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Testing for intraspecific variation for host tolerance or resistance in wild populations is important for informing conservation decisions about captive breeding, translocation, and disease treatment. Here, we test the importance of tolerance and resistance in multiple populations of boreal toads (Anaxyrus boreas boreas) against Batrachochytrium dendrobatidis (Bd), the amphibian fungal pathogen responsible for the greatest host biodiversity loss due to disease. Boreal toads have severely declined in Colorado (CO) due to Bd, but toad populations challenged with Bd in western Wyoming (WY) appear to be less affected. We used a common garden infection experiment to expose post-metamorphic toads sourced from four populations (2 in CO and 2 in WY) to Bd and monitored changes in mass, pathogen burden and survival for 8 weeks. We used a multi-state modelling approach to estimate weekly survival and transition probabilities between infected and cleared states, reflecting a dynamic infection process that traditional approaches fail to capture. We found that WY boreal toads are more tolerant to Bd infection with higher survival probabilities than those in CO when infected with identical pathogen burdens. WY toads also appeared more resistant to Bd with a higher probability of infection clearance and an average of 5 days longer to reach peak infection burdens. Our results demonstrate strong intraspecific differences in tolerance and resistance that likely contribute to why population declines vary regionally across this species. Our multi-state framework allowed us to gain inference on typically hidden disease processes when testing for host tolerance or resistance. Our findings demonstrate that describing an entire host species as 'tolerant' or 'resistant' (or lack thereof) is unwise without testing for intraspecific variation.
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Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.
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Envelhecimento/metabolismo , Anuros/metabolismo , Envelhecimento/fisiologia , Animais , Biodiversidade , Bufonidae/metabolismo , Mudança Climática/mortalidade , Europa (Continente) , Aquecimento Global/mortalidade , América do Norte , Ranidae/metabolismo , TemperaturaRESUMO
Invasive species and emerging infectious diseases are two of the greatest threats to biodiversity. American Bullfrogs (Rana [Lithobates] catesbeiana), which have been introduced to many parts of the world, are often linked with declines in native amphibians via predation and the spread of emerging pathogens such as amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]) and ranaviruses. Although many studies have investigated the potential role of bullfrogs in the decline of native amphibians, analyses that account for shared habitat affinities and imperfect detection have found limited support for clear effects. Similarly, the role of bullfrogs in shaping the patch-level distribution of pathogens is unclear. We used eDNA methods to sample 233 sites in the southwestern USA and Sonora, Mexico (2016-2018) to estimate how the presence of bullfrogs affects the occurrence of four native amphibians, Bd, and ranaviruses. Based on two-species, dominant-subordinate occupancy models fitted in a Bayesian context, federally threatened Chiricahua Leopard Frogs (Rana chiricahuensis) and Western Tiger Salamanders (Ambystoma mavortium) were eight times (32% vs. 4%) and two times (36% vs. 18%), respectively, less likely to occur at sites where bullfrogs occurred. Evidence for the negative effects of bullfrogs on Lowland Leopard Frogs (Rana yavapaiensis) and Northern Leopard Frogs (Rana pipiens) was less clear, possibly because of smaller numbers of sites where these native species still occurred and because bullfrogs often occur at lower densities in streams, the primary habitat for Lowland Leopard Frogs. At the community level, Bd was most likely to occur where bullfrogs co-occurred with native amphibians, which could increase the risk to native species. Ranaviruses were estimated to occur at 33% of bullfrog-only sites, 10% of sites where bullfrogs and native amphibians co-occurred, and only 3% of sites where only native amphibians occurred. Of the 85 sites where we did not detect any of the five target amphibian species, we also did not detect Bd or ranaviruses; this suggests other hosts do not drive the distribution of these pathogens in our study area. Our results provide landscape-scale evidence that bullfrogs reduce the occurrence of native amphibians and increase the occurrence of pathogens, information that can clarify risks and aid the prioritization of conservation actions.
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Quitridiomicetos , Animais , Rana catesbeiana/microbiologia , Teorema de Bayes , Anfíbios , Ranidae , BiodiversidadeRESUMO
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.
