Threat-Sensitive Responses to Predator Attacks in a Damselfly

The threat sensitivity hypothesis predicts that prey species assess and adjust their behavior flexibly in accordance with the magnitude of the threat imposed by a predator. We tested this hypothesis with regard to escape behavior and thanatosis (feigning of death to escape predation) in larvae of the damselfly Ischnura elegans. We manipulated the perceived predation threat of the larvae by changing three factors: lamellae autotomy (an escape strategy where animals sacrifice a body part when grasped by a predator; lamellae present or absent), kairomone type (odors released by predators; control, dragonfly kairomones or fish kairomones), and population of origin (fishpond or fishless pond). We demonstrated that thanatosis increased survival both when confronted with dragonfly and fish predators. We could show, for the first time, costs of past autotomy to be predator‐dependent: larvae without lamellae suffered higher predation mortality but only in the presence of a dragonfly predator and not in the presence of a fish predator. This is in accordance with the observed reduced escape speed of larvae after autotomy, which may affect escape probability toward dragonfly predators but not to the very fast fish predators. Unexpectedly, kairomone type did not affect the escape response of the larvae. In accordance with the threat sensitivity hypothesis, after an unsuccessful attack, larvae without lamellae had a higher frequency to enter thanatosis than larvae with lamellae and larvae from the fishpond showed longer thanatosis durations than larvae from the fishless pond. Consistent with the hypothesis, the reaction of the larvae to a simulated attack depended jointly on lamellae status and population. In fishless ponds, larvae with lamellae swam away more frequently than larvae without lamellae; in fishponds both groups almost never swam away and relied mostly upon immobility. Given the obvious benefits of adaptively varying escape responses we hypothesize this threat sensitivity to be widespread. Moreover, we argue that former inconsistencies between studies with regard to escape behavior may have been partly because of such adaptive variation.     

Keystone nonconsumptive effects within a diverse predator community

The number of prey killed by diverse predator communities is determined by complementarity and interference among predators, and by traits of particular predator species. However, it is less clear how predators' nonconsumptive effects (NCEs) scale with increasing predator biodiversity. We examined NCEs exerted on Culex mosquitoes by a diverse community of aquatic predators. In the field, mosquito larvae co‐occurred with differing densities and species compositions of mesopredator insects; top predator dragonfly naiads were present in roughly half of surveyed water bodies. We reproduced these predator community features in artificial ponds, exposing mosquito larvae to predator cues and measuring resulting effects on mosquito traits throughout development. Nonconsumptive effects of various combinations of mesopredator species reduced the survival of mosquito larvae to pupation, and reduced the size and longevity of adult mosquitoes that later emerged from the water. Intriguingly, adding single dragonfly naiads to ponds restored survivorship of larval mosquitoes to levels seen in the absence of predators, and further decreased adult mosquito longevity compared with mosquitoes emerging from mesopredator treatments. Behavioral observations revealed that mosquito larvae regularly deployed “diving” escape behavior in the presence of the mesopredators, but not when a dragonfly naiad was also present. This suggests that dragonflies may have relaxed NCEs of the mesopredators by causing mosquitoes to abandon energetically costly diving. Our study demonstrates that adding one individual of a functionally unique species can substantially alter community‐wide NCEs of predators on prey. For pathogen vectors like mosquitoes, this could in turn influence disease dynamics.     

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.     

Predator-induced morphological plasticity across local populations of a freshwater snail

The expression of anti-predator adaptations may vary on a spatial scale, favouring traits that are advantageous in a given predation regime. Besides, evolution of different developmental strategies depends to a large extent on the grain of the environment and may result in locally canalized adaptations or, alternatively, the evolution of phenotypic plasticity as different predation regimes may vary across habitats. We investigated the potential for predator-driven variability in shell morphology in a freshwater snail, Radix balthica, and whether found differences were a specialized ecotype adaptation or a result of phenotypic plasticity. Shell shape was quantified in snails from geographically separated pond populations with and without molluscivorous fish. Subsequently, in a common garden experiment we investigated reaction norms of snails from populations' with/without fish when exposed to chemical cues from tench (Tinca tinca), a molluscivorous fish. We found that snails from fish-free ponds had a narrow shell with a well developed spire, whereas snails that coexisted with fish had more rotund shells with a low spire, a shell morphology known to increase survival rate from shell-crushing predators. The common garden experiment mirrored the results from the field survey and showed that snails had similar reaction norms in response to chemical predator cues, i.e. the expression of shell shape was independent of population origin. Finally, we found significant differences for the trait means among populations, within each pond category (fish/fish free), suggesting a genetic component in the determination of shell morphology that has evolved independently across ponds.     

