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

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

Multiple predator defence strategies in Daphnia pulex and their relation to native habitat

Daphnia may respond with an array of anti-predator defences(behavioural, morphological and life history) to a chemicalcue (kairomone) exuded by its predators: fish and Chaoborus.Given the wide array of potential responses, it is an interestingquestion whether anti-predator defences are coupled or independentof each other. Since anti-predator responses are costly andeven possessing the genetic information to respond to a certainpredator might involve a cost, clones may only react to predatorsthey co-occur with in nature. In this study, we provide evidencefor an uncoupling of responses by Daphnia pulex in several anti-predatordefences against Chaoborus. We were unable to detect a correlationbetween behavioural (migration), morphological (neck-spine induction)and life history [growth rate, neonate size and size at firstreproduction (SFR)] responses. Furthermore, anti-predator responsesdid not always comply with what is commonly believed. We foundthat Daphnia clones can migrate up or down when exposed to fishor Chaoborus kairomone and that population growth rate, neonatesize and SFR can increase or decrease in response to Chaoboruskairomone. We also show patterns in anti-predator defences thatseem to relate to the habitat from which clones were derived.Daphnia clones that were collected in habitats with Chaoborusas the dominant predator tended to react strongly to Chaoboruskairomone by migrating upward and producing neck-spines. Themigration behaviour against fish kairomone in these clones wasoften an unexpected upward migration. The Daphnia clone thatco-existed with fish predators showed a downward migration inthe presence of fish as well as Chaoborus kairomone. Clonesthat had occurred with either both or no predators had mixedresponses. We sometimes found an upward migration in combinationwith smaller body size as a response to Chaoborus kairomone.This may be interpreted as a behavioural defence against Chaoborusand a life-history defence against fish. Daphnia seem not toexhibit defence behaviour against predators they do not co-occurwith. It might be costly for Daphnia to maintain genetic informationto respond to these predators and protect that information fromgenetic drift.     

萼花臂尾轮虫对晶囊轮虫反捕食行为及形态响应的母体效应

为研究轮虫通过母体效应诱导能否产生行为响应, 以萼花臂尾轮虫(Brachionus calyciflorus)为例, 研究其反捕食漂浮行为响应的母体效应。通过控制轮虫母体在捕食者诱导液中的暴露时间及带卵状态, 收集母体产生的后代, 再将这些后代再次用捕食者诱导液处理, 观察后代的漂浮行为及形态特征。研究发现: 暴露于捕食者诱导液诱导较长时间的母体产生的后代个体, 当再次暴露于捕食者诱导液时, 其产生的行为响应强于没有母体暴露经历的后代; 母体暴露时间越长, 后代形态和行为响应均更加强烈。研究显示萼花臂尾轮虫可通过母体效应产生漂浮行为响应。     

Reciprocity in predator–prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology

A vast body of literature exists documenting the morphological, behavioural and life history changes that predators induce in prey. However, little attention has been paid to how these induced changes feed back and affect the predators’ life history and morphology. Larvae of the phantom midge Chaoborus flavicans are intermediate predators in a food web with Daphnia pulex as the basal resource and planktivorous fish as the top predator. C. flavicans prey on D. pulex and are themselves prey for fish; as D. pulex induce morphological defences in the presence of C. flavicans this is an ideal system in which to evaluate the effects of defended prey and top predators on an intermediate consumer. We assessed the impact on C. flavicans life history and morphology of foraging on defended prey while also being exposed to the non-lethal presence of a top fish predator. We tested the basic hypothesis that the effects of defended prey will depend on the presence or absence of top predator predation risk. Feeding rate was significantly reduced and time to pupation was significantly increased by defended morph prey. Gut size, development time, fecundity, egg size and reproductive effort respond to fish chemical cues directly or significantly alter the relationship between a trait and body size. We found no significant interactions between prey morph and the non-lethal presence of a top predator, suggesting that the effects of these two biological factors were additive or singularly independent. Overall it appears that C. flavicans is able to substantially modify several aspects of its biology, and while some changes appear mere consequences of resource limitation others appear facultative in nature.     

