Selection for phenotypic plasticity in Rana sylvatica tadpoles

The hypothesis that phenotypic plasticity is an adaptation to environmental variation rests on the two assumptions that plasticity improves the performance of individuals that possess it, and that it evolved in response to selection imposed in heterogeneous environments. The first assumption has been upheld by studies showing the beneficial nature of plasticity. The second assumption is difficult to test since it requires knowing about selection acting in the past. However, it can be tested in its general form by asking whether natural selection currently acts to maintain phenotypic plasticity. We adopted this approach in a study of plastic morphological traits in larvae of the wood frog, Rana sybatica. First we reared tadpoles in artificial ponds for 18 days, in either the presence or absence of Anax dragonfly larvae (confined within cages to prevent them from killing the tadpoles). These conditioning treatments produced dramatic differences in size and shape: tadpoles from ponds with predators were smaller and had relatively short bodies and deep tail fins. We estimated selection by Anax on the two kinds of tadpoles by testing for non-random mortality in overnight predation trials. Dragonflies imposed strong selection by preferentially killing individuals with relatively shallow and short tail fins, and narrow tail muscles. The same traits that exhibited the strongest plasticity were under the strongest selection, except that tail muscle width exhibited no plasticity but experienced strong increasing selection. A laboratory competition experiment, testing for selection in the absence of predators, showed that tadpoles with deep tail fins grew relatively slowly. In the cattle tanks, where there were also no free predators, the predator-induced phenotype survived more poorly and developed slowly, but this cost was apparently not associated with particular morphological traits. These results indicate that selection is currently promoting morphological plasticity in R. sylvatica, and support the hypothesis that plasticity represents an adaptation to variable predator environments.     

NATURAL SELECTION FOR ENVIRONMENTALLY INDUCED PHENOTYPES IN TADPOLES

Models suggest that phenotypic plasticity is maintained in situations where the optimal phenotype differs through time or space, so that selection acts in different directions in different environments. Some empirical work supports the general premise of this prediction because phenotypes induced by a particular environment sometimes perform better than other phenotypes when tested in that environment. We have extended these results by estimating the targets of selection in Pseudacris triseriata tadpoles in environments without predators and with larval Anax dragonflies. Tadpoles displayed significant behavioral and morphological plasticity when reared in the presence and absence of nonlethal dragonflies for 32 days in cattle tanks. We measured selection in the absence of free predators by regressing growth and survival in the tanks against activity and several measures of tail and body shape. We measured selection in the presence of predators by exposing groups of 10 tadpoles to Anax in overnight predation trials and regressing the average phenotype of survivors against the number of tadpoles killed. Selection in the two environments acted in opposite directions on both tail and body shape, although the affected fitness components were different. In the presence of Anax, tadpoles with shallow and narrow body, deep tail fin, and wide tail muscle survived best. In the absence of free predators, tadpoles with narrow tail muscle grew significantly faster, and those with shallow tail fin and deep body grew somewhat faster. Activity was unrelated to survival or growth in either environment. Developmental plasticity in tail shape closely paralleled selection, because tail fin depth increased after long-term exposure to Anax and tail muscle width tended to increase. In contrast, there was no plasticity in body shape in spite of strong selection for decreasing body depth. Thus, when confronted with a dragonfly predator, P. triseriata tadpoles adjusted their tail shape (but not body shape) almost exactly in the direction of selection imposed by Anax. These results suggest that phenotypic plasticity in some morphological traits, such as tail depth and tail muscle width, has evolved under intermittent selection by dragonflies. Other traits that undergo selection by dragonflies, such as body morphology, appear developmentally rigid, perhaps because of historically strong opposing selection in nature or other constraints.     

