RESUMEN
Chytridiomycosis has been a key driver of global frog declines and extinctions, particularly for high-altitude populations across Australia and the Americas. While recent evidence shows some species are recovering, the extent of such recoveries and the mechanisms underpinning them remain poorly resolved. We surveyed the historical latitudinal and elevational range of four Australian rainforest frogs that disappeared from upland sites between 1989 and 1994 to establish their contemporary distribution and elevational limits, and investigate factors affecting population recovery. Five rainforest streams were surveyed from mountain-base to summit (30 sites in total), with swabs collected from the target species (Litoria dayi, L. nannotis, L. rheocola, and L. serrata) to determine their infection status, and data loggers deployed to measure microclimatic variation across the elevational gradient. Infection probability increased with elevation and canopy cover as it was tightly and inversely correlated with stream-side air temperature. Occupancy patterns suggest varying responses to this disease threat gradient. Two species, L. rheocola and L. serrata, were found over their full historical elevational range (≥1,000 m above sea level [asl]), while L. dayi was not detected above 400 m (formerly known up to 900 m asl) and L. nannotis was not detected above 800 m (formerly known up to 1,200 m asl). Site occupancy probability was negatively related to predicted infection prevalence for L. dayi, L. nannotis, and L. rheocola, but not L. serrata, which appears to now tolerate high fungal burdens. This study highlights the importance of environmental refuges and connectivity across disease risk gradients for the persistence and natural recovery of frogs susceptible to chytridiomycosis. Likewise, in documenting both interspecific variation in recovery rates and intraspecific differences between sites, this study suggests interactions between disease threats and host selection exist that could be manipulated. For example, translocations may be warranted where connectivity is poor or the increase in disease risk is too steep to allow recolonization, combined with assisted selection or use of founders from populations that have already undergone natural selection.
Asunto(s)
Quitridiomicetos , Micosis , Altitud , Animales , Anuros , Australia , Bosque LluviosoRESUMEN
Biodiversity offsetting schemes permit habitat destruction, provided that losses are compensated by gains elsewhere. While hundreds of offsetting schemes are used around the globe, the optimal timing of habitat creation in such projects is poorly understood. Here, we developed a spatially explicit metapopulation model for a single species subject to a habitat compensation scheme. Managers could compensate for destruction of a patch by creating a new patch either before, at the time of, or after patch loss. Delaying patch creation is intuitively detrimental to species persistence, but allowed managers to invest financial compensation, accrue interest, and create a larger patch at a later date. Using stochastic dynamic programming, we found the optimal timing of patch creation that maximizes the number of patches occupied at the end of a 50-yr habitat compensation scheme when a patch is destroyed after 10 yr. Two case studies were developed for Australian species subject to habitat loss but with very different traits: the endangered growling grass frog (Litoria raniformis) and the critically endangered Mount Lofty Ranges Southern Emu-wren (Spititurus malachurus intermedius). Our results show that adding a patch either before or well after habitat destruction can be optimal, depending on the occupancy state of the metapopulation, the interest rate, the area of the destroyed patch and metapopulation parameters of the focal species. Generally, it was better to delay patch creation when the interest rate was high, when the species had a relatively high colonization rate, when the patch nearest the new patch was occupied, and when the destroyed patch was small. Our framework can be applied to single-species metapopulations subject to habitat loss, and demonstrates that considering the timing of habitat compensation could improve the effectiveness of offsetting schemes.
