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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.

Ranaviruses are emerging pathogens that have caused mortality events in amphibians worldwide. Despite the negative effects of ranaviruses on amphibian populations, monitoring efforts are still lacking in many areas, including in the Prairie Pothole Region (PPR) of North America. Some PPR wetlands in Montana and North Dakota (USA) have been contaminated by energy-related saline wastewaters, and increased salinity has been linked to greater severity of ranavirus infections. In 2017, we tested tissues from larvae collected at 7 wetlands that ranged in salinity from 26 to 4103 mg Cl l-1. In 2019, we used environmental DNA (eDNA) to test for ranaviruses in 30 wetlands that ranged in salinity from 26 to 11754 mg Cl l-1. A previous study (2013-2014) found that ranavirus-infected amphibians were common across North Dakota, including in some wetlands near our study area. Overall, only 1 larva tested positive for ranavirus infection, and we did not detect ranavirus in any eDNA samples. There are several potential reasons why we found so little evidence of ranaviruses, including low larval sample sizes, mismatch between sampling and disease occurrence, larger pore size of our eDNA filters, temporal variation in outbreaks, low host abundance, or low occurrence or prevalence of ranaviruses in the wetlands we sampled. We suggest future monitoring efforts be conducted to better understand the occurrence and prevalence of ranaviruses within the PPR.

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.

The emerging amphibian pathogen Batrachochytrium salamandrivorans (Bsal) is a severe threat to global urodelan (salamanders, newts, and related taxa) biodiversity. Bsal has not been detected, to date, in North America, but the risk is high because North America is one of the global hotspots for urodelan biodiversity. The North American and United States response to the discovery of Bsal in Europe was to take a risk-based approach to preventive management actions, including interim regulations on importation of captive salamanders and a large-scale surveillance effort. Risk-based approaches to decision-making can extend to adaptive management cycles by periodically incorporating new information that reduces uncertainty in an estimate of risk or to assess the effect of mitigation actions which reduce risk directly. Our objectives were to evaluate the effects of regulatory action on the introduction of Bsal to the U.S., quantify how a large-scale surveillance effort impacted consequence risk, and to combine other new information on species susceptibility to re-evaluate Bsal risk to the U.S. Import regulations effectively reduced import volume of targeted species, but new research on species susceptibility suggests the list of regulated species was incomplete regarding Bsal reservoir species. Not detecting Bsal in an intensive surveillance effort improved confidence that Bsal was not present, however, the overall risk-reduction impact was limited because of the expansive area of interest (conterminous United States) and limited time frame of sampling. Overall, the preventive actions in response to the Bsal threat did reduce Bsal risk in the U.S. and we present an updated risk assessment to provide information for adaptive decision-making.

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.

We describe biotic and abiotic factors that interact with field work to contribute to gradients in human-mediated herpetofaunal pathogen transmission (i.e., translocation) risk between sites. Using biotic and abiotic criteria, we identify site conditions that correspond to high risk for pathogen import [to a site] or high risk for pathogen export [from a site] for implementation of enhanced between-site biosecurity procedures to forestall human-mediated pathogen transmission. Our field-site criteria are based on seven contexts of the pathogen (occurrence, habitat), host(s) (occurrence, habitat, species richness), and geography (distance/topography, geopolitical land use) (Table 1). We do not provide an explicit decision tree because site contexts can be complex, and single contexts may be weighted heavily in some biosecurity decisions, warranting case-by-case decisions. A more conceptual decision tree (Fig. 1) about pathogen export or import can be more flexibly applied as site context vary. Our aim is to provide a rapid process to develop a qualitative narrative to support decisions for between-site herpetological disease biosecurity.