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Bufonidae , Microbiota , Humanos , Animais , Bufonidae/microbiologia , Larva/microbiologia , Bactérias/genética , Pele/microbiologiaRESUMO
Quantifying how contaminants change across life cycles of species that undergo metamorphosis is critical to assessing organismal risk, particularly for consumers. Pond-breeding amphibians can dominate aquatic animal biomass as larvae and are terrestrial prey as juveniles and adults. Thus, amphibians can be vectors of mercury exposure in both aquatic and terrestrial food webs. However, it is still unclear how mercury concentrations are affected by exogenous (e.g., habitat or diet) vs endogenous factors (e.g., catabolism during hibernation) as amphibians undergo large diet shifts and periods of fasting during ontogeny. We measured total mercury (THg), methylmercury (MeHg), and isotopic compositions (δ 13C, δ15N) in boreal chorus frogs (Pseudacris maculata) across five life stages in two Colorado (USA) metapopulations. We found large differences in concentrations and percent MeHg (of THg) among life stages. Frog MeHg concentrations peaked during metamorphosis and hibernation coinciding with the most energetically demanding life cycle stages. Indeed, life history transitions involving periods of fasting coupled with high metabolic demands led to large increases in mercury concentrations. The endogenous processes of metamorphosis and hibernation resulted in MeHg bioamplification, thus decoupling it from the light isotopic proxies of diet and trophic position. These step changes are not often considered in conventional expectations of how MeHg concentrations within organisms are assessed.
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Mercúrio , Compostos de Metilmercúrio , Poluentes Químicos da Água , Animais , Lagoas , Mercúrio/análise , Compostos de Metilmercúrio/metabolismo , Ecossistema , Cadeia Alimentar , Anfíbios/metabolismo , Poluentes Químicos da Água/análise , Monitoramento Ambiental , Peixes/metabolismoRESUMO
Mercury (Hg) is a toxic contaminant that has been mobilized and distributed worldwide and is a threat to many wildlife species. Amphibians are facing unprecedented global declines due to many threats including contaminants. While the biphasic life history of many amphibians creates a potential nexus for methylmercury (MeHg) exposure in aquatic habitats and subsequent health effects, the broad-scale distribution of MeHg exposure in amphibians remains unknown. We used nonlethal sampling to assess MeHg bioaccumulation in 3,241 juvenile and adult amphibians during 2017-2021. We sampled 26 populations (14 species) across 11 states in the United States, including several imperiled species that could not have been sampled by traditional lethal methods. We examined whether life history traits of species and whether the concentration of total mercury in sediment or dragonflies could be used as indicators of MeHg bioaccumulation in amphibians. Methylmercury contamination was widespread, with a 33-fold difference in concentrations across sites. Variation among years and clustered subsites was less than variation across sites. Life history characteristics such as size, sex, and whether the amphibian was a frog, toad, newt, or other salamander were the factors most strongly associated with bioaccumulation. Total Hg in dragonflies was a reliable indicator of bioaccumulation of MeHg in amphibians (R2 ≥ 0.67), whereas total Hg in sediment was not (R2 ≤ 0.04). Our study, the largest broad-scale assessment of MeHg bioaccumulation in amphibians, highlights methodological advances that allow for nonlethal sampling of rare species and reveals immense variation among species, life histories, and sites. Our findings can help identify sensitive populations and provide environmentally relevant concentrations for future studies to better quantify the potential threats of MeHg to amphibians.