Escape behaviour and ultimate causes of specific induced defences in an anuran tadpole

Induced defences, such as the predator avoidance morphologies in amphibians, result from spatial or temporal variability in predation risk. One important component of this variability should be the difference in hunting strategies between predators. However, little is known about how specific and effective induced defences are to different types of predators. We analysed the impact of both pursuing (fish, Gasterosteus aculeatus) and sit-and-wait (dragonfly, Aeshna cyanea) predators on tadpole (Rana dalmatina) morphology and performance (viz locomotive performance and growth rate). We also investigated the potential benefits of the predator-induced phenotype in the presence of fish predators. Both predators induced deeper tail fins in tadpoles exposed to threat of predation, and stickleback presence also induced longer tails and deeper tail muscles. Morphological and behavioural differences resulted in better escape ability of stickleback-induced tadpoles, leading to improved survival in the face of stickleback predation. These results clearly indicate that specific morphological responses to different types of predators have evolved in R. dalmatina. The specific morphologies suggest low correlations between the traits involved in the defence. Independence of traits allows prey species to fine-tune their response according to current predation risk, so that the benefit of the defence can be maximal.     

Fish and dragonfly nymph predators induce opposite shifts in color and morphology of tadpoles

Many prey species, including amphibian larvae, can adaptively alter coloration and morphology to become more or less conspicuous to predators. Despite abundant research on predator-induced plasticity in tadpoles, the combination of color and morphological responses to predators remains largely unexplored. We measured predator-induced morphological and color plasticity in tadpoles. We reared tadpoles of the neotropical treefrog Dendropsophus ebraccatus with dragonfly nymph or fish predators, or in a predator-free control. After 10 days, we digitally photographed tadpoles and measured eight morphometric variables and five tail color variables. Tadpoles reared with nymphs developed the largest and reddest tails, but incurred a developmental cost, being the smallest overall. Cues from fish induced an opposite tail phenotype in tadpoles, causing shallow achromatic tails. Control tadpoles developed intermediate tail phenotypes. This provides the first experimental evidence that tadpoles can shift both color and morphology in opposite, predator-specific directions in response to a fish and an odonate predator. Despite mean differences, however, there was substantial variation in the degree of phenotype induction across treatments. Tail redness was correlated with tail spot size, but not perfectly, indicating that color and morphology may be partially decoupled in D. ebraccatus . Balancing selection from multiple conflicting predators may result in genetic variation for developmental plasticity.     

Factors determining tadpole vulnerability to predators: can prior experience compensate for a suboptimal shape?

We investigated the role of constitutive morphology and previous experience in predator avoidance in two anuran species associated with different larval habitats. In Rana temporaria, deeper tails and larger body size conferred selective advantage against dragonfly predation. Previous experience with predators had a positive influence on the survival of R. temporaria tadpoles equivalent to predator selection. By contrast, survival in Bufo bufo seems unrelated to tail shape or experience. This suggests that B. bufo lacks constitutive morphological defenses against insect predators, and that morphological and behavioral defenses could result more effective than chemical deterrents for these insect predators. A key novelty of this study is the observation that Rana tadpoles having prior experience with predators have an enhanced success in further encounters, and this occurs before the morphological induced defense has been established. This induced modification for R. temporaria, and its lack of for B. bufo, may be an important determinant of larval survival.     

The effects of perceived predation risk on pre- and post-metamorphic phenotypes in the common frog

Where organisms undergo radical changes in habitat during ontogeny, dramatic phenotypic reshaping may be required. However, physiological and functional interrelationships may constrain the extent to which an individual's phenotype can be equally well adapted to their habitat throughout the life cycle. The phenotypic response of tadpoles to the presence of a predator has been reported for several species of anuran but the potential post-metamorphic consequences have rarely been considered. We reared common frog Rana temporaria tadpoles in the presence or absence of a larval odonate predator, Aeshna juncea , and examined the consequences of the resulting phenotypic adjustment in the aquatic larval stage of the life cycle for the terrestrial juvenile phenotype. In early development tadpoles developed deeper tail fins and muscles in response to the predator and, in experimental trials, swam further than those reared in the absence of a predator. While the difference in swimming ability remained significant throughout the larval period, by the onset of metamorphosis we could no longer detect any differences in the morphological parameters measured. The corresponding post-metamorphic phenotypes also did not initially differ in terms of morphology. At 12 weeks post-metamorphosis, however, froglets that developed from predator-exposed tadpoles swam more slowly and less far than those that developed from tadpoles reared in the absence of predators, the opposite trend to that observed in the larval stage of the life cycle, and had narrower femurs. These results suggest that there may be long-term costs for subsequent life-history stages of tailoring the larval phenotype to prevailing environmental conditions.     

