Demographic effects of phenological variation in natural populations of two pond-breeding salamanders.

Phenology is a key driver of population and community dynamics. Phenological metrics (e.g., first date that an event occurred) often simplify information from the full phenological distribution, which may undermine efforts to determine the importance of life history events. Data regarding full phenological distributions are especially needed as many species are shifting phenology with climatic change which can alter life-history patterns and species dynamics. We tested whether skewness, kurtosis or maximum duration of breeding phenology affected juvenile emigration phenology and survival in natural populations of ringed (Ambystoma annulatum) and spotted salamanders (A. maculatum) spanning a 7-year period at two study locations. We evaluated the relative importance of different phenological metrics in breeding phenology and larval density dependence on emigration phenology and survival. We found that variability in emigration phenology differed by species, with ringed salamanders having a shorter duration and distributions that were more often right-skewed and leptokurtic compared to spotted salamanders. Emigration phenology was not linked to any measure of variability in breeding phenology, indicating phenological variability operates independently across life stages and may be subject to stage-specific influences. Emigration duration and skewness were partially explained by larval density, which demonstrates how phenological distributions may change with species interactions. Further tests that use the full phenological distribution to link variability in timing of life history events to demographic traits such as survival are needed to determine if and how phenological shifts will impact species persistence.

Leaf litter input to ponds can dramatically alter amphibian morphological phenotypes.

Phenotypic plasticity in growth and development is commonly examined, but morphology can exhibit plasticity as well. Leg length plasticity is important, because it impacts mobility, which affects predator avoidance, prey capture, and seasonal movements. Differences in relative (i.e., body size adjusted) hind leg lengths > 5% in anurans affect jumping abilities, and resource levels and predation can generate these differences. Leaf litter input can alter larval growth and development and likely morphology as well. I show that relative leg length [leg length/snout-to-vent length (SVL) × 100%] can be quite variable, ranging from 44% of SVL to 120% of SVL across the following species: Hyla versicolor, Lithobates sylvaticus, L. sphenocephalus, and Anaxyrus americanus. Within species variability was highest in L. sylvaticus and almost as great as across species. I measured relative leg length for metamorphs from aquatic mesocosm studies examining the effects of plant litter type and quality. I also examined the relative importance of different environmental variables, including water quality, predation, resource level, and temperature. Good predictors were found only for the two ranids, where leaf litter input was the only variable found to affect relative leg length. Ranid frogs had longer legs when emerging from mesocosms with grass than mesocosms with no litter input, and deciduous leaves produced metamorphs intermediate in leg length. These results suggest that habitat changes in vegetation from land use change, invasive species, and climate change may affect the mobility and fitness of individuals through changes in metamorph relative leg length.

Modelling Ranavirus Transmission in Populations of Common Frogs (Rana temporaria) in the United Kingdom.

Ranaviruses began emerging in common frogs (Rana temporaria) in the United Kingdom in the late 1980s and early 1990s, causing severe disease and declines in the populations of these animals. Herein, we explored the transmission dynamics of the ranavirus(es) present in common frog populations, in the context of a simple susceptible-infected (SI) model, using parameters derived from the literature. We explored the effects of disease-induced population decline on the dynamics of the ranavirus. We then extended the model to consider the infection dynamics in populations exposed to both ulcerative and hemorrhagic forms of the ranaviral disease. The preliminary investigation indicated the important interactions between the forms. When the ulcerative form was present in a population and the hemorrhagic form was later introduced, the hemorrhagic form of the disease needed to be highly contagious, to persist. We highlighted the areas where further research and experimental evidence is needed and hope that these models would act as a guide for further research into the amphibian disease dynamics.

A general modeling framework for describing spatially structured population dynamics.

