Will pre‐adaptation buffer the impacts of climate change on novel species interactions?

Species are expected to alter their ranges as climates change. Climate‐induced range expansions of predators could threaten evolutionarily naïve prey populations, leading to high mortality at the invasion front. If prey can apply existing defenses against local predators to novel predation threats induced by climate change, mortality threats will be less than expected. Here, we examine if spotted salamander larvae Ambystoma maculatum from populations that coexist with native red‐spotted newts Notophthalmus viridescens survive better when exposed to a novel predator, the marbled salamander Ambystoma opacum. We show that regional mean winter temperatures warmed 2.0°C over 116 yr in the region, and that A. opacum survival increases in ponds with higher winter temperatures. Hence as winters continue to warm, this apex predator will likely colonize ponds north of their current range limit. Next, we performed common garden experiments to determine if local adaptations to native N. viridescens and exposure to A. opacum or N. viridescens kairomones (predator chemical cues) altered A. maculatum survival in predation trials. We did not find evidence for local adaptation to N. viridescens. However, A. maculatum from high‐N. viridescens ponds that were reared with A. opacum kairomones suffered significantly higher mortality from the native predator N. viridescens. This outcome suggests an unanticipated interaction between local adaptation and plastic responses to novel kairomones from a potentially range‐expanding predator. Current projections of biodiversity losses from climate change generally ignore the potential for eco‐evolutionary interactions between native and range‐expanding species and thus could be inaccurate.     

Predator size and phenology shape prey survival in temporary ponds

Theoretical efforts suggest that the relative sizes of predators and their prey can shape community dynamics, the structure of food webs, and the evolution of life histories. However, much of this work has assumed static predator and prey body sizes. The timing of recruitment and the growth patterns of both predator and prey have the potential to modify the strength of predator–prey interactions. In this study, I examined how predator size dynamics in 40 temporary ponds over a 3-year period affected the survival of spotted salamander (Ambystoma maculatum) larvae. Across communities, gape-limited predator richness, but not size, was correlated with habitat duration (pond permanence). Within communities, mean gape-limited predator size diminished as the growing season progressed. This size reduction occurred because prey individuals grew into a body size refuge and because the largest of the predators left ponds by mid-season. Elevated gape-limited predation risk across time and space was predicted by the occurrence of two large predatory salamanders: marbled salamander larvae (Ambystoma opacum) and red-spotted newt adults (Notophthalmus viridescens). The presence of the largest gape-limited predator, A. opacum, predicted A. maculatum larval survival in the field. The distribution of large predatory salamanders among ponds and across time is expected to lead to differing community dynamics and to generate divergent natural selection on early growth and body size in A. maculatum. In general, a dynamic perspective on predator size often will be necessary to understand the ecology and evolution of species interactions. This will be especially true in frequently disturbed or seasonal habitats where phenology and ontogeny interact to determine body size asymmetries. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

STRONG SELECTION BARRIERS EXPLAIN MICROGEOGRAPHIC ADAPTATION IN WILD SALAMANDER POPULATIONS

Microgeographic adaptation occurs when populations evolve divergent fitness advantages across the spatial scales at which focal organisms regularly disperse. Although an increasing number of studies find evidence for microgeographic adaptation, the underlying causes often remain unknown. Adaptive divergence requires some combination of limited gene flow and strong divergent natural selection among populations. In this study, we estimated the relative influence of selection, gene flow, and the spatial arrangement of populations in shaping patterns of adaptive divergence in natural populations of the spotted salamander (Ambystoma maculatum). Within the study region, A. maculatum co‐occur with the predatory marbled salamander (Ambystoma opacum) in some ponds, and past studies have established a link between predation risk and adaptive trait variation in A. maculatum. Using 14 microsatellite loci, we found a significant pattern of genetic divergence among A. maculatum populations corresponding to levels of A. opacum predation risk. Additionally, A. maculatum foraging rate was strongly associated with predation risk, genetic divergence, and the spatial relationship of ponds on the landscape. Our results indicate the sorting of adaptive genotypes by selection regime and strongly suggest that substantial selective barriers operate against gene flow. This outcome suggests that microgeographic adaptation in A. maculatum is possible because strong antagonistic selection quickly eliminates maladapted phenotypes despite ongoing and substantial immigration. Increasing evidence for microgeographic adaptation suggests a strong role for selective barriers in counteracting the homogenizing influence of gene flow.     

