Roland A. Knapp

Dynamics of an emerging disease drive large-scale amphibian population extinctions

Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host–pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host–pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at ≈700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the near-simultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.

Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians

Chytridiomycosis, the disease caused by the chytrid fungus, Batrachochytrium dendrobatidis (Bd), has contributed to amphibian population declines and extinctions worldwide. The impact of this pathogen, however, varies markedly among amphibian species and populations. Following invasion into some areas of Californias Sierra Nevada, Bd leads to rapid declines and local extinctions of frog populations (Rana muscosa, R. sierrae). In other areas, infected populations of the same frog species have declined but persisted at low host densities for many years. We present results of a 5-year study showing that infected adult frogs in persistent populations have low fungal loads, are surviving between years, and frequently lose and regain the infection. Here we put forward the hypothesis that fungal load dynamics can explain the different population-level outcomes of Bd observed in different areas of the Sierra Nevada and possibly throughout the world. We develop a model that incorporates the biological details of the Bd-host interaction. Importantly, model results suggest that host persistence versus extinction does not require differences in host susceptibility, pathogen virulence, or environmental conditions, and may be just epidemic and endemic population dynamics of the same host–pathogen system. The different disease outcomes seen in natural populations may result solely from density-dependent host–pathogen dynamics. The model also shows that persistence of Bd is enhanced by the long-lived tadpole stage that characterize these two frog species, and by nonhost Bd reservoirs.

RESISTANCE AND RESILIENCE OF ALPINE LAKE FAUNA TO FISH INTRODUCTIONS

This paper reports on the response by amphibians, benthic macroinverte- brates, and zooplankton in naturally fishless alpine lakes to fish introductions and subsequent fish disappearance. We assessed resistance (the degree to which a system is altered when the environment changes) by comparing faunal distribution and abundance in lakes that have never been stocked with fish vs. the distribution and abundance in lakes that have been stocked and still contain fish. We assessed resilience (the degree and rate of a systems return to its previous configuration once the perturbation is removed) by comparing faunal distribution and abundance in lakes that were stocked at one time but have since reverted to a fishless condition (stocked-now-fishless lakes) vs. the distribution and abundance in lakes that have never been stocked. We quantified recovery rates and trajectories by com- paring faunal assemblages of stocked-now-fishless lakes that had been fishless for 5-10, 11-20, and .20 yr. Faunal assemblages in the study lakes had low resistance to fish introductions, but in general showed high resilience. The mountain yellow-legged frog (Rana muscosa), con- spicuous benthic macroinvertebrates, and large crustacean zooplankton (.1 mm) were dramatically reduced in distribution and abundance by fish introductions but generally recovered to predisturbance levels after fish disappearance. Inconspicuous benthic inver- tebrate taxa, small crustacean zooplankton (,1 mm), and rotiferan zooplankton (,0.2 mm) were either unaffected by fish or increased in the presence of fish. For both the benthic macroinvertebrate community and the zooplankton community as a whole, fish disappear- ance was followed by a steady change away from the configuration characteristic of fish- containing lakes and toward that of lakes that had never been stocked. Both communities remained markedly different from those in never-stocked lakes 5-10 yr after fish disap- pearance and converged on the configuration of never-stocked lakes only 11-20 yr after fish disappearance. Recovery was likely facilitated by the winged adult stages of many benthic macroin- vertebrates, resting eggs of zooplankton, and nearby source populations of frogs. However, many frog populations have disappeared since the time that lakes in this study reverted to a fishless condition, and the viability of zooplankton egg banks should decline in fish- containing lakes over time. As a result, faunal resilience may be lower in lakes that revert to a fishless condition today than is suggested by the results of our study. These findings have important implications for the restoration of alpine lake ecosystems.

