Tadpoles of three common anuran species from Thailand do not prey on mosquito larvae

Tadpoles are often considered to be predators of mosquito larvae and are therefore beneficial for the control of certain disease vectors. Nevertheless, only a few species have actually been recorded to prey on mosquito larvae. The mosquito larvae predation rates of tadpoles of three common Thai anuran species (Bufo melanostictus, Kaloula pulchra and Hylarana raniceps) were experimentally tested. Tadpoles in varying developmental stages were used to assess a size/age effect on the predation rate. In addition, different instars of Culex quinquefasciatus were used in order to assess a prey size effect on the predation rates. All three species failed to show any evidence of mosquito larvae predation. Neither small nor large tadpoles fed on mosquito larvae. Prey size also did not affect predation. Although tadpoles do not feed on mosquito larvae, there may be other direct or indirect inter‐specific interactions that adversely impact the development of larvae in shared habitats with tadpoles.     

COSTS AND BENEFITS OF A PREDATOR-INDUCED POLYPHENISM IN THE GRAY TREEFROG HYLA CHRYSOSCELIS

The phenotypes of gray treefrog (Hyla chrysoscelis) tadpoles vary depending on whether predators are present in the pond. Tadpoles reared in ponds with predatory dragonfly larvae are relatively inactive compared with tadpoles in predator-free ponds, and have relatively large, brightly colored tailfins with dark spots along the margins. Models for the evolution of plasticity predict that induced phenotypes such as this should confer high fitness relative to the typical phenotype when in the presence of predators, but should be costly when the predator is absent. Our study tested for the predicted fitness trade-off in H. chrysoscelis by first rearing tadpoles in mesocosms under conditions that induce the alternate phenotypes, and then comparing the performance of both phenotypes in both environments. We generated the two phenotypes by rearing tadpoles in 600-liter outdoor artificial ponds that contained either two caged dragonflies (Anax junius) or an empty cage. Tadpoles from the two environments showed significantly different behavior, tail shape, and tail color within two weeks of exposure. We compared the growth and survival of both phenotypes over four weeks in ponds where there was no actual risk of predation. Under these conditions, both phenotypes grew at the same rate, but the predator-induced phenotype had significantly lower survival than the typical phenotype, indicating that induced tadpoles suffered greater mortality from causes other than odonate predation. We tested the susceptibility of both phenotypes to predation by exposing them to dragonflies in 24-h predation trials. The predator-induced phenotype showed a significant survival advantage in these trials. These results confirm that the predator-induced phenotype in H. chrysoscelis larvae is associated with fitness costs and benefits that explain why the defensive phenotype is induced rather than constitutive.     

Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type

Many species alter their activity, microhabitat use, morphology and life history in response to predators. Predation risk is related to predator size and palatability of prey among others factors. We analyzed the predation risk of three species of tadpoles that occur in norwestern Patagonia, Argentina: Pleurodema thaul, Pleurodema bufoninum and Rhinella spinulosa. We sampled aquatic insect predators in 18 ponds to determine predator–tadpole assemblage in the study area. In laboratory conditions, we analysed the predation rate imposed by each predator on each tadpole species at different tadpole sizes. Finally, we tested whether tadpoles alter their activity in the presence of chemical and visual cues from predators. Small P. thaul and P. bufoninum tadpoles were the most vulnerable prey species, while small R. spinulosa tadpoles were only consumed by water bugs. Dragonflies and water bugs were the most dangerous tadpole predators. Small P. thaul tadpoles reduced their activity when they were exposed to all predators, while large tadpoles only reduced the activity in the presence of large predators (dragonfly larvae and water bugs). Small P. bufoninum tadpoles reduced the activity when they were exposed to beetle larvae and dragonfly larvae, while large tadpoles only reduced activity when they were exposed to larger predators (water bugs and dragonfly larvae). R. spinulosa tadpoles were the less sensitive to presence of predators, only larger tadpoles responded significantly to dragonfly larvae by reducing their activity. We conclude that behavioural responses of these anuran species were predator-specific and related to the risk imposed by each predator.     

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.     

Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae

Chemical signals are used as information by prey to assess predation risk in their environment. To evaluate the effects of multiple predators on prey growth, mediated by a change in prey activity, I exposed small and large bullfrog (Rana catesbeiana) larvae (tadpoles) to chemical cues from different combinations of bluegill sunfish (Lepomis macrochirus) and larval dragonfly (Anax junius) predators. Water was regularly transferred from predation trials (outdoor experiment) to aquaria (indoor experiment) in which activity and growth of tadpoles was measured. The highest predation mortality of small bullfrog larvae in the outdoor experiment was due to Anax, and it was slightly lower in the presence of both predators, probably resulting from interactions between predators. There was almost no mortality of prey with bluegill. The activity and growth of small bullfrog larvae was highest in the absence of predators and lowest in the presence of Anax. In the presence of bluegill only, or with both predators, the activity and growth of small bullfrog tadpoles was intermediate. Predators did not affect large tadpole activity and growth. Regressing mortality of small bullfrog tadpoles against activity and growth of bullfrog tadpoles revealed a significant effect for small bullfrog larvae but a non-significant effect for large bullfrog larvae. This shows that the response of bullfrog tadpoles to predators is related to their own body size. The experiment demonstrates that chemical cues are released both as predator odor and as alarm substances and both have the potential to strongly alter the activity and growth of prey. Different mechanisms by which chemical cues may be transmitted to species interactions in the food web are discussed. Received: 28 June 1999 / Accepted: 15 November 1999     

Direct and indirect effects of dragonfly (<Emphasis Type="Italic">Anax imperator</Emphasis>) nymphs on green toad (<Emphasis Type="Italic">Bufo viridis</Emphasis>) tadpoles

We conducted an artificial pond experiment to assess the direct and indirect effects of predation on Bufo viridis tadpoles. We ran three treatments: free Anax (unrestrained predatory dragonfly nymph Anax imperator), caged Anax (non-consumptive effects), and control (no Anax). Anax showed both strong consumptive and non-consumptive effects on Bufo tadpoles. Free Anax eliminated all of the tadpoles within six days. Tadpoles preferred the shady side of the ponds. Caged Anax caused tadpoles to increase their spatial preferences. Tadpoles avoided the center of the pond, and in the presence of the caged predator, they were found in the center even less. Tadpoles also showed a strong preference for crowding together, and in the presence of a caged Anax, they tended to crowd more. Moreover, Bufo metamorphosed earlier and at a larger size in the caged Anax ponds, possibly by providing extra food resources due to the extra organic matter excreted by the predators. Handling editor: K. Martens     

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.     

Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation

In many amphibian larvae a suite of morphological and behavioural characters varies together in an induced defence against predators, but it remains unclear which features are functionally related to defence. We independently manipulated behaviour and morphology in tadpoles of Hyla versicolor and assessed their consequences for swimming performance and predator escape. Data on burst swimming showed that tadpoles which accelerated rapidly were elongate, with shallow bodies and tails. Predator escape was measured by exposing tadpoles to predators (larval Anax dragonflies or larval Ambystoma salamanders) and recording time until death. Tadpoles were first reared for 30 days in ponds containing either caged Anax or no predators; individuals responded to predators by developing large brightly coloured tails and short bodies. We placed tadpoles of both morphological phenotypes into plastic tubs, and manipulated their behaviour using food and chemical cues from predators. Mortality risk experienced by the predator‐induced phenotype was about half that of the no‐predator phenotype, and risk increased with time spent swimming. An interaction between morphology and behaviour arose because increasing activity caused higher risk for tadpoles with deep tail fins but not shallow tail fins.     

Tadpole–odonate larvae interactions: influence of body size and diel rhythm

Several studies have shown that prey and predator body size may affect the outcome of predator–prey interactions. However, few studies have taken in account the changes on predator–prey interactions over 24 h. In a tropical freshwater system I evaluated how predator and prey size, and their diel rhythm in activity influenced the interaction between Physalaemus pustulosus tadpoles and dragonfly larvae. Tadpoles of different size classes were exposed to two size classes of the dragonfly larvae Rhionaeschna spec. Feeding trials were conducted during day and night. Tadpole activity showed a diel rhythm and affected size-selective predation of the smallest dragonfly larvae, but not of the larger ones. Predator and prey size had a significant effect on the prey survivorship and prey size had a significant effect on the preference of the predator. The interaction between both factors was significant, indicating that they did not operate independently. I conclude that the predator–prey interactions between odonate larvae and anuran tadpoles were mainly affected by the size of the prey and the predator, and less by the diel activity pattern of the prey.     

