Keith A. Berven

Factors Affecting Population Fluctuations in Larval and Adult Stages of the Wood Frog (Rana Sylvatica)

During a 7-yr population study on the wood frog, Rana sylvatica, the breed- ing population size fluctuated by a factor of 10 and juvenile production by a factor of 100. Variation in the adult population among years was largely due to variation in juvenile recruitment. Annual net replacement rates (Ro) varied from 0.009 to 7.49. Survivorship curves (calculated using the number of eggs deposited as the initial point) showed that most variation in the proportion of individuals surviving to adulthood was due to variation in larval survival; juvenile and adult survival was relatively constant among years. Male and female survival did not differ. Because females matured a year later than males, on average 2.3 times as many males as females from a given clutch survived to breed. This difference accounted for the observed male-biased sex ratio in breeding choruses. Pre- metamorphic survival and size at metamorphosis were negatively correlated with the number of eggs deposited. Length of larval period was positively correlated with number of eggs deposited. Survival was higher among juveniles that metamorphosed early and were large at metamorphosis. Larger juveniles matured earlier and were also larger as adults. The population appeared to be regulated through density-dependent factors affecting larval survival, larval size, and time of metamorphosis. Adult population size also nega- tively affected total clutch volume. Mean monthly rainfall positively affected adult survival.

Species Diversities of Herpetofaunal Samples From Similar Microhabitats at Two Tropical Sites

Amphibians and reptiles were collected from tree buttresses in two different regions to determine whether within-habitat species diversity differences were evident. Using the method suggested by Pielou (1966), the average species diversity per individual was H = 1.92 ± .47 for the collection of amphibians and reptiles taken from tree buttresses in a tropical dry forest formation in Thailand, H = 4.95 ± .84 for the tree buttress collection taken in Ecuador. Part of the within-habitat diversity differences are due to a difference in kind of organism: a large number of terrestrial frogs are present in Ecuador; there are no terrestrial frogs from the Thai site. Other differences are also operating, however. The number of lizard species are comparable in the two collections (8 from Thailand, 10 from Ecuador) , yet the Brillouin diversity measure of the Ecuadorian lizard collection was NH = 2.24, higher than the diversity of the Thai lizard collection, NH = 1.25. The diversity differences are postulated to be due to different sizes of the total forest herpetofaunas of the two regions.

Stoichiometric implications of a biphasic life cycle

Animals mediate flows of elements and energy in ecosystems through processes such as nutrient sequestration in body tissues, and mineralization through excretion. For taxa with biphasic life cycles, the dramatic shifts in anatomy and physiology that occur during ontogeny are expected to be accompanied by changes in body and excreta stoichiometry, but remain little-explored, especially in vertebrates. Here we tested stoichiometric hypotheses related to the bodies and excreta of the wood frog (Lithobates sylvaticus) across life stages and during larval development. Per-capita rates of nitrogen (N) and phosphorus (P) excretion varied widely during larval ontogeny, followed unimodal patterns, and peaked midway through development (Taylor–Kollros stages XV and XII, respectively). Larval mass did not increase steadily during development but peaked at stage XVII and declined until the termination of the experiment at stage XXII. Mass-specific N and P excretion rates of the larvae decreased exponentially during development. When coupled with population-biomass estimates, population-level excretion rates were greatest at stages VIII–X. Percent carbon (C), N, and C:N of body tissue showed weak trends across major life stages; body P and C:P, however, increased sixfold during development from egg to adult. Our results demonstrate that intraspecific ontogenic changes in nutrient contents of excretion and body tissues can be significant, and that N and P are not always excreted proportionally throughout life cycles. These results highlight the dynamic roles that species play in ecosystems, and how the morphological and physiological changes that accompany ontogeny can influence ecosystem-level processes.

Ecological stoichiometry quantitatively predicts responses of tadpoles to a food quality gradient

Ecological stoichiometry (ES) uses elemental ratios and mass balance to explain organismal growth, an important parameter in ecological systems. In this study, we tested quantitative predictions of the ES minimal model for the growth rates of two tadpole species (wood frogs, Lithobates sylvaticus and American toads, Anaxyrus americanus), by manipulating light and the quality of a leaf litter mixture in a seminatural mesocosm experiment. We predicted that wood frogs, which consume leaf litter as a resource, would respond more strongly to leaf litter quality than toads, which forage on periphyton and algae. The ES minimal model, parameterized from literature values, provided strikingly accurate quantitative predictions of nonlinear wood frog growth patterns across gradients of leaf litter quality, both in this experiment and when applied to previously published data on wood frog growth responses to various leaf litter species. In contrast, toad growth was best explained by the biomass of periphyton, which was driven primarily by light availability and only indirectly influenced by litter-derived soluble polyphenols. This study demonstrates the power of ES to predict organism growth rates, and highlights potential applications of this theory to predicting population- and community-level responses to changing forest environments.

Leaf Litter Inhibits Growth of an Amphibian Fungal Pathogen

Past studies have found a heterogeneous distribution of the amphibian chytrid fungal pathogen, Batrachochytrium dendrobatidis (Bd). Recent studies have accounted for some of this heterogeneity through a positive association between canopy cover and Bd abundance, which is attributed to the cooling effect of canopy cover. We questioned whether leaf litter inputs that are also associated with canopy cover might also alter Bd growth. Leaf litter inputs exhibit tremendous interspecific chemical variation, and we hypothesized that Bd growth varies with leachate chemistry. We also hypothesized that Bd uses leaf litter as a growth substrate. To test these hypotheses, we conducted laboratory trials in which we exposed cultures of Bd to leachate of 12 temperate leaf litter species at varying dilutions. Using a subset of those 12 litter species, we also exposed Bd to pre-leached litter substrate. We found that exposure to litter leachate and substrate reduced Bd spore and sporangia densities, although there was substantial variation among treatments. In particular, Bd densities were inversely correlated with concentrations of phenolic acids. We conducted a field survey of phenolic concentrations in natural wetlands which verified that the leachate concentrations in our lab study are ecologically relevant. Our study reinforces prior indications that positive associations between canopy cover and Bd abundance are likely mediated by water temperature effects, but this phenomenon might be counteracted by changes in aquatic chemistry from leaf litter inputs.