Nature of Predation Risk Cues in Container Systems: Mosquito Responses to Solid Residues From Predation

In aquatic systems, prey animals associate predation risk with cues that originate either from the predator or from injured conspecifics. Sources and benefits of these cues have received considerable attention in river, lake, and pond ecosystems but are less well understood in small container ecosystems that can hold less than a liter of water. Mosquitoes Aedes triseriatus (Say) and Aedes albopictus (Skuse) encounter predatory Corethrella appendiculata (Grabham) and Toxorhynchites rutilus (Coquillett) in small containers and show antipredatory behavioral responses. We investigated the sources of the predation cues to which these prey larvae respond. We tested whether Ae. albopictus larvae show behavioral responses to cues emanating from the predator or from damage to prey caused by the act of predation. We also tested whether Ae. triseriatus respond to cues present in fluid or solid residues from predator activity. Ae. albopictus showed behavioral modifications only in response to waterborne cues from a feeding predator and not to cues from a starving predator, indicating that Ae. albopictus respond to cues created by the act of predation, which could include substances derived from damaged prey or substances in predator feces. Ae. triseriatus showed behavioral responses to solid residues from predation but not to fluid without those solids, indicating that the cues to which they respond originate in predator feces or uneaten prey body parts. Our results suggest that cues in this system may be primarily chemicals that are detected upon contact with solid residues that are products of the feeding processes of these predators.     

Rapid habituation by mosquito larvae to predator kairomones

Larvae of some species of mosquitoes have been shown to respond to water‐borne kairomones from predators by reducing bottom‐feeding and replacing it with surface filter‐feeding, which uses less movement and is thus less likely to attract a predator. However, if no predator attack takes place, then it would be more efficient to use a risk allocation strategy of habituating their response depending on the predator and the overall risk. The larvae of Culiseta longiareolata Macquart live in temporary rain‐filled pools, where they are exposed to a high level of predation. Within one hour, they responded to kairomones from dragonfly or damselfly nymphs, or to the fish Aphanius, by significantly reducing bottom‐feeding activity. Continued exposure to the predator kairomones resulted in habituation of their response to damselflies, a slower habituation to fish, but no habituation to dragonflies even after 30 h. In contrast, the larvae of Culex quinquefasciatus Say normally live in highly polluted and thus anaerobic water, where the predation risk will be much lower. They also showed a significant reduction in bottom‐feeding after 1 h of exposure to predator kairomones but had completely habituated this response within 6 h of continuous exposure. Some species of mosquito larvae can thus show a very rapid habituation to predator kairomones, while others only habituate slowly depending on the predator and overall predation risk.     

Predator faunas past and present: quantifying the influence of waterborne cues in divergent ecotypes of the isopod Asellus aquaticus

Waterborne chemical cues are an important source of information for many aquatic organisms, in particular when assessing the current risk of predation. The ability to use chemical cues to detect and respond to potential predators before an actual encounter can improve prey chances of survival. We investigated predator recognition and the impact of chemical cues on predator avoidance in the freshwater isopod Asellus aquaticus. This isopod has recently colonised a novel habitat and diverged into two distinct ecotypes, which encounter different predator communities. Using laboratory-based choice experiments, we have quantified behavioural responses to chemical cues from predators typical of the two predator communities (larval dragonflies in the ancestral habitat, perch in the newly colonised habitat) in wild-caught and lab-reared Asellus of the two ecotypes. Individuals with prior experience of predators showed strong predator avoidance to cues from both predator types. Both ecotypes showed similar antipredator responses, but sexes differed in terms of threat-sensitive responses with males avoiding areas containing predator cues to a larger extent than females. Overall, chemical cues from fish elicited stronger predator avoidance than cues from larval dragonflies. Our results indicate that in these isopods, prior exposure to predators is needed to develop antipredator behaviour based on waterborne cues. Furthermore, the results emphasise the need to analyse predator avoidance in relation to waterborne cues in a sex-specific context, because of potential differences between males and females in terms of vulnerability and life history strategies.     