Non-lethal presence of predators modifies morphology and movement rates in <Emphasis Type="Italic">Euplotes</Emphasis>

Many species are able to modify aspects of their behaviour and morphology in the presence of predators. The aim of this study was to investigate the relationship between the expression of morphological and behavioural defences according to the framework proposed by DeWitt et al (1999). Experiments were carried out using hypotrich ciliates of the genus Euplotes as prey and turbellarians of the genus Stenostomum as predators. The smaller species Euplotes octocarinatus showed a greater proportional increase in width, a reduction in foraging movement rates and an increase in maximum movement rates following exposure to predator cues. The larger Euplotes aediculatus induced lesser changes in width, similar reductions in movement during foraging and no change in maximum speed following predator exposure. These results provide evidence of a cospecialised relationship between morphological and behavioural defences. Despite substantial differences in the absence of predators, movement rates and lateral body width were similar in both species following predator exposure. The observed changes may be considered adaptive, gape limited flatworm predators are unable to ingest large Euplotes and a reduction in movement rates during foraging reduces predator encounter rates, while an increase in maximal movement rates increases chances of predator evasion. Handling editor: S. I. Dodson     

Escape behaviour and ultimate causes of specific induced defences in an anuran tadpole

Induced defences, such as the predator avoidance morphologies in amphibians, result from spatial or temporal variability in predation risk. One important component of this variability should be the difference in hunting strategies between predators. However, little is known about how specific and effective induced defences are to different types of predators. We analysed the impact of both pursuing (fish, Gasterosteus aculeatus) and sit-and-wait (dragonfly, Aeshna cyanea) predators on tadpole (Rana dalmatina) morphology and performance (viz locomotive performance and growth rate). We also investigated the potential benefits of the predator-induced phenotype in the presence of fish predators. Both predators induced deeper tail fins in tadpoles exposed to threat of predation, and stickleback presence also induced longer tails and deeper tail muscles. Morphological and behavioural differences resulted in better escape ability of stickleback-induced tadpoles, leading to improved survival in the face of stickleback predation. These results clearly indicate that specific morphological responses to different types of predators have evolved in R. dalmatina. The specific morphologies suggest low correlations between the traits involved in the defence. Independence of traits allows prey species to fine-tune their response according to current predation risk, so that the benefit of the defence can be maximal.     

Costs and benefits of defences induced by predators differing in dangerousness

While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.     

Chimpanzee and felid diet composition is influenced by prey brain size

Prey use a wide variety of anti-predator defence strategies, including morphological and chemical defences as well as behavioural traits (risk-modulated habitat use, changes in activity patterns, foraging decisions and group living). The critical test of how effective anti-predator strategies are is to relate them to relative indices of mortality across predators. Here, we compare biases in predator diet composition with prey characteristics and show that chimpanzee (Pan troglodytes) and felid show the strongest and the most consistent predator bias towards small-brained prey. We propose that large-brained prey are likely to be more effective at evading predators because they can effectively alter their behavioural responses to specific predator encounters. Thus, we provide evidence for the hypothesis that brain size evolution is potentially driven by selection for more sophisticated and behaviourally flexible anti-predator strategies.     

Increasing conspecific density weakens the ability of intermediate predators to develop induced morphological defences to top predators

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Fleeing towards death – leech‐induced behavioural defences increase freshwater snail susceptibility to predatory fish

Prey species are often exposed to multiple predators, which presents several difficulties to prey species. This is especially true when the response to one predator influences the prey’s susceptibility to other predators. Predator‐induced defences have evolved in a wide range of prey species, and experiments involving predators with different hunting strategies allow researchers to evaluate how prey respond to multiple threats. Freshwater snails are known to respond to a variety of predators with both morphological and behavioural defences. Here we studied how freshwater snails Radix balthica responded behaviourally to fish and leech predators, both separately and together. Our aim was to explore whether conflicting predator‐induced responses existed and, if so, what effect they had on snail survival when both predatory fish and leeches were present. We found that although R. balthica increased refuge use when exposed to predatory fish, they decreased refuge use when exposed to predatory leeches. When both predators were present, snails showed a stronger response towards leech than fish and responded by leaving the refuge. This response made the snails more susceptible to fish predation, which increased snail mortality when exposed to both fish and leech compared to fish only. We show that predators that have a relatively low predation rate can substantially increase mortality rates by indirect effects. By forcing snails out of refuges such as rock and macrophyte habitats, leeches can indirectly increase predation from molluscivorous fish and may thus affect snail densities.     

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.     