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Mercúrio , Compostos de Metilmercúrio , Odonatos , Poluentes Químicos da Água , Animais , Poluentes Químicos da Água/análise , Mercúrio/análise , Anfíbios , Monitoramento AmbientalRESUMO
Research Highlight: Valenzuela-Sánchez, A., Azat, C., Cunningham, A. A., Delgado, S., Bacigalupe, L. D., Beltrand, J., Serrano, J. M., Sentenac, H., Haddow, N., Toledo, V., Schmidt, B. R., & Cayuela, H. (2022). Interpopulation differences in male reproductive effort drive the population dynamics of a host exposed to an emerging fungal pathogen. Journal of Animal Ecology, 00, 1- 12. https://doi.org/10.1111/1365-2656.13603. Understanding the nuances of population persistence in the face of a stressor can help predict extinction risk and guide conservation actions. However, the exact mechanisms driving population stability may not always be known. In this paper, Valenzuela-Sánchez et al. (2022) integrate long-term mark-recapture data, focal measurements of reproductive effort, a population matrix model and inferences on life-history variation to reveal differences in demographic response to disease in a susceptible frog species (Rhinoderma darwinii). Valenzuela-Sánchez et al. found that demographic compensation via recruitment explained the positive population growth rate in their high disease prevalence population whereas the low disease prevalence population did not compensate and thus had decreasing population growth. Compensatory recruitment was likely due to the high probability of males brooding, and the high number of brooded larvae in the high prevalence population compared to low prevalence and disease-free populations. Valenzuela-Sánchez et al. also document faster generation times in the high prevalence population, which may indicate a faster life history that may be contributing to the population's ability to compensate for reduced survival. Lastly, the authors find a positive relationship between disease prevalence and the proportion of juveniles in a given population that suggest that there may be a threshold for disease prevalence that triggers increased reproductive effort. Altogether, their study provides novel support for increased reproductive effort as the pathway for compensatory recruitment leading to increasing population growth despite strong negative effects of disease on adult survival. Their results also caution the overgeneralization of the effects of stressors (e.g. disease) on population dynamics, where context-dependent responses may differ among host populations of a given species.
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Anuros , Animais , Anuros/fisiologia , Masculino , Dinâmica PopulacionalRESUMO
When facing an emerging infectious disease of conservation concern, we often have little information on the nature of the host-parasite interaction to inform management decisions. However, it is becoming increasingly clear that the life-history strategies of host species can be predictive of individual- and population-level responses to infectious disease, even without detailed knowledge on the specifics of the host-parasite interaction. Here, we argue that a deeper integration of life-history theory into disease ecology is timely and necessary to improve our capacity to understand, predict and mitigate the impact of endemic and emerging infectious diseases in wild populations. Using wild vertebrates as an example, we show that host life-history characteristics influence host responses to parasitism at different levels of organisation, from individuals to communities. We also highlight knowledge gaps and future directions for the study of life-history and host responses to parasitism. We conclude by illustrating how this theoretical insight can inform the monitoring and control of infectious diseases in wildlife.
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Ecologia , Características de História de Vida , Animais , Animais Selvagens , Interações Hospedeiro-Parasita , Humanos , VertebradosRESUMO
The increasing frequency and severity of drought may exacerbate ongoing global amphibian declines. However, interactions between drought and coincident stressors, coupled with high interannual variability in amphibian abundances, can mask the extent and underlying mechanisms of drought impacts. We synthesized a decade (2009 - 2019) of regional-scale amphibian monitoring data (2273 surveys, 233 ponds, and seven species) from across California's Bay Area and used dynamic occupancy modeling to estimate trends and drivers of species occupancy. An extreme drought during the study period resulted in substantial habitat loss, with 51% of ponds drying in the worst year of drought, compared to <20% in pre-drought years. Nearly every species exhibited reduced breeding activity during the drought, with the occupancy of some species (American bullfrogs and California newts) declining by >25%. Invasive fishes and bullfrogs were also associated with reduced amphibian occupancy, and these taxa were locally extirpated from numerous sites during drought, without subsequent recovery-suggesting that drought may present an opportunity to remove invaders. Despite a historic, multi-year drought, native amphibians rebounded quickly to pre-drought occupancy levels, demonstrating evidence of resilience. Permanent waterbodies supported higher persistence of native species during drought years than did temporary waterbodies, and we therefore highlight the value of hydroperiod diversity in promoting amphibian stability.