Naturally occurring variation in tadpole morphology and performance linked to predator regime

Divergent natural selection drives a considerable amount of the phenotypic and genetic variation observed in natural populations. For example, variation in the predator community can generate conflicting selection on behavioral, life‐history, morphological, and performance traits. Differences in predator regime can subsequently increase phenotypic and genetic variations in the population and result in the evolution of reproductive barriers (ecological speciation) or phenotypic plasticity. We evaluated morphology and swimming performance in field collected Bronze Frog larvae (Lithobates clamitans) in ponds dominated by predatory fish and those dominated by invertebrate predators. Based on previous experimental findings, we hypothesized that tadpoles from fish‐dominated ponds would have small bodies, long tails, and large tail muscles and that these features would facilitate fast‐start speed. We also expected to see increased tail fin depth (i.e., the tail‐lure morphology) in tadpoles from invertebrate‐dominated ponds. Our results support our expectations with respect to morphology in affecting swimming performance of tadpoles in fish‐dominated ponds. Furthermore, it is likely that divergent natural selection is playing a role in the diversification on morphology and locomotor performance in this system.     

Predator induced phenotypic plasticity in the pinewoods tree frog,<Emphasis Type="Italic"> Hyla femoralis</Emphasis>: necessary cues and the cost of development

Predator-induced defenses can result from non-contact cues associated with the presence of a feeding predator; however, the nature of the predator cue has not been determined. We tested the role of two non-contact cues, metabolites of digestion of conspecific prey released by the predator and alarm pheromones released by attacked conspecific prey, in the development of inducible defenses by exposing pinewoods tree frog (Hyla femoralis) tadpoles to non-lethal dragonfly (Anax junius) larvae fed either inside experimental bins or removed from the bins for feeding to eliminate alarm pheromones. The costs associated with the development of the induced morphology were also investigated by providing the tadpoles with two food levels intended to provide adequate or growth limiting resources. The generalized morphological response of H. femoralis tadpoles to predators included the development of bodies and tails that were both deeper and shorter, smaller overall body size, and increased orange tail fin coloration and black tail outline. Metabolites of digestion were sufficient to initiate development of inducible defenses; however, the combination of metabolites and alarm cue resulted in a greater response. Furthermore, growth and development were slowed in tadpoles that expressed the induced morphology; however, this growth cost was insufficient to preclude the development of the induced morphology when food resources were low. These results indicate that two aspects of the indirect predator cue work together to trigger a morphological anti-predator response.     

Interacting effects of predation risk and resource level on escape speed of amphibian larvae along a latitudinal gradient

Fast‐growing genotypes living in time‐constrained environments are often more prone to predation, suggesting that growth‐predation risk trade‐offs are important factors maintaining variation in growth along climatic gradients. However, the mechanisms underlying how fast growth increases predation‐mediated mortality are not well understood. Here, we investigated if slow‐growing, low‐latitude individuals have faster escape swimming speed than fast‐growing high‐latitude individuals using common frog (Rana temporaria) tadpoles from eight populations collected along a 1500 km latitudinal gradient. We measured escape speed in terms of burst and endurance speeds in tadpoles raised in the laboratory at two food levels and in the presence and absence of a predator (Aeshna dragonfly larvae). We did not find any latitudinal trend in escape speed performance. In low food treatments, burst speed was higher in tadpoles reared with predators but did not differ between high‐food treatments. Endurance speed, on the contrary, was lower in high‐food tadpoles reared with predators and did not differ between treatments at low food levels. Tadpoles reared with predators showed inducible morphology (increased relative body size and tail depth), which had positive effects on speed endurance at low but not at high food levels. Burst speed was positively affected by tail length and tail muscle size in the absence of predators. Our results suggest that escape speed does not trade‐off with fast growth along the latitudinal gradient in R. temporaria tadpoles. Instead, escape speed is a plastic trait and strongly influenced by the interaction between resource level and predation risk.     