North America’s protected lands harbor significant biodiversity and provide habitats where species threatened by a variety of stressors in other environments can thrive. Yet disease, climate change, and other threats are not limited by land management boundaries and can interact with conditions within protected landscapes to affect sensitive populations. We examined the population dynamics of a boreal toad (Anaxyrus boreas) metapopulation at a wildlife refuge in northwestern Montana over a 16-year period (2003-2018). We used robust design capture-recapture models to estimate male population size, recruitment, and apparent survival over time and in relation to the amphibian chytrid fungus, Batrachochytrium dendrobatidis. We estimated female population size in years with sufficient captures. Finally, we examined trends in male and female toad body size and condition. We found no evidence of an effect of disease or time on male toad survival but detected a strong negative trend in recruitment of new males to the population. Estimates of male and female abundance decreased dramatically over time. Body size of males and females was inversely related to estimated population size, consistent with reduced recruitment to replace adults, but body condition of adult males was only weakly associated with abundance. Together, these results describe the demography of a near-extinction event, and point to dramatic decreases in the recruitment of new individuals to the breeding population as the cause of this decline. We surmise that processes related to the restoration of historical hydrology within the refuge adversely affected amphibian breeding habitat, and that these changes interacted with disease, life history, and other factors to restrict the recruitment of new individuals to the breeding population over time. Our results point to challenges in understanding and predicting drivers of population change and highlight that current metrics for assessing population status can have limited predictive ability.

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 organization, 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.

Batrachochytrium salamandrovorans (Bsal) is a fungal pathogen that can cause the emerging infectious disease Bsal chytridiomycosis in some amphibians, and is currently causing dramatic declines in European urodeles. To date, Bsal has not been detected in North America but has the potential to cause severe declines in naïve hosts if introduced. Therefore, it is critical that wildlife managers are prepared with effective management actions to combat the fungus. Research has been initiated to identify strategies; however, managers need guidance to prepare for an outbreak until results are available. Here, we conducted a workshop with participants of a Bsal symposium to describe the expected effect of eleven management actions that could be implemented for Bsal in three salamander communities in the northwestern, northeastern, and southeastern United States. Participants expected variation in the proposed management actions to decrease pathogen transmission and increase host survival, but also expected that the selection of a management action may depend on the specific membership of the amphibian community. Collectively, this assessment will help refine research and modeling priorities in an effort to mitigate the risk of Bsal to native U.S. amphibians.

Emerging infectious diseases can result in species declines and hamper recovery efforts for at-risk populations. Generalizing considerations for reducing the risk of pathogen introduction and mitigating the effects of disease remains challenging and inhibits our ability to provide guidance for species recovery planning. Given the growing rates of emerging pathogens globally, we identify key principles and mechanisms for maintaining sustainable populations in the face of emerging diseases (including minimizing the risk of pathogen introductions and their future effects on hosts). Our synthesis serves as a reference for minimizing the risk of future disease outbreaks, mitigating the deleterious effects of future disease outbreaks on species extinction risk, and a review of the theoretical and/or empirical examples supporting these considerations.

The U.S. Fish and Wildlife Service listed Anaxyrus canorus, the Yosemite toad, as federally threatened in 2014 based upon reported population declines and vulnerability to global-change factors. A. canorus lives only in California’s central Sierra Nevada at medium to sub-alpine elevations. Lands throughout its range are protected from development, but climate and other global-change factors potentially can limit populations. A. canorus reproduces in ultra-shallow wetlands that typically hydrate seasonally via melting of the winter snowpack. Lesser snowpacks in drier years can render wetland water volumes and hydroperiods insufficient to allow for successful breeding and reproduction. Additionally, breeding and embryogenesis occur very soon after wetlands thaw when overnight temperatures can be below freezing. Diseases, such as chytridiomycosis, which recently decimated regional populations of ranid species, also might cause declines of A. canorus populations. However, reported studies focused on whether climate interacts with any pathogens to affect fitness in A. canorus have been scarce. We investigated effects of these factors on A. canorus near Tioga Pass from 1996 to 2001. We found breeding subpopulations were distributed widely but inconsistently among potentially suitable wetlands and frequently consisted of small numbers of adults. We occasionally observed small but not alarming numbers of dead adults at breeding sites. In contrast, embryo mortality often was notably high, with the majority of embryos dead in some egg masses while mortality among coincidental Pseudacris regilla (Pacific treefrog) embryos in deeper water was lower. After sampling and experimentation, we concluded that freezing killed A. canorus embryos, especially near the tops of egg masses, which enabled Saprolegnia diclina (a water mold [Oomycota]) to infect and then spread through egg masses and kill more embryos, often in conjunction with predatory flatworms (Turbellaria spp.). We also concluded exposure to ultraviolet-B radiation did not play a role. Based upon our assessments of daily minimum temperatures recorded around snow-off during years before and after our field study, the freezing potential we observed at field sites during embryogenesis might have been commonplace beyond the years of our field study. However, interactions among snow quantity, the timing of snow-off, and coincidental air temperatures that determine such freezing potential make projections of future conditions highly uncertain, despite overall warming trends. Our results describe important effects from ongoing threats to the fitness and abundance of A. canorus via reduced reproduction success and demonstrate how climate conditions can exacerbate effects from pathogens to threaten the persistence of amphibian populations.