Asunto(s)
Biodiversidad , Restauración y Remediación Ambiental , Modelos Biológicos , Animales , Anuros , Passeriformes , Dinámica Poblacional , Factores de TiempoRESUMEN
How should managers choose among conservation options when resources are scarce and there is uncertainty regarding the effectiveness of actions? Well-developed tools exist for prioritizing areas for one-time and binary actions (e.g., protect vs. not protect), but methods for prioritizing incremental or ongoing actions (such as habitat creation and maintenance) remain uncommon. We devised an approach that combines metapopulation viability and cost-effectiveness analyses to select among alternative conservation actions while accounting for uncertainty. In our study, cost-effectiveness is the ratio between the benefit of an action and its economic cost, where benefit is the change in metapopulation viability. We applied the approach to the case of the endangered growling grass frog (Litoria raniformis), which is threatened by urban development. We extended a Bayesian model to predict metapopulation viability under 9 urbanization and management scenarios and incorporated the full probability distribution of possible outcomes for each scenario into the cost-effectiveness analysis. This allowed us to discern between cost-effective alternatives that were robust to uncertainty and those with a relatively high risk of failure. We found a relatively high risk of extinction following urbanization if the only action was reservation of core habitat; habitat creation actions performed better than enhancement actions; and cost-effectiveness ranking changed depending on the consideration of uncertainty. Our results suggest that creation and maintenance of wetlands dedicated to L. raniformis is the only cost-effective action likely to result in a sufficiently low risk of extinction. To our knowledge we are the first study to use Bayesian metapopulation viability analysis to explicitly incorporate parametric and demographic uncertainty into a cost-effective evaluation of conservation actions. The approach offers guidance to decision makers aiming to achieve cost-effective conservation under uncertainty.
Asunto(s)
Anuros/fisiología , Conservación de los Recursos Naturales/métodos , Especies en Peligro de Extinción , Animales , Teorema de Bayes , Conservación de los Recursos Naturales/economía , Análisis Costo-Beneficio , Toma de Decisiones , Ecosistema , Dinámica Poblacional , Incertidumbre , VictoriaRESUMEN
Metapopulation persistence in fragmented landscapes depends on habitat patches that can support resilient local populations and sufficient connectivity between patches. Yet epidemiological theory for metapopulations has largely overlooked the capacity of particular patches to act as refuges from disease, and has suggested that connectivity can undermine persistence. Here, we show that relatively warm and saline wetlands are environmental refuges from chytridiomycosis for an endangered Australian frog, and act jointly with connectivity to sustain frog metapopulations. We coupled models of microclimate and infection probability to map chytrid prevalence, and demonstrate a strong negative relationship between chytrid prevalence and the persistence of frog populations. Simulations confirm that frog metapopulations are likely to go extinct when they lack environmental refuges from disease and lose connectivity between patches. This study demonstrates that environmental heterogeneity can mediate host-pathogen interactions in fragmented landscapes, and provides evidence that connectivity principally supports host metapopulations afflicted by facultative pathogens.
Asunto(s)
Anuros/microbiología , Quitridiomicetos/patogenicidad , Especies en Peligro de Extinción , Interacciones Huésped-Patógeno , Modelos Biológicos , Humedales , Animales , Australia , Extinción Biológica , Microclima , Modelos Estadísticos , Micosis/transmisión , Micosis/veterinaria , Dinámica Poblacional , Salinidad , Estrés Fisiológico , TemperaturaRESUMEN
Identifying determinants of the probability and intensity of infections is important for understanding the epidemiology of wildlife diseases, and for managing their impact on threatened species. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, has decimated populations of some amphibians. However, recent studies have identified important environmental constraints on the disease, related to the pathogen's physiological tolerances. In this study, we identified several intrinsic and extrinsic determinants of the probability and intensity of chytrid infections for the threatened growling grass frog (Litoria raniformis) in southeastern Australia, and used mark-recapture to estimate the effect of chytrid infections on the probability of survival of these frogs. Water temperature and salinity had negative effects on both the probability and intensity of chytrid infections. We coupled models of the infection process with a model of the effect of chytrid infections on the probability of survival to assess variation in the impact of chytridiomycosis between wetlands with differing temperature and salinity profiles. Our results suggest that warm, saline wetlands may be refuges from chytridiomycosis for L. raniformis, and should be priorities for protection. Our results also suggest that management actions that increase water temperature (e.g., reducing canopy shading) and salinity (e.g., complementing inflows with groundwater) could be trialed to reduce the impacts of chytridiomycosis on this species. This and other recent studies highlight the value of research on environmental risk factors for chytridiomycosis.
