylogenetic generalized least squares, random forests, and neural networks. By comparing RL categories with the ensemble prediction and accounting for uncertainty among model algorithms, we identified species that should be prioritized for future reassessment based on the mismatch between predicted and observed values. The most important predicting variables across models were species' range size and spatial configuration of the range, biological traits, climate change, and land-use change. We compared our proposed prioritization index and the predicted RL changes with independent IUCN RL reassessments and found high performance of both the prioritization and the predicted directionality of changes in RL categories. Ensemble modeling of RL category is a promising tool for prioritizing species for reassessment while accounting for models' uncertainty. This approach is broadly applicable to all taxa on the IUCN RL and to regional and national assessments and may improve allocation of the limited human and economic resources available to maintain an up-to-date IUCN RL.

Uso del análisis comparativo del riesgo de extinción para priorizar la reevaluación de los anfibios en la Lista Roja de la UICN Resumen El análisis del riesgo de extinción de una especie con base en la Lista Roja (LR) de la Unión Internacional para la Conservación de la Naturaleza (UICN) es clave para guiar las políticas de conservación y reducir la pérdida de la biodiversidad. Sin embargo, este proceso demanda recursos y requiere de actualizaciones continuas, lo que se complica conforme se añaden especies nuevas a la LR. Los métodos automáticos, como los análisis comparativos usados para predecir la categoría de la especie en la LR, pueden ser una alternativa eficiente para mantener actualizados los análisis. Usamos a los anfibios como grupo de estudio para predecir cuáles especies tienen mayor probabilidad de cambiar de categoría en la LR y que, por lo tanto, se debería priorizar su reevaluación. Usamos las características biológicas de la especie, las variables ambientales e indicadores climáticos y del cambio de uso de suelo como predictores de la categoría en la LR. Elaboramos una predicción de ensamble de la categoría en la LR de la UICN para cada especie mediante la combinación de cuatro algoritmos diferentes: modelos de vínculo acumulativo, menor número de cuadros filogenéticos generalizados, bosques aleatorios y redes neurales. Con la comparación entre las categorías de la LR y la predicción de ensamble y con considerar la incertidumbre entre los algoritmos identificamos especies que deberían ser prioridad para futuras reevaluaciones con base en el desfase entre los valores predichos y los observados. Las variables de predicción más importantes entre los modelos fueron el tamaño de la distribución de la especie y su configuración espacial, las características biológicas, el cambio climático y el cambio de uso de suelo. Comparamos nuestra propuesta de índice de priorización y los cambios predichos en la LR con las reevaluaciones independientes de la LR de la UICN y descubrimos un buen desempeño tanto para la priorización como para la direccionalidad predicha de los cambios en las categorías de la LR. El modelo de ensamble de la categoría de la LR esa una herramienta prometedora para priorizar la reevaluación de las especies a la vez que considera la incertidumbre del modelo. Esta estrategia puede generalizarse para aplicarse a todos los taxones de la LR de la UICN y a los análisis regionales y nacionales. También podría mejorar la asignación de los recursos humanos y económicos limitados disponibles para mantener actualizada la LR de la UICN.

Quantitative support for the benefits of proactive management for wildlife disease control.

Finding effective pathogen mitigation strategies is one of the biggest challenges humans face today. In the context of wildlife, emerging infectious diseases have repeatedly caused widespread host morbidity and population declines of numerous taxa. In areas yet unaffected by a pathogen, a proactive management approach has the potential to minimize or prevent host mortality. However, typically critical information on disease dynamics in a novel host system is lacking, empirical evidence on efficacy of management interventions is limited, and there is a lack of validated predictive models. As such, quantitative support for identifying effective management interventions is largely absent, and the opportunity for proactive management is often missed. We considered the potential invasion of the chytrid fungus, Batrachochytrium salamandrivorans (Bsal), whose expected emergence in North America poses a severe threat to hundreds of salamander species in this global salamander biodiversity hotspot. We developed and parameterized a dynamic multistate occupancy model to forecast host and pathogen occurrence, following expected emergence of the pathogen, and evaluated the response of salamander populations to different management scenarios. Our model forecasted that taking no action is expected to be catastrophic to salamander populations. Proactive action was predicted to maximize host occupancy outcomes relative to wait-and-see reactive management, thus providing quantitative support for proactive management opportunities. The eradication of Bsal was unlikely under all the evaluated management options. Contrary to our expectations, even early pathogen detection had little effect on Bsal or host occupancy outcomes. Our results provide quantitative support that proactive management is the optimal strategy for promoting persistence of disease-threatened salamander populations. Our approach fills a critical gap by defining a framework for evaluating management options prior to pathogen invasion and can thus serve as a template for addressing novel disease threats that jeopardize wildlife and human health.