Effects of behavioral and morphological plasticity on risk of predation in a Neotropical tadpole

Predator-induced phenotypic plasticity is widespread among aquatic animals, however the relative contributions of behavioral and morphological shifts to reducing risk of predation remain uncertain. We tested the phenotypic plasticity of a Neotropical tadpole (Rana palmipes) in response to chemical cues from predatory Belostoma water bugs, and how phenotype affects risk of predation. Behavior, morphology, and pigmentation all were plastic, resulting in a predator-induced phenotype with lower activity, deeper tail fin and muscle, and darker pigmentation. Tadpoles in the predator cue treatment also grew more rapidly, possibly as a result of the nutrient subsidy from feeding the caged predator. For comparison to phenotypes induced in the experiment, we quantified the phenotype of tadpoles from a natural pool. Wild-caught tadpoles did not match either experimentally induced phenotype; their morphology was more similar to that produced in the control treatment, but their low swimming activity was similar to that induced by predator cues. Exposure of tadpoles from both experimental treatments and the natural pool to a free-ranging predator confirmed that predator-induced phenotypic plasticity reduces risk of predation. Risk of predation was comparable among wild-caught and predator-induced tadpoles, indicating that behavioral shifts can substantially alleviate risk in tadpoles that lack the typical suite of predator-induced morphological traits. The morphology observed in wild-caught tadpoles is associated with rapid growth and high competition in other tadpole species, suggesting that tadpoles may profitably combine a morphology suited to competition for food with behaviors that minimize risk of predation.     

Specific induced responses to different predator species in anuran larvae

Models of defence against multiple enemies predict that specialized responses to each enemy should evolve only under restrictive conditions. Nevertheless, tadpoles of Rana temporaria can differentiate among several predator species. Small tadpoles used a refuge when Notonecta backswimmers were in the pond, but showed a weaker hiding response to adult Triturus alpestris newts and no response to aeshnid dragonfly larvae (Aeshna and Anax). All predators caused a decline in feeding and swimming activity. Large tadpoles reserved the strongest behavioural response for dragonflies, while Triturus caused no response. The shift during development suggests that tadpoles distinguished among predators, rather than exhibiting a graded dosage response to a single cue associated with predation. Information on habitat distributions of predators suggests that they are regularly encountered, which would facilitate evolution of adaptive behavioural responses. Morphological responses to all predators were similar, perhaps because similar morphologies defend against all four predators. The evolutionary maintenance of specialized responses to multiple predators may be possible because adaptive responses do not conflict and the predators themselves do not interact strongly.     

Phenotypic plasticity in complex environments: effects of structural complexity on predator‐ and competitor‐induced phenotypes of tadpoles of the wood frog,Rana sylvatica

Theoretical and empirical research has demonstrated that phenotypically plastic responses to one environment are dependent on other environmental attributes. Such research is critical considering the complexity of natural habitats, yet few studies have examined how multiple environments affect patterns of plasticity and the adaptiveness of the resulting phenotypes within complex habitats. The present study examines how wood frog (Rana sylvatica) tadpoles alter their behavioural and morphological phenotypes in response to predation risk from larval diving beetles (Dytiscus spp.), competition from conspecifics, and physical structural complexity. It also tests whether structure affects selection intensities by Dytiscus larvae on tadpole morphological traits. Predation risk and competition induced typical changes to tadpole behaviour and morphology. Structure did not induce changes to any phenotype, nor did it interact with predation risk or competition in affecting phenotypes. Furthermore, structure did not affect the predator selection intensities on any morphological trait. Dytiscus larvae selected for shallow, short tailfins, and large tail muscles, yet tadpoles only developed deep tail muscles when raised in the presence of predator cues. These apparently maladaptive responses may have been a result of correlations between phenotypes. The present study expands plasticity research by examining the adaptiveness of plastic responses in complex environments. Additionally, the present study demonstrates that not all environments induce plastic responses. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 853–863.     

