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.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.     

Constrained plasticity in switching across life stages: pre- and post-switch predators elicit early hatching

The timing of many life history events shows phenotypic plasticity in response to the risk of predation. Theory predicts that increased risk of mortality in an early stage should select for switching earlier, while a higher risk after the transition should select for switching later. Here we examined the effects of stage-specific predation risk on the timing of hatching of Rana temporaria. Embryos were exposed to chemical cues from either an egg predator (Haemopis sanguisuda) or a tadpole predator (Aeshna cyanea) to evaluate three specific hypotheses: (1) a fixed intermediate response, (2) a ‘fixed predator’ response (i.e., either anticipation or delay), and (3) a specific predator response (both anticipation and delay). Rana temporaria embryos did not discern between pre- and post-hatching specific predators, and they hatched prematurely regardless predator type. These results suggest that R. temporaria embryos respond to predation risk in a fixed way by hatching early, and that they use cues stemming from injured conspecifics, which provides a simple, conservative mechanism of risk assessment. In conclusion, our data are not anticipated by the theoretical consideration that organisms should spend less time in more dangerous environments, but they confirm an invariable adjustment of hatching time in response to an inscrutable predation risk (response to a fixed-predator) in connection with a consistent mechanism mediating the perception of predation risk.     

Egg‐laying environment modulates offspring responses to predation risk in an amphibian

Predator‐induced plasticity has been in the focus of evolutionary ecological research in the last decades, but the consequences of temporal variation in the presence of cues predicting offspring environment have remained controversial. This is partly due to the fact that the role of early environmental effects has scarcely been scrutinized in this context while also controlling for potential maternal effects. In this study, we investigated how past environmental conditions, that is different combinations of risky or safe adult (prenatal) and oviposition (early post‐natal) environments, affected offspring's plastic responses in hatching time and locomotor activity to predation risk during development in the smooth newt (Lissotriton vulgaris). We found that females did not adjust their reproductive investment to the perceived level of risk in the adult environment, and this prenatal environment had generally negligible effect on offspring phenotype. However, when predator cues were absent during oviposition, larvae raised in the presence of predator cues delayed their hatching and exhibited a decreased activity compared to control larvae developing without predator cues, which responses are advantageous when predators pose a threat to hatched larvae. In the presence of predator cues during oviposition, the difference in hatching time persisted, but the difference in general locomotor activity disappeared between risk‐exposed and control larvae. Our findings provide clear experimental evidence that fine‐scale temporal variation in a predictive cue during and after egg‐laying interactively affects offspring phenotype, and highlight the importance of the early post‐natal environment, which may exert a substantial influence on progeny's phenotype also under natural conditions.     

Hatching responses of subsocial spitting spiders to predation risk

The carrying of eggs often renders parents vulnerable to predators due to increased conspicuousness or decreased mobility. Nonetheless, egg-carrying parents can escape from the predators to which they are vulnerable. Previous studies have demonstrated heavy predation by spider-eating jumping spiders (Portia labiata) on egg-carrying spitting spider (Scytodes pallida) females, but little predation on eggless females. If the timing of hatching is phenotypically plastic, then both S. pallida females and their eggs could reduce the risk of predation by hatching early. Hence, this study examines the hatching responses of S. pallida to chemical cues from P. labiata, both in the laboratory and in the field, and addresses the following questions. (i) Do cues from predatory P. labiata influence the hatching traits of S. pallida? (ii) Are the olfactory cues from predators sufficient for predator detection by S. pallida ? (iii) Are hatching responses to predatory P. labiata controlled by egg-carrying S. pallida females, or directly by their embryos? The study provides evidence of hatching as a life-history switch point, which shows an adaptive plasticity in response to predation risk in egg-carrying S. pallida. Egg-carrying S. pallida females, but not unattended eggs, adjust egg-hatching time (the interval between oviposition and hatching) in response to the threat of predation on both the female and her eggs by P. labiata. In the presence of P. labiata, eggs that are carried by females hatch sooner; the hatchlings of these eggs are therefore smaller than hatchlings born in the absence of P. labiata. Chemical cues that are released from the draglines of P. labiata are sufficient to elicit changes in the egg-hatching traits of S. pallida. Hatching early in response to this predator may benefit both females and their offspring. To my knowledge, this is the first direct experimental study to demonstrate predator-induced hatching plasticity in spiders and, in particular, in animals with parental care.     