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Conservation of at-risk species is aided by reliable forecasts of the consequences of environmental change and management actions on population viability. Forecasts from conventional population viability analysis (PVA) are made using a two-step procedure in which parameters are estimated, or elicited from expert opinion, and then plugged into a stochastic population model without accounting for parameter uncertainty. Recently developed statistical PVAs differ because forecasts are made conditional on models fitted to empirical data. The statistical forecasting approach allows for uncertainty about parameters, but it has rarely been applied in metapopulation contexts where spatially explicit inference is needed about colonization and extinction dynamics and other forms of stochasticity that influence metapopulation viability. We conducted a statistical metapopulation viability analysis (MPVA) using 11 yr of data on the federally threatened Chiricahua leopard frog (Lithobates chiricahuensis) to forecast responses to landscape heterogeneity, drought, environmental stochasticity, and management. We evaluated several future environmental scenarios and pond restoration options designed to reduce extinction risk. Forecasts over a 50-yr time horizon indicated that metapopulation extinction risk was <4% for all scenarios, but uncertainty was high. Without pond restoration, extinction risk is forecasted to be 3.9% (95% CI 0-37%) by year 2066. Restoring six ponds by increasing their hydroperiod reduced extinction risk to <1% and greatly reduced uncertainty (95% CI 0-2%). Our results suggest that managers can mitigate the impacts of drought and environmental stochasticity on metapopulation viability by maintaining ponds that hold water throughout the year and keeping them free of invasive predators. Our study illustrates the utility of the spatially explicit statistical forecasting approach to MPVA in conservation planning efforts.
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Secas , Lagoas , Ecossistema , Previsões , Modelos Biológicos , Dinâmica Populacional , IncertezaRESUMO
Understanding how natural and anthropogenic processes affect population dynamics of species with patchy distributions is critical to predicting their responses to environmental changes. Despite considerable evidence that demographic rates and dispersal patterns vary temporally in response to an array of biotic and abiotic processes, few applications of metapopulation theory have sought to explore factors that explain spatiotemporal variation in extinction or colonization rates. To facilitate exploring these factors, we extended a spatially explicit model of metapopulation dynamics to create a framework that requires only binary presence-absence data, makes few assumptions about the dispersal process, and accounts for imperfect detection. We apply this framework to 22 yr of biannual survey data for lowland leopard frogs, Lithobates yavapaiensis, an amphibian that inhabits arid stream systems in the southwestern United States and northern Mexico. Our results highlight the importance of accounting for factors that govern temporal variation in transition probabilities, as both extinction and colonization rates varied with hydrologic conditions. Specifically, local extinctions were more frequent during drought periods, particularly at sites without reliable surface water. Colonization rates increased when larval and dispersal periods were wetter than normal, which increased the probability that potential emigrants metamorphosed and reached neighboring sites. Extirpation of frogs from all sites in one watershed during a period of severe drought demonstrated the influence of site-level features, as frogs persisted only in areas where most sites held water consistently and where the amount of sediment deposited from high-elevation wildfires was low. Application of our model provided novel insights into how climate-related processes affected the distribution and population dynamics of an arid-land amphibian. The approach we describe has application to a wide array of species that inhabit patchy environments, can improve our understanding of factors that govern metapopulation dynamics, and can inform strategies for conservation of imperiled species.
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Secas , Hidrologia , Animais , México , Dinâmica Populacional , Sudoeste dos Estados UnidosRESUMO
Relocations are increasingly popular among wildlife managers despite often low rates of relocation success in vertebrates. In this context, understanding the influence of extrinsic (e.g., relocation design, habitat characteristics) and intrinsic factors (e.g., age and sex) on demographic parameters, such as survival, that regulate the dynamics of relocated populations is critical to improve relocation protocols and better predict relocation success. We investigated survival in naturally established and relocated populations of yellow-bellied toads (Bombina variegata), an amphibian that was nearly extinct in Belgium by the late 1980s. We quantified survival at three ontogenetic stages (juvenile, subadult, and adult) in the relocated population, the source population, and a control population. In the relocated population, we quantified survival in captive bred individuals and their locally born descendants. Then, using simulations, we examined how survival cost to relocation affects the self-sustainability of the relocated population. We showed that survival at juvenile and subadult stages was relatively similar in all populations. In contrast, relocated adult survival was lower than adult survival in the source and control populations. Despite this, offspring of relocated animals (the next generation, regardless of life stage) survived at similar rates to individuals in the source and control populations. Simulations revealed that the relocated population was self-sustaining under different scenarios and that the fate (e.g., stability or increase) of the simulated populations was highly dependent on the fecundity of relocated adults and their offspring. To summarize, our results indicate that survival in relocated individuals is lower than in non-relocated individuals but that this cost (i.e., reduced survival) disappears in the second generation. A finer understanding of how relocation affects demographic processes is an important step in improving relocation success of amphibians and other animals.