A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey

Behavioral and morphological traits often influence a key trade-off between resource acquisition and vulnerability to predation, and understanding trait differences between species can provide critical insight into their interactions with other species and their distributions. Such an approach should enhance our understanding of the criteria for coexistence between species that can interact through both competition and predation (i.e. intraguild predators and prey). I conducted a common garden experiment that revealed strong differences between three guild members (larval salamanders Ambystoma laterale, A. maculatum, and A. tigrinum) in behavior, morphology, and growth in the presence and absence of a shared top predator (the larval dragonfly Anax longipes). All three species also reduced their activity and modified their tail fin depth, tail muscle length, and body length in response to non-lethal Anax. Species that act as intraguild predators were more active and could grow faster than their intraguild prey species, but they also suffered higher mortality in laboratory predation trials with Anax. I also used survey data from natural communities to compare the distribution of Ambystoma species between ponds differing in abiotic characteristics and predatory invertebrate assemblages. An intraguild prey species (A. maculatum) was found more reliably, occurred at higher densities, and was more likely to persist late into the larval period in ponds with more diverse invertebrate predator assemblages. Taken together, these results indicate that top predators such as Anax may play an important role in influencing intraguild interactions among Ambystoma and ultimately their local distribution patterns.     

Population divergence in growth rate and antipredator defences in Rana arvalis

Growth and development rates often differ among populations of the same species, yet the factors maintaining this differentiation are not well understood. We investigated the antipredator defences and their efficiency in two moor frog Rana arvalis populations differing in growth and development rates by raising tadpoles in outdoor containers in the nonlethal presence and absence of three different predators (newt, fish, dragonfly larva), and by estimating tadpole survival in the presence of free-ranging predators in a laboratory experiment. Young tadpoles in both populations reduced activity in the presence of predators and increased hiding behaviour in the presence of newt and fish. Older tadpoles from the slow-growing Gotland population (G) had stronger hiding behaviour and lower activity in all treatments than tadpoles from the fast-growing Uppland population (U). However, both populations showed a plastic behavioural response in terms of reduced activity. The populations differed in induced morphological defences especially in response to fish. G tadpoles responded with relatively long and deep body, short tail and shallow tail muscle, whereas the responses in U tadpoles were often the opposite and closer to the responses induced by the other predators. U tadpoles metamorphosed earlier, but at a similar size to G tadpoles. There was no evidence that growth rate was affected by predator treatments, but tadpoles metamorphosed later and at larger size in the predator treatments. G tadpoles survived better in the presence of free-ranging predators than U tadpoles. These results suggest that in these two populations, low growth rate was linked with low activity and increased hiding, whereas high growth rate was linked with high activity and less hiding. The differences in behaviour may explain the difference in survival between the populations, but other mechanisms (i.e. differences in swimming speed) may also be involved. There appears to be considerable differentiation in antipredator responses between these two R. arvalis populations, as well as with respect to different predators.     

Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae

This study examined the effects of multiple predators on size‐specific behavior and mortality of two species of anuran larvae. Particularly, we focused on how trait changes in predators and prey may be transmitted to other species in the food web. In laboratory experiments, we examined the effects of bluegill sunfish, Lepomis macrochirus, and the odonate larva Anax junius on behavior and mortality of tadpoles of the bullfrog, Rana catesbeiana, and the green frog R. clamitans. Experiments were conducted with predators alone and together to assess effects on behavior and mortality of the tadpoles. The experiments were replicated on five size classes of the tadpoles to evaluate how responses varied with body size.
Predation rates by Anax were higher on bullfrogs than on green frogs, and both bullfrogs and green frogs suffered greater mortality from Anax than from bluegill. Bluegill only consumed green frogs. Predation rates by both predators decreased with increasing tadpole size and decreased in the non‐lethal (caged) presence of the other predator. Both anuran larvae decreased activity when exposed to predators. Bullfrogs, however, decreased activity more in the presence of Anax than in the presence of bluegill, whereas green frogs decreased activity similarly in the presence of both predators. The largest size class of green frogs, but not of bullfrogs, exhibited spatial avoidance of bluegill. These responses were directly related to the risk posed by the different predators to each anuran species. Anax activity (speed and move frequency) also was higher when alone than in the non‐lethal presence of bluegill. We observed decreased predation rate of each predator in the non‐lethal presence of the other, apparently caused by two different mechanisms. Bluegill decreased Anax mortality on tadpoles by restricting the Anax activity. In contrast, Anax decreased bluegill mortality on tadpoles by reducing tadpole activity. We discuss how the activity and spatial responses of the tadpoles interact with palatability and body size to create different mortality patterns in the prey species and the implications of these results to direct and indirect interactions in this system.     