Apoyo cuantitativo para los beneficios de la gestión proactiva del control de enfermedades silvestres Resumen Uno de los mayores retos en la actualidad es encontrar estrategias eficaces de mitigación de patógenos. En el contexto de la fauna silvestre, las enfermedades infecciosas emergentes han causado en varias ocasiones una morbilidad generalizada de los hospedadores y el declive de las poblaciones de numerosos taxones. En zonas aún no afectadas por un patógeno, un enfoque de gestión proactivo tiene el potencial de minimizar o prevenir la mortalidad de los hospederos. Sin embargo, en general se carece de información crítica sobre la dinámica de la enfermedad en el nuevo sistema huésped, las pruebas empíricas sobre la eficacia de las intervenciones de gestión son limitadas y faltan modelos predictivos validados. Por lo tanto, no existe un apoyo cuantitativo para identificar intervenciones de gestión eficaces y a menudo se pierde la oportunidad de una gestión proactiva. Consideramos la posible invasión del hongo quitridio Batrachochytrium salamandrivorans (Bsal), cuya aparición prevista en América del Norte supone una grave amenaza para cientos de especies de salamandras en este punto caliente de la biodiversidad mundial de salamandras. Desarrollamos y parametrizamos un modelo dinámico de ocupación multiestado para predecir la presencia de hospederos y patógenos, tras la aparición esperada del patógeno, y evaluamos la respuesta de las poblaciones de salamandras a diferentes escenarios de gestión. Nuestro modelo predijo que no tomar ninguna medida sería catastrófico para las poblaciones de salamandras. También predijo que la acción proactiva maximizaría los resultados de ocupación de hospederos en relación con la gestión reactiva de esperar y ver, proporcionando así un apoyo cuantitativo a las oportunidades de gestión proactiva. La erradicación de Bsal fue improbable bajo todas las opciones de gestión evaluadas. Contrariamente a nuestras expectativas, incluso la detección temprana del patógeno tuvo poco efecto sobre los resultados de ocupación de Bsal o del hospedador. Nuestros resultados apoyan cuantitativamente a la gestión proactiva como la estrategia óptima para promover la persistencia de poblaciones de salamandras amenazadas por la enfermedad. Nuestro enfoque llena un vacío crítico al definir un marco para evaluar las opciones de gestión antes de la invasión de patógenos y, por lo tanto, puede servir como plantilla para hacer frente a nuevas amenazas de enfermedades que ponen en peligro la vida silvestre y la salud humana.

Integrating adult occurrence and reproduction data to identify conservation measures for amphibians.

Monitoring programs are pivotal to establishing sound management. Due to economic, logistic, and time limitations, monitoring programs often overlook differences among life-history stages. However, species occurrence does not necessarily mean population viability, and it is unclear to what extent monitoring programs that do not consider separately adult presence and reproduction provide effective management indications. Unfortunately, collecting data on certain life stages requires high sampling effort, leading to a trade-off between model reliability and resources needed for monitoring. We collected data on presence and reproduction of amphibians by monitoring 207 waterbodies in Lombardy (northern Italy) in 2017-2022. We then used multistate occupancy models to test whether certain environmental features, namely, pond area, hydroperiod, forest cover, shade, aquatic vegetation, and predators' presence, differentially affected adult occurrence and breeding probabilities of multiple amphibian species. To assess optimal sampling efforts, we modeled the detection probabilities of adults and reproduction across multiple species. Finally, we identified the optimal monitoring strategy under different scenarios of resource availability, comparing adult-only monitoring versus joint assessment of the occurrence of adults and reproduction. In many cases, the main drivers of adult occurrence and reproduction did not coincide because most investigated ecological variables affected one life stage or the other. Forest area, for instance, increased occurrence probabilities of adults of the endemic Rana latastei but showed no effect on their reproduction probabilities. Quantitative estimates of the sampling effort showed that occurrence of adults was easier to spot in 4 out of 7 species. Multicriteria decision analyses showed that when resources were scarce, monitoring adults was the optimal strategy for those 4 species. Conversely, with more resources, monitoring both adults and reproduction emerged as the best strategy for all the considered species. Integrated monitoring of adults and reproduction is essential to comprehensively identify effective conservation measures for amphibians.

Integración de datos de presencia adulta y de reproducción para identificar medidas de conservación para los anfibios Resumen Los programas de monitoreo son fundamentales para establecer una gestión adecuada. Debido a limitaciones económicas, logísticas y de tiempo, los programas de seguimiento suelen pasar por alto las diferencias entre las distintas fases del ciclo de vida. Sin embargo, la presencia de especies no significa necesariamente la viabilidad de la población, y no está claro hasta qué punto los programas de seguimiento que no consideran por separado la presencia de adultos y la reproducción proporcionan indicaciones eficaces para la gestión. Desgraciadamente, la recolección de datos sobre etapas determinadas del ciclo de vida requiere un gran esfuerzo de muestreo, lo que lleva a un compromiso entre la fiabilidad del modelo y los recursos necesarios para el seguimiento. Recopilamos datos sobre la presencia y reproducción de anfibios mediante el monitoreo de 207 cuerpos de agua en Lombardía (norte de Italia) entre 2017 y 2022. Después utilizamos modelos de ocupación multiestado para comprobar si determinadas características ambientales (superficie de los estanques, hidroperiodo, cubierta forestal, sombra, vegetación acuática y presencia de depredadores) afectaban de forma diferencial la presencia de adultos y a las probabilidades de reproducción de múltiples especies de anfibios. Para evaluar los esfuerzos de muestreo óptimos, modelamos las probabilidades de detección de adultos y reproducción de múltiples especies. Por último, identificamos la estrategia de seguimiento óptima en diferentes escenarios de disponibilidad de recursos y comparamos el seguimiento exclusivo de adultos frente a la evaluación conjunta de la presencia de adultos y reproducción. En muchos casos, los principales factores en la presencia de adultos y en la reproducción no coincidían, ya que la mayoría de las variables ecológicas investigadas afectaban a una u otra etapa del ciclo. La cubierta forestal, por ejemplo, aumentó la probabilidad de presencia de adultos de la especie endémica Rana latastei pero no mostraron un efecto sobre su probabilidad de reproducción. Las estimaciones cuantitativas del esfuerzo de muestreo mostraron que la presencia de adultos era más fácil de detectar en cuatro de las siete especies. Los análisis de decisión multicriterio mostraron que, cuando los recursos eran escasos, el seguimiento de los adultos era la estrategia óptima para esas cuatro especies. Por el contrario, con más recursos, el seguimiento tanto de los adultos como de la reproducción resultó ser la mejor estrategia para todas las especies consideradas. El seguimiento integrado de los adultos y la reproducción es esencial para identificar de forma exhaustiva medidas de conservación eficaces para los anfibios.

Prioritizing the reassessment of data-deficient species on the IUCN Red List.