An examination of multiple factors affecting community structure in an aquatic amphibian community

Summary The potential effects of multiple factors structuring certain larval amphibian communities were studied using a pen experiment in a natural pond. Potential factors (predation and competition from other species) were allowed to act in a stepwise fashion such that their relative importance could be evaluated. Based on a previous study, it was hypothesized that predation by Ambystoma salamander larvae on other larval amphibian species would be the most important factor. Survival of Ambystoma jeffersonianum salamander larvae and Rana sylvatica tadpoles was significantly depressed only by Ambystoma opacum predation. Survival of Ambystoma maculatum salamander larvae was significantly greater in the absence of both A. opacum and A. jeffersonianum predators. The virtual elimination of Hyla chrysoscelis larvae in all treatments also can be largely attributed to Ambystoma predation. Thus, Ambystoma predation was the dominant factor determining larval survival of four amphibian prey species in the experimental communities.     

Interactions between fish and salamander larvae

Summary Two species of salamander larvae (Ambystoma talpoideum and A. maculatum) were reared separately in the presence and absence of a fish (Lepomis macrochirus) in artificial ponds to measure the effects of a predator on the growth, survival, diet, and activity of larvae. The presence of L. macrochirus reduced body sizes of larvae by 18% in A. talpoideum and by 16% in A. maculatum. L. macrochirus apparently preyed on the smallest individuals. Survival in the presence of L. macrochirus decreased by 61% in A. talpoideum and by 97% in A. maculatum compared with larvae reared alone. Species identity did not significantly effect body size or survival, but an interaction effect suggested that A. maculatum was more severely affected by predators than was A. talpodeum. Activity of larvae in the water column was dramatically reduced in the presence of L. macrochirus, when larvae were restricted to the leaf litter of the benthic zone. There was overlap in the diets of fish and salamander larvae. Larvae reared in the presence of fish, however, consumed different taxa of prey as well as reduced number of prey compared to larvae reared alone. A. talpoideum larvae were more nocturnal than diurnal in the absence of fish, whereas A. maculatum larvae were equally active day and night. This experiment suggests that predator-prey relationships can change with shifts in species attributes and potentially confound apparent costs of predator avoidance with competition. Measuring the long-term dynamics of the cost-benefit relationship will help elucidate how prey balance the demands of their life history with the demands of predators.     

Evolution mediates the effects of apex predation on aquatic food webs

Ecological and evolutionary mechanisms are increasingly thought to shape local community dynamics. Here, I evaluate if the local adaptation of a meso-predator to an apex predator alters local food webs. The marbled salamander (Ambystoma opacum) is an apex predator that consumes both the spotted salamander (Ambystoma maculatum) and shared zooplankton prey. Common garden experiments reveal that spotted salamander populations which co-occur with marbled salamanders forage more intensely than those that face other predator species. These foraging differences, in turn, alter the diversity, abundance and composition of zooplankton communities in common garden experiments and natural ponds. Locally adapted spotted salamanders exacerbate prey biomass declines associated with apex predation, but dampen the top-down effects of apex predation on prey diversity. Countergradient selection on foraging explains why locally adapted spotted salamanders exacerbate prey biomass declines. The two salamander species prefer different prey species, which explains why adapted spotted salamanders buffer changes in prey composition owing to apex predation. Results suggest that local adaptation can strongly mediate effects from apex predation on local food webs. Community ecologists might often need to consider the evolutionary history of populations to understand local diversity patterns, food web dynamics, resource gradients and their responses to disturbance.     

