Larval life history and anti-predator strategies are affected by breeding phenology in an amphibian

Seasonal time constraints can pose strong selection on life histories. Time-constrained animals should prioritise fast development over predation risk to avoid unfavourable growing conditions. However, changes in phenology could alter the balance between anti-predator and developmental needs. We studied variation of anti-predator strategies in common frog (Rana temporaria) tadpoles in four populations from the two extremes of a latitudinal gradient across Sweden. We examined, under common conditions in the laboratory, the anti-predator responses and life histories of tadpoles raised with predatory Aeshna dragonfly larvae in two consecutive years with a difference of 20 days in breeding time in the north, but no difference in breeding time in the nouth. In a year with late breeding, northern tadpoles did not modify their behaviour and morphology in the presence of predators, and metamorphosed faster and smaller than tadpoles born in a year with early breeding. In the year with early breeding, northern tadpoles showed a completely different anti-predator strategy by reducing activity and developing morphological defences in the presence of predators. We discuss the possible mechanisms that could activate these responses (likely a form of environmentally-mediated parental effect). To our knowledge, this is the first study to show that a vertebrate modifies the anti-predator strategy of its offspring in response to natural variation in reproductive phenology, which highlights the need to consider phenology in studies of life-history evolution.     

Nonlethal injury caused by an invasive alien predator and its consequences for an anuran tadpole

Nonlethal tail injury resulting from unsuccessful predation attempts is common in anuran larvae and can potentially induce significant fitness costs in terms of survival and growth. We tested the hypotheses that the alien red swamp crayfish, Procambarus clarkii, is an important inducer of tail injury in tadpoles of the Iberian spadefoot toad, Pelobates cultripes, and that tail damage can have important consequences for the tadpoles’ life history and morphology. This was investigated by first estimating frequencies of caudal injury in P. cultripes tadpoles in temporary ponds, with and without crayfish. Secondly, we performed a laboratory experiment in which four levels of tail injury frequency were combined with two levels of food availability.The frequency of tadpoles with damaged tails was higher in ponds with crayfish and the presence of this predator was the strongest predictor of tail injury frequency in a pond. Induced tail loss decreased larval survivorship and affected tail morphology, with injured tadpoles developing deeper tail muscles and shallower tail fins. The magnitude of these effects depended on injury frequency, as well as on food availability. The results suggest that P. clarkii is inflicting tail injuries at much higher levels than those occurring before its introduction; these injuries affect tadpole morphology and may induce delayed fitness costs.     

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.     

Density is more important than predation risk for predicting growth and developmental outcomes in tadpoles of spotted tree frog,Litoria spenceri (Dubois 1984)

The diverse benefits of group living include protection against predators through dilution effects and greater group vigilance. However, intraspecific aggregation can decrease developmental rates and survival in prey species. We investigated the impact on tadpole development and behaviour of the interaction between population density and predation risk. Spotted tree frog (Litoria spenceri: Hylidae, Dubois 1984) tadpoles were kept at one of three different densities (two tadpoles per litre, five tadpoles per litre or 10 tadpoles per litre) until metamorphosis in the presence or absence of predatory cues. We aimed to determine the influence of population density, predation and the interaction of both factors in determining growth rates in tadpoles. Tadpoles were measured weekly to assess growth and development and filmed to quantify differences in activity and feeding frequency between groups. Generally, tadpoles housed without predators had longer developmental periods when housed with a predator, but there was no effect on tail length or total length. There was no effect of either predation cues or density on percentage of individuals feeding or moving. Although the effects of the presence of predators alone may appear to be less than the effects of the presence of competitors, the prioritisation of competitiveness over predator avoidance may increase vulnerability of tadpoles to the lethal threat of predators. This is particularly important in species such as L. spenceri, which is at risk from introduced fish predators.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Invasive predatory crayfish do not trigger inducible defences in tadpoles