Populations of pond-breeding amphibians often have boom and bust patterns in recruitment, with large numbers of individuals metamorphosing in some years and few or none in other years. Environmental processes, such as pond freezing and drying, and biological factors (e.g., disease and predator community) can influence survival of early life stages and the probability of complete reproductive failure for amphibian populations. We used multi-state occupancy models to estimate probability of breeding and successful metamorphosis (the complements of reproductive failure), and explored environmental and biological factors influencing these processes.We applied both static and dynamic multistate occupancy modeling techniques to ten years (2001-2010) of boreal toad (Anaxyrus boreas boreas) data from 116 sites, and tested relationships between these probabilities and the presence of a pathogen (Batrachochytrium dendrobatidis), elevation, hydrology, relative snowpack in a given year, and the presence of trout (Onchorhyncus spp., Salvelinus fontinalis, and Salmo trutta). The probability of breeding at a site was influenced by elevation, with higher-elevation sites more likely to support breeding. The probability of metamorphosis, given breeding, was influenced by an interaction between hydrology and relative annual snowpack. The probability of metamorphosis was higher at ephemeral sites in years of relatively high snowpack, while at permanent sites, years of low snowpack lead to higher probabilities of metamorphosis. Across all sites, the probability of metamorphosis was high (0.75) for years with median snowpack levels at sites with recent breeding attempts, but lower (0.25) at newly colonized sites. Our results suggest that boreal toads are well-adapted to their current habitat, with both ephemeral and permanent sites likely to support breeding in years of median snowpack. However shifts in precipitation patterns or temperatures may have negative impacts on this species.

Understanding the demographic consequences of interactions among pathogens, hosts, and weather conditions is critical in determining how amphibian populations respond to disease and in identifying site-specific conservation actions that can be developed to bolster persistence of amphibian populations. We investigated population dynamics in Boreal Toads relative to abiotic (fall temperatures and snowpack) and biotic (the abundance of another anuran host and disease) characteristics of the local environment in Wyoming, USA. We used capture-recapture data and a multi-state model where state is treated as a hidden Markov process to incorporate disease state uncertainty and assess our a priori hypotheses. Our results indicate that snowpack during the coldest week of the winter is more influential to toad survival, disease transition probabilities, and the population-level prevalence of the amphibian chytrid fungus (Batrachochytrium dendrobatidis) in the spring, than temperatures in the fall or the presence of another host. As hypothesized, apparent survival at low (i.e., <25 cm) snowpack (https://0.22 [CI: 0.15–0.31]) was lower than apparent survival at high snowpack (https://90.65 [CI: 0.50–0.78]). Our findings highlight the potential for local environmental factors, like snowpack, to influence disease and host persistence, and demonstrate the ecological complexity of disease effects on population demography in natural environments. This work further emphasizes the need for improved understanding of how climate change may influence the relationships among pathogens, hosts, and their environment for wild animal populations challenged by disease.

Tracking and understanding variation in pathogens such as Batrachochytrium dendrobatidis
(Bd), the agent of amphibian chytridiomycosis, which has caused population declines
globally, is a priority for many land managers. However, relatively little sampling of amphibian
communities has occurred at high latitudes. We used skin swabs collected during 2005?2017 from
boreal toads Anaxyrus boreas (n = 248), in southeast Alaska (USA; primarily in and near Klondike
Gold Rush National Historical Park [KLGO]) and northwest British Columbia (Canada) to determine
how Bd prevalence varied across life stages, habitat characteristics, local species richness,
and time. Across all years, Bd prevalence peaked in June and was >3 times greater for adult toads
(37.5%) vs. juveniles and metamorphs (11.2%). Bd prevalence for toads in the KLGO area, where
other amphibian species are rare or absent, was highest from river habitats (55.0%), followed by
human-modified upland wetlands (32.3%) and natural upland wetlands (12.7%)—the same rankorder
these habitats are used for toad breeding. None of the 12 Columbia spotted frogs Rana
luteiventris or 2 wood frogs R. sylvatica from the study area tested Bd-positive, although all were
from an area of low host density where Bd has not been detected. Prevalence of Bd on toads in the
KLGO area decreased during 2005?2015. This trend from a largely single-species system may be
encouraging or concerning, depending on how Bd is affecting vital rates, and emphasizes the
need to understand effects of pathogens before translating disease prevalence into management
actions.

