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.     

Bulgy tadpoles: inducible defense morph

Predator induced morphological defenses are marked morphological shifts induced directly by cues associated with a predator. Generally, remote cues, i.e., chemical substances emitted from predators or injured conspecifics, are considered to be ideal signals to induce morphological change in aquatic environments rather than close cues, i.e., close chemical or tactile cues, since chemical substances that can propagate over relatively long distances and persist for a long period may allow organisms to keep safe and to deliberately change their morph. In fact, most organisms adopting an inducible morphological defense utilize remote chemical cues to detect predation risk and to produce morphological defenses. In this paper, we report a unique and functionally well designed inducible morphological defense strategy where the induction process requires close cues from a predator. The tadpoles of Rana pirica exhibited a bulgy bodied morphology when threatened with predation by larval salamanders, Hynobius retardatus, in close proximity. Predation trials and a function experiment showed that the induced bulgy morph is an adaptive defense phenotype against the gape-limited predator larval H. retardatus. Furthermore, R. pirica tadpoles use two adaptive strategies in terms of cost saving, i.e., adjustment of the extent of bulginess according to predation risk and reversibility by actual shrink of bulgy body after removing the predation threat. In general, R. pirica hatch earlier than H. retardatus. In natural ponds, during the early developmental stage R. pirica tadpoles live in close proximity to young H. retardatus larvae. As they grow, the salamanders gradually become serious predators and the predator–prey interaction becomes intimate. After a while, predation, cannibalism and metamorphosis decrease the number of salamanders in the ponds, and the predator–prey interaction weakens. Such a phenology in the predator–prey interaction allows the evolution of a close-cue detection system and adaptive cost-saving strategies. Our results highlight that the characteristics of the inducible defense depend on the intensity and specificity of the predator–prey system.     

Cue reliability, risk sensitivity and inducible morphological defense in a marine snail

Reliable cues that communicate current or future environmental conditions are a requirement for the evolution of adaptive phenotypic plasticity, yet we often do not know which cues are responsible for the induction of particular plastic phenotypes. I examined the single and combined effects of cues from damaged prey and predator cues on the induction of plastic shell defenses and somatic growth in the marine snail Nucella lamellosa. Snails were exposed to chemical risk cues from a factorial combination of damaged prey presented in isolation or consumed by predatory crabs (Cancer productus). Water-borne cues from damaged conspecific and heterospecific snails did not affect plastic shell defenses (shell mass, shell thickness and apertural teeth) or somatic growth in N. lamellosa. Cues released by feeding crabs, independent of prey cue, had significant effects on shell mass and somatic growth, but only crabs consuming conspecific snails induced the full suite of plastic shell defenses in N. lamellosa and induced the greatest response in all shell traits and somatic growth. Thus the relationship between risk cue and inducible morphological defense is dependent on which cues and which morphological traits are examined. Results indicate that cues from damaged conspecifics alone do not trigger a response, but, in combination with predator cues, act to signal predation risk and trigger inducible defenses in this species. This ability to “label” predators as dangerous may decrease predator avoidance costs and highlights the importance of the feeding habits of predators on the expression of inducible defenses.     

水生生态环境中捕食信息素的生态学效应

捕食信息素是捕食者释放的,能够引发猎物反捕食反应的化学信号。在水生生态系统中,捕食信息素在捕食者和猎物之间信息传递及协同进化过程中发挥着重要的作用,其生态学效应在国际上受到广泛关注。捕食信息素的来源有多种形式,研究中常使用养殖过捕食者的水溶液作为捕食信息素的来源。捕食信息素的作用效果受到捕食者和猎物的种类、信息素的浓度、观察的指标等多方面因素的影响。捕食信息素可以对水生生物的行为、形态和生活史特征等方面造成影响。水生生物通过感知捕食信息素来提前预知潜在的被捕食风险,并作出适应性调整,以降低被捕食的风险。在某些情况下,捕食信息素可以与污染物产生交互作用,从而干扰污染物对水生生物的毒性。对水生环境中捕食信息素的研究现状做了综述,介绍了当前对捕食信息素来源和理化性质等本质问题的认识,总结捕食信息素对水生生物行为、形态和生活史特征的影响,以及捕食信息素对污染物毒性的干扰,并分析了这一研究领域尚存在的困难和今后的研究方向。加强对捕食信息素的研究,将为解析水生环境中捕食者和猎物的生态关系提供新依据。     