Freezing behaviour facilitates bioelectric crypsis in cuttlefish faced with predation risk

Cephalopods, and in particular the cuttlefish Sepia officinalis, are common models for studies of camouflage and predator avoidance behaviour. Preventing detection by predators is especially important to this group of animals, most of which are soft-bodied, lack physical defences, and are subject to both visually and non-visually mediated detection. Here, we report a novel cryptic mechanism in S. officinalis in which bioelectric cues are reduced via a behavioural freeze response to a predator stimulus. The reduction of bioelectric fields created by the freeze-simulating stimulus resulted in a possible decrease in shark predation risk by reducing detectability. The freeze response may also facilitate other non-visual cryptic mechanisms to lower predation risk from a wide range of predator types.     

Population divergence in growth rate and antipredator defences in Rana arvalis

Growth and development rates often differ among populations of the same species, yet the factors maintaining this differentiation are not well understood. We investigated the antipredator defences and their efficiency in two moor frog Rana arvalis populations differing in growth and development rates by raising tadpoles in outdoor containers in the nonlethal presence and absence of three different predators (newt, fish, dragonfly larva), and by estimating tadpole survival in the presence of free-ranging predators in a laboratory experiment. Young tadpoles in both populations reduced activity in the presence of predators and increased hiding behaviour in the presence of newt and fish. Older tadpoles from the slow-growing Gotland population (G) had stronger hiding behaviour and lower activity in all treatments than tadpoles from the fast-growing Uppland population (U). However, both populations showed a plastic behavioural response in terms of reduced activity. The populations differed in induced morphological defences especially in response to fish. G tadpoles responded with relatively long and deep body, short tail and shallow tail muscle, whereas the responses in U tadpoles were often the opposite and closer to the responses induced by the other predators. U tadpoles metamorphosed earlier, but at a similar size to G tadpoles. There was no evidence that growth rate was affected by predator treatments, but tadpoles metamorphosed later and at larger size in the predator treatments. G tadpoles survived better in the presence of free-ranging predators than U tadpoles. These results suggest that in these two populations, low growth rate was linked with low activity and increased hiding, whereas high growth rate was linked with high activity and less hiding. The differences in behaviour may explain the difference in survival between the populations, but other mechanisms (i.e. differences in swimming speed) may also be involved. There appears to be considerable differentiation in antipredator responses between these two R. arvalis populations, as well as with respect to different predators.     

Know thy enemy: Behavioural response of a native mammal (Rattus lutreolus velutinus) to predators of different coexistence histories

Abstract Predation is recognized as a major selective pressure influencing population dynamics and evolutionary processes. Prey species have developed a variety of predator avoidance strategies, not least of which is olfactory recognition. However, within Australia, European settlement has brought with it a number of introduced predators, perhaps most notably the red fox (Vulpes vulpes) and domestic cat (Felis catus), which native prey species may be unable to recognize and thus avoid due to a lack of coexistence history. This study examined the response of native Tasmanian swamp rats (Rattus lutreolus velutinus) to predators of different coexistence history (native predator‐ spotted‐tail quoll (Dasyurus maculatus), domestic cats and the recently introduced red fox). We used an aggregate behavioural response of R. l. velutinus to predator integumental odour in order to assess an overall behavioural response to predation risk. Rattus lutreolus velutinus recognized the integumental odour of the native quoll (compared with control odours) but did not respond to either cat or fox scent (compared with control odur). In contrast, analyses of singular behaviours resulted in the conclusion that rats did not respond differentially to either native or introduced predators, as other studies have concluded. Therefore, measuring risk assessment behaviours at the level of overall aggregate response may be more beneficial in understanding and analysing complex behavioural patterns such as predator detection and recognition. These results suggest that fox and cat introductions (and their interactive effects) may have detrimental impacts upon small native Tasmanian mammals due to lack of recognition and thus appropriate responses.     

Behavioural and life history responses to predation risk by common frog tadpoles exposed to two predators during ontogeny

The presence of predators can induce changes in both the morphology and behaviour of Anuran larvae, affecting both their size and developmental stage at metamorphosis and, consequently, the fitness of adult individuals. Tadpoles have been shown to be capable of finely tuning their defensive responses according to the actual risk perceived, which is expected to vary according to the prey-to-predator size ratio. In this study, we exposed common frog (Rana temporaria) tadpoles (Gosner stages 28–30), for a period of 2 weeks, to the non-lethal presence of dragonfly larvae (Anax imperator) and backswimmers (Notonecta glauca). In such a narrow window of time, we expected behavioural responses to be similar for both predators and exposure to predation risk to have negligible effects on tadpole development and weight. Overall, tadpoles increased hiding behaviour and were less active when predators were present in the experimental mesocosms, but behavioural responses were constrained to the early phase of the ontogeny and were no longer used when tadpoles reached a threshold size. Developmental rate slightly slowed down for predator treatments in comparison to controls, possibly as a consequence of energetic investment in unrecorded morphological defences. Although variation in laboratory conditions and protocols makes it hard to compare the results of different experiments, our results contribute to verify the consistency of behavioural responses in Anuran larvae.     