When can embryos learn? A test of the timing of learning in embryonic amphibians

Learning is crucial to the survival of organisms across their life span, including during embryonic development. We set out to determine when learning becomes possible in amphibian development by exposing spotted salamander (Ambystoma maculatum) embryos to chemical stimuli from a predator (Ambystoma opacum), nonpredator (Lithobates clamitans), or control at developmental stages 16–21 or 36–38 (Harrison 1969 ). Once exposures were completed and embryos hatched, we recorded the number of movements and time spent moving of individuals in both groups and all treatments. There was no significant difference in number of movements or time spent moving among any of the treatments. The groups that were exposed to predator stimuli and a blank control at stages 36–38 were also tested to determine whether there was a difference in refuge preference or difference in survivorship when exposed to a predator (marbled salamander). There was no difference in survival or refuge preference between individuals; however, all individuals preferred vegetated over open areas regardless of treatment type. We discuss hypotheses for the absence of embryonic learning in this species and suggest it may be the result of the intensity of the predator–prey interaction between the predator, large marbled salamander larvae, and the prey, spotted salamander larvae.     

Salamander evolution across a latitudinal cline in gape-limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape-limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape-limited and gape-unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape-limited predator salamanders A. opacum and gape-unconstrained beetle larvae Dytiscus . In common garden experiments, prey from sites with high gape-limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape-limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape-limited predation risk. Results point to an important role for cross-community generalizations based on functional classifications of predators by their gape constraints and inter-site genetic variation in prey growth rates and behaviors.     

Macrogeographic variation of a pond predator's top-down effects in a common garden environment

Geographic variation in species behavior and life history has been well documented in biology. Species with wide geographic distributions (i.e., across a continent) but small home ranges (i.e., <1 km²) likely experience wide variability in abiotic environments across the entirety of their range, possibly exhibiting strong local adaptation. Understanding variation across a large geographic scale is especially important when considering species that have strong ecological importance, such as keystone species. Yet, few studies have compared the potential cascading ecological effects of a predator with a keystone role in at least part of its range. To understand how keystone ability in pond food webs can vary across a large geographic range, we conducted an artificial pond experiment with a known keystone predator in at least part of its range, the marbled salamander (Ambystoma opacum). To do so, we collected size-matched salamander larvae from three geographically distant populations (>650 km apart) in Ohio, Mississippi, and North Carolina and placed them in mesocosms with a suite of spring breeding amphibian prey species. We observed differential survival of some prey species leading to differences in spring-breeding amphibian diversity among the three predator populations, indicating that keystone predation may vary at a geographic scale. Prey diversity was lowest with predators from northern (Ohio) populations of salamanders. Further understanding of large-scale variability in ecologically important predators and the potential effects of translocating wide-ranging ambystomatid species is needed to direct future conservation efforts and preserve biodiversity.     

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators

A predator''s functional response determines predator–prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator–prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander (Ambystoma maculatum) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.     

Do Experience and Body Size Play a Role in Responses of Larval Ringed Salamanders,Ambystoma annulatum,to Predator Kairomones? Laboratory and Field Assays

Prey may experience ontogenetic changes in vulnerability to some predators, either because of changes in morphology or experience. If prey match their level of antipredator behavior to the level of predatory threat, prey responses to predators should reflect the appropriate level of threat for their stage of development. For larval salamanders, responses to predators may change with body size because larger larvae are less vulnerable to predation by gape‐limited predators or because fleeing responses by large salamanders may be more effective than for smaller salamanders. In a field experiment, small larval ringed salamanders, Ambystoma annulatum, responded to chemical stimuli (‘kairomones’) from predatory newts, Notophthalmus viridescens, with an antipredator response (decreased activity). Laboratory‐reared larvae decreased their activity following exposure to newt kairomones, indicating that larval ringed salamanders do not require experience with newts to recognize them as predators. In both experiments, larvae distinguished between chemical stimuli from newts and stimuli from tadpoles (non‐predators) and a blank control. In a third experiment, field‐caught (experienced) larvae showed a graded response to newt kairomones based on their body size: small larvae tended to decrease their activity while larger larvae showed no change or an increase in activity. This graded response was not observed for neutral stimuli, indicating that it is predator‐specific. Therefore, ringed salamander larvae exhibit threat‐sensitive ontogenetic changes in their response to chemical stimuli from predatory newts.     