Variation in movement across time and space fundamentally shapes the abundance and distribution of populations. Although a variety of approaches model structured population dynamics, they are limited to specific types of spatially structured populations and lack a unifying framework. Here, we propose a unified network-based framework sufficiently novel in its flexibility to capture a wide variety of spatiotemporal processes including metapopulations and a range of migratory patterns. It can accommodate different kinds of age structures, forms of population growth, dispersal, nomadism and migration, and alternative life-history strategies. Our objective was to link three general elements common to all spatially structured populations (space, time and movement) under a single mathematical framework. To do this, we adopt a network modeling approach. The spatial structure of a population is represented by a weighted and directed network. Each node and each edge has a set of attributes which vary through time. The dynamics of our network-based population is modeled with discrete time steps. Using both theoretical and real-world examples, we show how common elements recur across species with disparate movement strategies and how they can be combined under a unified mathematical framework. We illustrate how metapopulations, various migratory patterns, and nomadism can be represented with this modeling approach. We also apply our network-based framework to four organisms spanning a wide range of life histories, movement patterns, and carrying capacities. General computer code to implement our framework is provided, which can be applied to almost any spatially structured population. This framework contributes to our theoretical understanding of population dynamics and has practical management applications, including understanding the impact of perturbations on population size, distribution, and movement patterns. By working within a common framework, there is less chance that comparative analyses are colored by model details rather than general principles.

Quantitative tools for implementing the new definition of significant portion of the range in the U.S. Endangered Species Act.

In 2014, the Fish and Wildlife Service (FWS) and National Marine Fisheries Service announced a new policy interpretation for the U.S. Endangered Species Act (ESA). According to the act, a species must be listed as threatened or endangered if it is determined to be threatened or endangered in a significant portion of its range (SPR). The 2014 policy seeks to provide consistency by establishing that a portion of the range should be considered significant if the associated individuals' "removal would cause the entire species to become endangered or threatened." We reviewed 20 quantitative techniques used to assess whether a portion of a species' range is significant according to the new guidance. Our assessments are based on the 3R criteria-redundancy (i.e., buffering from catastrophe), resiliency (i.e., ability to withstand stochasticity), and representation (i.e., ability to evolve)-that the FWS uses to determine if a species merits listing. We identified data needs for each quantitative technique and considered which methods could be implemented given the data limitations typical of rare species. We also identified proxies for the 3Rs that may be used with limited data. To assess potential data availability, we evaluated 7 example species by accessing data in their species status assessments, which document all the information used during a listing decision. In all species, an SPR could be evaluated with at least one metric for each of the 3Rs robustly or with substantial assumptions. Resiliency assessments appeared most constrained by limited data, and many species lacked information on connectivity between subpopulations, genetic variation, and spatial variability in vital rates. These data gaps will likely make SPR assessments for species with complex life histories or that cross national boundaries difficult. Although we reviewed techniques for the ESA, other countries require identification of significant areas and could benefit from this research.

Advancing research on animal-transported subsidies by integrating animal movement and ecosystem modelling.

Connections between ecosystems via animals (active subsidies) support ecosystem services and contribute to numerous ecological effects. Thus, the ability to predict the spatial distribution of active subsidies would be useful for ecology and conservation. Previous work modelling active subsidies focused on implicit space or static distributions, which treat passive and active subsidies similarly. Active subsidies are fundamentally different from passive subsidies, because animals can respond to the process of subsidy deposition and ecosystem changes caused by subsidy deposition. We propose addressing this disparity by integrating animal movement and ecosystem ecology to advance active subsidy investigations, make more accurate predictions of subsidy spatial distributions, and enable a mechanistic understanding of subsidy spatial distributions. We review selected quantitative techniques that could be used to accomplish integration and lead to novel insights. The ultimate objective for these types of studies is predictions of subsidy spatial distributions from characteristics of the subsidy and the movement strategy employed by animals that transport subsidies. These advances will be critical in informing the management of ecosystem services, species conservation and ecosystem degradation related to active subsidies.

Relative Importance of Climate Variables to Population Vital Rates: A Quantitative Synthesis for the Lesser Prairie-Chicken.