Despite being central to the implementation of conservation policies, the usefulness of the International Union for Conservation of Nature (IUCN) Red List of Threatened Species is hampered by the 14% of species classified as data-deficient (DD) because information to evaluate these species' extinction risk was lacking when they were last assessed or because assessors did not appropriately account for uncertainty. Robust methods are needed to identify which DD species are more likely to be reclassified in one of the data-sufficient IUCN Red List categories. We devised a reproducible method to help red-list assessors prioritize reassessment of DD species and tested it with 6887 DD species of mammals, reptiles, amphibians, fishes, and Odonata (dragonflies and damselflies). For each DD species in these groups, we calculated its probability of being classified in a data-sufficient category if reassessed today from covariates measuring available knowledge (e.g., number of occurrence records or published articles available), knowledge proxies (e.g., remoteness of the range), and species characteristics (e.g., nocturnality); calculated change in such probability since last assessment from the increase in available knowledge (e.g., new occurrence records); and determined whether the species might qualify as threatened based on recent rate of habitat loss determined from global land-cover maps. We identified 1907 species with a probability of being reassessed in a data-sufficient category of >0.5; 624 species for which this probability increased by >0.25 since last assessment; and 77 species that could be reassessed as near threatened or threatened based on habitat loss. Combining these 3 elements, our results provided a list of species likely to be data-sufficient such that the comprehensiveness and representativeness of the IUCN Red List can be improved.

Priorización de la reevaluación de las especies con datos deficientes en la Lista Roja de la UICN Resumen No obstante que es fundamental para la implementación de políticas de conservación, la utilidad de la Lista Roja de Especies Amenazadas de la Unión Internacional para la Conservación de la Naturaleza (UICN) está limitada por el 14% de especies clasificadas con datos deficientes (DD) debido a que la información para evaluar el riesgo de extinción de estas especies no existía cuando fueron evaluadas la última vez o porque los evaluadores no consideraron la incertidumbre apropiadamente. Se requieren métodos robustos para identificar las especies DD con mayor probabilidad de ser reclasificadas en alguna de las categorías en la Lista Roja UICN con datos suficientes. Diseñamos un método reproducible para ayudar a que los evaluadores de la lista roja prioricen la reevaluación de especies DD y lo probamos con 6,887 especies DD de mamíferos, reptiles, anfibios, peces y Odonata (libélulas y caballitos del diablo). Para cada una de las especies DD en estos grupos, calculamos la probabilidad de ser clasificadas en una categoría con datos suficientes si fuera reevaluada hoy a partir de covariables que miden el conocimiento disponible (e.g., número de registros de ocurrencia o artículos publicados disponibles), sustitutos de conocimiento (e.g., extensión del rango de distribución) y características de la especie ((e.g., nocturnidad); calculamos el cambio en tal probabilidad desde la última reevaluación a partir del incremento en el conocimiento disponible (e.g., registros de ocurrencia nuevos); y determinamos si las especies podrían calificar como amenazadas con base en pérdidas de hábitat recientes a partir de mapas globales de cobertura de suelo recientes. Identificamos 1,907 especies con una probabilidad >0.5 de ser reclasificados en una categoría con datos suficientes; 624 especies cuya probabilidad aumentó en >0.25 desde la última evaluación, y 77 especies que podrían ser reclasificadas como casi en peligro con base en la pérdida de hábitat. Combinando estos 3 elementos, nuestros resultados proporcionaron una lista de especies probablemente con datos suficientes de tal modo que la exhaustividad y la representatividad de la Lista Roja de la UICN pueden ser mejoradas.

Effect of glyphosate and ciprofloxacin exposure on enteric bacteria of tadpoles.

The high load of agrochemicals and antibiotics present in agricultural aquatic environments represents a risk for wildlife. Since enteric bacteria, which play a key role in the physiological functioning of their hosts, are sensitive to a wide variety of pollutants, their study allows to evaluate the health of organisms. This study aimed to evaluate the effects of commercial formulations of a glyphosate-based herbicide (GBH) and the antibiotic ciprofloxacin (CIP), individually and in mixture, on the bacterial diversity of the intestinal content of common toad (Rhinella arenarum) tadpoles. The diversity of cultivable fast-growing bacteria with low nutritional requirements was evaluated using classic microbiological tests and matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry identification. Bacterial diversity varied among treatments. Taxa diversity increased in the GBH-treated group but decreased in the CIP-treated group. Remarkably, Yersinia spp. and Proteus spp. were only found in the GBH-treated group. The prevalence of Klebsiella spp. and Pseudomonas spp. decreased in the intestinal microbiota of the GBH-CIP-treated group. To our knowledge, this is the first report on the alteration of cultivable enteric bacteria of autochthonous tadpoles due to two pollutants of emerging concern. Our results demonstrate that R. arenarum tadpoles can be used as non-conventional model organisms for environmental pollution monitoring. Our preliminary findings would contribute to understanding how the presence of GBH and CIP in freshwaters may represent a threat to wildlife and human health by causing enteric dysbiosis of part of the bacterial community.

Effects of bioenergy on biodiversity arising from land-use change and crop type.

Understanding how the world's flora and fauna will respond to bioenergy expansion is critical. This issue is particularly pronounced considering bioenergy's potential role as a driver of land-use change, the variety of production crops being considered and currently used for biomass, and the diversity of ecosystems that can potentially supply land for bioenergy across the planet. We conducted 2 global meta-analyses to determine how 8 of the most commonly used bioenergy crops may affect site-level biodiversity. One search was directed at finding data on biodiversity in different production land uses and the other at extracting energy-yield estimates of potential bioenergy crops. We used linear mixed-effect models to test whether effects on biodiversity varied with different individual bioenergy crop species, estimated energy yield, first- or second-generation crops, type of reference ecosystem considered, and magnitude of vertical change in habitat structure between any given crop and the reference ecosystem. Species diversity and abundance were generally lower in crops considered for bioenergy relative to the natural ecosystems they may replace. First-generation crops, derived from oils, sugars, and starches, tended to have greater effects than second-generation crops, derived from lignocellulose, woody crops, or residues. Crop yield had nonlinear effects on abundance and, to a lesser extent, overall biodiversity; biodiversity effects were driven by negative yield effects for birds but not other taxa. Our results emphasize that replacing natural ecosystems with bioenergy crops across the planet will largely be detrimental for biodiversity, with first generation and high-yield crops having the strongest negative effects. We argue that meeting energy goals with bioenergy using existing marginal lands or biomass extraction within existing production landscapes may provide more biodiversity-friendly alternatives than conversion of natural ecosystems for biofuel production.