Spatial and temporal niche partitioning in grassland ants

We examined whether the species composition of a community influences the persistence of larval Ambystoma maculatum in assemblages composed of two larger intraguild predators (A. opacum and A. jeffersonianum) and an alternative prey species (tadpoles of Rana sylvatica). We predicted a priori that A. maculatum would have higher survival in more diverse communities containing alternative species of prey and top predators (A. opacum), the latter of which may lower the abundance of intermediate predators (A. jeffersonianum) via intraguild predation. In a factorial experiment, we manipulated the presence of larval A. opacum, A. jeffersonianum, and R. sylvatica in replicated artificial ponds containing larval A. maculatum. The presence of all three species significantly depressed biomass production in A. maculatum: biomass was highest in ponds lacking the other species and was zero in ponds initially containing all four species. Tadpoles severely reduced the growth of filamentous algae in the ponds. This, in turn, may have affected the abundance of some herbivorous prey of larval salamanders, although this possibility was not tested. The presence of congeneric predators severely restricted the presence in the water column of larval A. maculatum, which otherwise exhibited significant diel patterns of activity in the absence of predators. Together, the presence of tadpoles and a predator-mediated reduction in activity patterns may have limited foraging opportunities for A. maculatum, thus exacerbating the direct impact of predation on survival in this species. These results suggest that diverse assemblages consisting of these particular species may actually inhibit, rather than promote, inclusion of A. maculatum in some communities of pond-breeding amphibians.     

Effects of predation risk on population variation in adult size in a stream-dwelling isopod

I used a combination of laboratory experiments and field surveys to examine the role that population-specific predation risk may play in shaping the life history strategy of a stream-dwelling isopod Lirceus fontinalis. Two focal populations were identified that were exposed to different predator types. The first population was exposed to larvae of the streamside salamander (Ambystoma barbouri) and the second to banded sculpin (Cottus carolinae). A laboratory experiment, in which different size classes of prey were offered simultaneously to individual predators, revealed that L. fontinalis suffered greatest mortality risk at small sizes with A. barbouri. Alternatively, with C. carolinae the risk of mortality was independent of size. Life history theory predicts that L. fontinalis from populations exposed to the gape-limited salamander larvae should be larger at maturity relative to individuals from populations exposed to C. carolinae. Field surveys on the two focal populations both within 1 year and across 4 years supported this prediction. Four other populations, two exposed to streamside salamander larvae and two to fish, provided additional support for the prediction. I concluded that L. fontinalis exhibited an adaptive response in size at maturity in response to population-specific predation risk. I then used gut content assays of the major predators to assess whether the population-specific life history strategies adopted by L. fontinalis were successful in avoiding predation.     

Differential vulnerability to predation and refuge use in competing larval salamanders

