Direct effects influence larval salamander size and density more than indirect effects.

Direct and indirect effects both influence population and community dynamics. The relative strengths of these pathways are often compared using experimental approaches, but their evaluation in situ has been less frequent. We examined how individual and aggregate impacts of direct and indirect effects of species densities, proxies for competition and predation pressure, and habitat variables influenced patterns of larval density and body size of ringed (Ambystoma annulatum) and spotted salamanders (A. maculatum). We surveyed > 150 ponds in Missouri, USA, from 2012 to 2014 to measure the density and body size of each focal species, the density of co-occurring pond food web members, and select habitat features. We used structural equation modeling to quantify the relative importance of direct and indirect pathways on both body size and larval density. Overall, both responses were explained through a combination of direct and indirect effects. However, the magnitudes of direct effects were often greater than indirect effects. Some of the direct and indirect relationships with larval salamander size and density were also consistent with results from experimental studies. Finally, total direct and indirect effects were often weaker due to habitat and density variables negating each other's impacts. Overall, our study shows that direct effects were equivalent to, or more important than, indirect effects. We also demonstrate that the effects stemming from individual relationships can sum to produce net patterns that are negligible in magnitude. Further work on direct and indirect effects with observational data are needed to examine their magnitudes in natural communities.

A framework for linking competitor ecological differences to coexistence.

Not all ecological differences among competing species affect their ability to locally coexist. Rather, the differences that promote stable coexistence can be those which cause each species to experience stronger intraspecific than interspecific competition. Recent approaches have established how to detect the demographic signature of these competitive effects, but alone they cannot elucidate the ecological differences among species that yield these patterns. Here, we present a unifying experimental and observational framework that identifies potential ecological differences among species shaping their responses to intra- and interspecific competition. We first describe a conceptual model establishing why the strength of intra- and interspecific competitive interactions should vary along environmental gradients related to species ecological differences. We then show how to apply the framework using Enallagma damselflies, a diverse group of predatory aquatic insects. To determine how species responded to intra- and interspecific competition along environmental gradients, we experimentally manipulated the relative abundances of three species and replicated this across five lakes which varied in environmental conditions affecting larval damselfly per capita growth and mortality rates-key vital rates regulating their populations. Results suggest Enallagma are ecologically differentiated in ways that in some communities can result in intraspecific competition exceeding interspecific competition. However, in many cases the opposite was true, or the effects of intra- and interspecific competition were equivalent via growth and mortality responses. Moreover, these effects tended to be weak and asymmetrical among competitors, which suggests that differential responses of larval growth and mortality to intra- and interspecific competition may not contribute strongly to the maintenance of Enallagma diversity. Different environmental factors appear to shape these demographic responses to competition, providing insight into the ecological mechanisms regulating damselfly assemblages. This framework can be broadly applied to identify the ecological differences among species that may promote coexistence, advancing knowledge of the mechanisms underlying coexistence and overcoming some limitations of purely phenomenological approaches.

An ecological and evolutionary perspective on species coexistence under global change.

Whether assemblages of insect species locally coexist or are only being slowly lost from communities remains an enduring question. Addressing this question is especially critical in the wake of global change, which is expected to reshuffle biological communities and create novel interspecific interactions. In reviewing studies of putative insect species coexistence, we find that few have demonstrated necessary criteria to conclude that species coexist. We also find that few integrate ecological and evolutionary perspectives towards understanding coexistence. Yet, both micro-evolutionary and macroevolutionary processes can play a critical role in shaping species coexistence mechanisms, especially in response to global change. We suggest that understanding how global change may affect the makeup of communities can be best achieved by developing a research program focused on the joint contribution of ecological and evolutionary processes.

The influence of breeding phenology on the genetic structure of four pond-breeding salamanders.

Understanding metapopulation dynamics requires knowledge about local population dynamics and movement in both space and time. Most genetic metapopulation studies use one or two study species across the same landscape to infer population dynamics; however, using multiple co-occurring species allows for testing of hypotheses related to different life history strategies. We used genetic data to study dispersal, as measured by gene flow, in three ambystomatid salamanders (Ambystoma annulatum, A. maculatum, and A. opacum) and the Central Newt (Notophthalmus viridescens louisianensis) on the same landscape in Missouri, USA. While all four salamander species are forest dependent organisms that require fishless ponds to reproduce, they differ in breeding phenology and spatial distribution on the landscape. We use these differences in life history and distribution to address the following questions: (1) Are there species-level differences in the observed patterns of genetic diversity and genetic structure? and (2) Is dispersal influenced by landscape resistance? We detected two genetic clusters in A. annulatum and A. opacum on our landscape; both species breed in the fall and larvae overwinter in ponds. In contrast, no structure was evident in A. maculatum and N. v. louisianensis, species that breed during the spring. Tests for isolation by distance were significant for the three ambystomatids but not for N. v. louisianensis. Landscape resistance also contributed to genetic differentiation for all four species. Our results suggest species-level differences in dispersal ability and breeding phenology are driving observed patterns of genetic differentiation. From an evolutionary standpoint, the observed differences in dispersal distances and genetic structure between fall breeding and spring breeding species may be a result of the trade-off between larval period length and size at metamorphosis which in turn may influence the long-term viability of the metapopulation. Thus, it is important to consider life history differences among closely related and ecologically similar species when making management decisions.

Non-additive response of larval ringed salamanders to intraspecific density.