EMERGING INFECTIOUS DISEASE AS A PROXIMATE CAUSE OF AMPHIBIAN MASS MORTALITY

A newly discovered infectious disease of amphibians, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, is implicated in population declines and possible extinctions throughout the world. The purpose of our study was to examine the effects of B. dendrobatidis on the mountain yellow-legged frog (Rana muscosa) in the Sierra Nevada of California (USA). We (1) quantified the prevalence and incidence of B. dendrobatidis through repeat surveys of several hundred R. muscosa populations in the southern Sierra Nevada; (2) described the population-level effects of B. dendrobatidis on R. muscosa population abundance; and (3) compared the mortality rates of infected and uninfected R. muscosa individuals from pre- through post-metamorphosis using both laboratory and field experiments. Mouthpart inspections conducted in 144 and 132 R. muscosa populations in 2003 and 2004, respectively, indicated that 19% of R. muscosa populations in both years showed indications of chytridiomycosis. Sixteen percent of populations that were uninfected in 2003 became infected by 2004. Rana muscosa population sizes were reduced by an average of 88% following B. dendrobatidis outbreaks at six sites, but at seven B. dendrobatidis-negative sites, R. muscosa population sizes increased by an average of 45% over the same time period. In the laboratory, all infected R. muscosa developed fatal chytridiomycosis after metamorphosis, while all uninfected individuals remained healthy. In the field experiment in which R. muscosa tadpoles were caged at infected and uninfected sites, 96% of the individuals that metamorphosed at infected sites died vs. 5% at the uninfected sites. These studies indicate that chytridiomycosis causes high mortality in post-metamorphic R. muscosa, that this emerging disease is the proximate cause of numerous observed R. muscosa population declines, and that the disease threatens this species with extirpation at numerous sites in Californias Sierra Nevada.

INVESTIGATING THE POPULATION‐LEVEL EFFECTS OF CHYTRIDIOMYCOSIS: AN EMERGING INFECTIOUS DISEASE OF AMPHIBIANS

Chytridiomycosis is an emerging infectious disease that has recently been reported in amphibian populations throughout the world. It has been associated with many cases of population declines and extinctions. In some areas of the Sierra Nevada of Cali- fornia the disease appears to be the causal factor in the rapid extinction of local populations of the mountain yellow-legged frog, Rana muscosa, within a few years of the first detection of the disease. In other areas, however, R. muscosa populations appear to persist for many years, despite high levels of infection in tadpoles. Here we present simple models of the dynamics of the disease within an individual lake and ask whether our current understanding of the disease is consistent with the field survey observations of: (a) extinction due to the disease over a wide range of host population sizes, and (b) persistence of frog populations with the disease at some sites. Despite our laboratory observation of chytridiomycosis being invariably lethal to postmetamorphic frogs, the observed long-term persistence of infected frog populations can only be explained if at least some infected adult frogs survive and reproduce.

Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis

Global amphibian decline by chytridiomycosis is a major environmental disaster that has been attributed to either recent fungal spread or environmental change that promotes disease. Here, we present a population genetic comparison of Batrachochytrium dendrobatidis isolates from an intensively studied region of frog decline, the Sierra Nevada of California. In support of a novel pathogen, we find low diversity, no amphibian-host specificity, little correlation between fungal genotype and geography, local frog extirpation by a single fungal genotype, and evidence of human-assisted fungus migration. In support of endemism, at a local scale, we find some diverse, recombining populations. Therefore neither epidemic spread nor endemism alone explains this particular amphibian decline. Recombination raises the possibility of resistant sporangia and a mechanism for rapid spread as well as persistence that could greatly complicate global control of the pathogen.

