Erin Muths

Quantitative evidence for the effects of multiple drivers on continental-scale amphibian declines

Since amphibian declines were first proposed as a global phenomenon over a quarter century ago, the conservation community has made little progress in halting or reversing these trends. The early search for a “smoking gun” was replaced with the expectation that declines are caused by multiple drivers. While field observations and experiments have identified factors leading to increased local extinction risk, evidence for effects of these drivers is lacking at large spatial scales. Here, we use observations of 389 time-series of 83 species and complexes from 61 study areas across North America to test the effects of 4 of the major hypothesized drivers of declines. While we find that local amphibian populations are being lost from metapopulations at an average rate of 3.79% per year, these declines are not related to any particular threat at the continental scale; likewise the effect of each stressor is variable at regional scales. This result - that exposure to threats varies spatially, and populations vary in their response - provides little generality in the development of conservation strategies. Greater emphasis on local solutions to this globally shared phenomenon is needed.

Evidence for disease-related amphibian decline in Colorado

The recent discovery of a pathogenic fungus (Batrachochytrium dendrobatidis) associated with declines of frogs in the American and Australian tropics, suggests that at least the proximate cause, may be known for many previously unexplained amphibian declines. We have monitored boreal toads in Colorado since 1991 at four sites using capture–recapture of adults and counts of egg masses to examine the dynamics of this metapopulation. Numbers of male toads declined in 1996 and 1999 with annual survival rate averaging 78% from 1991 to 1994, 45% in 1995 and 3% between 1998 and 1999. Numbers of egg masses also declined. An etiological diagnosis of chytridiomycosis consistent with infections by the genus Batrachochytrium was made in six wild adult toads. Characteristic histomorphological features (i.e. intracellular location, shape of thalli, presence of discharge tubes and rhizoids) of chytrid organisms, and host tissue response (acanthosis and hyperkeratosis) were observed in individual toads. These characteristics were indistinguishable from previously reported mortality events associated with chytrid fungus. We also observed epizootiological features consistent with mortality events associated with chytrid fungus: an increase in the ratio of female:male toads captured, an apparent spread of mortalities within the metapopulation and mortalities restricted to post metamorphic animals. Eleven years of population data suggest that this metapopulation of toads is in danger of extinction, pathological and epizootiological evidence indicates that B. dendrobatidis has played a proximate role in this process Published by Elsevier Science Ltd.

Mitigating amphibian disease: strategies to maintain wild populations and control chytridiomycosis

BackgroundRescuing 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.ResultsWe 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.ConclusionsBecause 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.

Trends in Amphibian Occupancy in the United States

Though a third of amphibian species worldwide are thought to be imperiled, existing assessments simply categorize extinction risk, providing little information on the rate of population losses. We conducted the first analysis of the rate of change in the probability that amphibians occupy ponds and other comparable habitat features across the United States. We found that overall occupancy by amphibians declined 3.7% annually from 2002 to 2011. Species that are Red-listed by the International Union for Conservation of Nature (IUCN) declined an average of 11.6% annually. All subsets of data examined had a declining trend including species in the IUCN Least Concern category. This analysis suggests that amphibian declines may be more widespread and severe than previously realized.

Effects of Amphibian Chytrid Fungus on Individual Survival Probability in Wild Boreal Toads

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.

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

Habitat loss and exposure to pesticides are likely primary factors contributing to amphibian decline in agricultural landscapes. Conservation efforts have attempted to restore wetlands lost through landscape modifications to reduce contaminant loads in surface waters and providing quality habitat to wildlife. The benefits of this increased wetland area, perhaps especially for amphibians, may be negated if habitat quality is insufficient to support persistent populations. We examined the presence of pesticides and nutrients in water and sediment as indicators of habitat quality and assessed the bioaccumulation of pesticides in the tissue of two native amphibian species Pseudacris maculata (chorus frogs) and Lithobates pipiens (leopard frogs) at six wetlands (3 restored and 3 reference) in Iowa, USA. Restored wetlands are positioned on the landscape to receive subsurface tile drainage water while reference wetlands receive water from overland run-off and shallow groundwater sources. Concentrations of the pesticides frequently detected in water and sediment samples were not different between wetland types. The median concentration of atrazine in surface water was 0.2 μg/L. Reproductive abnormalities in leopard frogs have been observed in other studies at these concentrations. Nutrient concentrations were higher in the restored wetlands but lower than concentrations thought lethal to frogs. Complex mixtures of pesticides including up to 8 fungicides, some previously unreported in tissue, were detected with concentrations ranging from 0.08 to 1,500 μg/kg wet weight. No significant differences in pesticide concentrations were observed between species, although concentrations tended to be higher in leopard frogs compared to chorus frogs, possibly because of differences in life histories. Our results provide information on habitat quality in restored wetlands that will assist state and federal agencies, landowners, and resource managers in identifying and implementing conservation and management actions for these and similar wetlands in agriculturally dominated landscapes.