Climate change is expected to affect temperature and precipitation means and extremes, which can affect population vital rates. With the added complexity of accounting for both means and extremes, it is important to understand whether one aspect is sufficient to predict a particular vital rate or if both are necessary. To compare the predictive ability of climate means and extremes with geographic, individual, and habitat variables, we performed a quantitative synthesis on the vital rates of lesser prairie-chickens (Tympanuchus pallidictinus) across their geographic range. We used an information theoretic approach to rank models predicting vital rates. We were able to rank climate models for three vital rates: clutch size, nest success, and subadult/adult seasonal survival. Of these three vital rates, a climate model was never the best predictor even when accounting for potentially different relationships between climate variables and vital rates between different ecoregions. Clutch size and nest success were both influenced by nesting attempt with larger clutches and greater success for first nesting attempts than second nesting attempts. Clutch size also increased with latitude for first nesting attempts but decreased with latitude for second nesting attempts. This resulted in similar clutch sizes for first and second nest attempts at southern latitudes but larger clutches for first nest attempts than second nest attempts at northern latitudes. Survival was greater for subadults than adults, but there were few estimates of subadult survival for comparison. Our results show that individual characteristics and geographic variables are better for predicting vital rates than climate variables. This may due to low samples sizes, which restricted our statistical power, or lack of precision in climate estimates relative to microclimates actually experienced by individuals. Alternatively, relationships between climate variables and vital rates may be constrained by time lags or local adaptation.

Ranavirus could facilitate local extinction of rare amphibian species.

There is growing evidence that pathogens play a role in population declines and species extinctions. For small populations, disease-induced extinction may be especially probable. We estimated the susceptibility of two amphibian species of conservation concern (the dusky gopher frog [Lithobates sevosus] and boreal toad [Anaxyrus boreas boreas]) to an emerging pathogen (ranavirus) using laboratory challenge experiments, and combined these data with published demographic parameter estimates to simulate the potential effects of ranavirus exposure on extinction risk. We included effects of life stage during pathogen exposure, pathogen exposure interval, hydroperiod of breeding habitat, population carrying capacity, and immigration in simulations. We found that both species were highly susceptible to ranavirus when exposed to the pathogen in water at environmentally relevant concentrations. Dusky gopher frogs experienced 100 % mortality in four of six life stages tested. Boreal toads experienced 100 % mortality when exposed as tadpoles or metamorphs, which were the only life stages tested. Simulations showed population declines, greater extinction probability, and faster times to extinction with ranavirus exposure. These effects were more evident with more frequent pathogen exposure intervals and lower carrying capacity. Immigration at natural rates did little to mitigate effects of ranavirus exposure unless immigration occurred every 2 years. Our results demonstrate that disease-induced extinction by emerging pathogens, such as ranavirus, is possible, and that threat may be especially high for species with small population sizes. For the species in this study, conservation organizations should incorporate ranavirus surveillance into monitoring programs and devise intervention strategies in the event that disease outbreaks occur.

Abundance and phenology patterns of two pond-breeding salamanders determine species interactions in natural populations.

Phenology often determines the outcome of interspecific interactions, where early-arriving species often dominate interactions over those arriving later. The effects of phenology on species interactions are especially pronounced in aquatic systems, but the evidence is largely derived from experimental studies. We examined whether differences in breeding phenology between two pond-breeding salamanders (Ambystoma annulatum and A. maculatum) affected metamorph recruitment and demographic traits within natural populations, with the expectation that the fall-breeding A. annulatum would negatively affect the spring-breeding A. maculatum. We monitored populations of each species at five ponds over 4 years using drift fences. Metamorph abundance and survival of A. annulatum were affected by intra- and interspecific processes, whereas metamorph size and date of emigration were primarily influenced by intraspecific effects. Metamorph abundance, snout-vent length, date of emigration and survival for A. maculatum were all predicted by combinations of intra- and interspecific effects, but often showed negative relationships with A. annulatum metamorph traits and abundance. Size and date of metamorphosis were strongly correlated within each species, but in opposite patterns (negative for A. annulatum and positive for A. maculatum), suggesting that the two species use alternative strategies to enhance terrestrial survival and that these factors may influence their interactions. Our results match predictions from experimental studies that suggest recruitment is influenced by intra- and interspecific processes which are determined by phenological differences between species. Incorporating spatiotemporal variability when modeling population dynamics is necessary to understand the importance of phenology in species interactions, especially as shifts in phenology occur under climate change.

Effects of tannin source and concentration from tree leaves on two species of tadpoles.