Predator exposure alters stress physiology in guppies across timescales

In vertebrates, glucocorticoids mediate a wide-range of responses to stressors. For this reason, they are implicated in adaptation to changes in predation pressure. Trinidadian guppies (Poecilia reticulata) from high-predation environments have repeatedly and independently colonized and adapted to low-predation environments, resulting in parallel changes in life history, morphology, and behavior. We validated methods for non-invasive waterborne hormone sample collection in this species, and used this technique to examine genetic and environmental effects of predation on basal glucocorticoid (cortisol) levels. To examine genetic differences, we compared waterborne cortisol levels in high- and low-predation fish from two distinct population pairs. We found that fish from high-predation localities had lower cortisol levels than their low-predation counterparts. To isolate environmental influences, we compared waterborne cortisol levels in genetically similar fish reared with and without exposure to predator chemical cues. We found that fish reared with predator chemical cues had lower waterborne cortisol levels than those reared without. Comparisons of waterborne and whole-body cortisol levels demonstrated that populations differed in overall cortisol levels in the body, whereas rearing conditions altered the release of cortisol from the body into the water. Thus, evolutionary history with predators and lifetime exposure to predator cues were both associated with lower cortisol release, but depended on distinct physiological mechanisms.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

The influence of predator regime on the behaviour and mortality of a freshwater amphipod, <Emphasis Type="Italic">Gammarus pulex</Emphasis>

In species with restricted dispersal, traits may become genetically fixed leading to local adaptations. Therefore, predator avoidance in a prey species may differ between populations experiencing different predator regimes, but also between sexes within a population due to different vulnerability to predators. In this study we used male and female Gammarus pulex from two different predator regimes: fishless ponds, where invertebrates are the dominant predators and ponds with predatory fish. In the laboratory we examined refuge use, mortality, leaf decomposition rate and pair-formation in G. pulex when exposed to predator cues from either invertebrate predators or fish. Individuals from fish ponds spent more time in refuge and had a higher mortality than those from fishless ponds independent of predator cues. There was no effect of pond predator regime or predator cues on leaf decomposition rates. Further, fewer individuals formed pairs in G. pulex from fish ponds than from fishless ponds. Male G. pulex had a higher mortality and a higher decomposition rate than females independent of predator cues. However, there was no difference in refuge use between sexes. Our study shows that there are general differences in behaviour traits, both between predator regimes and sexes in G. pulex.     

The Rate of Degradation of Chemical Cues Indicating Predation Risk: An Experiment and Review

Many prey taxa use kairomones or alarm pheromones to assess the risk of predation in aquatic environments, and the rate at which these cues attenuate determines how precisely they indicate the local density of predators. We estimated the rate of degradation of chemical cues generated by Aeshna dragonfly larvae feeding on Rana temporaria tadpoles. The half‐life of the cue was 35 h and was not influenced by whether it was aged in pond water or tap water or whether other tadpoles were present in the container in which cue‐aging occurred. A review of other published estimates of predator cue half‐life revealed values of 0.2–126 h, and variation among studies was unrelated to the type of aging water, the venue in which water was aged or prey behavior observed (laboratory, field), or the type of behavior that was recorded. We conclude that factors affecting the persistence of predator cues remain uncertain in spite of their importance for understanding the evolution of induced defenses.     

Habitat-Specific variation in eyespot size of a benthic cladoceran

Summary Pigmented eyespot size of the benthic cladoceran Simocephalus exspinosus was measured in individuals sampled from four freshwater ponds that differed in the extent of visually-oriented predation. In ponds with such predation (from fish, salamander larvae, and dragonfly nymphs), eyespot size was found to be significantly smaller, relative to body size, than in a pond without visually-oriented predation. Reduction in pigmented eyespot size may represent an adaptation to reduce vulnerability to predation.     

Past and Present Risk: Exposure to Predator Chemical Cues Before and after Metamorphosis Influences Juvenile Wood Frog Behavior

Animals are exposed to different predators over their lifespan. This raises the question of whether exposure to predation risk in an early life stage affects the response to predators in subsequent life stages. In this study, we used wood frogs (Rana sylvatica) to test whether exposure to cues indicating predation risk from dragonfly larvae during the wood frog larval stage affected post‐metamorphic activity level and avoidance of garter snake chemical cues. Dragonfly larvae prey upon wood frogs only during the larval stage, whereas garter snakes prey upon wood frogs during both the larval stage and the post‐metamorphic stage. Exposure to predation risk from dragonflies during the larval stage caused post‐metamorphic wood frog juveniles to have greater terrestrial activity than juvenile wood frogs that were not exposed to larval‐stage predation risk from dragonflies. However, exposure to predation risk as larvae did not affect juvenile wood frog responses to chemical cues from garter snakes. Wood frogs exposed as larvae to predation risk from dragonfly larvae avoided garter snake chemical cues to the same extent as wood frog larvae not exposed to predation risk from dragonfly larvae. Our results demonstrate that while some general behaviors exhibit carry‐over effects from earlier life stages, behavioral responses to predators may remain independent of conditions experienced in earlier life stages.     