Home Range and Movements of Boreal Toads in Undisturbed Habitat

Abstract I sampled movements and amount of area used by boreal toads (Bufo boreas) between June and October for 3 yr. Females were found farther from the breeding site than were males, and mean home ranges, as calculated by the adaptive kernel method, were four times larger for females than for males. Temperature and snow accumulation were comparable over the study, but data collection was hampered by mortality of animals caused by an outbreak of amphibian chytridiomycosis in yr 2. These data provide insight into use of habitat by boreal toads in undisturbed areas but may not be typical of a completely healthy population.

ESTIMATION OF TEMPORARY EMIGRATION IN MALE TOADS

Male boreal toads (Bufo boreas) are thought to return to the breeding site every year but, if absent in a particular year, will be more likely to return the following year. Using Pollocks robust design we estimated temporary emigration (the probability a male toad is absent from a breeding site in a given year) at three locations in Colorado, USA: two in Rocky Mountain National Park and one in Chaffee County. We present data that suggest that not all male toads return to the breeding site every year. Our analyses indicate that temporary emigration varies by site and time (for example, from 1992 to 1998, the probability of temporary emigration ranged from 10% to 29% and from 3% to 95% at Lost Lake and Kettle Tarn, respectively). Although the results provide weak evidence that males are more likely to return after a years hiatus, a general pattern of state-dependent temporary emigration was not supported. We also hypothesized relationships between temporary emigration and a number of weather variables. While some competitive models included weather covariates, imprecise and variable estimates of the effects of these covariates precluded fully defining their impact on temporary emigration.

VARIABLE BREEDING PHENOLOGY AFFECTS THE EXPOSURE OF AMPHIBIAN EMBRYOS TO ULTRAVIOLET RADIATION

Reduced water depth in dry years has been proposed to interact with ultra- violet-B (UV-B) radiation and a pathogenic fungus to cause episodes of high mortality of amphibian embryos. Observations of breeding phenology of boreal chorus frogs (Pseudacris maculata) in Colorado from 1986 to 2001 show that dry years result in earlier breeding. The earliest and latest dates of maximum calling activity by males were 20 May and 16 June, and the date of maximum calling was strongly related to the amount of snow accu- mulation during the winter. Surface UV-B flux, estimated from satellite-based measure- ments, was positively related to date of maximum calling. In dry years, surface UV-B during calling was reduced by an amount similar to that attributed to reduced depth. Al- though there was a significant trend of increasing UV-B from 1978 to 2001 on the average date (2 June) of maximum calling activity, there was no relationship between year and surface UV-B at actual dates of maximum calling. Exposure to extreme temperatures is an alternative explanation for increased mortality of amphibian embryos in shallow water.

A COMPARISON IN COLORADO OF THREE METHODS TO MONITOR BREEDING AMPHIBIANS

We surveyed amphibians at 4 montane and 2 plains lentic sites in northern Col- orado using 3 techniques: standardized call surveys, automated recording devices (frog-log- gers), and intensive surveys including capture-recapture techniques. Amphibians were ob- served at 5 sites. Species richness varied from 0 to 4 species at each site. Richness scores, the sums of species richness among sites, were similar among methods: 8 for call surveys, 10 for frog-loggers, and 11 for intensive surveys (9 if the non-vocal salamander Ambystoma tigrinum is excluded). The frog-logger at 1 site recorded Spea bombifrons which was not active during the times when call and intensive surveys were conducted. Relative abundance scores from call surveys failed to reflect a relatively large population of Bufo woodhousii at 1 site and only weakly differentiated among different-sized populations of Pseudacris maculata at 3 other sites. For ex- tensive applications, call surveys have the lowest costs and fewest requirements for highly trained personnel. However, for a variety of reasons, call surveys cannot be used with equal effectiveness in all parts of North America.