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.     

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     

Effects of food-deprivation on migratory restlessness and diurnal activity in the garden warbler Sylvia borin

Summary The effects of tadpole body size, tadpole sibship, and fish body size on predation of gray treefrog tadpoles, Hyla chrysoscelis, were studied in laboratory and artificial pond experiments. Tadpole body size had a significantly positive effect on the survival of tadpoles in all experiments. The relationship between tadpole biomass eaten and biomass available suggested that fish were not satiated when consuming the largest tadpoles. Large tadpoles were probably better able to evade predators. A difference in survival among full sib families of tadpoles was only present in one family, suggesting that genetic differences in predator avoidance behavior or palatability were probably secondarily important to body size per se. Fish body size had a significantly negative effect on the survival of tadpoles. Larger fish consumed a larger number and proportion of tadpoles as well as greater biomass. These results indicate that environmental factors affecting the growth rate of tadpoles cand dramatically alter their vulnerability to gape-limited predators.     

Effects of size and size structure on predation and inter-cohort competition in red-eyed treefrog tadpoles

Individual and relative body size are key determinants of ecological performance, shaping the strength and types of interactions within and among species. Size-dependent performance is particularly important for iteroparous species with overlapping cohorts, determining the ability of new cohorts to invade habitats with older, larger conspecifics. We conducted two mesocosm experiments to examine the role of size and size structure in shaping growth and survival in tadpoles of the red-eyed treefrog (Agalychnis callidryas), a tropical species with a prolonged breeding season. First, we used a response surface design to quantify the competitive effect and response of two tadpole size classes across three competitive environments. Large tadpoles were superior per capita effect competitors, increasing the size difference between cohorts through time at high resource availability. Hatchlings were better per biomass response competitors, and maintained the size difference between cohorts when resource availability was low. However, in contrast to previous studies, small tadpoles never closed the size gap with large tadpoles. Second, we examine the relationship between body size, size structure, and predation by dragonfly nymphs (Anax amazili) on tadpole survival and growth. Hatchlings were more vulnerable to predation; predator and large competitor presence interacted to reduce hatchling growth. Again, the size gap between cohorts increased over time, but increased marginally more with predators present. These findings have implications for understanding how variation in resources and predation over the breeding season will shape population size structure through time and the ability of new cohorts to invade habitats with older conspecifics.     

Effects of predator interactions, prey palatability and habitat structure on survival of natterjack toad Bufo calamita larvae in replicated semi-natural ponds

The significance of predation and aquatic habitat structures to the survivorship of natterjack toad Bufo calamita larvae was investigated by manipulating predator numbers and pond characteristics in a series of replicated semi-natural pools over three consecutive years Two species of fish (common carp Cyprinus carpio and perch Perca fluviatilis) increased the survival of small tadpoles severalfold by selectively consuming predatory invertebrates, but a third species of fish (rudd Scardinius erythrophthalmus) devoured tadpoles and invertebrates indiscriminately Survival of larger tadpoles later in larval development was less affected by the reduction of invertebrate predation pressure from carp and perch, probably because abiotic factors (pond desiccation and anoxia) were stronger agents of tadpole mortality In ponds of low pH (ca 4 5) there was greatly increased spawn mortality and reduced tadpole growth rates but no significant change in tadpole predation compared with circumneutral controls Neutralisation of acid ponds to pH 7 by addition of Ca(OH)₂ restored spawn viability and tadpole growth rates to control levels without affecting predation level Addition of organic nutrients stimulated tadpole growth rates significantly m ohgotrophic ponds but not sufficiently to improve survival of small larvae in the face of predation Extensive growths of macrophytes increased predator numbers up to more than twofold but effects on tadpole mortality rates differed between experiments Replacement of natural substrates by concrete basins substantially increased tadpole survival throughout development, probably because both predation by invertebrates and abiotic mortality factors were ameliorated Predation was a strong force early in natterjack tadpole development irrespective of chemical and biological conditions within ponds, but became much less important compared with abiotic factors as an agent of mortality at later tunes     

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.     

Interactions of bullfrog tadpole predators and an insecticide: predation release and facilitation