The aquatic larvae of two species of salamanders coexist as a result of differences in their competitive abilities: Ambystoma talpoideum is a superior aggressor, whereas A. maculatum is a superior forager. I examined the behavioral mechanisms that permit these species to coexist with their predatory congener, A. opacum. I asked whether the two prey species differ in their vulnerability to predation and in their use of structural and spatial refugia when under the risk of predation; such inter-specific variation may allow predation to contribute indirectly to prey coexistence. Larval A. maculatum (the superior forager) was more vulnerable to predation by A. opacum than was A. talpoideum, and only the latter species significantly increased its use of structural refugia (leaf litter) in the presence of the predator. In pond enclosures, both species of prey exhibited diel patterns of microhabitat use; significantly more larvae occupied shallow regions of enclosures during the day and migrated to deeper water (a spatial refugium) at night. However, when considered separately, neither (1) the presence of a predatory larval A. opacum nor (2) an increased density of intra- and interspecific competitors significantly altered this habitat shift for either prey species. Rather, diel microhabitat usage in A. talpoideum was significantly affected by an interaction between predator presence and competitor density. My results demonstrate the importance of refugia to coexistence in this predator-prey assemblage. Furthermore, predation by A. opacum may mediate prey competition; that is, preferential consumption of A. maculatum may reduce the competitive impact of this superior forager on A. talpoideum, thus enhancing their coexistence.     

The evolution of prey body size reaction norms in diverse communities

1. Heterogeneous predation risks can select for predator-specific plastic defences in prey populations. However, diverse predation threats can generate diffuse selection, which, in turn, can lead to the evolution of more generalized reaction norms. Unreliable predator cues also can select for more generalized plasticity in prey. 2. Here, I evaluated the extent to which variation in risk from a focal predator vs. variation in risk from predator diversity and composition were associated with variation in body mass reaction norms in 18 prey populations. Toward this end, I assayed the body mass reaction norms in a common garden experiment for spotted salamander larvae Ambystoma maculatum in response to marbled salamander predators Ambystoma opacum, local predator richness and the densities of two auxiliary predator species. 3. When raised under controlled conditions, prey larvae generally were smaller when exposed to A. opacum kairomones. Among populations, the mean and slope of body mass variation was unrelated to A. opacum's local density. 4. Predator richness and several key environmental factors were not associated with reaction norm variation. Instead, the density of an auxiliary newt predator species was correlated with reduced mass reaction norm slopes. Results suggest that diffuse selection from auxiliary predators can modify the evolution of life-history plasticity.     

Increasing conspecific density weakens the ability of intermediate predators to develop induced morphological defences to top predators

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Threat of predation alters aggressive interactions among spotted salamander (Ambystoma maculatum) larvae

Intraspecific aggression represents a major source of mortality for many animals and is often experienced alongside the threat of predation. The presence of predators can strongly influence ecological systems both directly by consuming prey and indirectly by altering prey behavior or habitat use. As such, the threat of attack by higher level predators may strongly influence agonistic interactions among conspecifics via nonconsumptive (e.g., behaviorally mediated) predator effects. We sought to investigate these interactions experimentally using larval salamanders (Ambystoma maculatum) as prey and dragonfly nymphs (Anax junius) as predators. Specifically, we quantified salamander behavioral responses to perceived predation risk (PPR) from dragonfly nymphs and determined the degree to which PPR influenced intraspecific aggression (i.e., intraspecific biting and cannibalism) among prey. This included examining the effects of predator exposure on the magnitude of intraspecific biting (i.e., extent of tail damage) and the resulting change in performance (i.e., burst swim speed). Salamander larvae responded to PPR by reducing activity and feeding, but did not increase refuge use. Predator exposure did not significantly influence overall survival; however, the pattern of survival differed among treatments. Larvae exposed to PPR experienced less tail damage from conspecifics, and maximum burst swim speed declined as tail damage became more extensive. Thus, escape ability was more strongly compromised by intraspecific aggression occurring in the absence of predation risk. We conclude that multitrophic indirect effects may importantly modulate intraspecific aggression and should be considered when evaluating the effects of intraspecific competition.     