Asunto(s)
Quitridiomicetos , Especies en Peligro de Extinción , Micosis/veterinaria , Ranidae/microbiología , Humedales , Envejecimiento , Animales , Monitoreo del Ambiente , Micosis/microbiología , Dinámica Poblacional , Factores de Riesgo , Salinidad , TemperaturaRESUMEN
Anthropogenic climate change is a key threat to global biodiversity. To inform strategic actions aimed at conserving biodiversity as climate changes, conservation planners need early warning of the risks faced by different species. The IUCN Red List criteria for threatened species are widely acknowledged as useful risk assessment tools for informing conservation under constraints imposed by limited data. However, doubts have been expressed about the ability of the criteria to detect risks imposed by potentially slow-acting threats such as climate change, particularly because criteria addressing rates of population decline are assessed over time scales as short as 10 years. We used spatially explicit stochastic population models and dynamic species distribution models projected to future climates to determine how long before extinction a species would become eligible for listing as threatened based on the IUCN Red List criteria. We focused on a short-lived frog species (Assa darlingtoni) chosen specifically to represent potential weaknesses in the criteria to allow detailed consideration of the analytical issues and to develop an approach for wider application. The criteria were more sensitive to climate change than previously anticipated; lead times between initial listing in a threatened category and predicted extinction varied from 40 to 80 years, depending on data availability. We attributed this sensitivity primarily to the ensemble properties of the criteria that assess contrasting symptoms of extinction risk. Nevertheless, we recommend the robustness of the criteria warrants further investigation across species with contrasting life histories and patterns of decline. The adequacy of these lead times for early warning depends on practicalities of environmental policy and management, bureaucratic or political inertia, and the anticipated species response times to management actions.
Asunto(s)
Cambio Climático , Conservación de los Recursos Naturales , Extinción Biológica , Animales , Anuros , Australia , Biodiversidad , Especies en Peligro de Extinción , Política Ambiental , Medición de RiesgoRESUMEN
Deepening droughts and unprecedented wildfires are at the leading edge of climate change. Such events pose an emerging threat to species maladapted to these perturbations, with the potential for steeper declines than may be inferred from the gradual erosion of their climatic niche. This study focused on two species of amphibians-Philoria kundagungan and Philoria richmondensis (Limnodynastidae)-from the Gondwanan rainforests of eastern Australia that were extensively affected by the "Black Summer" megafires of 2019/2020 and the severe drought associated with them. We sought to assess the impact of these perturbations by quantifying the extent of habitat affected by fire, assessing patterns of occurrence and abundance of calling males post-fire, and comparing post-fire occurrence and abundance with that observed pre-fire. Some 30% of potentially suitable habitat for P. kundagungan was fire affected, and 12% for P. richmondensis. Field surveys revealed persistence in some burnt rainforest; however, both species were detected at a higher proportion of unburnt sites. There was a clear negative effect of fire on the probability of site occupancy, abundance and the probability of persistence for P. kundagungan. For P. richmondensis, effects of fire were less evident due to the limited penetration of fire into core habitat; however, occupancy rates and abundance of calling males were depressed during the severe drought that prevailed just prior to the fires, with the reappearance of calling males linked to the degree of rehydration of breeding habitat post-fire. Our results highlight the possibility that severe negative impacts of climate change for montane rainforest endemics may be felt much sooner than commonly anticipated under a scenario of gradual (decadal-scale) changes in mean climatic conditions. Instead, the increased rate of severe stochastic events places these narrow range species at a heightened risk of extinction in the near-term.
RESUMEN
Global change is causing an unprecedented restructuring of ecosystems, with the spread of invasive species being a key driver. While population declines of native species due to invasives are well documented, much less is known about whether new biotic interactions reshape niches of native species. Here we quantify geographic range and realized-niche contractions in Australian frog species following the introduction of amphibian chytrid fungus Batrachochytrium dendrobatidis, a pathogen responsible for catastrophic amphibian declines worldwide. We show that chytrid-impacted species experienced proportionately greater contractions in niche breadth than geographic distribution following chytrid emergence. Furthermore, niche contractions were directional, with contemporary distributions of chytrid-impacted species characterized by higher temperatures, lower diurnal temperature range, higher precipitation and lower elevations. Areas with these conditions may enable host persistence with chytrid through lower pathogenicity of the fungus and/or greater demographic resilience. Nevertheless, contraction to a narrower subset of environmental conditions could increase host vulnerability to other threatening processes and should be considered in assessments of extinction risk and during conservation planning. More broadly, our results emphasize that biotic interactions can strongly shape species realized niches and that large-scale niche contractions due to new species interactions-particularly emerging pathogens-could be widespread.