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.     

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.     

Chemical defense of toad tadpoles under risk by four predator species

Many organisms use inducible defenses as protection against predators. In animals, inducible defenses may manifest as changes in behavior, morphology, physiology, or life history, and prey species can adjust their defensive responses based on the dangerousness of predators. Analogously, prey may also change the composition and quantity of defensive chemicals when they coexist with different predators, but such predator‐induced plasticity in chemical defenses remains elusive in vertebrates. In this study, we investigated whether tadpoles of the common toad (Bufo bufo) adjust their chemical defenses to predation risk in general and specifically to the presence of different predator species; furthermore, we assessed the adaptive value of the induced defense. We reared tadpoles in the presence or absence of one of four caged predator species in a mesocosm experiment, analyzed the composition and quantity of their bufadienolide toxins, and exposed them to free‐ranging predators. We found that toad tadpoles did not respond to predation risk by upregulating their bufadienolide synthesis. Fishes and newts consumed only a small percentage of toad tadpoles, suggesting that bufadienolides provided protection against vertebrate predators, irrespective of the rearing environment. Backswimmers consumed toad tadpoles regardless of treatment. Dragonfly larvae were the most voracious predators and consumed more predator‐naïve toad tadpoles than tadpoles raised in the presence of dragonfly cues. These results suggest that tadpoles in our experiment had high enough toxin levels for an effective defense against vertebrate predators even in the absence of predator cues. The lack of predator‐induced phenotypic plasticity in bufadienolide synthesis may be due to local adaptation for constantly high chemical defense against fishes in the study population and/or due to the high density of conspecifics.     

Evaluating predation pressure on green treefrog larvae across a habitat gradient

The effect of a predator on the abundance of a prey species depends upon the predators abundance and its ability to capture that prey. The objectives of this research were to evaluate the community structure of predators of green treefrog (Hyla cinerea) tadpoles across habitat types and evaluate the effectiveness of individual predators on H. cinerea tadpoles. Correspondence and cluster analyses of predator frequencies across 23 aquatic habitats indicated that the majority of variance in predator communities was due to a division between permanent and temporary habitats. Experimental work demonstrated that survival of the smallest H. cinerea tadpoles was significantly lower than survival of medium and large tadpoles with the most effective predators, indicating that H. cinerea tadpoles attain a refuge from predation at larger body sizes. We combined the effectiveness of predators in experiments with the abundance of each predator species from the predator community survey to demonstrate that predation pressure on H. cinerea tadpoles is higher in temporary ponds. This pattern may explain in part why this species generally breeds successfully only in permanent habitats. It also confirms that discussions about an increasing gradient of predation pressure from temporary to permanent aquatic habitats should be restricted to individual prey species for which such a gradient has been demonstrated.     

Temporary pools are not `enemy-free'

Temporary pools are traditionally considered as refuges where the conspicuous anostracans are protected from predation. While this is true for the size-selective predation by fish, there is compelling evidence that invertebrate predation is an important biotic stress regulating temporary pool communities. In rock pools in southeastern Botswana, we studied the impact of some suspected invertebrate predators on populations of the freshwater anostracan Branchipodopsis wolfi by means of observations and manipulative experiments. In a survey of 45 pools, the relationship between B. wolfi natural population sizes and the abundance of suspected predators were never negative for turbellarians and mosquito larvae. When dragonfly larvae, notonectids or tadpoles were present, the anostracan populations were generally non-existent or very small. In enclosure experiments with turbellarians, there was a significant effect of predation within one hour of the start; the average daily predation rate was about 1/4 anostracan per turbellarian. Anostracans from a pool with few turbellarians were slightly less vulnerable than those from a turbellarian-rich pool. Furthermore, there was an indication of males being predated on more than females. With dragonfly larvae and notonectids, the predation effect was marked with all six anostracans in an experiment eaten in less than one day by a single predator (predation rate: about one anostracan every 2 h per predator). In a behavioral study, both sexes of B. wolfi avoided swimming above sediment that held more turbellarians than the open patches; there was no evidence for chemical communication with respect to this behavior.     