Effects of perceived predation risk and social environment on the development of three‐spined stickleback (Gasterosteus aculeatus) morphology

Phenotypically plastic changes in response to variation in perceived predation risk are widespread, but little is known about if and how social environment modulates induced responses to predation risk. We investigated the influence of perceived predation risk (i.e. chemical cues from a predator) and social environment (i.e. one, two or 20 individuals reared together) on three‐spined stickleback (Gasterosteus aculeatus) morphology in a factorial common garden experiment. We found that exposure to chemical cues from potential predators did not influence growth or body condition or induce more robust morphological defences (i.e. lateral plate numbers and dorsal spine lengths). However, sticklebacks exposed to predator cues developed longer caudal peduncles and larger eyes as compared with fish from the control treatment. As these responses may improve sticklebacks’ ability to avoid piscine predation, they might be adaptive. Social environment/density also influenced expression of some traits, but these effects were independent of predation‐risk treatment effects. In general, these results suggest that apart from the classic morphological defence structures, which appear mostly constitutive, three‐spined sticklebacks are capable of expressing potentially adaptive morphological responses to chemical cues from potential predators.     

Effects of fish chemical cues on tadpole survival

The indirect effects of goldfish chemical cues on tadpole survival and predation by other predators (e.g. dragonfly nymph and crayfish) were tested in a field experiment. Fish chemical cues were found to affect tadpole survival when dragonfly nymphs were present. In contrast, this indirect effect was not detected in the presence of crayfish. The results from the present study found that predators, even without predation, can affect the predatory efficiency of other predators, and that the degree of such an indirect effect may differ among the foraging strategies of predators.     

Does acoustically simulated predation risk affect settlement and reproduction of a migratory passerine?

Nest predation is one of the most important drivers of avian life history evolution and population dynamics. Increasing evidence suggests that birds are able to assess nest predation risk and avoid settling in high‐risk areas to increase their reproductive performance. However, the cues used for settlement decisions are poorly known in most species. Population sizes of the migratory wood warbler Phylloscopus sibilatrix are characterized by strong annual fluctuations, which are negatively correlated with the number of forest rodents. Wood warblers might avoid rodent‐rich areas to reduce predation risk arising either from rodents, from rodent‐hunting predators attracted to such areas or from predators not linked to rodents. To evaluate these hypotheses, we conducted a large‐scale field experiment to test whether wood warblers avoided settling in plots with high predation risk simulated by broadcasting vocalizations of rodents or predators. Moreover, we tested whether reproductive performance varied in relation to simulated predation risk. Settlement patterns did not differ between plots with rodent, predator and noise control treatments. Likewise, measures of reproductive performance did not seem to differ across treatments. Thus, the broadcasted vocalizations of rodents and predators did not seem to be perceived as threat by wood warblers. Alternatively, the species might use other cues than those presented here, either other acoustic cues, visual and/or olfactory cues or a combination of cue types during settlement. Further experimental investigations to pin point cues and senses relevant for settlement decisions in wood warblers and birds in general are needed to better understand their life history and population dynamics.     

Inducible reproductive plasticity of the guppy Poecilia reticulata in response to predation cues

Predation has long been described as one of the major driving forces in evolution. Guppies (Poecilia reticulata) from natural populations exposed to different predation pressures, were found to have different life history traits. Reproductive plasticity in response to direct predation cues has mainly been reported for invertebrates. The goals of the present study were to determine whether exposure to predation cues would induce reproductive phenotypic plasticity in female guppies and to determine whether the effective cues are visual, chemical, or a combination of both. In our first experiment, female guppies exposed to predation cues of the african cichlids Aulonocara nyassae increased their reproductive output by almost two fold, having larger brood-sizes and shorter brood-interval at the first spawn. This effect disappeared in the second spawn in the absence of predators. In the second experiment we found that exposure to the predators induced an increase in the brood-size regardless of whether the cue was: only visual, only chemical, visual and chemical or visual, chemical and tactile. The impacts of these cues were equally powerful on the tested variables and they did not have any cumulative effect. Similar to the results of the first experiment, this effect disappeared in the second spawn, in the absence of predation cues. The present study demonstrates a direct immediate and reversible effect of predation cues on guppy reproduction.     

Behavioural response of bullfrog tadpoles to chemical cues of predation risk are affected by cue age and water source

When confronted by signals of predators presence, many aquatic organisms modify their phenotype (e.g., behaviour or morphology) to reduce their risk of predation. A principal means by which organisms assess predation risk is through chemical cues produced by the predators and/or prey during predation events. Such responses to predation risk can directly affect prey fitness and indirectly affect the fitness of species with which the prey interacts. Accurate assessment of the cue will affect the adaptive nature, and hence evolution, of the phenotypic response. It is therefore, important to understand factors affecting the assessment of chemical cues. Here I examined the effect of the age of chemical cues arising from an invertebrate predator, a larval dragonfly (Anax junius), which was fed bullfrog tadpoles, on the behavioural response (activity level and position) of bullfrog tadpoles. The bullfrog response to chemical cues declined as a function of chemical cue age, indicating the degradation of the chemical cue was on the order of 2–4 days. Further, the decay occurred more rapidly when the chemical cue was placed in pond water rather than well water. These results indicate a limitation of the tadpoles to interpret factors that affect the magnitude of the chemical cue and hence accurately assess predation risk. These findings also have implications for experimental design and the adaptation of phenotypic responses to chemical cues of predation risk.     

Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

Prey detect their predators through predator signals and cues and, consequently, respond with anti‐predatory behaviours to inhibit the action of their aggressors. Lepidopterans can intercept signals emitted by predators and may defend themselves through chemical, morphological or behavioural responses. In this study, we investigated the effect of acoustic stimuli of different predators on defensive behaviour of gregarious caterpillars. Our results demonstrated that Hylesia nigricans (Lepidoptera, Saturniidae) caterpillars alter their behaviour (i.e. abruptly raising the head) in response to the acoustic stimulus of the predators (i.e. predation risk signals from birds and wasps). The magnitude of this response depended on predator identity and caterpillar body size. Larger caterpillars responded more strongly to predatory stimuli than smaller caterpillars. However, regardless of the size of the caterpillars, they responded more strongly to the stimuli of wasps. In addition, we identified that H. nigricans caterpillars emit ultrasonic noise after detecting the stimuli of the predators – this noise seems to function as an alert about the risk of predation during the early stages of development (second and fifth instars). The duration of ultrasonic emission (i.e. milliseconds) increases with the number of repetitions of the stimuli (i.e. wing‐beat sounds of the wasps and insectivorous birds). These results provide novel information about predation risk in interactions among caterpillars and their predators, and indicate possible communication among invertebrates mediated by the risk of predation.     

Predation risk affects egg mortality and carry over effects in the larval stages in damselflies

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Predator-induced life history changes in amphibians: egg predation induces hatching

The timing of transitions between life history stages should be affected by factors that influence survival and growth of organisms in adjacent life history stages. In a series of laboratory experiments, we examined the influence of predation risk as a cue to trigger a life history switch in amphibians. In the Oregon Cascade Mountains, some populations of Pacific treefrogs ( Hyla regilla ) and Cascades frogs ( Rana cascadae ) are under intense egg predation by predatory leeches (families Glossiphonidae and Erpobdellidae). We document that both treefrogs and Cascades frogs show plasticity in hatching characteristics in response to the threat of egg predation. Pacific treefrogs hatch sooner and at an earlier developmental stage when either predatory leeches or non-predatory earthworms are allowed direct contact with the developing egg mass. The same response is elicited even without direct contact. Chemical cues of predatory leeches and chemicals released from injured eggs appear to elicit the same early hatching response in treefrogs. For Cascades frogs, cues of leeches, but not those of injured eggs, elicit an early hatching response. Hatching early in response to egg predators may reduce predation. Plasticity of hatching characteristics has rarely been examined. However, we suspect that it may be common, particularly in populations or species that experience high variability in predation pressure between years.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

Exclusion of ground predators improves Northern Lapwing Vanellus vanellus chick survival

Many farmland‐breeding wader species have declined across Europe, probably due to reductions in reproductive output caused by high nest losses as a result of agriculture or predation, or low chick survival between hatching and fledging. Most studies have focused on nest failures, and the factors affecting post‐hatching survival of chicks are poorly known. In an experimental approach, we fenced parts of the arable foraging areas of Northern Lapwing Vanellus vanellus families to quantify chick survival simultaneously in the presence and absence of ground predators. Lapwing chicks were radiotagged to estimate survival probabilities by daily locations, applying multistate capture–recapture models. During the night, chick survival was considerably lower outside fenced plots than within. During the day, chick survival was higher than at night and did not differ between protected and unprotected plots. This suggests that nocturnal ground predators such as Red Foxes Vulpes vulpes were responsible for a significant proportion of chick mortality. Cumulative survival probability from hatching to fledging was 0.24 in chicks within fenced plots, but virtually zero in chicks outside fenced plots. In farmland, temporary electric fences can be effective in minimizing the impact of ground predators and offer a promising short‐term method to increase fledging success of precocial birds.     

Sequential predator effects across three life stages of the African tree frog, <Emphasis Type="Italic">Hyperolius spinigularis</Emphasis>