RESUMEN: Es de suma importancia entender cómo responderán la flora y la fauna mundial ante la expansión de la bioenergía. Este tema es acentuado particularmente si consideramos el papel potencial que tiene la bioenergía como causante del cambio en el uso de suelo, la variedad de producción de cultivos que se está considerando y que se usa actualmente para la biomasa y la diversidad de ecosistemas que potencialmente pueden proporcionar tierras para la bioenergía en todo el planeta. Realizamos dos meta-análisis mundiales para determinar cómo ocho de los cultivos que se usan con mayor frecuencia para la bioenergía podrían afectar a la biodiversidad a nivel de sitio. Una búsqueda estuvo dirigida al hallazgo de datos sobre la biodiversidad en diferentes usos de suelo para producción y la otra hacia la extracción de estimaciones de producción de energía de los cultivos potenciales para la bioenergía. Usamos modelos de efectos lineales mixtos para probar si los efectos sobre la biodiversidad variaron con diferentes especies individuales de cultivos para bioenergía, la producción de energía estimada, los cultivos de primera o segunda generación, el tipo de ecosistema de referencia considerado y la magnitud del cambio vertical en la estructura del hábitat entre cualquier cultivo dado y el ecosistema de referencia. La diversidad y la abundancia de especies fueron generalmente más bajas para los cultivos considerados para la bioenergía en relación con el ecosistema natural que podrían reemplazar. Los cultivos de primera generación, derivados de aceites, azúcares y almidones, tendieron a tener efectos más grandes que los cultivos de segunda generación, derivados de la lignocelulosa, cultivos leñosos o residuos. La producción de cultivos tuvo efectos no lineales sobre la abundancia y, a una menor extensión, sobre la biodiversidad en general; los efectos de la biodiversidad fueron causados por los efectos negativos de producción para las aves pero no para otros taxones. Nuestros resultados enfatizan que el reemplazo de ecosistemas naturales por cultivos para la bioenergía en todo el planeta será considerablemente perjudicial para la biodiversidad, con los efectos negativos más fuertes ocasionados por los cultivos de primera generación o de alta producción. Argumentamos que lograr los objetivos de energía por medio de bioenergía usando las tierras marginales existentes o la extracción de biomasa dentro de paisajes existentes de producción puede proporcionar alternativas más amigables para la biodiversidad que la conversión de los ecosistemas naturales para la producción de biocombustibles.

Effects of the Argentine ant venom on terrestrial amphibians.

Invasive species have major impacts on biodiversity and are one of the primary causes of amphibian decline and extinction. Unlike other top ant invaders that negatively affect larger fauna via chemical defensive compounds, the Argentine ant (Linepithema humile) does not have a functional sting. Nonetheless, it deploys defensive compounds against competitors and adversaries. We estimated levels of ant aggression toward 3 native terrestrial amphibians by challenging juveniles in field ant trails and in lab ant foraging arenas. We measured the composition and quantities of toxin in L. humile by analyzing pygidial glands and whole-body contents. We examined the mechanisms of toxicity in juvenile amphibians by quantifying the toxin in amphibian tissues, searching for histological damages, and calculating toxic doses for each amphibian species. To determine the potential scope of the threat to amphibians, we used global databases to estimate the number, ranges, and conservation status of terrestrial amphibian species with ranges that overlap those of L. humile. Juvenile amphibians co-occurring spatially and temporally with L. humile die when they encounter L. humile on an ant trail. In the lab, when a juvenile amphibian came in contact with L. humile the ants reacted quickly to spray pygidial-gland venom onto the juveniles. Iridomyrmecin was the toxic compound in the spray. Following absorption, it accumulated in brain, kidney, and liver tissue. Toxic dose for amphibian was species dependent. Worldwide, an estimated 817 terrestrial amphibian species overlap in range with L. humile, and 6.2% of them are classified as threatened. Our findings highlight the high potential of L. humile venom to negatively affect amphibian juveniles and provide a basis for exploring the largely overlooked impacts this ant has in its wide invasive range.

Efectos del Veneno de la Hormiga Argentina sobre los Anfibios Terrestres Resumen Las especies invasoras tienen un impacto importante sobre la biodiversidad y son una de las causas principales del declive y extinción de los anfibios. A diferencia de otras hormigas super-invasoras que afectan negativamente a animales más grandes por medio de compuestos químicos de defensa, la hormiga argentina (Linepithema humile) no tiene unaguijón funcional. Sin embargo, esta hormiga despliega compuestos defensivos contra sus competidores y adversarios. Estimamos los niveles de agresión de las hormigas hacia tres anfibios terrestres nativos exponiendo a los anfibios juveniles en pistas de hormigas en el campo y en las arenas de forrajeo de las hormigas en el laboratorio. Medimos la composición y las cantidades de toxina que presenta L. humile por medio del análisis de las glándulas pigidiales y el contenido en el cuerpo completo. Examinamos los mecanismos de la toxicidad en los anfibios juveniles cuantificando la toxina en el tejido del anfibio, buscando daños histológicos y calculando las dosis tóxicas para cada especie de anfibio. Para determinar el alcance potencial de la amenaza para los anfibios usamos bases de datos mundiales para estimar el número, distribución y estado de conservación de las especies terrestres de anfibios con distribuciones que se solapan con la de L. humile. Los anfibios juveniles que co-ocurren temporal y espacialmente con L. humile mueren al encontrarse con esta especie de hormiga en sus pistas. En el laboratorio, cuando un anfibio juvenil entró en contacto con L. humile, las hormigas reaccionaron rápidamente rociando a estos juveniles con veneno proveniente de las glándulas pigidiales. La iridomyrmecina fue el compuesto tóxico que encontramos en las glándulas pigidiales. Después de ser absorbida por la piel del anfibio, se acumuló en el cerebro, los riñones y el hígado. La dosis tóxica para los anfibios depende de la especie. A nivel mundial, se estima que 817 especies de anfibios terrestres tienen una distribución que se solapa con la de L. humile, y el 6.2% de estas especies se encuentran clasificadas como amenazadas. Nuestros hallazgos resaltan el potencial alto del veneno de L. humile para tener efectos negativos sobre los anfibios juveniles y también proporcionan una base para la exploración de los impactos de esta hormiga en su amplio rango invasivo, los cuales generalmente son ignorados.