Vegetation in and around freshwater ecosystems can affect aquatic organisms through the production of secondary compounds, which are retained in leaves after senescence and are biologically active. Tannins can be toxic to tadpoles, but the plant source of tannins and tannin concentration have been confounded in experimental designs in previous studies. To examine the effects of the concentration and source of tannins (tree species), we examined the effects of 4 factors on tadpole survival, growth, and development: tannin source (red oak [Quercus rubra], white oak [Quercus alba], or sugar maple [Acer saccharum]); tannin concentration (including a control); diet protein level; and tadpole species (American toad [Anaxyrus americanus] and spring peepers [Pseudacris crucifer]). Tannin source and concentration affected spring peeper survival, but American toads had uniformly high survival. Spring peepers had a lower survival rate in high tannin concentrations of oak leachate but a high survival rate in both concentrations of sugar maple leachate. These differences in survival did not correspond with changes in dissolved oxygen, and no effect of dietary protein level on tadpole performance was observed. The presence of plant leachate resulted in increased tadpole growth in both species, but the mechanism for this finding is unclear. The results of the present study show that tannin concentration and source are important factors for tadpole performance, adding further evidence that plant chemistry can affect aquatic organisms.

Introduction of ranavirus to isolated wood frog populations could cause local extinction.

Amphibian declines and extinction have been attributed to many causes, including disease such as chytridiomycosis. Other pathogens may also contribute to declines, with ranavirus as the most likely candidate given reoccurring die-offs observed in the wild. We were interested in whether it is possible for ranavirus to cause extinction of a local, closed population of amphibians. We used susceptibility data from experimental challenges on different life stages combined with estimates of demographic parameters from a natural population to predict the likelihood of extinction using a stage-structured population model for wood frogs (Lithobates sylvaticus). Extinction was most likely when the larval or metamorph stage was exposed under frequent intervals in smaller populations. Extinction never occurred when only the egg stage was exposed to ranavirus. Under the worst-case scenario, extinction could occur in as quickly as 5 years with exposure every year and 25-44 years with exposure every 2 years. In natural wood frog populations, die-offs typically occur in the larval stage and can reoccur in subsequent years, indicating that our simulations represent possible scenarios. Additionally, wood frog populations are particularly sensitive to changes in survival during the pre-metamorphic stages when ranavirus tends to be most pathogenic. Our results suggest that ranavirus could contribute to amphibian species declines, especially for species that are very susceptible to ranavirus with closed populations. We recommend that ranavirus be considered in risk analyses for amphibian species.

Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export.

Spatial subsidies are resources transferred from one ecosystem to another and which can greatly affect recipient systems. Increased subsidy quantity is known to increase these effects, but subsidy quality is likely also important. We examined the effects of leaf litter quality (varying in nutrient and tannin content) in pond mesocosms on gray treefrog (Hyla versicolor) biomass export, as well as water quality and ecosystem processes. We used litter from three different tree species native to Missouri [white oak (Quercus alba), northern red oak (Quercus rubra), and sugar maple (Acer saccharum)], one non-native tree [white pine (Pinus strobus)], and a common aquatic grass [prairie cordgrass (Spartina pectinata)]. We found that leaf litter species affected almost every variable we measured. Gray treefrog biomass export was greatest in mesocosms with grass litter and lowest with white oak litter. Differences in biomass export were affected by high tannin concentrations (or possibly the correlated variable, dissolved oxygen) via their effects on survival, and by primary production, which altered mean body mass. Effects of litter species could often be traced back to the characteristics of the litter itself: leaf nitrogen, phosphorus, and tannin content, which highlights the importance of plant functional traits in affecting aquatic ecosystems. This work and others stress that changes in forest species composition could greatly influence aquatic systems and aquatic-terrestrial linkages.

Carryover effects in amphibians: are characteristics of the larval habitat needed to predict juvenile survival?

Carryover effects occur when experiences early in life affect an individual's performance at a later stage. Many studies have shown carryover effects to be important for future performance. However, it is currently unclear whether variation in later environments could overwhelm factors from an earlier life stage. We were interested in whether similar patterns would emerge under the same experimental design with similar taxa. To examine this, we implemented a four-way factorial experimental design with different forestry practices on three species of anurans (each examined in different years) in the aquatic larval environment and terrestrial juvenile environment in outdoor mesocosms in central Missouri, USA. Using Cormack-Jolly-Seber mark-recapture models implemented in program MARK, we investigated whether one environment or both environments best predicted terrestrial juvenile survival. We found only limited evidence of carryover effects for one of three species in one time period. These were the effects of time to metamorphosis and body condition at metamorphosis predicting leopard frog (Lithobates sphenocephalus) survival. However, both effects were counterintuitive and/or very weak. For wood frogs (L. sylvaticus), all of the variables predicting survival had confidence intervals that included zero, but very low survival may have limited our ability to estimate parameters. The terrestrial environment was important for predicting survival in both American toads (Anaxyrus americanus) and southern leopard frogs. The partial harvest forest tended to increase survival relative to control forest and early-successional forest in American toads. Alternately, early-successional forest with downed wood removed increased survival for leopard frogs, but this treatment was no different from control forest for American toads. Previous studies have shown negative effects of recent clearcuts on terrestrial amphibians. It appears that vegetative regrowth after just a few years can mitigate these initial negative effects. Our study shows that variation in later environments probably can overwhelm variation from earlier environments. However, previous evidence of carryover effects suggests that more research is needed to predict when carryover effects are likely to occur.