Body size and group size of Cuban tree frog (<Emphasis Type="Italic">Osteopilus septentrionalis</Emphasis>) tadpoles influence their escape behaviour

Tadpoles risk attack from both aquatic and aerial predators. We investigated how body size and group size influenced the behaviour of tadpoles before and during a predatory attack from above to test the predictions of the theoretical economic escape model. We examined escape (swimming) response of small and large Cuban tree frog (Osteopilus septentrionalis) tadpoles kept under three density treatments and predicted that increased group size, body size and depth in the water column would all reduce perceived risk and, therefore, escape responses to simulated predation. Compared with the lower density groups, tadpoles in higher density groups moved shorter distances, and many individuals did not even move away in response to being touched. Contrary to our predictions based on the economic escape model, smaller tadpoles (which should be more vulnerable to a greater suite of predators) were less reactive than larger tadpoles, and this result may reflect different costs of escape. Finally, although tadpoles might be exposed to a wider range of predator species (aerial as well as aquatic predators), we found no effect of initial depth on escape responses. In conclusion, it appears that the main benefit of increased group density in O. septentrionalis tadpoles is likely to be predator dilution, and that variation in densities of tadpoles influences the escape behaviour of individual tadpoles, regardless of tadpole size.     

Reversibility of predator‐induced plasticity and its effect at a life‐history switch point

In natural systems, organisms are frequently exposed to spatial and temporal variation in predation risk. Prey organisms are known to develop a wide array of plastic defences to avoid being eaten. If inducible plastic defences are costly, prey living under fluctuating predation risk should be strongly selected to develop reversible plastic traits and adjust their defences to the current predation risk. Here, we studied the induction and reversibility of antipredator defences in common frog Rana temporaria tadpoles when confronted with a temporal switch in predation risk by dragonfly larvae. We examined the behaviour and morphology of tadpoles in experimental treatments where predators were added or withdrawn at mid larval development, and compared these to treatments with constant absence or presence of predators. As previous studies have overlooked the effects that developing reversible anti‐predator responses could have later in life (e.g. at life history switch points), we also estimated the impact that changes in antipredator responses had on the timing of and size at metamorphosis. In the presence of predators, tadpoles reduced their activity and developed wider bodies, and shorter and wider tails. When predators were removed tadpoles switched their behaviour within one hour to match that found in the constant environments. The morphology matched that in the constant environments in one week after treatment reversal. All these responses were highly symmetrical. Short time lags and symmetrical responses for the induction/reversal of defences suggest that a strategy with fast switches between phenotypes could be favoured in order to maximise growth opportunities even at the potential cost of phenotypic mismatches. We found no costs of developing reversible responses to predators in terms of life‐history traits, but a general cost of the induction of the defences for all the individuals experiencing predation risk during some part of the larval development (delayed metamorphosis). More studies examining the reversibility of plastic defences, including other type of costs (e.g. physiological), are needed to better understand the adaptive value of these flexible strategies.     

Flexible architecture of inducible morphological plasticity

1. Predator-induced morphological defences are produced in response to an emergent predator regime. In natural systems, prey organisms usually experience temporal shifting of the composition of the predator assemblage and of the intensity of predation risk from each predator species. Although, a repetitive morphological change in response to a sequential shift of the predator regime such as alteration of the predator species or diminution of the predation risk may be adaptive, such flexible inducible morphological defences are not ubiquitous. 2. We experimentally addressed whether a flexible inducible morphological defence is accomplished in response to serial changes in the predation regime, using a model prey species which adopt different defensive morphological phenotypes in response to different predator species. Rana pirica (Matsui) tadpoles increased body depth and tail depth against the predatory larval salamander Hynobius retardatus (Dunn); on the other hand, they only increased tail depth against the predatory larval dragonfly Aeshna nigroflava (Martin). 3. Rana pirica tadpoles with the predator-specific phenotypes were subjected to removal or exchange of the predator species. After removal of the predator species, tadpoles with each predator-specific phenotype changed their phenotype to the nondefensive basic one, suggesting that both predator-specific phenotypes are costly to maintain. After an exchange of the predator species, tadpoles with each predator-specific phenotype reciprocally, flexibly shifted their phenotype to the now more suitable predator-specific one only by modifying their body part. The partial modification can effectively reduce time and energy expenditures involved in repetitive morphological changes, and therefore suggest that the costs of the flexible morphological changes are reduced.     