Linking Morphological and Behavioural Defences: Prey Fish Detect the Morphology of Conspecifics in the Odour Signature of their Predators

Predation is a strong selective force acting on both morphology and behaviour of prey animals. While morphological defences (e.g. crypsis, presence of armours or spines or specific body morphologies) and antipredator behaviours (e.g. change in foraging or reproductive effort, or hiding and fleeing behaviours) have been widely studied separately, few studies have considered the interplay between the two. The question raised in our study is whether antipredator behaviours of a prey fish to predator odours could be influenced by the morphology of prey conspecifics in the diet of the predator. We used goldfish (Carassius auratus) as our test species; goldfish exposed to predation risk significantly increase their body depth to length ratio, which gives them a survival advantage against gape‐limited predators. We exposed shallow‐bodied and deep‐bodied goldfish to the odour of pike (Esox lucius) fed either form of goldfish. Deep‐bodied goldfish displayed lower intensity antipredator responses than shallow‐bodied ones, consistent with the hypothesis that individuals with morphological defences should exhibit less behavioural modification than those lacking such defences. Moreover, both shallow‐ and deep‐bodied goldfish displayed their strongest antipredator responses when exposed to the odour of pike fed conspecifics of their own morphology, indicating that goldfish are able to differentiate the morphology of conspecifics through predator diet cues. For a given individual, predator threat increases as the prey become more like the individual eaten, revealing a surprising level of sophistication of chemosensory assessment by prey fish.     

Habitat and food specificity in aphidophagous predators

Current knowledge of the processes underlying prey location and choice by aphidophagous predators is reviewed by considering the succession of behavioural mechanisms required for the predator to obtain prey. The predator may locate areas where prey are likely to be found by responding to physical aspects of the habitat, or to semiochemicals produced by the host plant. The predator may then respond to visual or olfactory cues to locate the aphid prey. The predator's readiness to attack and consume aphids is influenced by any behavioural or chemical defence strategies, and by the palatability or nutrient value of the aphids. Toxic allelochemicals ingested by aphids from their host plant may have a detrimental effect on predators.     

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.     

Evidence for carry-over effects of predator exposure on pathogen transmission potential

Accumulating evidence indicates that species interactions such as competition and predation can indirectly alter interactions with other community members, including parasites. For example, presence of predators can induce behavioural defences in the prey, resulting in a change in susceptibility to parasites. Such predator-induced phenotypic changes may be especially pervasive in prey with discrete larval and adult stages, for which exposure to predators during larval development can have strong carry-over effects on adult phenotypes. To the best of our knowledge, no study to date has examined possible carry-over effects of predator exposure on pathogen transmission. We addressed this question using a natural food web consisting of the human malaria parasite Plasmodium falciparum, the mosquito vector Anopheles coluzzii and a backswimmer, an aquatic predator of mosquito larvae. Although predator exposure did not significantly alter mosquito susceptibility to P. falciparum, it incurred strong fitness costs on other key mosquito life-history traits, including larval development, adult size, fecundity and longevity. Using an epidemiological model, we show that larval predator exposure should overall significantly decrease malaria transmission. These results highlight the importance of taking into account the effect of environmental stressors on disease ecology and epidemiology.     

Predator avoidance and immune defence: costs and trade-offs in snails

Organisms are often confronted by both predators and pathogens. Defending against such widely divergent enemies requires more than one type of defence. Multiple defences, however, raise the possibility of trade-offs among defences. We tested for such trade-offs by manipulating the level of predator-avoidance behaviour and immune function in the freshwater snail Lymnaea stagnalis (Gastropoda: Pulmonata). Our results show that predator avoidance and immune function had clear costs in terms of reproduction and survival. Further, we show that increased levels of predator-avoidance behaviour reduced the snails' ability to defend against potential pathogens. Predator-avoidance behaviour may thus have the additional indirect cost of reduced immunocompetence and increased susceptibility to pathogens. Our results suggest that ecological factors (e.g. predator density) may considerably modify the expression and costs of immune defences.