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Many studies have noted apparent differences in microbes associated with animals reared in captivity compared to their wild counterparts. Few studies have examined how microbes change when animals are reintroduced to the wild after being reared in captivity. 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 of boreal toads (Anaxyrus boreas) after reintroduction to the wild following captive rearing. Boreal toads, a long-lived high elevation species, are endangered in Colorado primarily due to chytridiomycosis. Previous studies demonstrate that developmental life stage of boreal toads is an important factor in their microbiomes such that microbiomes change over the course of development. i) comparisons of the skin, mouth, and gut bacteria of boreal toads across four developmental life stages in captivity and the wild, ii) pre-metamorphic tadpole skin bacteria before and after reintroduction to the wild, and iii) adult skin bacteria during reintroduction to the wild. We used barcoded amplicon sequencing of the 16S small subunit of the rRNA gene on the Illumina MiSeq platform to characterize the bacterial communities. We demonstrated that differences occur across the skin gut and mouth microbes in captive versus wild boreal toads, and that the degree of difference depend on developmental stage. Skin bacteria from captive versus wild tadpoles were more similar relative to post-metamorphic life stages. When captive reared tadpoles were introduced to a wild site, their skin bacteria changed to mirror wild boreal toads within weeks. Similarly, the microbiome of reintroduced adult boreal toads also shifted to mirror wild-type microbes. Our results indicate that the microbial signature of boreal toads reared in captivity does not persist after release into natural habitat. The relationship between changing microbes and host health is not well understood for the majority of animal species but is an important part of wildlife conservation.

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 bullfrogonly
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.

Recent work has shown that many amphibians are biofluorescent. Biofluorescence describes an organism’s ability to absorb visible and ultraviolet light and re-emit it at a lower energy level (e.g., blue light re-emitted as green fluorescence). However, the function of fluorescence in amphibians is unclear. We observed paedomorphic western tiger salamanders at Lily Lake in Rocky Mountain National Park and obtained the first images recorded at this park of biofluorescence in these animals in response to blue light.

Dr. Cecil Schwalbe passed away on 3 April 2022 from complications after a heart attack and pneumonia. Cecil was one of the early Principal Investigators for ARMI. His lab provided long term data from the desert southwest on summer breeding amphibians, bullfrog eradication, disease, and leopard frog conservation. Cecil’s work at Buenos Aires National Wildlife Refuge laid a foundation for additional ARMI efforts in expanding model development on occupancy, spatially explicit metapopulation theory, Chiricahua leopard frog survival, and habitat connectivity. ARMI post doc Richard Chandler and graduate students Chris Jarchow and Paige Howell led this work, but Cecil was supportive and interested in the research and how it contributed to conservation efforts (e.g., Chandler et al. 2015, Jarchow et al. 2016, Howell et al. 2016, 2018, 2019).

Cecil also contributed to collaborative ARMI efforts (e.g., Muths et al. 2005) and was always present at ARMI meetings to keep things field-oriented and to maintain an appropriate sense of humor. He retired from ARMI and the USGS in 2013, but remained active in the herpetological community. Cecil was an old-school herpetologist and while he would rather be investigating frog populations in the field or showing Gila monsters to school kids, he would thoughtfully listen to the reasoning behind monitoring protocols and models and provide input on field implementation for ARMI projects.

In addition to his PhD in zoology and physiology from the University of Arizona and a master’s degree from Washington State, Cecil held a bachelor’s degree in mechanical engineering from Rice University and was Arizona’s first State Herpetologist. His enthusiasm and dedication to conservation influenced many young scientists including some of us in ARMI. In recognition of his mentoring and influence, Cecil received the Jarchow Conservation Award in 1997 and the Charlie W. Painter Memorial Award in 2021 from SW Partners in Amphibian and Reptile Conservation.

Cecil is survived by his wife Carol, sons Adam and Ethan, two granddaughters, and his sister. The family requests that in lieu of flowers, donations be made in memory of Cecil, to the Cold-Blooded Research Fund in the School of Natural Resources and the Environment at the University of Arizona: https://give.uafoundation.org/cecilschwalbe. In keeping with Cecil’s profession and passion, the annual payout from this endowed fund will support research awards for undergraduate students, graduate students and faculty members who are studying amphibians, reptiles, or fish.

Cecil’s laugh and his off-color sense of humor will be missed by all of us and the herpetofauna that he cared about.

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.

We observed multiple toads in amplexus and depositing egg strings among the vegetation. The following night (2230 h on 28 May 2021) a convergence of over a dozen Western Tiger Salamander (Ambystoma mavortium) individuals was observed consuming A. boreas eggs that had been deposited 24-48 hours earlier

Data used in the manuscript presenting 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.

Data used in manuscript that examines several potential factors influencing disease dynamics in the boreal toad–disease system: geographic isolation of populations, amphibian community richness, elevational differences, and habitat permanence.

Data used in Bayesian formulation of an open population capture-recapture model with >30 years of data to examine intrinsic and extrinsic factors regulating two populations of adult boreal chorus frogs (Pseudacris maculata).