The effect of a contaminant on a community may not be easily predicted, given that complex changes in food resources and predator-prey dynamics may result. The objectives of our study were to determine the interactive effects of the insecticide carbaryl and predators on body size, development, survival, and activity of tadpoles of the bullfrog (Rana catesbeiana). We conducted the study in cattle tank mesocosm ponds exposed to 0, 3.5, or 7.0 mg/l carbaryl, and no predators or two red-spotted newts (Notophthalmus viridescens), bluegill sunfish (Lepomis macrochirus), or crayfish (Orconectes sp.). Carbaryl negatively affected predator survival by eliminating crayfish from all ponds, and by eliminating bluegill sunfish from ponds exposed to the highest concentration of carbaryl; carbaryl exposure did not effect survival of red-spotted newts. Because crayfish were eliminated by carbaryl, bullfrogs were released from predation and survival was near that of predator controls at low concentrations of carbaryl exposure. High concentrations of carbaryl reduced tadpole survival regardless of whether predators survived carbaryl exposure or not. Presence of crayfish and newts reduced tadpole survival, while bluegill sunfish appeared to facilitate bullfrog tadpole survival. Presence of carbaryl stimulated bullfrog tadpole mass and development. Our study demonstrates that the presence of a contaminant stress can alter community regulation by releasing prey from predators that are vulnerable to contaminants in some exposure scenarios.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Antagonistic indirect interactions between large and small conspecific prey via a heterospecific predator

Intrapopulation size variation strongly influences ecological interactions because individuals belonging to different size groups have distinct functions. Most demonstrations of the impacts of size variation in trophic systems have focused on size variation in predator species, and the consequences of size variation in prey species are less well understood. We investigated how prey size structure shapes intra‐ and interspecific interactions in experiments with a gape‐limited predator (larvae of the salamander Hynobius retardatus) and its heterospecific prey (frog tadpoles, Rana pirica). We found that large and small tadpole size groups each increased mortality in the other group by intensifying salamander predation; this type of indirect interactions is called apparent competition. The antagonistic impacts on the prey size groups were caused by different size‐specific mechanisms. By consuming small tadpoles, the salamanders grew large enough to consume large tadpoles. The activity of large tadpoles, by increasing the activity of the small tadpoles, may increase the number of encounters with the predator and thus small tadpole mortality. These results suggest that the magnitude of a predator's ecological role, such as whether a top–down trophic cascade is initiated, depends on size variation in its heterospecific 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.     

Effects of size structure and habitat complexity on predator–prey interactions

1. A predator's ability to suppress its prey depends on the level of interference among predators. While interference typically decreases with increasing habitat complexity, it often increases with increasing size differences among individuals. However, little is known about how variation in intrinsic factors such as population size structure alters predator–prey interactions and how this intrinsic variation interacts with extrinsic variation. 2. By experimentally varying the level of vegetation cover and the size structure of the predatory damselfly Ischnura posita Hagen, we examined the individual and interactive effects of variation in habitat complexity and predator size structure on prey mortality. 3. Copepod prey survival linearly increased as the I. posita size ratio decreased and differed by up to 31% among different predator size structures. Size classes had an additive effect on prey survival, most likely because intraspecific aggression appeared size‐independent and size classes differed in microhabitat preference: large I. posita spent 14% more time foraging on the floor than small larvae and spent more time in the vegetation with increasing habitat complexity. Despite this difference in microhabitat use among size classes, habitat structure did not influence predation rates or interference among size classes. 4. In general, results suggest that seasonal and spatial variation in the size structure of populations could drive some of the discrepancies in predator‐mediated prey suppression observed in nature, and this variation could exceed the effects of variation in habitat structure.     

The Effect of Refuge on Dermestes ater (Coleoptera: Dermestidae) Predation on Musca domestica (Diptera: Muscidae): Refuge for Prey or the Predator?

It is believed that habitat heterogeneity can change the extent of predator-prey interactions. Therefore, in this study we examined the effect of habitat heterogeneity (characterized here as an addition of refuge) on D. ater predation on M. domestica. Predation of D. ater on M. domestica larvae was carried out in experimental habitats with and without refuge, and examined at different prey densities. The number of prey eaten by beetles over 24 h of predator-prey interaction was recorded, and we investigated the strength of interaction between prey and predator in both experimental habitats by determining predator functional response. The mean number of prey eaten by beetles in the presence of refuge was significantly higher than in the absence of refuge. Females had greater weight gains than males. Logistic regression analyses revealed the type II functional response for both experimental habitats, even though data did not fit well into the random predator model. Results suggest that the addition of refuge in fact enhanced predation, as prey consumption increased in the presence of refuge. Predators kept in the presence of refuge also consumed more prey at high prey densities. Thus, we concluded that the addition of refuge was an important component mediating D. ater-M. domestica population interactions. Refuge actually acted as a refuge for predators from prey, since prey behaviors detrimental to predators were reduced in this case.     