A framework for evaluating the impact of the IUCN Red List of threatened species.

The International Union for Conservation of Nature (IUCN) Red List of Threatened Species, a species extinction risk assessment tool, has been guiding conservation efforts for over 5 decades. It is widely assumed to have been instrumental in preventing species from moving closer to extinction and driving recoveries. However, the impact of the IUCN Red List in guiding conservation has not been evaluated. We conducted, transcribed, and coded interviews with experts who use the IUCN Red List across a range of sectors to understand how the list is used in conservation. We developed a theory of change to illustrate how and why change is expected to occur along causal pathways contributing to the long-term goal of the IUCN Red List and an evaluation framework with indicators for measuring the impact of the IUCN Red List in generating scientific knowledge, raising awareness among stakeholders, designating priority conservation sites, allocating funding and resources, influencing development of legislation and policy, and guiding targeted conservation action (key themes). Red-list assessments were the primary input leading to outputs (scientific knowledge, raised awareness), outcomes (better informed priority setting, access to funding and resource availability, improved legislation and policy), and impact (implemented conservation action leading to positive change) that have resulted in achievement of IUCN Red List goals. To explore feasibility of attributing the difference made by the IUCN Red List across themes, we studied increased scientific knowledge, raised awareness, access to funding and resource allocation, and increased conservation activity. The feasibility exploration showed increased scientific knowledge over time identified through positive trends in publications referring to the IUCN Red List in the literature; raised awareness of the list following high IUCN activity identified by peaks in online search activity; an increased proportion of conservation funding bodies requesting IUCN Red List status in the application process; and, based on interviews with Amphibian Specialist Group members, red-list assessments were essential in connecting relevant stakeholders and ensuring conservation action. Although we identified the IUCN Red List as a vital tool in global conservation efforts, it was challenging to measure specific impacts because of its ubiquitous nature. We are the first to identify the influence of the IUCN Red List on conservation.

Un Marco de Referencia para la Evaluación del Impacto de la Lista Roja de Especies Amenazadas de la UICN Resumen La Lista Roja de Especies Amenazadas de la Unión Internacional para la Conservación de la Naturaleza (UICN), una herramienta para la valoración del riesgo de extinción de las especies ha guiado los esfuerzos de conservación durante más de cinco décadas. A partir de esto, se ha asumido como generalidad que la lista ha sido determinante para prevenir que las especies se acerquen más a la extinción y para impulsar la recuperación de especies. Sin embargo, todavía no se ha evaluado el impacto que la Lista Roja de la UICN ha tenido en las directrices de la conservación. Realizamos, transcribimos y codificamos entrevistas con expertos que usan la Lista Roja de la UICN en una gama de sectores para así entender cómo se usa la lista para la conservación. Desarrollamos una teoría de cambio para ilustrar cómo y por qué se espera que ocurra un cambio en Atorno a las vías causales que contribuyen al objetivo de largo plazo que tiene la Lista Roja de la UICN. También formulamos un marco de trabajo con los indicadores necesarios para evaluar el impacto que tiene la Lista Roja de la UICN en la generación de conocimiento científico, la creación de conciencia entre los actores sociales, la designación de sitios prioritarios para la conservación, la asignación de fondos y recursos, la influencia sobre el desarrollo de la legislación y de las políticas, y la orientación de acciones de conservación enfocadas (temas clave). Las evaluaciones de la lista roja fueron los aportadores principales que derivaron en resultados (conocimiento científico, creación de conciencia), consecuencias (establecimiento de prioridades mejor informadas, acceso a financiamiento y disponibilidad de recursos, mejorías en la legislación y en la política) e impactos (acciones implementadas de conservación que derivaron en cambios positivos) que han resultado en la obtención de objetivos de la Lista Roja de la UICN. Para explorar la viabilidad de la atribución de la diferencia que genera la Lista Roja de la UICN en todos los temas clave estudiamos el incremento en el conocimiento científico, la conciencia generada, el acceso a financiamientos y la asignación de recursos, y el crecimiento en las acciones de conservación. Esta exploración de la viabilidad mostró un incremento con el tiempo del conocimiento científico, identificado por medio de tendencias positivas en las publicaciones de la literatura referidas a la Lista Roja de la UICN. También mostró una mayor conciencia por la lista tras una alta actividad de la UICN, la cual identificamos por medio de picos en la actividad de búsqueda en línea. Finalmente, la exploración arrojó una proporción crecida de organizaciones de financiamiento para la conservación que solicitaron el estado de la especie en la Lista Roja de la UICN durante el proceso de aplicación y, con base en entrevistas realizadas a miembros del Grupo Especialista en Anfibios, que las valoraciones de la lista roja fueron esenciales para conectar entre sí a los actores relevantes y para asegurar las acciones de conservación. Aunque identificamos que la Lista Roja de la UICN es una herramienta vital para los esfuerzos mundiales de conservación, fue todo un reto medir los impactos específicos debido a su naturaleza ubicua. Somos los primeros en identificar la influencia que tiene la Lista Roja de la UICN sobre la conservación.