Conspecific density determines the magnitude and character of predator-induced phenotype

The benefits in survival gained from predator-induced phenotypes often come at a cost to other components of fitness. Therefore, the level of expression of an induced phenotype should mirror the level of risk in the environment. When a predator exhibits a saturating functional response the risk of mortality to a given prey decreases as prey density increases. Therefore, for a given predator threat, investment in defense should be lower in prey at high density relative to those at low density. In this study, I test whether the magnitude of predator-induced morphological plasticity decreases with increasing conspecific density by exposing pine woods tree frog (Hyla femoralis) tadpoles at three different densities to predators (present or absent) in a factorial experiment. Tadpole morphology was not affected by changes in density in the absence of predators. However, predators had a significant, density-dependent effect on tadpole morphology. Specifically, the magnitude of morphological response was graded and larger for animals in the low density (high risk) environment. This study demonstrates that tadpoles can modulate phenotypic plasticity in response to mortality risk as a function of both the density of conspecifics and chemical cues from predators, which suggests that they are able to detect and respond to fine-scale changes in the threat environment. In addition, this study highlights the need for analytical approaches that allow morphological plasticity studies to elucidate allometric relationships in addition to simply quantifying size-corrected traits. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Knowing the Risk: Crickets Distinguish between Spider Predators of Different Size and Commonness

Predators unintentionally release chemical and other cues into their environment that can be used by prey to assess predator presence. Prey organisms can therefore perform specific antipredator behavior to reduce predation risk, which can strongly shape the outcome of trophic interactions. In contrast to aquatic systems, studies on cue‐driven antipredator behavior in terrestrial arthropods cover only few species to date. Here, we investigated occurrence and strength of antipredator behavior of the wood cricket Nemobius sylvestris toward cues of 14 syntopic spider species that are potential predators of wood crickets. We used two different behavioral arena experiments to investigate the influence of predator cues on wood cricket mobility. We further tested whether changes in wood cricket mobility can be explained by five predator‐specific traits: hunting mode, commonness, diurnal activity, predator–prey body–size ratio, and predator–prey life stage differences. Crickets were singly recorded (1) in separate arenas, either in presence or absence of spider cues, to analyze changes in mobility on filter paper covered with cues compared with normal mobility on filter paper without cues; and (2) in subdivided arenas partly covered with spider cues, where the crickets could choose between cue‐bearing and cue‐less areas to analyze differences in residence time and mobility when crickets are able to avoid cues. Crickets either increased or reduced their mobility in the presence of spider cues. In the experiments with cues and controls in separate arenas, the magnitude of behavioral change increased significantly with increasing predator–prey body size ratio. When crickets could choose between spider cues and control, their mobility was significantly higher in the presence of cues from common spider species than from rare spiders. We therefore conclude that wood crickets distinguish between cues from different predator species and that spiders unintentionally release a species‐specific composition and size‐dependent quantity of cues, which lead to distinct antipredator behavior in wood crickets.     

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.     

Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms

Trait-mediated indirect effects (TMIs) are changes in the density of one species that are caused by induced changes in one or more traits of an intervening species. For example, induced defense in a prey species may alter the nature of indirect effects that are mediated through that prey species. In the present study, we investigated the TMIs that stem from an interaction between a carnivorous whelk ( Acanthina angelica ) and an intertidal barnacle ( Chthamalus anisopoma) . Depending on the timing of the interaction, the predator either kills the barnacle or induces a predation-resistant morph. Based on previous work that addressed the direct interactions between Chthamalus and other species in the community we predicted and subsequently found that community structure varies as a function of these differing effects. Specifically, we found that Acanthina has a positive indirect effect on mussels when it interacts with (kills) undefended adult barnacles. In contrast, the predator has a positive indirect effect on an encrusting algae ( Ralfsia ) when it comes into contact with juvenile barnacles, causing the induction of the predator-resistant morph. We suggest that further research should consider the role of environmentally induced polymorphisms in structuring communities.     