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.     

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.     

Behavioral responses of American toad and bullfrog tadpoles to the presence of cues from the invasive fish, Gambusia affinis

The introduction of non-native predators is thought to have important negative effects on native prey populations. The susceptibility of native prey to non-native or introduced predators may depend on their ability to respond appropriately to the presence of these non-native predators. We conducted a laboratory based behavioral experiment to examine the response of American toad (Bufo americanus) and bullfrog (Rana catesbeiana) tadpoles to the presence of cues from the introduced mosquitofish (Gambusia affinis), a potential tadpole predator. Neither the American toad tadpoles nor the bullfrog tadpoles responded behaviorally to the presence of mosquitofish cues. If tadpoles are unable to respond to the presence of mosquitofish cues appropriately, then their ability to avoid predation by mosquitofish may be compromised and this may contribute to the impacts of mosquitofish on some tadpole populations.     

Divergent responses of exposed and naive Pacific tree frog tadpoles to invasive predatory crayfish

Invasive predators can devastate native species and ecosystems. However, native species may be able to coexist with invasive predators through a variety of mechanisms, such as changes in morphology or behavior due to a plastic response or selection on fixed anti-predator traits. We examined whether exposed and naive populations of Pacific tree frog tadpoles (Pseudacris regilla) display divergent morphological and behavioral traits in response to the invasive predatory red swamp crayfish (Procambarus clarkii). Tadpoles were collected from three study streams with and three without crayfish, in the Santa Monica Mountains of Southern California. We analyzed tadpole morphology and tested anti-predator behavior and survival in the laboratory. Tadpoles from streams with crayfish had shallower, narrower tails than tadpoles from streams without crayfish. Tadpoles from streams with and without crayfish were less active after exposure to crayfish chemical cues. The divergent morphology of naive and exposed tadpoles is consistent with tadpoles exhibiting a plastic response to crayfish or undergoing selection from crayfish predation. In laboratory predation experiments, we found no difference in survival between tadpoles from streams with and without crayfish but tadpoles that survived predation had deeper tail muscles than those that were killed or injured. Our results suggest that deeper tails are advantageous in the presence of crayfish, yet tadpoles from crayfish streams had shallower tails than those from crayfish-free streams. Shallower tails may have an alternative unmeasured advantage or there may be a physiological constraint to developing deeper tails in the wild. These results highlight the ability of a native frog to respond to an invasive predatory crayfish, potentially allowing for coexistence.     

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 role of introduced mosquitofish (Gambusia holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from original habitats in south-eastern Australia

The introduction of fish has decimated many amphibian populations through increased predation, primarily on their larvae. Some amphibian species now occupy marginal habitats as a response to the presence of introduced fish predators. Such habitats may include ephemeral water bodies where fish do not usually occur, although breeding in these suboptimal environments may incur some cost to a species if its larvae are not adapted to develop under these conditions. We investigated this scenario of amphibian decline using the endangered green and golden bell frog (Litoria aurea) and the introduced mosquitofish (Gambusia holbrooki) in a factorial experiment to determine the responses of tadpoles to declining water levels and the introduced predator. Tadpoles metamorphosed asynchronously but did not accelerate development in declining water or when housed with mosquitofish. Mass at metamorphosis was 30% less in declining water. Mass increased with time to metamorphosis in constant water-level treatments, but decreased in declining water. Tadpoles did not respond to mosquitofish and were therefore assumed to be naive to this predator. These results suggest that ephemeral habitats may be suboptimal for breeding, and tadpoles appear better suited to develop in permanent water bodies free of introduced fish. Intra-clutch variability in larval development (i.e. bet-hedging) may allow L. aurea to cope with unpredictable pond duration, whereby even permanent water bodies may occasionally dry out. The responses observed in L. aurea suggest that introduced fish may have reduced the suitability of permanent water bodies as breeding sites for other pond-breeding amphibian species. The use of less favourable ephemeral habitats as breeding sites may be responsible for some of the declines reported in amphibians since the 1970s.