Larval Ischnura verticalis (Odonata: Coenagrionidae) Respond to Visual Cues of Predator Presence

Larvae of some species of damselflies respond to chemical cues of fish predators but, while larvae of many species are thought to detect prey through vision, there is little evidence that larvae respond to visual cues of predator presence. This laboratory study indicated larval Ischnura verticalis behaviours are affected by visual cues and, to a much lesser extent, chemical cues of fish; there was no significant interaction between the effects of visual and chemical cues. Responses to chemical cues of fish did not depend on whether fish were fed I. verticalis larvae versus commercial fish food. Larvae were more active in the spring than the fall when they were likely in diapause. Results suggest larvae can use vision to detect large, active predators but can also detect predators through olfaction when visual cues are unreliable.     

Are behavioural responses to predation cues linked across life cycle stages?

1. Prey organisms can perceive cues to predation hazard and adopt low‐risk behaviours to increase survival. Animals with complex life cycles, such as insects, can exhibit such anti‐predatory behaviours in multiple life stages. 2. Cues to predation risk may induce ovipositing females to choose habitats with low predation risk. Cues to predation risk may also induce larvae to adopt facultative behaviours that reduce risk of predation. 3. One hypothesis postulates that anti‐predation behaviours across adult and larval stages may be negatively associated because selection for effective anti‐predator behaviour in one stage leads to reduced selection for avoidance of predators in other stages. An alternative hypothesis suggests that selection by predation favours multi‐component defences, with both avoidance of oviposition and facultative adoption of low‐risk behaviours by larvae. 4. Laboratory and field experiments were used to determine whether defensive responses of adult and larval mosquitoes are positively or negatively associated. The study tested effects of waterborne cues from predatory Toxorhynchites theobaldi on oviposition choices and larval behaviours of three of its common prey: Culex mollis, Limatus durhamii and Aedes albopictus. 5. Culex mollis shows strong anti‐predator responses in both life stages, consistent with the hypothesis of a multi‐component behavioural defence. The other two species showed no detectable responses to waterborne predator cues in either adult or larval stages. Larvae of these unresponsive species were significantly more vulnerable to this predator than was C. mollis. 6. For these mosquitoes, species appear either to have been selected for multi‐component defences against predation or to act in ways that could be called predator‐naïve.     

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

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.     

Non-interactive multiple predator effects on tadpole survival

Interactions among and within three species of predators were estimated in terms of their effects on prey survival using short-term predation experiments. The prey were tadpoles (Rana temporaria), and the predators were dragonfly larvae (Anax imperator), newts (Triturus alpestris), and backswimmers (Notonecta glauca). Mortality rate per predator imposed by Triturus and Notonecta did not decline with predator density, whereas the predation rate of Anax was strongly reduced when the number of predator individuals increased. Impacts of all three predators were not altered by the presence of other species in pairwise combinations. This system is therefore characterized by interference between individual dragonflies but relatively independent effects of predator species. These results were largely predictable based on the natural history of the predators and are encouraging for attempts to model communities as assemblages of interacting species.     

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.     

Ontogenetic Shift in Efficacy of Antipredator Mechanisms in a Top Aquatic Predator,Anax junius (Odonata: Aeshnidae)

The ability of prey to escape predation often lies in the occurrence and efficacy of their predator avoidance and antipredator behaviors, which are often coupled with specialized morphology. How the use and efficacy of these behaviors change throughout ontogeny may be indicative of the vulnerability and ecological roles these animals experience throughout their lives. We examined the antipredator behavior of a large dragonfly nymph, Anax junius, from a historically fishless pond where these animals have traditionally been classified as top predators. These dragonfly nymphs displayed a series of distinct aggressive antipredator behaviors when grasped that involved stabbing with lateral and posterior spines and seizing with labial hooks. Larger (older) nymphs displayed these aggressive behaviors significantly more than smaller (younger) animals in simulated predation trials. During encounters with live larval salamander predators (Ambystoma tigrinum), all large nymphs, but only 12.5% of small nymphs successfully escaped predation attempts by the amphibians through the use of antipredator behavior. Large nymphs were also significantly more active than smaller nymphs in the presence of salamander larvae. Despite often being considered top predators in fishless ponds, our study demonstrates that their true role is more complex, depending on ontogeny and body size, and that effective antipredator behavior is likely necessary for survival in these systems.