Invasive species cause deep impacts on ecosystems worldwide, contributing to the decline and extinction of indigenous species. Effective defences against native biological threats in indigenous species, whether structural or inducible, often seem inoperative against invasive species. Here, we show that tadpoles of the Iberian green frog detect chemical cues from indigenous predators (dragonfly nymphs) and respond by reducing their activity and developing an efficient defensive morphology against them (increased tail depth and pigmentation). Those defensive responses, however, were not activated against a highly damaging invasive predator (red swamp crayfish). Induced defences increased tadpole survival when faced against either indigenous dragonflies or invasive crayfish, so its inactivation in the presence of the invasive predator seems to be due to failure in cue recognition. Furthermore, we tested for local adaptation to the invasive predator by comparing individuals from ponds either exposed to or free from crayfish. In both cases, tadpoles failed to express inducible defences against crayfish, indicating that ca 30 years of contact with the invasive species (roughly 10-15 frog generations) have been insufficient for the evolution of recognition of invasive predator cues.     

Embryonic and larval defensive responses of agile frog (Rana dalmatina) to alien crayfish

Red swamp crayfish Procambarus clarkii, a widespread invasive alien crayfish, represents a serious threat for several freshwater species, including amphibians, which are declining at a global scale. As a shared coevolutionary history is the main factor determining the emergence of antipredator responses, Anuran tadpoles may not be able to cope effectively with this introduced predator. We performed two experiments to assess agile frog's (Rana dalmatina) defensive responses to both P. clarkii and native dragonfly larvae (Anax imperator). First, we conditioned embryos (collected from two ponds 30 km away from each other) with predators’ chemical cues to explore possible variation in hatching time caused by predation risk. In the second experiment, to evaluate how predators’ diet affects tadpole behavior, we conditioned tadpoles for a 5‐week period with cues from tadpole‐fed and gammarid‐fed predators and recorded behavioral and morphological responses. Embryos did not alter hatching time in the presence of any predator cue, while tadpoles from both populations strongly reduced activity and visibility when raised in the presence of tadpole‐fed dragonfly larvae. Morphological changes were less straightforward and were induced only in one population, for which broader tails and a slight increase in body size of tadpoles exposed to tadpole‐fed predators were observed. The lack of defensive responses in crayfish‐exposed tadpoles suggests that the spreading of this invasive species in agricultural lowlands of northern Italy may represent a further threat to their conservation.     

Assessing the risk effects of native predators on the exotic American bullfrog (Lithobates catesbeianus) and their indirect consequences to ecosystem function

Understanding the factors and mechanisms that affect the impacts of invasive species in invaded environments has been widely debated among researchers. However, few studies about invasive species have explored the effects of predation risks by native predators on exotic prey. Herein, the traditional invasive predator-native prey framework was reversed. We tested if tadpoles, of the worldwide invasive American Bullfrog Lithobates catesbeianus, were affected by the predation risk imposed by native predators. We used two different species of belostomatid predators and tested whether and how predation-induced phenotypic plasticity on L. catesbeianus reverberated in morphological, physiological, and ecosystem-level processes. Individuals of L. catesbeianus modified their morphological (tail muscle width), behavioral (activity and foraging), and physiological (growth and growth efficiency) traits in the presence of predation risk. Based on the observed morphological changes, our results suggest that prey may recognize predator-specific cues. In addition, we observed that L. catesbeianus' responses to predation risk can affect ecosystem-level properties, by inducing trophic cascades and reducing animal-mediated nutrient recycling rates. In summary, our study supports that exotic prey species who are subjected to native predators may display anti-predator responses, with implications for their development, as well as possible ecosystem-level effects.     

Complex impact of an invasive crayfish on freshwater food webs

Invasive alien species can have complex effects on native ecosystems, and interact with multiple components of food webs, making it difficult a comprehensive quantification of their direct and indirect effects. We evaluated the relationships between the invasive crayfish, Procambarus clarkii, amphibian larvae and predatory insects, to quantify crayfish impacts on multiple levels of food webs, and to evaluate whether crayfish predation of aquatic insects has indirect consequences for their preys. We used pipe sampling to assess the abundance of crayfish, amphibian larvae and their major predators (Ditiscidae, Notonectidae and larvae of Anisoptera) in invaded and uninvaded ponds within a human dominated landscape. We disentangled the multivariate effects of P. clarkii on different components of food web through a series of constrained redundancy analyses. The crayfish had a negative, direct impact on both amphibian communities and their predators. Amphibian abundance was negatively related to both predators. However, the negative, direct effects of crayfish on amphibians were much stronger than predation by native insects. Our results suggest that this crayfish impacts multiple levels of food webs, disrupting natural prey-predator relationships.     