Use of stochastic patch occupancy models in the California red-legged frog for Bayesian inference regarding past events and future persistence.

Assessing causes of population decline is critically important to management of threatened species. Stochastic patch occupancy models (SPOMs) are popular tools for examining spatial and temporal dynamics of populations when presence-absence data in multiple habitat patches are available. We developed a Bayesian Markov chain method that extends existing SPOMs by focusing on past environmental changes that may have altered occupancy patterns prior to the beginning of data collection. Using occupancy data from 3 creeks, we applied the method to assess 2 hypothesized causes of population decline-in situ die-off and residual impact of past source population loss-in the California red-legged frog. Despite having no data for the 20-30 years between the hypothetical event leading to population decline and the first data collected, we were able to discriminate among hypotheses, finding evidence that in situ die-off increased in 2 of the creeks. Although the creeks had comparable numbers of occupied segments, owing to different extinction-colonization dynamics, our model predicted an 8-fold difference in persistence probabilities of their populations to 2030. Adding a source population led to a greater predicted persistence probability than did decreasing the in situ die-off, emphasizing that reversing the deleterious impacts of a disturbance may not be the most efficient management strategy. We expect our method will be useful for studying dynamics and evaluating management strategies of many species.

Uso de Modelos Estocásticos de Ocupación de Fragmentos de la Rana Californiana de Patas Rojas para la Inferencia Bayesiana con Respecto a Eventos Pasados y su Persistencia en el Futuro Resumen La evaluación de las causas de la declinación poblacional es de importancia crítica para el manejo de especies amenazadas. Los modelos estocásticos de ocupación de parches (SPOMs, en inglés) son herramientas populares para examinar las dinámicas espaciales y temporales de las poblaciones cuando están disponibles los datos de presencia-ausencia para múltiples parches de hábitat. Desarrollamos un método bayesiano de cadena de Markov que extiende a los SPOMs existentes al enfocarse en los cambios ambientales pasados que podrían haber alterado los patrones de ocupación previos al inicio de la recolección de datos. Con los datos de ocupación de tres arroyos, aplicamos este método para evaluar dos causas hipotéticas de la declinación poblacional - muerte in situ e impacto residual de causas anteriores de pérdida de una poblacion fuente - de la rana californiana de patas rojas. A pesar de no tener datos para 20 - 30 años entre el evento hipotético que derivó en la declinación poblacional y los primeros datos recolectados, pudimos discriminar entre las hipótesis, encontrando evidencia de que la muerte in situ incrementó en dos de los arroyos. Aunque los arroyos tuvieron un número comparable de segmentos ocupados, debido a diferentes dinámicas de colonización - extinción, nuestro modelo predijo una diferencia ocho veces mayor en las probabilidades de persistencia de las poblaciones hasta el 2030. La suma de una población fuente resultó en una mayor probabilidad de persistencia pronosticada que con la reducción de la muerte in situ, enfatizando que la reversión de los impactos dañinos de una perturbación puede no ser la mejor estrategia de manejo. Esperamos que nuestro método sea útil para el estudio de las dinámicas y para la evaluación de las estrategias de manejo de muchas especies.

Patterns and biases of climate change threats in the IUCN Red List.

International Union for Conservation of Nature (IUCN) Red List assessments rely on published data and expert inputs, and biases can be introduced where underlying definitions and concepts are ambiguous. Consideration of climate change threat is no exception, and recently numerous approaches to assessing the threat of climate change to species have been developed. We explored IUCN Red List assessments of amphibians and birds to determine whether species listed as threatened by climate change display distinct patterns in terms of habitat occupied and additional nonclimatic threats faced. We compared IUCN Red List data with a published data set of species' biological and ecological traits believed to infer high vulnerability to climate change and determined whether distributions of climate change-threatened species on the IUCN Red List concur with those of climate change-threatened species identified with the trait-based approach and whether species possessing these traits are more likely to have climate change listed as a threat on the IUCN Red List. Species in some ecosystems (e.g., grassland, shrubland) and subject to particular threats (e.g., invasive species) were more likely to have climate change as a listed threat. Geographical patterns of climate change-threatened amphibians and birds on the IUCN Red List were incongruent with patterns of global species richness and patterns identified using trait-based approaches. Certain traits were linked to increases or decreases in the likelihood of a species being threatened by climate change. Broad temperature tolerance of a species was consistently related to an increased likelihood of climate change threat, indicating counterintuitive relationships in IUCN assessments. To improve the robustness of species assessments of the vulnerability or extinction risk associated with climate change, we suggest IUCN adopt a more cohesive approach whereby specific traits highlighted by our results are considered in Red List assessments. To achieve this and to strengthen the climate change-vulnerability assessments approach, it is necessary to identify and implement logical avenues for further research into traits that make species vulnerable to climate change (including population-level threats).

Practitioner and scientist perceptions of successful amphibian conservation.

Conservation requires successful outcomes. However, success is perceived in many different ways depending on the desired outcome. Through a questionnaire survey, we examined perceptions of success among 355 scientists and practitioners working on amphibian conservation from over 150 organizations in more than 50 countries. We also sought to identify how different types of conservation actions and respondent experience and background influenced perceptions. Respondents identified 4 types of success: species and habitat improvements (84% of respondents); effective program management (36%); outreach initiatives such as education and public engagement (25%); and the application of science-based conservation (15%). The most significant factor influencing overall perceived success was reducing threats. Capacity building was rated least important. Perceptions were influenced by experience, professional affiliation, involvement in conservation practice, and country of residence. More experienced practitioners associated success with improvements to species and habitats and less so with education and engagement initiatives. Although science-based conservation was rated as important, this factor declined in importance as the number of programs a respondent participated in increased, particularly among those from less economically developed countries. The ultimate measure of conservation success-population recovery-may be difficult to measure in many amphibians; difficult to relate to the conservation actions intended to drive it; and difficult to achieve within conventional funding time frames. The relaunched Amphibian Conservation Action Plan provides a framework for capturing lower level processes and outcomes, identifying gaps, and measuring progress.