Dynamic Risk Assessment: Prey Rapidly Adjust Flight Initiation Distance to Changes in Predator Approach Speed

The pre‐eminent model of flight initiation distance assumes that the function relating predation risk to distance between predator and prey is constant. However, the risk–distance function can change dramatically during approaches by predators. Changes in predator behavior during approach and in availability of benefits (e.g. food or potential mates) may alter risks and/or costs during encounters. Thus, prey should be able to respond appropriately to changes in cues to risk, such as predator approach speed. Under the assumption that prey assess risk in real time, it was predicted that flight initiation distance (distance between predator and prey when escape begins) decreases when approach speed increases and increases when approach speed decreases during an encounter. Effects of single, abrupt changes from slower to faster approach or the reverse were studied in a lizard, Anolis lineatopus. Flight initiation distances were determined solely by final approach speed, being nearly identical for: (1) continuously fast approaches and approaches initially at the slower and finally at the faster speed and (2) for continuously slower approaches and approaches initially at faster and finally at slower speed. Escape should be adjusted to match changes in risk and cost caused by changes in predator behavior, ability to escape, and costs of escape as attacks unfold. A recent model by Broom and Ruxton [Behavioural Ecology (2004) vol. 16, pp. 534—540] predicts that cryptic prey should stay motionless until detected, then flee immediately. Our results suggest that current escape models can be applied to prey escape strategies when cues to risk change, by assuming that prey base decisions on the current relationship between risk and distance. Empirical studies are needed to test predictions concerning continuous risk assessment.     

Predator induced phenotypic plasticity in the pinewoods tree frog,<Emphasis Type="Italic"> Hyla femoralis</Emphasis>: necessary cues and the cost of development

Predator-induced defenses can result from non-contact cues associated with the presence of a feeding predator; however, the nature of the predator cue has not been determined. We tested the role of two non-contact cues, metabolites of digestion of conspecific prey released by the predator and alarm pheromones released by attacked conspecific prey, in the development of inducible defenses by exposing pinewoods tree frog (Hyla femoralis) tadpoles to non-lethal dragonfly (Anax junius) larvae fed either inside experimental bins or removed from the bins for feeding to eliminate alarm pheromones. The costs associated with the development of the induced morphology were also investigated by providing the tadpoles with two food levels intended to provide adequate or growth limiting resources. The generalized morphological response of H. femoralis tadpoles to predators included the development of bodies and tails that were both deeper and shorter, smaller overall body size, and increased orange tail fin coloration and black tail outline. Metabolites of digestion were sufficient to initiate development of inducible defenses; however, the combination of metabolites and alarm cue resulted in a greater response. Furthermore, growth and development were slowed in tadpoles that expressed the induced morphology; however, this growth cost was insufficient to preclude the development of the induced morphology when food resources were low. These results indicate that two aspects of the indirect predator cue work together to trigger a morphological anti-predator response.     

Predator recognition and defence strategies in crucian carp, Carassius carassius

Crucian carp from populations that lack piscivores are extremely vulnerable to predation. However, in the presence of piscivores these fish develop an inducible morphological defence, a deep body. This switch from a vulnerable, shallow-bodied morph to a morphologically defended morph makes this species very suitable for investigations of anti-predator strategies, and trade-offs between morphological and behavioural defences. To address these questions, we performed eight different experiments. We found that crucian carp exhibited fright responses to chemical cues from unfamiliar predators (northern pike, perch) when these were fed prey that contained alarm substance (for northern pike: crucian carp, roach; for perch: crucian carp). Cues from small pike that were fed prey that lacked alarm substance (swordtails) caused no significant fright response whereas cues from larger pike with the same diet did. Perch on a chironomid diet elicited weaker but significant fright responses. Starved predators caused as strong fright reactions as recently fed ones did, whereas no response was exhibited towards nonpredatory fish (roach, crucian carp). Crucian carp were able to detect the presence of pike after cues had been diluted to an equivalent of 21 000 l, and larger predators elicited stronger fright responses. Prior experience of predators decreased fright responses. In particular, individuals from populations that coexisted with northern pike responded less to chemical cues from northern pike than individuals without prior experience did. Thus, crucian carp may use both alarm-substance related and predator-related cues to identify predators. Further, they were able to discriminate between large and small predators. Finally, individuals from populations that coexist with predators exhibit less pronounced fright responses. These fish have an induced morphological defence, a deep body, which most likely decreases the need for strong antipredator behaviour.     