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Anuros , Ecossistema , Adulto , Animais , Cruzamento , DemografiaRESUMO
Metapopulation ecology and landscape ecology aim to understand how spatial structure influences ecological processes, yet these disciplines address the problem using fundamentally different modeling approaches. Metapopulation models describe how the spatial distribution of patches affects colonization and extinction, but often do not account for the heterogeneity in the landscape between patches. Models in landscape ecology use detailed descriptions of landscape structure, but often without considering colonization and extinction dynamics. We present a novel spatially explicit modeling framework for narrowing the divide between these disciplines to advance understanding of the effects of landscape structure on metapopulation dynamics. Unlike previous efforts, this framework allows for statistical inference on landscape resistance to colonization using empirical data. We demonstrate the approach using 11 yr of data on a threatened amphibian in a desert ecosystem. Occupancy data for Lithobates chiricahuensis (Chiricahua leopard frog) were collected on the Buenos Aires National Wildlife Refuge (BANWR), Arizona, USA from 2007 to 2017 following a reintroduction in 2003. Results indicated that colonization dynamics were influenced by both patch characteristics and landscape structure. Landscape resistance increased with increasing elevation and distance to the nearest streambed. Colonization rate was also influenced by patch quality, with semi-permanent and permanent ponds contributing substantially more to the colonization of neighboring ponds relative to intermittent ponds. Ponds that only hold water intermittently also had the highest extinction rate. Our modeling framework can be widely applied to understand metapopulation dynamics in complex landscapes, particularly in systems in which the environment between habitat patches influences the colonization process.
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Ecossistema , Modelos Biológicos , Arizona , Ecologia , Dinâmica PopulacionalRESUMO
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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Altitude , Bufonidae/microbiologia , Quitridiomicetos/fisiologia , Interações Hospedeiro-Patógeno , Animais , Modelos Biológicos , Dinâmica PopulacionalRESUMO
Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.
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Caracteres Sexuais , Cromossomos Sexuais , Envelhecimento/genética , Anfíbios/genética , Animais , Feminino , Masculino , Processos de Determinação Sexual , Cromossomo YRESUMO
Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.
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Envelhecimento , Anfíbios , Evolução Biológica , Répteis , Anfíbios/classificação , Anfíbios/fisiologia , Animais , Longevidade , Filogenia , Répteis/classificação , Répteis/fisiologiaRESUMO
BACKGROUND: Rescuing amphibian diversity is an achievable conservation challenge. Disease mitigation is one essential component of population management. Here we assess existing disease mitigation strategies, some in early experimental stages, which focus on the globally emerging chytrid fungus Batrachochytrium dendrobatidis. We discuss the precedent for each strategy in systems ranging from agriculture to human medicine, and the outlook for each strategy in terms of research needs and long-term potential. RESULTS: We find that the effects of exposure to Batrachochytrium dendrobatidis occur on a spectrum from transient commensal to lethal pathogen. Management priorities are divided between (1) halting pathogen spread and developing survival assurance colonies, and (2) prophylactic or remedial disease treatment. Epidemiological models of chytridiomycosis suggest that mitigation strategies can control disease without eliminating the pathogen. Ecological ethics guide wildlife disease research, but several ethical questions remain for managing disease in the field. CONCLUSIONS: Because sustainable conservation of amphibians in nature is dependent on long-term population persistence and co-evolution with potentially lethal pathogens, we suggest that disease mitigation not focus exclusively on the elimination or containment of the pathogen, or on the captive breeding of amphibian hosts. Rather, successful disease mitigation must be context specific with epidemiologically informed strategies to manage already infected populations by decreasing pathogenicity and host susceptibility. We propose population level treatments based on three steps: first, identify mechanisms of disease suppression; second, parameterize epizootiological models of disease and population dynamics for testing under semi-natural conditions; and third, begin a process of adaptive management in field trials with natural populations.