Conditions experienced in early developmental stages can have long-term consequences for individual fitness. High intraspecific density during the natal period can affect juvenile and eventually adult growth rates, metabolism, immune function, survival, and fecundity. Despite the important ecological and evolutionary effects of early developmental density, the form of the relationship between natal density and resulting juvenile phenotype is poorly understood. To test competing hypotheses explaining responses to intraspecific density, we experimentally manipulated the initial larval density of ringed salamanders (Ambystoma annulatum), a pond-breeding amphibian, over 11 densities. We modeled the functional form of the relationship between natal density and juvenile traits, and compared the relative support for the various hypotheses based on their goodness of fit. These functional form models were then used to parameterize a simple simulation model of population growth. Our data support non-additive density dependence and presents an alternate hypothesis to additive density dependence, self-thinning and Allee effects in larval amphibians. We posit that ringed salamander larvae may be under selective pressure for tolerance to high density and increased efficiency in resource utilization. Additionally, we demonstrate that models of population dynamics are sensitive to assumptions of the functional form of density dependence.

Life history differences influence the impacts of drought on two pond-breeding salamanders.

Drought is a strong density-independent environmental filter that contributes to population regulation and other ecological processes. Not all species respond similarly to drought, and the overall impacts can vary depending on life histories. Such differences can necessitate management strategies that incorporate information on individual species to maximize conservation success. We report the effects of a short-term drought on occupancy and reproductive success of two pond-breeding salamanders that differ in breeding phenology (fall vs. spring breeder) across an active military base landscape in Missouri, USA: We surveyed ~200 ponds for the presence of eggs, larvae, and metamorphs from 2011 to 2013. This period coincided with before, during, and after a severe drought that occurred in 2012. The two species showed contrasting responses to drought, where high reproductive failure (34% of ponds) was observed for the spring breeder during a single drought year. Alternatively, the fall breeder only showed a cumulative 8% failure over two years. The number of breeding ponds available for use in the fall decreased during the drought due to pond drying and/or a lack of re-filling. Estimates of occupancy probability declined for the fall-breeding salamander between 2012 and 2013, whereas occupancy probability estimates of the spring breeder increased post-drought. The presence of fish, hydroperiod, the amount of forest cover surrounding ponds, and canopy cover were all found to affect estimates of occupancy probabilities of each species. Pond clustering (distance to nearest pond and the number of ponds within close proximity), hydroperiod, forest cover, and canopy cover influenced both estimates of colonization and extinction probabilities. Our results show life history variation can be important in determining the relative susceptibility of a species to drought conditions, and that sympatric species experiencing the same environmental conditions can respond differently. Consideration of the spatial network and configuration of habitat patches that act as refuges under extreme environmental conditions will improve conservation efforts, such as the placement of permanent ponds for aquatic organisms. A better awareness of species-specific tolerances to environmental filters such as drought can lead to improved management recommendations to conserve and promote habitat for a greater diversity of species across landscapes of spatially connected populations.

Intermediate pond sizes contain the highest density, richness, and diversity of pond-breeding amphibians.

We present data on amphibian density, species richness, and diversity from a 7140-ha area consisting of 200 ponds in the Midwestern U.S. that represents most of the possible lentic aquatic breeding habitats common in this region. Our study includes all possible breeding sites with natural and anthropogenic disturbance processes that can be missing from studies where sampling intensity is low, sample area is small, or partial disturbance gradients are sampled. We tested whether pond area was a significant predictor of density, species richness, and diversity of amphibians and if values peaked at intermediate pond areas. We found that in all cases a quadratic model fit our data significantly better than a linear model. Because small ponds have a high probability of pond drying and large ponds have a high probability of fish colonization and accumulation of invertebrate predators, drying and predation may be two mechanisms driving the peak of density and diversity towards intermediate values of pond size. We also found that not all intermediate sized ponds produced many larvae; in fact, some had low amphibian density, richness, and diversity. Further analyses of the subset of ponds represented in the peak of the area distribution showed that fish, hydroperiod, invertebrate density, and canopy are additional factors that drive density, richness and diversity of ponds up or down, when extremely small or large ponds are eliminated. Our results indicate that fishless ponds at intermediate sizes are more diverse, produce more larvae, and have greater potential to recruit juveniles into adult populations of most species sampled. Further, hylid and chorus frogs are found predictably more often in ephemeral ponds whereas bullfrogs, green frogs, and cricket frogs are found most often in permanent ponds with fish. Our data increase understanding of what factors structure and maintain amphibian diversity across large landscapes.

Habitat traits and species interactions differentially affect abundance and body size in pond-breeding amphibians.

In recent studies, habitat traits have emerged as stronger predictors of species occupancy, abundance, richness and diversity than competition. However, in many cases, it remains unclear whether habitat also mediates processes more subtle than competitive exclusion, such as growth, or whether intra- and interspecific interactions among individuals of different species may be better predictors of size. To test whether habitat traits are a stronger predictor of abundance and body size than intra- and interspecific interactions, we measured the density and body size of three species of larval salamanders in 192 ponds across a landscape. We found that the density of larvae was best predicted by models that included habitat features, while models incorporating interactions among individuals of different species best explained the body size of larvae. Additionally, we found a positive relationship between focal species density and congener density, while focal species body size was negatively related to congener density. We posit that salamander larvae may not experience competitive exclusion and thus reduced densities, but instead compensate for increased competition behaviourally (e.g. reduced foraging), resulting in decreased growth. The discrepancy between larval density and body size, a strong predictor of fitness in this system, also highlights a potential shortcoming in using density or abundance as a metric of habitat quality or population health.