Benefits,costs and reactivity of inducible defences: an experimental test with rotifers

1. A key aspect of the ecology and evolution of adaptive prey responses to predator risk is the timing by which the former develop a defensive trait in response to inducing signals released by the latter. This property, called reactivity, has been shown to affect population stability and persistence. 2. Theoretically, the minimal predator density required by prey to exhibit induced defences is expected to increase with the effectiveness of the defence and decrease with its cost. Likewise, the time required for the prey population to exhibit an induced defence is expected to increase together with cost. 3. The freshwater rotifers Brachionus calyciflorus and B. havanaensis and their predator Asplanchna brightwelli were used to test the hypothesis that prey species exhibiting defences that offer a larger fitness benefit and lower fitness cost are more reactive to predator signals, in terms of requiring shorter exposure time and lower signal concentration to trigger a morphological defence reaction. 4. Our results showed that both prey species exhibited costly and effective defences after induction by predator infochemicals. Faster reactions were observed at higher levels of predator cues. Nevertheless, the observed relationship between reactivity and benefit/cost of defences did not agree with our expectations. 5. To our knowledge, this is the first study in which the timing of induction of morphological defences is experimentally assessed over a gradient of risk signals. We propose new research directions to disentangle the mechanisms and project the consequences of prey decisions at the morphological level.     

Indirect predator effects influence behaviour but not morphology of juvenile coral reef Ambon damselfish Pomacentrus amboinensis

A 6-week laboratory experiment exposed juvenile Ambon damselfish Pomacentrus amboinensis to visual and chemical cues of either a predator, a herbivore or a null control (sea water) and found no effect of predator cues on prey morphology (proportion of ocellus to eye diameter, body depth, standard length and fin area). Nonetheless, behaviour was significantly affected by predator presence, with prey less active and taking half as many feeding strikes when exposed to predators compared to fish from the null control. The presence of a herbivore also affected prey behaviour similar to that of the predator, suggesting that the presence of a non-predator may have important effects on development.     

Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey

Prey organisms reduce predation risk by altering their behavior, morphology, or life history. Avoiding or deterring predators often incurs costs, such as reductions in growth or fecundity. Prey minimize costs by limiting predator avoidance or deterrence to situations that pose significant risk of injury or death, requiring them to gather information regarding the relative threat potential predators pose. Chemical cues are often used for risk evaluation, and we investigated morphological responses of oysters (Crassostrea virginica) to chemical cues from injured conspecifics, from heterospecifics, and from predatory blue crabs (Callinectes sapidus) reared on different diets. Previous studies found newly settled oysters reacted to crab predators by growing heavier, stronger shells, but that adult oysters did not. We exposed oysters at two size classes (newly settled oyster spat and juveniles ~2.0 cm) to predation risk cue treatments including predator or injured prey exudates and to seawater controls. Since both of the size classes tested can be eaten by blue crabs, we hypothesized that both would react to crab exudates by producing heavier, stronger shells. Oyster spat grew heavier shells that required significantly more force to break, an effective measure against predatory crabs, when exposed to chemical exudates from blue crabs as compared to controls. When exposed to chemical cues from injured conspecifics or from injured clams (Mercenaria mercenaria), a sympatric bivalve, shell mass and force were intermediate between predator treatments and controls, indicating that oysters react to injured prey cues but not as strongly as to cues released by predators. Juvenile oysters of ~ 2.0 cm did not significantly alter their shell morphology in any of the treatments. Thus, newly settled oysters can differentiate between predatory threats and adjust their responses accordingly, with the strongest responses being to exudates released by predators, but oysters of 2.0 cm and larger do not react morphologically to predatory threats.     

Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus

Predation imposes selection on the ability of prey to recognize and respond to potential threats. Many prey species detect predators via chemoreception, particularly in aquatic environments. Also, chemical cues from injured prey are often perceived as an indication of predation risk. However, because antipredatory behavior can be costly, prey responses should depend on the current level of risk that each predator poses, which may depend on the type of chemical cues detected. We exposed larval newts, Triturus pygmaeus, to chemical cues from predator larval beetles or to alarm cues from conspecific larval newts and examined the behavioral changes of larval newts. Results showed that larval newts reduced activity levels when conspecific alarm cues were present but not when the predator cues alone were present. These results might suggest that larval newts are unable to recognize predator chemicals. To avoid costs of unnecessary antipredatory behaviors, larval newts may benefit by avoiding only predators that represent a current high level of threat, showing only antipredatory responses when they detect conspecific alarm cues indicating that an actual predatory attack has occurred.     

