Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA.

From 1999 to 2006, we sampled > 1200 amphibians for the fungal pathogen Batrachochytrium dendrobatidis (Bd) at 30 sites in the southeastern USA. Using histological techniques or PCR assays, we detected chytrid infection in 10 species of aquatic-breeding amphibians in 6 states. The prevalence of chytrid infection was 17.8% for samples of postmetamorphic amphibians examined using skin swab-PCR assays (n = 202 samples from 12 species at 4 sites). In this subset of samples, anurans had a much higher prevalence of infection than caudates (39.2% vs. 5.5%, respectively). Mean prevalence in ranid frogs was 40.7%. The only infected salamanders were Notophthalmus viridescens at 3 sites. We found infected amphibians from late winter through late spring and in 1 autumn sample. Although we encountered moribund or dead amphibians at 9 sites, most mortality events were not attributed to Bd. Chytridiomycosis was established as the probable cause of illness or death in fewer than 10 individuals. Our observations suggest a pattern of widespread and subclinical infections. However, because most of the sites in our study were visited only once, we cannot dismiss the possibility that chytridiomycosis is adversely affecting some populations. Furthermore, although there is no evidence of chytrid-associated declines in our region, the presence of this pathogen is cause for concern given global climate change and other stressors. Although presence-absence surveys may still be needed for some taxa, such as bufonids, we recommend that future researchers focus on potential population-level effects at sites where Bd is now known to occur.

Ranavirus in wood frogs (Rana sylvatica): potential sources of transmission within and between ponds.

Members of the genus Ranavirus (family Iridoviridae) can cause catastrophic mortality of pond-breeding amphibians and are associated with an emerging infectious disease that may be contributing to amphibian declines. We conducted three experiments to examine factors that may affect transmission both within and between local breeding populations of the wood frog (Rana sylvatica). In a laboratory study, when exposed to moribund tadpoles collected during a local ranaviral die-off, uninfected tadpoles died as soon as 4 days after exposure. The onset of death was accelerated when tadpoles were allowed to scavenge on carcasses of infected tadpoles. In a mesocosm experiment that was conducted in outdoor wading pools, die-offs of tadpoles began approximately 19 days after infected tadpoles were added to pools containing uninfected tadpoles. Mass die-offs with greater than 98% mortality occurred in all pools, regardless of the initial tadpole density. In a second mesocosm experiment, the addition of water and bottom sediments that were collected from a pond during a ranaviral die-off did not result in lower tadpole survival or growth relative to controls. Only a small percentage of tadpoles appeared to be sick, and most tadpoles survived until the first individuals began metamorphosing within a pool. However, tests for ranavirus using polymerase chain reaction were positive for most pools that received contaminated sediment, suggesting that some infections were sublethal. Our results indicate that transmission within ponds is enhanced by scavenging and that spread between local ponds could occur via the transport of contaminated sediment by animals or humans.

Density of an intraguild predator mediates feeding group size, intraguild egg predation, and intra- and interspecific competition.

Intraguild predation (IGP) is common in most communities, but many aspects of density-dependent interactions of IG predators with IG prey are poorly resolved. Here, we examine how the density of an IG predator can affect feeding group size, IG egg predation, and the growth responses of IG prey. We used laboratory feeding trials and outdoor mesocosm experiments to study interactions between a social intraguild predator (larvae of the wood frog; Rana sylvatica) and its prey (spotted salamander; Ambystoma maculatum). Larvae of R. sylvatica could potentially affect A. maculatum by consuming shared larval food resources or by consuming eggs and hatchlings. However, successful egg predation requires group feeding by schooling tadpoles. We established from five to 1,190 hatchlings of R. sylvatica in mesocosms, then added either 20 A. maculatum hatchlings to study interspecific competition, or a single egg mass to examine IGP. Crowding strongly suppressed the growth of R. sylvatica, and IGP was restricted to the egg stage. In the larval competition experiment, growth of A. maculatum was inversely proportional to R. sylvatica density. In the predation experiment, embryonic mortality of A. maculatum was directly proportional to the initial density of R. sylvatica and the mean number of tadpoles foraging on egg masses. IGP on eggs reduced A. maculatum hatchling density, which accelerated larval growth. Surprisingly, the density of R. sylvatica had no overall effect on A. maculatum growth because release from intraspecific competition via egg predation was balanced by increased interspecific competition. Our results demonstrate that the density of a social IG predator can strongly influence the nature and intensity of interactions with a second guild member by simultaneously altering the intensity of IGP and intra- and interspecific competition.

Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes.