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First-order dynamic occupancy models (FODOMs) are a class of state-space model in which the true state (occurrence) is observed imperfectly. An important assumption of FODOMs is that site dynamics only depend on the current state and that variations in dynamic processes are adequately captured with covariates or random effects. However, it is often difficult to understand and/or measure the covariates that generate ecological data, which are typically spatiotemporally correlated. Consequently, the non-independent error structure of correlated data causes underestimation of parameter uncertainty and poor ecological inference. Here, we extend the FODOM framework with a second-order Markov process to accommodate site memory when covariates are not available. Our modeling framework can be used to make reliable inference about site occupancy, colonization, extinction, turnover, and detection probabilities. We present a series of simulations to illustrate the data requirements and model performance. We then applied our modeling framework to 13 yr of data from an amphibian community in southern Arizona, USA. In this analysis, we found residual temporal autocorrelation of population processes for most species, even after accounting for long-term drought dynamics. Our approach represents a valuable advance in obtaining inference on population dynamics, especially as they relate to metapopulations.
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Secas , Modelos Biológicos , Arizona , Ecossistema , Dinâmica PopulacionalRESUMO
Chytridiomycosis is linked to the worldwide decline of amphibians, yet little is known about the demographic effects of the disease. We collected capture-recapture data on three populations of boreal toads (Bufo boreas [Bufo = Anaxyrus]) in the Rocky Mountains (U.S.A.). Two of the populations were infected with chytridiomycosis and one was not. We examined the effect of the presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]; the agent of chytridiomycosis) on survival probability and population growth rate. Toads that were infected with Bd had lower average annual survival probability than uninfected individuals at sites where Bd was detected, which suggests chytridiomycosis may reduce survival by 31-42% in wild boreal toads. Toads that were negative for Bd at infected sites had survival probabilities comparable to toads at the uninfected site. Evidence that environmental covariates (particularly cold temperatures during the breeding season) influenced toad survival was weak. The number of individuals in diseased populations declined by 5-7%/year over the 6 years of the study, whereas the uninfected population had comparatively stable population growth. Our data suggest that the presence of Bd in these toad populations is not causing rapid population declines. Rather, chytridiomycosis appears to be functioning as a low-level, chronic disease whereby some infected individuals survive but the overall population effects are still negative. Our results show that some amphibian populations may be coexisting with Bd and highlight the importance of quantitative assessments of survival in diseased animal populations.
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Bufonidae/microbiologia , Quitridiomicetos , Micoses/veterinária , Animais , Colorado , Modelos Biológicos , Montana , Micoses/mortalidade , Dinâmica Populacional , Análise de Sobrevida , Temperatura , WyomingRESUMO
The salamander chytrid fungus (Batrachochytrium salamandrivorans [Bsal]) is causing massive mortality of salamanders in Europe. The potential for spread via international trade into North America and the high diversity of salamanders has catalyzed concern about Bsal in the U.S. Surveillance programs for invading pathogens must initially meet challenges that include low rates of occurrence on the landscape, low prevalence at a site, and imperfect detection of the diagnostic tests. We implemented a large-scale survey to determine if Bsal was present in North America designed to target taxa and localities where Bsal was determined highest risk to be present based on species susceptibility and geography. Our analysis included a Bayesian model to estimate the probability of occurrence of Bsal given our prior knowledge of the occurrence and prevalence of the pathogen. We failed to detect Bsal in any of 11,189 samples from 594 sites in 223 counties within 35 U.S. states and one site in Mexico. Our modeling indicates that Bsal is highly unlikely to occur within wild amphibians in the U.S. and suggests that the best proactive response is to continue mitigation efforts against the introduction and establishment of the disease and to develop plans to reduce impacts should Bsal establish.