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Erin L. Muths

Publications and source records attributed to Erin L. Muths.

At least 37 records · Page 2Linked to original sources

Empirical evidence for effects of invasive American Bullfrogs on occurrence of native amphibians and emerging pathogens

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 of native amphibians via predation and spreading emerging pathogens such as amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and ranaviruses. Although many studies have investigated the potential role of bullfrogs in declines 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 presence of bullfrogs affects occurrence of 4 native amphibians, Bd, and ranaviruses. Based on 2-species, dominant-subordinate occupancy models fitted in a Bayesian context, federally threatened Chiricahua Leopard Frogs ( R. chiricahuensis ) and Western Tiger Salamanders ( Ambystoma mavortium ) were 8 times (32% vs. 4%) and 2 times (36% vs. 18%), respectively, less likely to occur at sites where bullfrogs occurred. Evidence for negative effects of bullfrogs on Lowland Leopard Frogs ( R. yavapaiensis ) and Northern Leopard Frogs ( R. pipiens ) was less clear, possibly because of smaller numbers of sites where these native species still occur 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 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 5 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 occurrence of native amphibians and increase occurrence of pathogens, information that can clarify risks and aid the prioritization of conservation actions.

Ecological Applications

Compensatory recruitment unlikely in high-elevation amphibian populations challenged with disease

Understanding the causes of population variation in host response to disease, and the mechanisms of persistence, can serve as vital information for species conservation. One such mechanism of population persistence that has gained support is the demographic process of compensatory recruitment. Host populations may persist by increasing recruitment to compensate for reduced survival due to infection, thus limiting the negative effects of the disease on population trajectories. However, high-elevation populations are inherently vulnerable to stochastic processes and may be limited in their ability to exhibit compensatory recruitment relative to lower elevation populations. We use long-term mark–recapture data from five populations of boreal toads Anaxyrus boreas boreas , across an elevational gradient in Colorado, before and after pathogen arrival to assess whether populations can persist with Batrachochytrium dendrobatidis ( Bd ) via compensatory recruitment. Prior to pathogen arrival, we found a life-history trade-off between survival and recruitment across elevations, where high-elevation toads have high survival but lower recruitment and vice versa at lower elevations. Pathogen arrival had a strong negative effect on apparent annual survival and recruitment leading to negative population growth rates and dramatically reduced host abundances. The data did not support the occurrence of compensatory recruitment. Synthesis and applications . Our unique dataset indicates that demographic responses to pathogens may be environmentally (i.e. elevationally) context dependent and highlights the value of long-term monitoring. We recommend that practitioners verify that potential persistence mechanisms occur across multiple populations and relevant environmental gradients to counter any assumptions of the mechanism existing species-wide. Quantifying variation in population responses to disease will aid in understanding the bounds of such persistence mechanisms and identify particularly vulnerable populations where mechanisms are nonexistent.

Journal of Applied Ecology

Context-dependent variation in persistence of host populations in the face of disease

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.

Journal of Animal Ecology

Sex‐related differences in aging rate are associated with sex chromosome system in amphibians

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.

Evolution

The role of monitoring and research in the Greater Yellowstone Ecosystem in framing our understanding of the effects of disease on amphibians

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.

Wyoming

Looking ahead, guided by the past: The role of U.S. national parks in amphibian research and conservation

Protected areas like national parks are essential elements of conservation because they limit human influence on the landscape, which protects biodiversity and ecosystem function. The role of national parks in conservation, however, often goes far beyond limiting human influence. The U.S. National Park Service and its system of land units contribute substantively to conservation by providing protected lands where researchers can document trends in species distributions and abundances, examine characteristics important for generating these trends, and identify and implement conservation strategies to preserve biodiversity. We reviewed the contribution of U.S. national parks to amphibian research and conservation and highlight important challenges and findings in several key areas. First, U.S. national parks were instrumental in providing strong support that amphibian declines were real and unlikely to be simply a consequence of habitat loss. Second, research in U.S. national parks provided evidence against certain hypothesized causes of decline, like UV-B radiation, and evidence for others, such as introduced species and disease. However, describing declines and identifying causes contributes to conservation only if it leads to management; importantly, U.S. national parks have implemented many conservation strategies and evaluated their effectiveness in recovering robust amphibian populations. Among these, removal of invasive species, especially fishes; conservation translocations; and habitat creation and enhancement stand out as examples of successful conservation strategies with broad applicability. Successful management for amphibians is additionally complicated by competing mandates and stakeholder interests; for example, past emphasis on increasing visitor enjoyment by introducing fish to formerly fishless lakes had devastating consequences for many amphibians. Other potential conflicts with amphibian conservation include increasing development, increased risk of introductions of disease and exotic species with increased visitation, and road mortality. Decision science and leveraging partnerships have proven to be key components of effective conservation under conflicting mandates in national parks. As resource managers grapple with large-scale drivers that are outside local control, public-private partnerships and adaptive strategies are increasing in importance. U.S. national parks have played an important role in many aspects of identifying and ameliorating the amphibian decline crisis and will continue to be essential for the conservation of amphibians in the future.