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.     

Prey detection of aquatic predators: Assessing the identity of chemical cues eliciting prey behavioral plasticity

Chemical cues transmitted through the environment are thought to underlie many prey responses to predation risk, but despite the known ecological and evolutionary significance of such cues, their basic composition are poorly understood. Using anuran tadpoles (prey) and dragonfly larvae (predators), we identified chemical cues associated with predation risk via solid phase extraction and mass spectrometry of the extracts. We found that dragonfly larvae predators consistently produced a negative ion, m/z 501.3, when they fed on bullfrog (Rana catesbeiana) and mink frog (Rana septentrionalis) tadpoles, but this ion was absent when dragonflies were fasted or fed invertebrate prey. When tadpole behavioral responses to dragonfly chemical cues were examined, tadpoles reduced their activity, particularly in response to dragonflies feeding on tadpoles. Furthermore, a negative correlation was noted between the level of tadpole activity and the concentration of the m/z 501.3 compound in dragonfly feeding trials, indicating that this ion was possibly responsible for tadpole anti-predator behavior.     

Predator-prey relationships among larval dragonflies,salamanders, and frogs

Summary Tadpoles of the barking tree frog, Hyla gratiosa, are abundant in spring and summer in some ponds and Carolina bays on the Savannah River Plant near Aiken, South Carolina. To determine how these tadpoles survive in the presence of predaceous salamander larvae, Ambystoma talpoideum, and larvae of an aeshnid dragonfly, Anax junius, we determined fields densities and sizes of the predators and the prey and conducted predation experiments in the laboratory. Tadpoles rapidly grow to a size not captured by Ambystoma, although Anax larvae can capture slightly larger tadpoles. Differing habitat preferences among the tadpoles and the two predator species probably aid in reducing predation pressure. Preliminary work indicates that the tadpoles may have an immobility response to an attack by a predator. In addition, the smallest, most vulnerable tadpoles have a distinctive color pattern which may function to disrupt the body outline and make them indiscernable to predators.     

Chemosensory Perception of Predators by Larval Amphibians Depends on Water Quality

The acquisition of sensory information by animals is central to species interactions. In aquatic environments, most taxa use chemical cues to assess predation risk and other key ecological factors. A number of laboratory studies suggest that anthropogenic pollutants can disrupt chemoreception, even when at low, non-toxic concentrations, but there are few tests of whether real-world variation in water quality affects chemoreception. Here we investigate whether chemosensory perception of predators by the gray treefrog, Hyla versicolor, depends on water quality. We evaluated the anti-predator response of anuran tadpoles housed in water collected from three sites that represent strong contrasts in the concentration and types of dissolved solids: de-chlorinated tap water, water from an impaired stream, and treated wastewater effluent. Behavioral assays were conducted in laboratory aquaria. Chemical cues associated with predation were generated by feeding tadpoles to dragonfly predators held in containers, and then transferring aliquots of water from dragonfly containers to experimental aquaria. Tadpoles housed in tap water responded to predator cues with an activity reduction of 49%. Tadpoles housed in stream water and wastewater effluent responded to predator cues by reducing activity by 29% and 24% respectively. The results of factorial ANOVA support the hypothesis that the response to predator cues depended on water type. These results show that alteration of the chemical environment can mediate chemical perception of predators in aquatic ecosystems. Because most aquatic species rely on chemoreception to gather information on the location of food and predators, any impairment of sensory perception likely has important ecological consequences.     

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.     