A test of the substitution-habitat hypothesis in amphibians.

Most examples that support the substitution-habitat hypothesis (human-made habitats act as substitutes of original habitat) deal with birds and mammals. We tested this hypothesis in 14 amphibians by using percentage occupancy as a proxy of habitat quality (i.e., higher occupancy percentages indicate higher quality). We classified water body types as original habitat (no or little human influence) depending on anatomical, behavioral, or physiological adaptations of each amphibian species. Ten species had relatively high probabilities (0.16-0.28) of occurrence in original habitat, moderate probability of occurrence in substitution habitats (0.11-0.14), and low probability of occurrence in refuge habitats (0.05-0.08). Thus, the substitution-habitat hypothesis only partially applies to amphibians because the low occupancy of refuges could be due to the negligible human persecution of this group (indicating good conservation status). However, low occupancy of refuges could also be due to low tolerance of refuge conditions, which could have led to selective extinction or colonization problems due to poor dispersal capabilities. That original habitats had the highest probabilities of occupancy suggests amphibians have a good conservation status in the region. They also appeared highly adaptable to anthropogenic substitution habitats.

Toward reassessing data-deficient species.

One in 6 species (13,465 species) on the International Union for Conservation of Nature (IUCN) Red List is classified as data deficient due to lack of information on their taxonomy, population status, or impact of threats. Despite the chance that many are at high risk of extinction, data-deficient species are typically excluded from global and local conservation priorities, as well as funding schemes. The number of data-deficient species will greatly increase as the IUCN Red List becomes more inclusive of poorly known and speciose groups. A strategic approach is urgently needed to enhance the conservation value of data-deficient assessments. To develop this, we reviewed 2879 data-deficient assessments in 6 animal groups and identified 8 main justifications for assigning data-deficient status (type series, few records, old records, uncertain provenance, uncertain population status or distribution, uncertain threats, taxonomic uncertainty, and new species). Assigning a consistent set of justification tags (i.e., consistent assignment to assessment justifications) to species classified as data deficient is a simple way to achieve more strategic assessments. Such tags would clarify the causes of data deficiency; facilitate the prediction of extinction risk; facilitate comparisons of data deficiency among taxonomic groups; and help prioritize species for reassessment. With renewed efforts, it could be straightforward to prevent thousands of data-deficient species slipping unnoticed toward extinction.

Developments in amphibian captive breeding and reintroduction programs.

Captive breeding and reintroduction remain high profile but controversial conservation interventions. It is important to understand how such programs develop and respond to strategic conservation initiatives. We analyzed the contribution to conservation made by amphibian captive breeding and reintroduction since the launch of the International Union for Conservation of Nature (IUCN) Amphibian Conservation Action Plan (ACAP) in 2007. We assembled data on amphibian captive breeding and reintroduction from a variety of sources including the Amphibian Ark database and the IUCN Red List. We also carried out systematic searches of Web of Science, JSTOR, and Google Scholar for relevant literature. Relative to data collected from 1966 to 2006, the number of species involved in captive breeding and reintroduction projects increased by 57% in the 7 years since release of the ACAP. However, there have been relatively few new reintroductions over this period; most programs have focused on securing captive-assurance populations (i.e., species taken into captivity as a precaution against extinctions in the wild) and conservation-related research. There has been a shift to a broader representation of frogs, salamanders, and caecilians within programs and an increasing emphasis on threatened species. There has been a relative increase of species in programs from Central and South America and the Caribbean, where amphibian biodiversity is high. About half of the programs involve zoos and aquaria with a similar proportion represented in specialist facilities run by governmental or nongovernmental agencies. Despite successful reintroduction often being regarded as the ultimate milestone for such programs, the irreversibility of many current threats to amphibians may make this an impractical goal. Instead, research on captive assurance populations may be needed to develop imaginative solutions to enable amphibians to survive alongside current, emerging, and future threats.

Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations.

Contributing to the worldwide biodiversity crisis are emerging infectious diseases, which can lead to extirpations and extinctions of hosts. For example, the infectious fungal pathogen Batrachochytrium dendrobatidis (Bd) is associated with worldwide amphibian population declines and extinctions. Sensitivity to Bd varies with species, season, and life stage. However, there is little information on whether sensitivity to Bd differs among populations, which is essential for understanding Bd-infection dynamics and for formulating conservation strategies. We experimentally investigated intraspecific differences in host sensitivity to Bd across 10 populations of wood frogs (Lithobates sylvaticus) raised from eggs to metamorphosis. We exposed the post-metamorphic wood frogs to Bd and monitored survival for 30 days under controlled laboratory conditions. Populations differed in overall survival and mortality rate. Infection load also differed among populations but was not correlated with population differences in risk of mortality. Such population-level variation in sensitivity to Bd may result in reservoir populations that may be a source for the transmission of Bd to other sensitive populations or species. Alternatively, remnant populations that are less sensitive to Bd could serve as sources for recolonization after epidemic events.

Effects of pond salinization on survival rate of amphibian hosts infected with the chytrid fungus.