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     

Determinants and co‐expression of anti‐predator responses in amphibian tadpoles: a meta‐analysis

A wide range of taxa respond to perceived predation risk (PPR) through inducible defenses, and many prey are capable of responding both behaviorally and morphologically to the same risk event. In cases where multiple defenses confer protection by independent means (i.e. they are mechanistically independent) responses will either be co‐expressed, or the expression of one defense will limit the capacity (or need) to respond along another axis. Our ability to generate a broad understanding of these patters has been limited, in part, by difficulties in comparing results across studies that employ distinct experimental protocols. Using the extensive literature on tadpole responses to PPR, we conducted a meta‐analysis to identify the ecological and experimental determinants of inducible defence expression. We then assessed whether the magnitude of response to PPR along behavioural versus morphological response axes was positively, or negatively, correlated. The most commonly quantified responses to perceived risk in tadpoles included reductions in movement and swimming behaviour, and altered tail morphology. Our analyses reveal that tadpole behavioural responses are strongly influenced by prey family, predator taxon, evolutionary history with the predator (native versus non‐native), amount of prey consumed by the predator, and how perceived risk was manipulated (e.g. presence versus absence of alarm cues). Tail morphology was similarly influenced by these factors, but also whether the target prey was palatable to predators. Thus, our results identify ecological and experimental features that critically influence the observed effect size in tadpole responses to PPR. A positive correlation between behavioural and morphological responses in studies where both were measured indicates that trait co‐specialization is the predominant pattern of defense deployment in larval amphibians. This positive relationship suggests that survival tends to be maximized in tadpoles through equivalent co‐activation of multiple independent axes of protection, opposed to maximal expression along any single axis. Synthesis Our understanding of plastic responses to perceived predation risk (PPR) has benefited substantially from the vast amount of experimental work examining inducible defences in anuran tadpoles. Indeed this research has illustrated the wide variety of ways that prey animals can respond to the same risk event. We conducted a metaanalysis to identify the key ecological and experimental determinants of inducible defence expression. We then show that, in most cases, behavioural and morphological responses to PPR tend to be co‐expressed suggesting that responding along one axis (moving behaviour) does not limit their ability to respond along another distinct axis (tail morphology).     

Visual cues contribute to predator detection in anuran larvae

The ability of prey to detect predators directly affects their probability of survival. Chemical cues are known to be important for predator detection in aquatic environments, but the role of other potential cues is controversial. We tested for changes in behaviour of Rana temporaria tadpoles in response to chemical, visual, acoustic, and hydraulic cues originating from dragonfly larvae (Aeshna cyanea) and fish (Gasterosteus aculeatus). The greatest reduction in tadpole activity occurred when all cues were available, but activity was also significantly reduced by visual cues only. We did not find evidence for tadpoles lowering their activity in response to acoustic and hydraulic cues. There was no spatial avoidance of predators in our small experimental containers. The results show that anuran larvae indeed use vision for predator detection, while acoustic and hydraulic cues may be less important. Future studies of predator‐induced responses of tadpoles should not only concentrate on chemical cues but also consider visual stimuli. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Interactions between the information content of different chemical cues affect induced defences in tadpoles

Animals often alter their behaviour, morphology and physiology in the presence of predators. These induced defences can be fine‐tuned by a variety of environmental factors such as predator species, acute predation risk or food availability. It has, however, remained unclear what cues influence the extent and quality of induced defences and how the information content of these cues interact to determine the development of antipredator defences. We performed an experiment to study the significance of direct chemical cues, originating from the predators themselves, and indirect cues, released by attacked or consumed prey, for phenotypic responses in Rana dalmatina tadpoles. We reared tadpoles in the presence of caged predators (Triturus vulgaris, Aeshna cyanea) fed either one or three tadpoles every other day outside the tadpole‐rearing tanks. Fifteen hours after food provisioning, predators were put back into the tanks containing focal tadpoles either after washing (direct + digestion‐released cues) or with the water containing remnants of the prey (direct + all types of indirect cues). Our results suggest that direct cues together with digestion‐released cues can be sufficient to induce strong antipredator responses. Induced defences depended on both direct cues, affecting predator‐specific responses, and the quantity of indirect cues, resulting in graded responses to differences in predation threat. Moreover, direct and indirect cues interacted in behaviour, resulting in predator‐specific graded responses. We also observed a decrease in the extent of predator‐induced responses in large tadpoles as compared to small ones. Our results, thus, suggest that prey integrate multiple cues about predators to optimize induced defences and that this process changes during ontogeny.