•Emerging pathogens impact amphibians even in mostly intact & pristine ecosystems.•>20 yrs of disease data help frame understanding of amphibian response to disease.•Batrachochytrium dendrobatidis ...(Bd) ubiquitous in the Greater Yellowstone Ecosystem.•Long-term capture data show continued reduction in survival due to Bd.•Mortality events attributed to, or consistent with, ranaviruses are widespread.
Emerging infectious disease threatens amphibian biodiversity worldwide, including in landscapes that are protected from many anthropogenic stressors. We summarized data from studies in the Greater Yellowstone Ecosystem (GYE), one of the largest and most complete temperate-zone ecosystems on Earth, to assess the current state of knowledge about ranaviruses and the novel amphibian chytrid fungus (Bd) in this landscape, and to provide insight into future threats and conservation strategies. Our comprehension of these amphibian diseases in the GYE is based on >20 years of monitoring, surveys, population studies, and opportunistic observations of mortality events. Research indicates that local species are affected differently, depending on temperature, community structure, and location in the GYE. Bd has not been linked to die-offs in the GYE but evidence for ongoing reductions in survival contributes to foundational data about the effects of this pathogen in North America. Localized mortality events attributed to, or consistent with, disease from ranaviruses, are widespread in the GYE, but there is less information on how ranaviruses affect amphibian vital rates. The significance of disease in the long-term persistence of amphibians in the GYE is linked to anticipated changes in climate, especially drought. Additionally, expected increases in visitor use, and its associated impacts, have the potential to exacerbate the effects of disease. Long-term information from this large, intact landscape helps to frame our understanding of the effects of disease on amphibians and provides data that can contribute to management decisions, mitigation strategies, and forecasting efforts.
Many studies have noted differences in microbes associated with animals reared in captivity compared to their wild counterparts, but few studies have examined how microbes change when animals are ...reintroduced to the wild after captive rearing. As captive assurance populations and reintroduction programs increase, a better understanding of how microbial symbionts respond during animal translocations is critical. We examined changes in microbes associated with boreal toads (
Anaxyrus boreas
), a threatened amphibian, after reintroduction to the wild following captive rearing. Previous studies demonstrate that developmental life stage is an important factor in amphibian microbiomes. We collected 16S marker-gene sequencing datasets to investigate: (i) comparisons of the skin, mouth, and fecal bacteria of boreal toads across four developmental life stages in captivity and the wild, (ii) tadpole skin bacteria before and after reintroduction to the wild, and (iii) adult skin bacteria during reintroduction to the wild. We demonstrated that differences occur across skin, fecal, and mouth bacterial communities in captive versus wild boreal toads, and that the degree of difference depends on developmental stage. Skin bacterial communities from captive tadpoles were more similar to their wild counterparts than captive post-metamorphic individuals were to their wild counterparts. When captive-reared tadpoles were introduced to a wild site, their skin bacteria changed rapidly to resemble wild tadpoles. Similarly, the skin bacterial communities of reintroduced adult boreal toads also shifted to resemble those of wild toads. Our results indicate that a clear microbial signature of captivity in amphibians does not persist after release into natural habitat.
Mitigating amphibian chytridiomycoses in nature Garner, Trenton W. J.; Schmidt, Benedikt R.; Martel, An ...
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2016, Letnik:
371, Številka:
1709
Journal Article
Recenzirano
Odprti dostop
Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are ...conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems.
This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
Habitat loss and exposure to pesticides are likely primary factors contributing to amphibian decline in agricultural landscapes. Conservation efforts have attempted to restore wetlands lost through ...landscape modifications to reduce contaminant loads in surface waters and providing quality habitat to wildlife. The benefits of this increased wetland area, perhaps especially for amphibians, may be negated if habitat quality is insufficient to support persistent populations. We examined the presence of pesticides and nutrients in water and sediment as indicators of habitat quality and assessed the bioaccumulation of pesticides in the tissue of two native amphibian species Pseudacris maculata (chorus frogs) and Lithobates pipiens (leopard frogs) at six wetlands (3 restored and 3 reference) in Iowa, USA. Restored wetlands are positioned on the landscape to receive subsurface tile drainage water while reference wetlands receive water from overland run-off and shallow groundwater sources. Concentrations of the pesticides frequently detected in water and sediment samples were not different between wetland types. The median concentration of atrazine in surface water was 0.2μg/L. Reproductive abnormalities in leopard frogs have been observed in other studies at these concentrations. Nutrient concentrations were higher in the restored wetlands but lower than concentrations thought lethal to frogs. Complex mixtures of pesticides including up to 8 fungicides, some previously unreported in tissue, were detected with concentrations ranging from 0.08 to 1500μg/kg wet weight. No significant differences in pesticide concentrations were observed between species, although concentrations tended to be higher in leopard frogs compared to chorus frogs, possibly because of differences in life histories. Our results provide information on habitat quality in restored wetlands that will assist state and federal agencies, landowners, and resource managers in identifying and implementing conservation and management actions for these and similar wetlands in agriculturally dominated landscapes.