Predator Avoidance and Alarm-response Behaviour in Kin-discriminating Tadpoles (Rana cascadae)

When captured by predators, the tadpoles of some species of frogs and toads may release an alarm substance that alters the behaviour of conspecifics. Such ‘alarm response’ behaviour has been proposed as a potential mechanism whereby related conspecifics may ‘warn’ relatives of a predator's presence and thus, improve their inclusive fitness. We examined predator avoidance and alarm response behaviour in tadpoles of the Cascades frog (Rana cascadae) and tested whether such behaviour is influenced by kinship factors. Tadpoles reduced activity when in the presence of a predatory newt (Taricha granulosa). Individuals in sibling groups were more active than both solitary tadpoles and individuals in mixed groups of siblings and nonsiblings. However, we found no evidence of an alarm response in R. cascadae. Behaviour of tadpoles in groups exposed only to predators was not different from that of tadpoles in groups exposed to predators plus crushed conspecifics. Tadpoles in groups exposed to crushed tadpoles were as active as tadpoles in groups exposed to water controls, and some test individuals fed upon the dead tadpoles. Thus, while R. cascadae tadpoles reduce activity in response to newt predators, crushed tadpoles appear to initiate a feeding response rather than an alarm response as has been previously proposed.     

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.     

Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish

Background

Invasive predators may change the structure of invaded communities through predation and competition with native species. In Europe, the invasive signal crayfish Pacifastacus leniusculus is excluding the native white clawed crayfish Austropotamobius pallipes.

Methodology and Principal Findings

This study compared the predatory functional responses and prey choice of native and invasive crayfish and measured impacts of parasitism on the predatory strength of the native species. Invasive crayfish showed a higher (>10%) prey (Gammarus pulex) intake rate than (size matched) natives, reflecting a shorter (16%) prey handling time. The native crayfish also showed greater selection for crustacean prey over molluscs and bloodworm, whereas the invasive species was a more generalist predator. A. pallipes parasitised by the microsporidian parasite Thelohania contejeani showed a 30% reduction in prey intake. We suggest that this results from parasite-induced muscle damage, and this is supported by a reduced (38%) attack rate and increased (30%) prey handling time.

Conclusions and Significance

Our results indicate that the per capita (i.e., functional response) difference between the species may contribute to success of the invader and extinction of the native species, as well as decreased biodiversity and biomass in invaded rivers. In addition, the reduced predatory strength of parasitized natives may impair their competitive abilities, facilitating exclusion by the invader.     

Risk of predation affects aggregation size: a study with tadpoles of Phrynomantis microps (Anura: Microhylidae)

Tadpoles of the microhylid frog Phrynomantis microps form swarms near the water surface of savannah ponds during the day. Observations of tadpole distribution at night showed that these aggregations disappear and that tadpoles instead swim in a random distribution near the water surface. The clarity of pond water had significant effects on the distribution of tadpoles during the day. The size of aggregations, and the densities of tadpoles within them, both increased with increasing water clarity. Since tadpoles of this species are known to aggregate in response to visually hunting aquatic predators, these results suggest that tadpoles respond to high water clarity as an indicator of increased predation risk. This supports the hypothesis that, under conditions of increasing predation risk, animals should form larger and more dense groups up to a critical group size. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

The influence of evolution and plasticity on the behavior of an invasive crayfish

Invasion success can be enhanced by evolution and behavioral plasticity, but the importance of these processes for most invasions is not well understood. Previous research suggests there is a genetic basis for differences in growth rate between native and invaded range rusty crayfish (Orconectes rusticus). We hypothesized that invaded range O. rusticus achieve faster growth by allocating more time to foraging and less to defense. We conducted a laboratory experiment to test the effects of range (native or invaded) and plasticity (as induced by exposure to predators) on crayfish behavior. We collected O. rusticus adults and eggs from both ranges, hatched eggs in the lab, and reared juveniles in common conditions either with or without predatory fish. We then quantified adult and juvenile crayfish activity in an experiment with and without predatory fish. In support of our hypothesis, invaded range adults displayed reduced antipredator behavior compared to native range adults. Further, invaded range juveniles were more active than native range juveniles without predators, but all juveniles were inactive with predators. In addition, invaded range juveniles had greater plasticity in behavior than native range juveniles. These results suggest that activity level in the absence of predators has diverged in the invaded range. Because active crayfish consume more prey, this change in behavior may be responsible for rapid growth in the invaded range of O. rusticus, a trait that contributes to the strong ecological impacts of this invasive crayfish.