Data used in an assessment of the effects of snowpack, temperature and disease on demography in boreal toads in Wyoming.

comparison of handling times - PIT (passive integrated transponder) tagging versus photography for boreal toads in Wyoming and Colorado

In Focus: Valenzuela-Sanchez, 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, XX, XXXX-XXXX. 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-Sanchez 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-Sanchez et al. found that demographic compensation via compensatory 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-Sanchez 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 number of juveniles in a given population that suggest a possible prevalence threshold when increased reproductive effort may occur. 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.

Pathogens such as ranaviruses and the novel amphibian chytrid fungus (Bd) are threats to 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 (2001–2020) and Bd (2000–2020) and provide insight into future threats and conservation strategies. Our comprehension of amphibian disease in the GYE is based on >20 years of monitoring, surveys, population studies, and opportunistic observations of mortality events. Diseases caused by these pathogens affect local species differently, depending on temperature, community structure, and location in the GYE. Bd has not been linked to die-offs but evidence for ongoing negative effects on survival contributes to foundational data on the effects of this pathogen in North America. There is less information on how ranaviruses affect amphibian vital rates, partly because ranaviruses are more difficult to study than Bd, but local mortality events attributed to, or consistent with, disease from ranaviruses are widespread in the GYE. The significance of disease in the long-term persistence of amphibians in the GYE is linked to anticipated changes in climate, especially drought. Other stressors, such as expected increases in visitor use and its associated impacts, are likely to exacerbate the effects of disease. Long-term information from this large, intact landscape helps to frame our understanding of the response of amphibians to disease and provides data that can contribute to management decisions, mitigation strategies, and forecasting efforts.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging, yet ectothermic tetrapods are under-represented in this comparative landscape despite their suitability for testing evolutionary hypotheses. We provide the first comprehensive study of aging rates and longevity across tetrapod ectotherms in the wild, utilizing data from 107 populations (77 species) of reptiles and amphibians. We test hypotheses of how thermoregulatory mode, temperature, protective phenotypes, and pace of life contribute to aging. Controlling for phylogeny and body size, ectotherms displayed a higher diversity of aging rates than endotherms, and included many groups with negligible aging. Furthermore, protective phenotypes and life-history tactics further explained macroevolutionary patterns of aging. By including ectothermic tetrapods, our comparative analyses enhance our understanding of aging evolution.

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 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.

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. 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 complicated 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.

1. The increasing frequency and severity of drought has the potential to exacerbate existing 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-induced declines. The application of dynamic occupancy modeling to longitudinal monitoring data estimates the effect of specific variables on population change, providing key insights into potential management strategies for drought resilience.
2. We synthesized a decade (2009 – 2019) of amphibian survey data from multiple monitoring programs across the California Bay Area and used occupancy modeling to estimate the influence of drought, invasive species, and land use on species’ persistence and colonization probabilities. The geographic and temporal scale of our dataset, consisting of 2574 surveys of seven species in 473 ponds, allowed us to quantify regional trends for an entire community of pond-breeding amphibians.
3. An extreme drought from 2012 – 2015 resulted in losses of breeding sites, with 51% of ponds drying in 2014 compared to <10% in non-drought years. Pond drying reduced persistence rates, and nearly every species exhibited reduced occupancy during the drought, with some species (American bullfrogs and California newts) declining by > 25%. Drought reduced occupancy via additional mechanisms beyond habitat loss; for example, lower spring precipitation (an important cue for breeding) was associated with reduced colonization.
4. During drought, native species’ persistence was higher in permanent relative to temporary ponds, even though these sites were also more likely to contain invasive fish and bullfrogs, which generally reduced native amphibian occupancy. Many of these permanent ponds dried during the worst year of drought, leading to extirpations of invasive species that appeared long-lasting. In contrast, native species rebounded quickly with returning rains and showed evidence of full recovery.
5. Synthesis and applications: Despite experiencing one of most severe droughts in a millennium, native species displayed high resilience. Due to longer recovery times by non-native relative to native species, drought presents a valuable management opportunity to remove invaders from key refugia, and we highlight the value of maintaining hydroperiod diversity to promote the persistence of multiple species.

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 March 5 - March 30. Averaged across years, estimated probability of occupancy was https://0.58 (SE = 0.09) for historical sites and https://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 https://0.23 to https://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.

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 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, Rana temporaria) and Bufonidae (Anaxyrus boreas, 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 increase predicted by IPCC 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.

Sex-related differences in mortality are widespread in the living world. Although sexual selection and environmental conditions might drive sex-specific variation in lifespan, recent findings suggest that sex chromosome systems are also involved. However, the influence of sex chromosome systems on aging rate (i.e., the rate of increase of mortality with age), a mortality metric that only partially correlates with lifespan, has not been investigated so far, due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (with heterogametic females) sex-determination systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly switched over the past 200 million years we examine whether sex heterogamety can predict sex-differences in aging rates. We show that variation in aging rate only accounts for a moderate proportion of the variation in lifespan, similarly to what has been reported in mammals. Moreover, our results demonstrate that the system of genetic sex-determination has a critical impact on aging rate in clades that include closely related taxa with XY vs. ZW systems. In both systems the heterogametic sex experiences a higher aging rate compared to the homogametic sex. This new finding suggests 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.