Batrachochytrium dendrobatidis (Bd), a fungal pathogen that causes amphibian chytridiomycosis, has been implicated in population declines globally. To better understand how Bd affects survival and how threats vary spatially and temporally, we conducted long-term (range: 9–13 yrs) capture-recapture studies of boreal toads (Anaxyrus boreas) from three similar communities in western Montana. We also estimated temporal and spatial variation in population-level Bd prevalence among populations and the potential role of co-occurring Columbia spotted frogs (Rana luteiventris) in driving infection dynamics. Hierarchical models that accounted for detection uncertainty revealed Bd reduced apparent survival in one population that declined, was unassociated with survival in one stationary population, and was associated with increased survival in one population that is near extirpation. Despite different effects of Bd on hosts, pathogen prevalence was similar and synchronous across the populations separated by 111 – 176 km. Variation in Bd prevalence was driven partly by seasonal temperatures, but opposite the direction expected. Bd prevalence also decreased sharply over time across all populations, unrelated to trends in temperature, boreal toad survival, or infection dynamics of co-occurring Columbia spotted frogs. Toad Bd prevalence increased when frog abundance was high, consistent with an amplification effect. However, Bd prevalence of toads decreased as Bd prevalence of spotted frogs increased, consistent with a dilution effect. Our results reveal surprising variation in responses to Bd and show pathogen prevalence is not predictive of survival or population risk, and they illustrate the complexity in understanding disease dynamics across multiple populations.

Life history theory suggests that long-lived, pond-breeding amphibians should have low and highly variable early life-stage survival rates, but this theoretical expectation is often untested and the causes of variation are usually unknown. We evaluated the impact of hydroperiod, presence of a pathogen (Batrachochytrium dendrobatidis [Bd]), presence of a potential predator (cutthroat trout Oncorhychus clarki stomias), and whether animals had been reintroduced into a site, on survival of early life stages of boreal toads (Anaxyrus boreas boreas). We used a multi-state mark-recapture framework to estimate survival of boreal toad embryos from egg to metamorphosis at four sites over five years. We found substantial spatial and temporal variation in survival to metamorphosis and documented some evidence that monthly tadpole survival was lower in sites with Bd, and without trout, and at permanent sites. Our results support theories of amphibian life history, aid in the management of this species of conservation concern, and contribute to our knowledge of the ecology of the species. Additionally, we present methodology that allows practitioners to account for different lengths of time between sampling periods when estimating survival probabilities and which is especially applicable to organisms with distinct biological stages.

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a one-day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the fungal pathogen Batrachochytrium salamandrivorans in amphibians. Despite inevitable uncertainty, experts were able to suggest and discuss several possible strategies. However, their recommendations were undermined by imperfect definitions of the objectives and scope of management, a problem likely to arise in most real-world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial-temporal scale of mitigation decisions. Managers may feel under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes.

One of the leading causes of global amphibian decline is emerging infectious disease. We summarize the disease ecology of four major emerging amphibian infectious agents: chytrids, ranaviruses, trematodes, and Perkinsea. We focus on recently developed quantitative advances that build on well-established ecological theories and aid in studying epizootic and enzootic disease dynamics. For example, we identify ecological and evolutionary selective forces that determine disease outcomes and transmission pathways by borrowing ideas from population and community ecology theory. We outline three topics of general interest in disease ecology: (i) the relationship between biodiversity and disease risk, (ii) individual, species, or environmental transmission heterogeneity, and (iii) pathogen coinfections. Finally, we identify specific knowledge gaps impeding the success of conservation-related decisions for disease mitigation and the future of amphibian conservation success.