Ontogenetic changes in sensitivity to nutrient limitation of tadpole growth

According to ecological stoichiometry (ES), the growth of a consumer with abundant resources should increase as body and resource stoichiometry become more similar. However, for organisms with complex life cycles involving distinct changes in biology, nutrient demands might change in response to ontogenetic changes in body stoichiometry. Tadpole growth and development has been found to be largely nitrogen (N) limited, as predicted for organisms developing N-rich tissues like muscle. However, tadpole metamorphosis includes periods of rapid development of phosphorus (P)-rich bones in preparation for a terrestrial lifestyle. We hypothesized that tadpole growth and development will exhibit variable nutrient demands during different stages of ontogeny, due to predictable changes in body tissue stoichiometry. To test this, we raised tadpoles on four diets with varying N:P ratios and assessed growth and developmental rates. Specifically, we predicted that tadpoles would be sensitive to N limitation throughout ontogeny (consistent with previous studies), but also sensitive to P limitation during the process of long-bone ossification. Consistent with our prediction, tadpole growth rates and development were sensitive to N limitation throughout ontogeny. Increased dietary N led to a shorter time to metamorphosis and a larger mass at metamorphosis. Also as predicted, growth rates were sensitive to both N and P during the period of peak bone ossification, indicative of co-limitation. These results indicate that P limitation changes through tadpole ontogeny consistent with, and can be predicted by, shifts in body tissue stoichiometry. Future studies should investigate whether ontogenetic shifts in tadpole P limitation lead to seasonal shifts in wetland nutrient cycling.

Leaf litter resource quality induces morphological changes in wood frog (Lithobates sylvaticus) metamorphs

For organisms that exhibit complex life cycles, resource conditions experienced by individuals before metamorphosis can strongly affect phenotypes later in life. Such resource-induced effects are known to arise from variation in resource quantity, yet little is known regarding effects stemming from variation in resource quality (e.g., chemistry). For larval anurans, we hypothesized that variation in resource quality will induce a gradient of effects on metamorph morphology. We conducted an outdoor mesocosm experiment in which we manipulated resource quality by rearing larval wood frogs (Lithobates sylvaticus) under 11 leaf litter treatments. The litter species represented plant species found in open- and closed-canopy wetlands and included many plant species of current conservation concern (e.g., green ash, common reed). Consistent with our hypothesis, we found a gradient of responses for nearly all mass-adjusted morphological dimensions. Hindlimb dimensions and gut mass were positively associated with litter nutrient content and decomposition rate. In contrast, forelimb length and head width were positively associated with concentrations of phenolic acids and dissolved organic carbon. Limb lengths and widths were positively related with the duration of larval period, and we discuss possible hormonal mechanisms underlying this relationship. There were very few, broad differences in morphological traits of metamorphs between open- and closed-canopy litter species or between litter and no-litter treatments. This suggests that the effects of litter on metamorph morphology are litter species-specific, indicating that the effects of changing plant community structure in and around wetlands will largely depend on plant species composition.

Bottom‐up and trait‐mediated effects of resource quality on amphibian parasitism

Leaf litter subsidies are important resources for aquatic consumers like tadpoles and snails, causing bottom-up effects on wetland ecosystems. Recent studies have shown that variation in litter nutritional quality can be as important as litter quantity in driving these bottom-up effects. Resource subsidies likely also have indirect and trait-mediated effects on predation and parasitism, but these potential effects remain largely unexplored. We generated predictions for differential effects of litter nutrition and secondary polyphenolic compounds on tadpole (Lithobates sylvatica) exposure and susceptibility to Ribeiroia ondatrae, based on ecological stoichiometry and community-ecology theory. We predicted direct and indirect effects on key traits of the tadpole host (rates of growth, development and survival), the trematode parasite (production of the cercaria infective stages) and the parasites snail intermediate host (growth and reproduction). To test these predictions, we conducted a large-scale mesocosm experiment using a natural gradient in the concentrations of nutrients (nitrogen) and toxic secondary compounds (polyphenolics) of nine leaf litter species. To differentiate between effects on exposure vs. susceptibility to infection, we included multiple infection experiments including one with constant per capita exposure. We found that increased litter nitrogen increased tadpole survival, and also increased cercaria production by the snail intermediate hosts, causing opposing effects on tadpole per capita exposure to trematode infection. Increased litter polyphenolics slowed tadpole development, leading to increased infection by increasing both their susceptibility to infection and the length of time they were exposed to parasites. Based on these results, recent shifts in forest composition towards more nitrogen-poor litter species should decrease trematode infection in tadpoles via density- and trait-mediated effects on the snail intermediate hosts. However, these shifts also involve increased abundance of litter species with high polyphenolic levels, which should increase trematode infection via trait-mediated effects on tadpoles. Future studies will be needed to determine the relative strength of these opposing effects in natural wetland communities. [Correction added after online publication on 5 January 2017: wording changed to which should increase trematode infection via trait-mediated effects on tadpoles.].