Asunto(s)
Quitridiomicetos , Micosis , Animales , Ecosistema , Micosis/veterinaria , Micosis/epidemiología , Micosis/microbiología , Australia , AnurosRESUMEN
Spatial and temporal partitioning of resources underlies the coexistence of species with similar niches. In communities of frogs and toads, the phenology of advertisement calling provides insights into temporal partitioning of reproductive effort and its implications for community dynamics. This study assessed the phenology of advertisement calling in an anuran community from Melbourne, in southern Australia. We collated data from 1432 surveys of 253 sites and used logistic regression to quantify seasonality in the nightly probability of calling and the influence of meteorological variables on this probability for six species of frogs. We found limited overlap in the predicted seasonal peaks of calling among these species. Those shown to have overlapping calling peaks are unlikely to be in direct competition, due to differences in larval ecology (Crinia signifera and Litoria ewingii) or differences in calling behavior and acoustics (Limnodynastes dumerilii and Litoria raniformis). In contrast, closely related and ecologically similar species (Crinia signfera and Crinia parinsignifera;Litoria ewingii and Litoria verreauxii) appear to have staggered seasonal peaks of calling. In combination with interspecific variation in the meteorological correlates of calling, these results may be indicative of temporal partitioning of reproductive activity to facilitate coexistence, as has been reported for tropical and temperate anurans from other parts of the globe.
RESUMEN
Occupancy surveys should be designed to minimise false absences. This is commonly achieved by increasing replication or increasing the efficiency of surveys. In the case of destructive sampling designs, in which searches of individual microhabitats represent the repeat surveys, minimising false absences leads to an inherent trade-off. Surveyors can sample more low quality microhabitats, bearing the resultant financial costs and producing wider-spread impacts, or they can target high quality microhabitats were the focal species is more likely to be found and risk more severe impacts on local habitat quality. We show how this trade-off can be solved with a decision-theoretic approach, using the Millewa Skink Hemiergis millewae from southern Australia as a case study. Hemiergis millewae is an endangered reptile that is best detected using destructive sampling of grass hummocks. Within sites that were known to be occupied by H. millewae, logistic regression modelling revealed that lizards were more frequently detected in large hummocks. If this model is an accurate representation of the detection process, searching large hummocks is more efficient and requires less replication, but this strategy also entails destruction of the best microhabitats for the species. We developed an optimisation tool to calculate the minimum combination of the number and size of hummocks to search to achieve a given cumulative probability of detecting the species at a site, incorporating weights to reflect the sensitivity of the results to a surveyor's priorities. The optimisation showed that placing high weight on minimising volume necessitates impractical replication, whereas placing high weight on minimising replication requires searching very large hummocks which are less common and may be vital for H. millewae. While destructive sampling methods are sometimes necessary, surveyors must be conscious of the ecological impacts of these methods. This study provides a simple tool for identifying sampling strategies that minimise those impacts.
Asunto(s)
Modelos Logísticos , Reptiles , Animales , Australia , Especies en Peligro de Extinción , Humanos , Modelos Teóricos , Dinámica Poblacional , Encuestas y CuestionariosRESUMEN
Two pervasive and fundamental impacts of urbanization are the loss and fragmentation of natural habitats. From a genetic perspective, these impacts manifest as reduced genetic diversity and ultimately reduced genetic viability. The growling grass frog (Litoria raniformis) is listed as vulnerable to extinction in Australia, and endangered in the state of Victoria. Remaining populations of this species in and around the city of Melbourne are threatened by habitat loss, degradation and fragmentation due to urban expansion. We used mitochondrial DNA (mtDNA) and microsatellites to study the genetic structure and diversity of L. raniformis across Melbourne's urban fringe, and also screened four nuclear gene regions (POMC, RAG-1, Rhod and CRYBA1). The mtDNA and nuclear DNA sequences revealed low levels of genetic diversity throughout remnant populations of L. raniformis. However, one of the four regions studied, Cardinia, exhibited relatively high genetic diversity and several unique haplotypes, suggesting this region should be recognized as a separate Management Unit. We discuss the implications of these results for the conservation of L. raniformis in urbanizing landscapes, particularly the potential risks and benefits of translocation, which remains a contentious management approach for this species.