Alteration of Nutrient Cycles and Algal Production Resulting from Fish Introductions into Mountain Lakes

The introduction of salmonid fishes into naturally fishless lakes represents one of the most prevalent environmental modifications of aquatic ecosystems in western North America. Introduced fish may alter lake nutrient cycles and primary production, but the magnitude and variation of these effects have not been fully explored. We used bioenergetics modeling to estimate the contributions of stocked trout to phosphorus (P) cycles across a wide range of fish densities in lakes of the Sierra Nevada, California. We also assessed the larger effects of fish-induced changes in phosphorus cycling on primary production using paleolimnological analyses from lakes in the southern Canadian Rockies. Our analyses showed that total P recycling by fish was independent of fish density but positively related to fish biomass in the Sierra Nevada. In lakes with fish populations maintained by continued stocking, fish recycled P at over twice the rate of those in lakes where introduced fish populations are maintained by natural reproduction and stocking has been discontinued. We estimate that P regeneration by introduced fishes is approximately equivalent to atmospheric P deposition to these lakes. Paleolimnological analyses indicated that algal production increased substantially following trout introductions to Rocky Mountain lakes and was maintained for the duration of fish presence. The results of our modeling and paleolimnological analyses indicate that introduced trout fundamentally alter nutrient cycles and stimulate primary production by accessing benthic P sources that are not normally available to pelagic communities in oligotrophic mountain lakes. These effects pose a difficult challenge for managers charged with balancing the demand for recreational fisheries with the need to maintain natural ecosystem processes.

DEVELOPING PROBABILISTIC MODELS TO PREDICT AMPHIBIAN SITE OCCUPANCY IN A PATCHY LANDSCAPE

Human-caused fragmentation of habitats is threatening an increasing number of animal and plant species, making an understanding of the factors influencing patch occupancy ever more important. The overall goal of the current study was to develop probabilistic models of patch occupancy for the mountain yellow-legged frog (Rana mus- cosa). This once-common species has declined dramatically, at least in part as a result of habitat fragmentation resulting from the introduction of predatory fish. We first describe a model of frog patch occupancy developed using semiparametric logistic regression that is based on habitat characteristics, fish presence/absence, and a spatial location term (the latter to account for spatial autocorrelation in the data). This model had several limitations in- cluding being constrained in its use to only the study area. We therefore developed a more general model that incorporated spatial autocorrelation through the use of an autocovariate term that describes the degree of isolation from neighboring frog populations (autologistic model). After accounting for spatial autocorrelation in patch occupancy, both models in- dicated that the probability of frog presence was strongly influenced by lake depth, elevation, fish presence/absence, substrate characteristics, and the degree of lake isolation. Based on cross-validation procedures, both models provided good fits to the data, but the autologistic model was more useful in predicting patch occupancy by frogs. We conclude by describing a possible application of this model in assessing the likelihood of persistence by frog

MULTIPLE STRESSORS AND AMPHIBIAN DECLINES: DUAL IMPACTS OF PESTICIDES AND FISH ON YELLOW-LEGGED FROGS

More than 40% of Earths 5700+ amphibian species have undergone recent declines. Despite the likely involvement of multiple factors in driving these declines, most studies continue to focus on single stressors. In California (USA), separate studies have implicated either introduced fish or pesticides as causal agents. To date, however, no study has simultaneously evaluated the respective roles of these two potential stressors nor attempted to assess their relative importance, information critical for the development of effective conservation efforts and environmental policies. We examined the role and relative effect of fish and pesticides on the mountain yellow-legged frog (Rana muscosa) using unusually detailed data sets for a large portion of R. muscosas historic range in Californias Sierra Nevada. Habitat characteristics and presence/absence of R. muscosa and fish were quantified at each of 6831 sites during field surveys. Pesticide use upwind of each site was calculated from pesticide application records and predominant wind directions. Using generalized additive models, we found that, after accounting for habitat effects, the probability of R. muscosa presence was significantly reduced by both fish and pesticides, with the landscape-scale effect of pesticides much stronger than that of fish. The degree to which a site was sheltered from the predominant wind (and associated pesticides) was also a significant predictor of R. muscosa presence. Taken together, these results represent the strongest evidence to date that windborne pesticides are contributing to amphibian declines in pristine locations. Our results suggest that amphibian declines may have complex multi-factorial causes, and caution that single-factor studies that demonstrate the importance of one factor should not be used as evidence against the importance of other factors.

The Introduction of Nonnative Fish into Wilderness Lakes: Good Intentions, Conflicting Mandates, and Unintended Consequences

Abstract