Ecological Indicators

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity

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.

Science

Thermal conditions predict intraspecific variation in senescence rate in frogs and toads

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.

Proceedings of the National Academy of Sciences

Accommodating the role of site memory in dynamic species distribution models

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.

Arizona

Why disease ecology needs life-history theory: A host perspective

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

Ecology Letters

Resilience of native amphibian communities following catastrophic drought: Evidence from a decade of regional-scale monitoring

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.

California

Trade-offs in initial and long-term handling efficiency of PIT-tag and photographic identification methods

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.

Ecological Indicators

Amphibian population responses to mitigation: Relative importance of wetland age and design

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.

Ecological Indicators

Distribution of tiger salamanders in northern Sonora, Mexico: Comparison of sampling methods and possible implications for an endangered subspecies

Many aquatic species in the arid USA-Mexico borderlands region are imperiled, but limited information on distributions and threats often hinders management. To provide information on the distribution of the Western Tiger Salamander ( Ambystoma mavortium ), including the USA-federally endangered Sonoran Tiger Salamander ( Ambystoma mavortium stebbinsi ), we used traditional (seines, dip-nets) and modern (environmental DNA [eDNA]) methods to sample 91 waterbodies in northern Sonora, Mexico, during 2015-2018. The endemic Sonoran Tiger Salamander is threatened by introgressive hybridization and potential replacement by another sub-species of the Western Tiger Salamander, the non-native Barred Tiger Salamander ( A. m. mavortium ). Based on occupancy models that accounted for imperfect detection, eDNA sampling provided a similar detection probability (0.82 [95% CI: 0.56-0.94]) as seining (0.83 [0.46-0.96]) and much higher detection than dip-netting (0.09 [0.02-0.23]). Volume of water filtered had little effect on detection, possibly because turbid sites had greater densities of salamanders. Salamanders were estimated to occur at 51 sites in 3 river drainages in Sonora. These results indicate tiger salamanders are much more widespread in northern Sonora than previously documented, perhaps aided by changes in land and water management practices. However, because the two subspecies of salamanders cannot be reliably distinguished based on morphology or eDNA methods that are based on mitochondrial DNA, we are uncertain if we detected only native genotypes or if we documented recent invasion of the area by the non-native sub-species. Thus, there is an urgent need for methods to reliably distinguish the subspecies so managers can identify appropriate interventions.

Sonora

Staggered-entry analysis of breeding phenology and occupancy dynamics of Arizona toads from historically occupied habitats of New Mexico, USA

For species with variable phenology, it is often challenging to produce reliable estimates of population dynamics or changes in occupancy. The Arizona Toad ( Anaxyrus microscaphus ) is a southwestern USA endemic that has been petitioned for legal protection, but status assessments are limited by a lack of information on population trends. Also, timing and consistency of Arizona Toad breeding varies greatly, making it difficult to predict optimal survey times or effort required for detection. To help fill these information gaps, we conducted breeding season call surveys during 2013–2016 and 2019 at 86 historically occupied sites and 59 control sites across the species' range in New Mexico. We estimated variation in mean dates of arrival and departure from breeding sites, changes in occupancy, and site-level extinction since 1959 with recently developed multi-season staggered-entry models, which relax the within-season closure assumption common to most occupancy models. Optimal timing of surveys in our study areas was approximately 5–30 March. Averaged across years, estimated probability of occupancy was 0.58 (SE = 0.09) for historical sites and 0.19 (SE = 0.08) for control sites. Occupancy increased from 2013 through 2019. Notably, even though observer error was trivial, annual detection probabilities varied from 0.23 to 0.75 and declined during the study; this means naïve occupancy values would have been misleading, indicating apparent declines in toad occupancy. Occupancy was lowest during the first year of the study, possibly due to changes in stream flows and conditions in many waterbodies following extended drought and recent wildfires. Although within-season closure was violated by variable calling phenology, simple multi-season models provided nearly identical estimates as staggered-entry models. Surprisingly, extinction probability was unrelated to the number of years since the first or last record at historically occupied sites. Collectively, our results suggest a lack of large, recent declines in occupancy by Arizona Toads in New Mexico, but we still lack population information from most of the species' range.

New Mexico

Density dependence and adult survival drive the dynamics in two high elevation amphibian populations

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.

Colorado