The chytrid fungus Batrachochytrium dendrobatidis has been implicated in the decline and extinction of amphibian populations worldwide, but management options are limited. Recent studies show that sodium chloride (NaCl) has fungicidal properties that reduce the mortality rates of infected hosts in captivity. We investigated whether similar results can be obtained by adding salt to water bodies in the field. We increased the salinity of 8 water bodies to 2 or 4 ppt and left an additional 4 water bodies with close to 0 ppt and monitored salinity for 18 months. Captively bred tadpoles of green and golden bell frog (Litoria aurea) were released into each water body and their development, levels of B. dendrobatidis infection, and survival were monitored at 1, 4, and 12 months. The effect of salt on the abundance of nontarget organisms was also investigated in before and after style analyses. Salinities remained constant over time with little intervention. Hosts in water bodies with 4 ppt salt had a significantly lower prevalence of chytrid infection and higher survival, following metamorphosis, than hosts in 0 ppt salt. Tadpoles in the 4 ppt group were smaller in length after 1 month in the release site than those in the 0 and 2 ppt groups, but after metamorphosis body size in all water bodies was similar . In water bodies with 4 ppt salt, the abundance of dwarf tree frogs (Litoria fallax), dragonfly larvae, and damselfly larvae was lower than in water bodies with 0 and 2 ppt salt, which could have knock-on effects for community structure. Based on our results, salt may be an effective field-based B. dendrobatidis mitigation tool for lentic amphibians that could contribute to the conservation of numerous susceptible species. However, as in all conservation efforts, these benefits need to be weighed against negative effects on both target and nontarget organisms.

Factors mediating co-occurrence of an economically valuable introduced fish and its native frog prey.

Habitat characteristics mediate predator-prey coexistence in many ecological systems but are seldom considered in species introductions. When economically important introduced predators are stocked despite known negative impacts on native species, understanding the role of refuges, landscape configurations, and community interactions can inform habitat management plans. We measured these factors in basins with introduced trout (Salmonidae) and the Cascades frog (Rana cascadae) to determine, which are responsible for observed patterns of co-occurrence of this economically important predator and its native prey. Large, vegetated shallows were strongly correlated to co-occurrence, and R. cascadae larvae occur in shallower water when fish are present, presumably to escape predation. The number of nearby breeding sites of R. cascadae was also correlated to co-occurrence, but only when the western toad (Anaxyrus boreas) was present. Because A. boreas larvae are unpalatable to fish and resemble R. cascadae, they may provide protection from trout via Batesian mimicry. Although rescue-effect dispersal from nearby populations may maintain co-occurrence, within-lake factors proved more important for predicting co-occurrence. Learning which factors allow co-occurrence between economically important introduced species and their native prey enables managers to make better-informed stocking decisions.

Interventions for reducing extinction risk in chytridiomycosis-threatened amphibians.

Wildlife diseases pose an increasing threat to biodiversity and are a major management challenge. A striking example of this threat is the emergence of chytridiomycosis. Despite diagnosis of chytridiomycosis as an important driver of global amphibian declines 15 years ago, researchers have yet to devise effective large-scale management responses other than biosecurity measures to mitigate disease spread and the establishment of disease-free captive assurance colonies prior to or during disease outbreaks. We examined the development of management actions that can be implemented after an epidemic in surviving populations. We developed a conceptual framework with clear interventions to guide experimental management and applied research so that further extinctions of amphibian species threatened by chytridiomycosis might be prevented. Within our framework, there are 2 management approaches: reducing Batrachochytrium dendrobatidis (the fungus that causes chytridiomycosis) in the environment or on amphibians and increasing the capacity of populations to persist despite increased mortality from disease. The latter approach emphasizes that mitigation does not necessarily need to focus on reducing disease-associated mortality. We propose promising management actions that can be implemented and tested based on current knowledge and that include habitat manipulation, antifungal treatments, animal translocation, bioaugmentation, head starting, and selection for resistance. Case studies where these strategies are being implemented will demonstrate their potential to save critically endangered species.

Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis.

Assessing the effects of diseases on wildlife populations can be difficult in the absence of observed mortalities, but it is crucial for threat assessment and conservation. We performed an intensive capture-mark-recapture study across seasons and years to investigate the effect of chytridiomycosis on demographics in 2 populations of the threatened common mist frog (Litoria rheocola) in the lowland wet tropics of Queensland, Australia. Infection prevalence was the best predictor for apparent survival probability in adult males and varied widely with season (0-65%). Infection prevalence was highest in winter months when monthly survival probabilities were low (approximately 70%). Populations at both sites exhibited very low annual survival probabilities (12-15%) but high recruitment (71-91%), which resulted in population growth rates that fluctuated seasonally. Our results suggest that even in the absence of observed mortalities and continued declines, and despite host-pathogen co-existence for multiple host generations over almost 2 decades, chytridiomycosis continues to have substantial seasonally fluctuating population-level effects on amphibian survival, which necessitates increased recruitment for population persistence. Similarly infected populations may thus be under continued threat from chytridiomycosis which may render them vulnerable to other threatening processes, particularly those affecting recruitment success.

Roles of patch characteristics, drought frequency, and restoration in long-term trends of a widespread amphibian.

Despite the high profile of amphibian declines and the increasing threat of drought and fragmentation to aquatic ecosystems, few studies have examined long-term rates of change for a single species across a large geographic area. We analyzed growth in annual egg-mass counts of the Columbia spotted frog (Rana luteiventris) across the northwestern United States, an area encompassing 3 genetic clades. On the basis of data collected by multiple partners from 98 water bodies between 1991 and 2011, we used state-space and linear-regression models to measure effects of patch characteristics, frequency of summer drought, and wetland restoration on population growth. Abundance increased in the 2 clades with greatest decline history, but declined where populations are considered most secure. Population growth was negatively associated with temporary hydroperiods and landscape modification (measured by the human footprint index), but was similar in modified and natural water bodies. The effect of drought was mediated by the size of the water body: populations in large water bodies maintained positive growth despite drought, whereas drought magnified declines in small water bodies. Rapid growth in restored wetlands in areas of historical population declines provided strong evidence of successful management. Our results highlight the importance of maintaining large areas of habitat and underscore the greater vulnerability of small areas of habitat to environmental stochasticity. Similar long-term growth rates in modified and natural water bodies and rapid, positive responses to restoration suggest pond construction and other forms of management can effectively increase population growth. These tools are likely to become increasingly important to mitigate effects of increased drought expected from global climate change. Papeles de las Características del Fragmento, Frecuencia de Sequía y Restauración en las Tendencias a Largo Plazo de un Anfibio Ampliamente Distribuido.