Morphological and life‐history responses of anurans to predation by an invasive crayfish: an integrative approach

Predator‐induced phenotypic plasticity has been widely documented in response to native predators, but studies examining the extent to which prey can respond to exotic invasive predators are scarce. As native prey often do not share a long evolutionary history with invasive predators, they may lack defenses against them. This can lead to population declines and even extinctions, making exotic predators a serious threat to biodiversity. Here, in a community‐wide study, we examined the morphological and life‐history responses of anuran larvae reared with the invasive red swamp crayfish, Procambarus clarkii, feeding on conspecific tadpoles. We reared tadpoles of nine species until metamorphosis and examined responses in terms of larval morphology, growth, and development, as well as their degree of phenotypic integration. These responses were compared with the ones developed in the presence of a native predator, the larval dragonfly Aeshna sp., also feeding on tadpoles. Eight of the nine species altered their morphology or life history when reared with the fed dragonfly, but only four when reared with the fed crayfish, suggesting among‐species variation in the ability to respond to a novel predator. While morphological defenses were generally similar across species (deeper tails) and almost exclusively elicited in the presence of the fed dragonfly, life‐history responses were very variable and commonly elicited in the presence of the invasive crayfish. Phenotypes induced in the presence of dragonfly were more integrated than in crayfish presence. The lack of response to the presence of the fed crayfish in five of the study species suggests higher risk of local extinction and ultimately reduced diversity of the invaded amphibian communities. Understanding how native prey species vary in their responses to invasive predators is important in predicting the impacts caused by newly established predator–prey interactions following biological invasions.     

Determinants and co‐expression of anti‐predator responses in amphibian tadpoles: a meta‐analysis

A wide range of taxa respond to perceived predation risk (PPR) through inducible defenses, and many prey are capable of responding both behaviorally and morphologically to the same risk event. In cases where multiple defenses confer protection by independent means (i.e. they are mechanistically independent) responses will either be co‐expressed, or the expression of one defense will limit the capacity (or need) to respond along another axis. Our ability to generate a broad understanding of these patters has been limited, in part, by difficulties in comparing results across studies that employ distinct experimental protocols. Using the extensive literature on tadpole responses to PPR, we conducted a meta‐analysis to identify the ecological and experimental determinants of inducible defence expression. We then assessed whether the magnitude of response to PPR along behavioural versus morphological response axes was positively, or negatively, correlated. The most commonly quantified responses to perceived risk in tadpoles included reductions in movement and swimming behaviour, and altered tail morphology. Our analyses reveal that tadpole behavioural responses are strongly influenced by prey family, predator taxon, evolutionary history with the predator (native versus non‐native), amount of prey consumed by the predator, and how perceived risk was manipulated (e.g. presence versus absence of alarm cues). Tail morphology was similarly influenced by these factors, but also whether the target prey was palatable to predators. Thus, our results identify ecological and experimental features that critically influence the observed effect size in tadpole responses to PPR. A positive correlation between behavioural and morphological responses in studies where both were measured indicates that trait co‐specialization is the predominant pattern of defense deployment in larval amphibians. This positive relationship suggests that survival tends to be maximized in tadpoles through equivalent co‐activation of multiple independent axes of protection, opposed to maximal expression along any single axis. Synthesis Our understanding of plastic responses to perceived predation risk (PPR) has benefited substantially from the vast amount of experimental work examining inducible defences in anuran tadpoles. Indeed this research has illustrated the wide variety of ways that prey animals can respond to the same risk event. We conducted a metaanalysis to identify the key ecological and experimental determinants of inducible defence expression. We then show that, in most cases, behavioural and morphological responses to PPR tend to be co‐expressed suggesting that responding along one axis (moving behaviour) does not limit their ability to respond along another distinct axis (tail morphology).