•Habitat quality was similar between restored and reference wetlands in Iowa.•Complex mixtures of pesticides are detected in frog tissues (liver and whole body).•The number of fungicides (up to 8) in frog tissues is largest reported to date.•Life history has the potential to impact pesticide bioaccumulation in frogs.
•Amphibians occupy created wetlands at lower rates than reference wetlands.•Amphibians occupy impacted and reference wetlands at similar rates.•Amphibian occupancy changes over time in created ...wetlands.•Wetland design is important in mitigation wetland creation.
Wetland creation is a common practice to mitigate for the loss of natural wetlands. However, there is still uncertainty about how effectively created wetlands replace habitat provided by natural wetlands. This uncertainty is due in part because post-construction monitoring of biological communities, and vertebrates especially, is rare and typically short-term (<5 years). We estimated occupancy of 4 amphibian species in 8 created mitigation wetlands, 7 impacted wetlands, and 7 reference wetlands in the Greater Yellowstone Ecosystem in Wyoming, USA. Mitigation wetlands were created to replace wetland habitat that was lost during road construction and ranged in age from 1 to 10 years when sampled. Impacted wetlands were natural wetlands partially filled by road construction and were adjacent to a highway. We sampled for amphibian larvae during 6 summers from 2013 to 2020 and used multi-species occupancy models that estimated detection and occupancy of each of 4 amphibian species to determine how amphibian responses changed over time, especially in mitigation wetlands. Occupancy did not differ between impacted and reference wetlands for any of the 4 amphibian species. Western Toads (Anaxyrus boreas) were most common (although briefly) in created wetlands, and occupancy of Columbia Spotted Frogs (Rana luteiventris), Western Tiger Salamanders (Ambystoma mavortium), and Boreal Chorus Frogs (Pseudacris maculata) was lower in created wetlands than in impacted or reference wetlands. Individual wetland area was positively associated with occupancy for all 4 species and wetland vegetation cover was positively associated with Boreal Chorus Frog and Columbia Spotted Frog occupancy; these results emphasize the importance of design characteristics when planning mitigation wetlands. The link between wetland age and occupancy was complex and included threshold and quadratic relationships for three of the four species, but only Boreal Chorus Frog occupancy was still increasing slowly at the end of our study. Our results indicate created wetlands did not attain the suitability of impacted and natural wetlands for local amphibians, even several years after construction. The complex relationships between wetland age and species-specific occupancy illustrate the importance of long-term monitoring in describing population responses to the construction of wetlands as mitigation for wetland loss.
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•Marking methods for identification differ in handling time (a proxy for stress).•Cumulative handling time depends on species and study characteristics.•Species survival, capture ...probabilities,and study design: Important considerations.•Some amphibians incur less handling time using PIT tags vs photography.•Shiny App calculates handling time using species- and study-specific parameters.
Individual identification is required for long-term investigations that examine population-level changes in survival or abundance, and mechanisms associated with these changes in wild populations. Such identification generally requires the application of a unique mark, or the documentation of characteristics distinctive to each individual animal. To minimize impacts to often declining populations, scientific and ethical concerns encourage marking strategies that minimize handling time (i.e., stress) for captured individuals. We examined the relative efficacy of passive integrated transponder (PIT)-tagging and photo-identification to identify individual Boreal toads (Anaxyrus boreas boreas) in field and indoor settings. We evaluated whether initial handling time was influenced by identification method (PIT-tag or photo-identification) or environment (field or indoor) and assessed the applicability of each method in long-term monitoring programs. Initial handling time was higher for PIT-tagging than photo-identification and higher in the field than in an indoor environment; however, handling time for previously PIT-tagged individuals was greatly reduced such that photo-identification led to > 5.5 times more handling time than PIT-tagging over the course of a toad's lifetime. Investigators must determine the trade-off between initial and subsequent handling times to minimize the expected (mean) cumulative handling time for an individual over the course of a study. Cumulative handling time is a function of the study design and the species’ survival and detection probabilities. We developed a Shiny Application to allow investigators to determine the identification method that minimizes handling time for their own study system.
Amphibian conservation has progressed from the identification of declines to mitigation, but efforts are hampered by the lack of nuanced information about the effects of environmental characteristics ...and stressors on mechanistic processes of population regulation. Challenges include a paucity of long-term data and scant information about the relative roles of extrinsic (e.g., weather) and intrinsic (e.g., density dependence) factors. We used a Bayesian formulation of an open population capture-recapture model and >30 years of data to examine intrinsic and extrinsic factors regulating two adult boreal chorus frogs (Pseudacris maculata) populations. We modelled population growth rate and apparent survival directly, assessed their temporal variability, and derived estimates of recruitment. Populations were relatively stable (geometric mean population growth rate >1) and regulated by negative density dependence (i.e., higher population sizes reduced population growth rate). In the smaller population, density dependence also acted on adult survival. In the larger population, higher population growth was associated with warmer autumns. Survival estimates ranged from 0.30–0.87, per-capita recruitment was <1 in most years, and mean seniority probability was >0.50, suggesting adult survival is more important to population growth than recruitment. Our analysis indicates density dependence is a primary driver of population dynamics for P. maculata adults.