Reciprocal subsidies in ponds: does leaf input increase frog biomass export?

Reciprocal subsidies occur when ecosystems are paired, both importing and exporting resources to each other. The input of subsidies increases reciprocal subsidy export, but it is unclear how this changes with other important factors, such as ambient resources. We provide a conceptual framework for reciprocal subsidies and empirical data testing this framework using a pond-forest system in Missouri, USA. Our experiment used in situ pond mesocosms and three species of anurans: wood frogs, American toads, and southern leopard frogs. We predicted that increases in ambient resources (primary productivity) and detrital subsidy input (deciduous tree leaves) into pond mesocosms would increase reciprocal export (frog biomass) to the surrounding terrestrial ecosystem. In contrast, we found that increases in primary productivity consistently decreased frog biomass, except with leaf litter inputs. With leaf inputs, primary productivity did not affect the export of frogs, indicating that leaf detritus and associated microbial communities may be more important than algae for frog production. We found that subsidy inputs tended to increase reciprocal exports, and thus partial concordance with our conceptual framework.

Effects of leachate from tree leaves and grass litter on tadpoles.

Tree species composition can change as a result of succession, climate change, fire suppression, and invasive species. These changes clearly affect forests, but they can also affect aquatic ecosystems based on differences in the input quality of leaf litter, such as plant secondary compounds. These compounds vary in type and concentration depending on species and can be toxic to aquatic organisms. To examine toxic effects on Pseudacris maculata and Pseudacris crucifer tadpoles, we conducted 60-d laboratory experiments to compare leaf litter leachate from a dominant canopy species (red oak) and nonnative species (white pine) with an aquatic grass (prairie cordgrass) and plain water control. An additional experiment examined the effects of white pine on Bufo americanus, Hyla versicolor, and tannin concentrations in natural ponds. Compared with the control and grass, tree leaf extracts resulted in reduced tadpole survival. Leached compounds from pine reduced tadpole survival to 3 d or less. Tadpoles were able to metamorphose in significant numbers only from the two controls. The lowered survival with the red oak treatment might have been caused by lowered dissolved oxygen or high tannin concentrations. However, pine is known to have high concentrations of toxic monoterpenes, which should be investigated further. We found that tannin concentrations in natural ponds were much lower than the test concentrations, indicating that these results may represent worst-case scenarios or unrealistic concentrations.

Effects of pulsed nitrate exposure on amphibian development.

Most toxicity tests investigate constant concentrations of a chemical. Concentrations of many compounds in the environment are dynamic, however, and individuals may be more sensitive to pulses of a chemical initiated at specific points during development. Realistic toxicity tests are important to accurately assess the toxicity of a compound. Bufo americanus and Hyla chrysoscelis tadpoles were exposed to concentrations of nitrate, a pervasive stressor in the environment, up to 5 mg/L of NO3-N in constant concentrations and in pulses at three different points during development. At the termination of the experiments, individuals were measured for developmental stability (DS) and traditional fitness correlates (size, body condition, and time to metamorphosis). No significant differences were found in these measures between treatments and controls in B. americanus tadpoles. In H. chrysoscelis, however, more extreme directional asymmetry was found in the middle and late pulses, indicating that the sudden change in concentration of nitrate decreased the level of DS in tadpoles. These results indicate that nitrate has subtle but important effects at low doses, and they suggest that species may be better able to deal with pulses that occur early rather than late in development. A greater understanding about the effects of pulses will help conservation biologists to manage populations and prevent population declines.