While theoretical studies of the timing of key switch points in complex life cycles such as hatching and metamorphosis have stressed the importance of considering multiple stages, most empirical work has focused on a single life stage. However, the relationship between the fitness components of different life stages may be complex. Ontogenetic switch points such as hatching and metamorphosis do not represent new beginnings—carryover effects across stages can arise when environmental effects on the density and/or traits of early ontogenetic stages subsequently alter mortality or growth in later stages. In this study, I examine the effects of egg- and larval-stage predators on larval performance, size at metamorphosis, and post-metamorphic predation in the African tree frog Hyperolius spinigularis. I monitored the density and survival of arboreal H. spinigularis clutches in the field to estimate how much egg-stage predation reduced the input of tadpoles into the pond. I then conducted experiments to determine: (1) how reductions in initial larval density due to egg predators affect larval survival and mass and age at metamorphosis in the presence and absence of aquatic larval predators, dragonfly larvae, and (2) how differences in mass or age at metamorphosis arising from predation in the embryonic and larval environments affect encounters with post-metamorphic predators, fishing spiders. Reduction in larval densities due to egg predation tended to increase per capita larval survival, decrease larval duration and increase mass at metamorphosis. Larval predators decreased larval survival and had density-dependent effects on larval duration and mass at metamorphosis. The combined effects of embryonic and larval-stage predators increased mass at metamorphosis of survivors by 91%. Larger mass at metamorphosis may have immediate fitness benefits, as larger metamorphs had higher survival in encounters with fishing spiders. Thus, the effects of predators early in ontogeny can alter predation risk even two life stages later.     

Predation Risk Avoidance by Terrestrial Amphibians: The Role of Prey Experience and Vulnerability to Native and Exotic Predators

We studied avoidance, by four amphibian prey species (Rana luteiventris, Ambystoma macrodactylum, Pseudacris regilla, Tarichia granulosa), of chemical cues associated with native garter snake (Thamnophis elegans) or exotic bullfrog (R. catesbeiana) predators. We predicted that avoidance of native predators would be most pronounced, and that prey species would differ in the intensity of their avoidance based on relative levels of vulnerability to predators in the wild. Adult R. luteiventris (presumably high vulnerability to predation) showed significant avoidance of chemical cues from both predators, A. macrodactylum (intermediate vulnerability to predation) avoided T. elegans only, while P. regilla (intermediate vulnerability to predation) and T. granulosa (low vulnerability to predation) showed no avoidance of either predator. We assessed if predator avoidance was innate and/or learned by testing responses of prey having disparate levels of prior exposure to predators. Wild‐caught (presumably predator‐exposed) post‐metamorphic juvenile R. luteiventris and P. regilla avoided T. elegans cues, while laboratory‐reared (predator‐naive) conspecifics did not; prior exposure to R. catesbeiana was not related to behavioural avoidance among adult or post‐metamorphic juvenile wild‐reared A. macrodactylum and P. regilla. These results imply that (i) some but not all species of amphibian prey avoid perceived risk from garter snake and bullfrog predators, (ii) the magnitude of this response probably differs according to prey vulnerability to predation in the wild, and (iii) avoidance tends to be largely learned rather than innate. Yet, the limited prevalence and intensity of amphibian responses to predation risk observed herein may be indicative of either a relatively weak predator–prey relationship and/or the limited importance of predator chemical cues in this particular system.     

Induced hatching to avoid infectious egg disease in whitefish.

Reacting to a threat before physical contact, e.g., induced by air- or water-borne substances, appears to be an elegant way of defense. The reaction may be behavioral, developmental, morphological, or physiological, and it can involve a shift in niche or life history. Hatching from eggs is a shift in niche and in life history. From niche shift and life history models, one would predict that the timing of hatching is, to some degree, phenotypically plastic, i.e., early or delayed hatching is likely to be inducible. Temporary increased larval mortality (e.g., increased predation on larvae) would favor delayed hatching, while relatively high egg mortality would favor early hatching. Here, I show experimentally that eggs of the whitefish (Coregonus sp.) hatch earlier in the presence of a virulent egg parasite and that this early hatching is induced by water-borne cues emitted from infected eggs.     

Local adaptation and embryonic plasticity affect antipredator traits in hatchling pond snails

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Phenotypically plastic responses of green frog embryos to conflicting predation risk

Predators have been shown to alter the timing of switch points between life history stages, but few studies have addressed switch point plasticity in prey exposed simultaneously to conflicting predation pressure. We tested hatching responses of green frog (Rana clamitans) embryos subject to perceived predation risk from chemical cues released by two stage-specific predators, predicting that these predators would elicit: (1) directional hatching responses when presented independently, and (2) intermediate phenotypic responses when presented simultaneously. R. clamitans embryos in outdoor exclosures were exposed to cues from an egg predator (freshwater leeches; Nephelopsis obscura), a larval predator (dragonfly nymphs, Aeschna canadensis), and both predators in a 2 × 2 factorial experiment, and changes in hatchling size, hatchling developmental stage, and hatching time were compared to those for control embryos. Leeches alone induced embryos to hatch at a smaller size and an earlier developmental stage than controls, while dragonfly nymphs elicited a delay in egg hatching time that was associated with larger size and later developmental stage at hatching. Embryos failed to respond to simultaneous exposure to both predators, implying that responses to each occurred concurrently and were therefore dampened. Our results indicate that prey under threat from conflicting predators may manifest intermediate defensive phenotypes. Such intermediate responses may result in elevated rates of prey mortality with possible consequences at the population level.