Ovipositing insects may avoid aquatic sites where there is high predation risk to their offspring, but the proximate mechanisms that mediate avoidance behavior are poorly resolved. We conducted an experiment to determine whether mosquitoes would reduce oviposition rates in pools containing chemicals of the mosquitofish (Gambusia affinis), a voracious predator that is widely employed to control mosquitoes. Experimental treatments consisted of outdoor pools that contained known concentrations of fish chemicals (low, medium, or high) or no fish chemicals (control). The pools were arranged in a randomized block design, and the number of mosquito larvae in each pool served as the response variable to estimate relative oviposition rate. Members of the Culex pipiens complex were the main colonizers of the pools. The mean number of larvae per pool differed among treatments (P = 0.026) and was about three times greater in control pools compared with those receiving medium and high concentrations of fish chemicals. Pairwise comparisons indicate that only medium and high treatments differed significantly from controls, suggesting that a threshold concentration exists below which mosquitoes cannot reliably detect predators. Our data suggest that the effectiveness of Gambusia affinis in controlling mosquitoes may be compromised if adult mosquitoes respond to fish stocking by shifting to nearby breeding sites that lack fish. We discuss issues conceming the use of Gambusia in biological control programs within the context of these new findings.

Pond tadpoles with generalized morphology: is it time to reconsider their functional roles in aquatic communities?

With rare exceptions, anuran larvae have traditionally been considered to occupy lower trophic levels in aquatic communities where they function as microphagous suspension feeders. This view is being challenged by studies showing that tadpoles with generalized morphology often function as macrophagous predators. Here, we review the literature concerning macrophagy by tadpoles and provide two additional examples involving generalized tadpoles. In the first, we demonstrate with laboratory and field experiments that wood frog (Rana sylvatica) tadpoles are major predators of macroinvertebrates in ponds. In the second, we show that green frog (R. clamitans) tadpoles can cause catastrophic reproductive failure of the wood frog via egg predation. These results and data from other studies challenge the assumption that generalized tadpoles function as filter-feeding omnivores, and question the general applicability of community organization models which assume that predation risk increases with pond permanence. We suggest that predation risk is greater in temporary ponds than in more permanent ponds for many organisms that are vulnerable to predation by tadpoles. This being so, a conditional model based upon interactions that are species-specific, life-stage-specific, and context-dependent may better explain community organization along hydrological gradients than models which assume that temporary ponds have few or no predators.

HABITAT DURATION, LENGTH OF LARVAL PERIOD, AND THE EVOLUTION OF A COMPLEX LIFE CYCLE OF A SALAMANDER, AMBYSTOMA TEXANUM.

In many organisms, genotypic selection may be a less effective means of adapting to unpredictable environments than is selection for phenotypic plasticity. To determine whether genotypic selection is important in the evolution of complex life cycles of amphibians that breed in seasonally ephemeral habitats, we examined whether mortality risk from habitat drying in natural populations of small-mouthed salamanders (Ambystoma texanum) corresponded to length of larval period when larvae from the same populations were grown in a common laboratory environment. Comparisons were made at two levels of organization within the species: 1) among geographic races that are under strongly divergent selection regimes associated with the use of pond and stream habitats and 2) among populations within races that use the same types of breeding habitats. Morphological evidence indicates that stream-breeding A. texanum evolved from pond-breeding populations that recently colonized streams. Larvae in streams incur heavy mortality from stream drying, so the upper bound on length of larval period is currently set by the seasonal duration of breeding sites. We hypothesized that selection would reduce length of larval period of pond-breeders that colonize streams if their larval periods are inherently longer than those of stream-breeders. The results of laboratory experiments support this hypothesis. When grown individually in a common environment, larvae from stream populations had significantly shorter larval periods than larvae from pond populations. Within races, however, length of larval period did not correlate significantly with seasonal duration of breeding sites. When males of both races were crossed to a single pond female, offspring of stream males had significantly shorter larval periods than offspring of pond males. Collectively, these data suggest that differences in complex life cycles among pond and stream-breeders are due to genotypic selection related to mortality from habitat drying. Stream larvae in the common-environment experiment were significantly smaller at metamorphosis than pond larvae. Yet, the evolution of metamorphic size cannot be explained readily by direct selection: there are no intuitively obvious advantages of being relatively small at metamorphosis in streams. A positive phenotypic correlation was observed between size at metamorphosis and length of larval period in most laboratory populations. A positive additive genetic correlation between these traits was demonstrated recently in another amphibian. Thus, we suspect that metamorphic size of stream-breeders evolved indirectly as a consequence of selection to shorten length of larval period.