GENE FLOW AND INEFFECTIVE ANTIPREDATOR BEHAVIOR IN A STREAM-BREEDING SALAMANDER

Predators often feed on prey that show ineffective antipredator behavior. Gene flow among populations may constrain evolution of effective antipredator ability in larvae of the streamside salamander, Ambystoma barbouri, a species that occupies distinctly different habitats with conflicting selection pressures. Some streams are ephemeral, where larvae should be active to feed and reach metamorphosis before stream drying. In contrast, other streams are more permanent and contain pools with predatory fish, where larvae should remain inactive to avoid fish predation. Feeding rates and predator escape behavior were assayed for laboratory-reared larvae from 15 populations. Larval survival was also compared among populations in artificial streams with natural predators. Five populations represented streams subjected to fish predation along a gradient of genetic and geographic isolation from populations without fish; the remaining 10 populations were ephemeral and without fish. Individuals from populations with fish had significantly stronger behavioral responses to fish (i.e., decreased feeding rate associated with the presence of fish and increased escape response) than individuals from fishless populations. Larvae from populations containing fish that were more isolated from fishless populations showed stronger antipredator responses than less isolated populations. Further, larvae from more isolated populations survived longer in the predation experiment, indicating that the behaviors measured were related with survival. These results suggest that gene flow between populations with conflicting selection pressures limits local adaptation in some salamander populations with fish. While previous studies have typically focused on the role of gene flow in pairs of populations, the results of this study suggest that gene flow is acting to swamp local adaptation across several populations.     

Field Response of Tadpoles to Conspecific and Heterospecific Alarm

Many organisms use chemical cues from a variety of sources to mediate predator avoidance. Response to heterospecific alarm cues has been demonstrated for tadpoles within but not among taxa and alarm response behavior has seldom been examined under field conditions. This study examined the response of three sympatric amphibian larvae and predaceous larval Dytiscus sp. (diving beetle) to damage-release signals in natural ponds by using capture rates from treated funnel traps as an index of larval behavior. Hyla regilla (Pacific tree frog) tadpoles avoided traps treated with either crushed conspecifics or with Rana aurora (red-legged frog) tadpoles but the larger ranids and Ambystoma macrodactylum (long-toed salamander) did not respond to either treatment. H. regilla tadpoles were likely susceptible to any potential predators of ranid tadpoles in these ponds and this result is consistent with the hypothesis that a response to heterospecific alarm occurs in sympatric prey with shared predators.     

Prey size-distributions and size-specific foraging success of Ambystoma larvae

Summary We examined how prey size-distributions influence size-specific foraing rate and food gain, i.e., food intake scaled to metabolic demands, in Jefferson's and small-mouth salamander larvae. Ambystoma jeffersonianum larvae sampled on 17 dates from a farm pond whose fauna was dominated by macrozooplankton and chironomid larvae were rarely gape-limited, and total volume of food in the stomach (VS) showed only a slight tendency to increase with larval size. Although 15 of 17 correlation coefficients of VS with larval size were positive, only 1 of 17 correlations were statistically significant, and body size explained only 8% of the overall variation in VS. Correlation coefficients of food gain and body size were positive in 9 cases and negative in 8, but only 3 were statistically significant.In contrast, Ambystoma texanum larvae in 42 samples taken from five sites dominated by macrozooplankton as well as relatively large isopods and amphipods were almost always gape-limited, and VS tended to increase markedly with larval size. 40 of 42 correlation coefficients of VS and larval size were positive, and 19 correlations were statistically significant. Body size in turn explained about 35% of the overall variation in VS. Correlation coefficients of food gain and larval size were positive in 32 of 42 samples, and 9 of 10 significant correlations were positive.When food is limiting and prey selection is not limited by gape, smaller larvae may grow as fast or in some cases faster than larger larvae because they are nearly as effective foragers, but have lower metabolic demands. Larger larvae may in turn grow faster than smaller larvae in environments which support a broad size spectrum of prey, particularly when gape limitations are highly disproportionate among size classes. The growth rate of larvae in one size class relative to another depends primarily on the extent to which increased foraging rate compensates for higher energy demands as body size increases. Size-specific foraging rate may in turn be strongly influenced by the prey size-distribution within a habitat. These relationships suggest that relative size is not always a good a priori predictor of exploitative competitive ability.