The reintroduction of a species into its historic range is a critical component of conservation programmes designed to restore extirpated metapopulations. However, many reintroduction efforts fail, ...and the lack of rigorous monitoring programmes and statistical models have prevented a general understanding of the factors affecting metapopulation viability following reintroduction. Spatially explicit metapopulation theory provides the basis for understanding the dynamics of fragmented populations linked by dispersal, but the theory has rarely been used to guide reintroduction programmes because most spatial metapopulation models require presence–absence data from every site in the network, and they do not allow for observation error such as imperfect detection. We develop a spatial occupancy model that relaxes these restrictive assumptions and allows for inference about metapopulation extinction risk and connectivity. We demonstrate the utility of the model using six years of data on the Chiricahua leopard frog Lithobates chiricahuensis, a threatened desert‐breeding amphibian that was reintroduced to a network of sites in Arizona USA in 2003. Our results indicate that the model can generate precise predictions of extinction risk and produce connectivity maps that can guide conservation efforts following reintroduction. In the case of L. chiricahuensis, many sites were functionally isolated, and 82% of sites were characterized by intermittent water availability and high local extinction probabilities (0·84, 95% CI: 0·64–0·99). However, under the current hydrological conditions and spatial arrangement of sites, the risk of metapopulation extinction is estimated to be <3% over a 50‐year time horizon. Low metapopulation extinction risk appears to result from the high dispersal capability of the species, the high density of sites in the region and the existence of predator‐free permanent wetlands with low local extinction probabilities. Should management be required, extinction risk can be reduced by either increasing the hydroperiod of existing sites or by creating new sites to increase connectivity. Synthesis and applications. This work demonstrates how spatio‐temporal statistical models based on ecological theory can be applied to forecast the outcomes of conservation actions such as reintroduction. Our spatial occupancy model should be particularly useful when management agencies lack the funds to collect intensive individual‐level data.
Habitat loss and degradation are leading causes of biodiversity declines, therefore assessing the capacity of created mitigation wetlands to replace habitat for wildlife has become a management ...priority. We used single season occupancy models to compare the occurrence of larvae of four species of pond‐breeding amphibians in wetlands created for mitigation, wetlands impacted by road construction, and unimpacted reference wetlands along a highway corridor in the Greater Yellowstone Ecosystem, United States. Created wetlands were shallow and had less aquatic vegetation and surface area than impacted and reference wetlands. Occupancy of barred tiger salamander (Ambystoma mavortium) and boreal chorus frog (Pseudacris maculata) larvae was similar across wetland types, whereas boreal toads (Anaxyrus boreas) occurred more often in created wetlands than reference and impacted wetlands. However, the majority of created wetlands (>80%) dried partially or completely before amphibian metamorphosis occurred in both years of our study, resulting in heavy mortality of larvae and, we suspect, little to no recruitment. Columbia spotted frogs (Rana luteiventris), which require emergent vegetation that is not common in newly created wetlands, occurred commonly in impacted and reference wetlands but were found in only one created wetland. Our results show that shallow created wetlands with little aquatic vegetation may be attractive breeding areas for some amphibians, but may result in high mortality and little recruitment if they fail to hold water for the entire larval period.
Emerging infectious diseases are an increasingly common threat to wildlife. Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), is an emerging infectious disease that ...has been linked to amphibian declines around the world. Few studies exist that explore amphibian–Bd dynamics at the landscape scale, limiting our ability to identify which factors are associated with variation in population susceptibility and to develop effective in situ disease management. Declines of boreal toads (Anaxyrus boreas boreas) in the southern Rocky Mountains are largely attributed to chytridiomycosis but variation exists in local extinction of boreal toads across this metapopulation. Using a large-scale historic data set, we explored several potential factors influencing disease dynamics in the boreal toad–Bd system: geographic isolation of populations, amphibian community richness, elevational differences, and habitat permanence. We found evidence that boreal toad extinction risk was lowest at high elevations where temperatures may be suboptimal for Bd growth and where small boreal toad populations may be below the threshold needed for efficient pathogen transmission. In addition, boreal toads were more likely to recolonize high elevation sites after local extinction, again suggesting that high elevations may provide refuge from disease for boreal toads. We illustrate a modeling framework that will be useful to natural resource managers striving to make decisions in amphibian–Bd systems. Our data suggest that in the southern Rocky Mountains high elevation sites should be prioritized for conservation initiatives like reintroductions.
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