Differences in predator composition alter the direction of structure‐mediated predation risk in macrophyte communities

Structural complexity strongly influences the outcome of predator–prey interactions in benthic marine communities affecting both prey concealment and predator hunting efficacy. How habitat structure interacts with species‐specific differences in predatory style and antipredatory strategies may therefore be critical in determining higher trophic functions. We examined the role of structural complexity in mediating predator–prey interactions across several macrophyte habitats along a gradient of structural complexity in three different bioregions: western Mediterranean Sea (WMS), eastern Indian Ocean (EIO) and northern Gulf of Mexico (NGM). Using sea urchins as model prey, we measured survival rates of small (juveniles) and medium (young adults) size classes in different habitat zones: within the macrophyte habitat, along the edge and in bare sandy spaces. At each site we also measured structural variables and predator abundance. Generalised linear models identified biomass and predatory fish abundance as the main determinants of predation intensity but the efficiency of predation was also influenced by urchin size class. Interestingly though, the direction of structure‐mediated effects on predation risk was markedly different between habitats and bioregions. In WMS and NGM, where predation by roving fish was relatively high, structure served as a critical prey refuge, particularly for juvenile urchins. In contrast, in EIO, where roving fish predation was low, predation was generally higher inside structurally complex environments where sea stars were responsible for much of the predation. Larger prey were generally less affected by predation in all habitats, probably due to the absence of large predators. Overall, our results indicate that, while the structural complexity of habitats is critical in mediating predator–prey interactions, the direction of this mediation is strongly influenced by differences in predator composition. Whether the regional pool of predators is dominated by visual roving species or chemotactic benthic predators may determine if structure dampens or enhances the influence of top–down control in marine macrophyte communities.     

Effects of turbidity and risk of predation on habitat selection decisions by Fathead Minnow (<Emphasis Type="Italic">Pimephales promelas</Emphasis>)

Within aquatic ecosystems, turbid environments will have a significant impact upon predator-prey interactions if both the predator and their prey rely upon vision as their primary sense. Increasing water turbidity will reduce the probability of being detected by a predator, and once detected should provide prey with cover that is close and ubiquitous. We tested the extent that these features of a turbid environment will have in affecting the impact of predation risk on habitat quality using Fathead Minnow (Pimephales promelas) as the prey, and Yellow Perch (Perca flavescens) and Black Bullhead (Ameiurus melas) as visual and non-visual predators, respectively. Our experiments demonstrated a strong preference for turbid habitats in the absence of a predator. When a predator was present in a turbid habitat, the minnows reduced their use of this location but still preferred it to a clear habitat with no predator. These data suggest turbidity confers a benefit to feeding Fathead Minnow that more than compensates for the cost of predation risk.     

Spatial variability in prey phenology determines predator movement patterns and prey survival

Species have phenological variation among local habitats that are located at relatively small spatial scales. However, less studies have tested how this spatial variability in phenology can mediate intra-/inter-specific interactions. When predators track phenological variation of prey among local habitats, survival of prey within a local habitat strongly influenced by phenological synchrony with their conspecifics in adjacent habitats. Theory predicts that phenological synchrony among local habitats increases prey survival in local habitat within spatially structured environments because the predators have to make a habitat choice for foraging. Consequently, total survival of prey at regional scale should be higher. By using a spatially explicit field experiment, we tested above hypothesis using a prey–predator interaction between tadpole (Rhacophorus arboreus) and newt (Cynops pyrrhogaster). We established enclosures (≈regional scale) consisting of two tanks (≈local habitat scale) with different degree of prey phenological synchrony. We found that phenological synchrony of prey between tanks within each enclosure decreased the mean residence time of the predator in each tank, which resulted in higher survival of prey at a local habitat scale, supporting the theoretical prediction. Furthermore, individual-level variation in predator residence time explained the between-tank variation in prey survival in enclosures with phenological synchrony, implying that movement patterns of the predator can mediate variation in local population dynamics of their prey. However, total survival at each enclosure was not higher under phenological synchrony. These results suggest the importance of relative timing of prey phenology, not absolute timing, among local habitats in determining prey–predator interactions.     

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.     

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.     

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.     

Predation risk and habitat complexity modify intermediate predator feeding rates and energetic efficiencies in a tri‐trophic system

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Trait-mediated interactions: influence of prey size, density and experience

1. The role of non-consumptive predator effects in structuring ecological communities has become an important area of study for ecologists. Numerous studies have shown that adaptive changes in prey in response to a predator can improve survival in subsequent encounters with that predator. 2. Prey-mediated changes in the shapes of predators' functional response surfaces determine the qualitative predictions of theoretical models. However, few studies have quantified the effects of adaptive prey responses on the shape of predator functional responses. 3. This study explores how prey density, size and previous predator experience interact to change the functional response curves of different-sized predators. 4. We use a response surface design to determine how previous exposure to small or large odonate predators affected the short-term survival of squirrel tree frog (Hyla squirella) tadpoles across a range of sizes and densities (i.e. the shape of odonate functional response curves). 5. Predator-induced tadpoles in a given size class did not differ in shape, although induction changed tadpole behaviour significantly. Induced tadpoles survived better in lethal encounters with either predator than did similar-sized predator-naive tadpoles. 6. Induction by either predator resulted in increased survival with both predators at a given size. However, different mechanisms led to increased survival for induced tadpoles. Attack rate for the small predators, whereas handling time increased for the large predators.