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.     

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.     

Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae

A central issue in predator–prey interactions is how predator associated chemical cues affect the behaviour and life history of prey. In this study, we investigated how growth and behaviour during ontogeny of a damselfly larva (Coenagrion hastulatum) in high and low food environments was affected by the diet of a predator (Aeshna juncea). We reared larvae in three different predator treatments; no predator, predator feeding on conspecifics and predator feeding on heterospecifics. We found that, independent of food availability, larvae displayed the strongest anti-predator behaviours where predators consumed prey conspecifics. Interestingly, the effect of predator diet on prey activity was only present early in ontogeny, whereas late in ontogeny no difference in prey activity between treatments could be found. In contrast, the significant effect of predator diet on prey spatial distribution was unaffected by time. Larval size was affected by both food availability and predator diet. Larvae reared in the high food treatment grew larger than larvae in the low food treatment. Mean larval size was smallest in the treatment where predators consumed prey conspecifics, intermediate where predators consumed heterospecifics and largest in the treatment without predators. The difference in mean larval size between treatments is probably an effect of reduced larval feeding, due to behavioural responses to chemical cues associated with predator diet. Our study suggests that anti-predator responses can be specific for certain stages in ontogeny. This finding shows the importance of considering where in its ontogeny a study organism is before results are interpreted and generalisations are made. Furthermore, this finding accentuates the importance of long-term studies and may have implications for how results generated by short-term studies can be used.     

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.     

Prey-induced changes to a predator's behaviour and morphology: Implications for shell-claw covariance in the northwest Atlantic

Whereas many plasticity studies demonstrate the importance of inducible defences among prey, far fewer investigate the potential role of inducible offences among predators. Here we ask if natural differences in a snail's shell hardness can induce developmental changes to a predatory crab's claw size. To do this, we fed Littorina obtusata snails from either thick- or thin-shelled populations to captive European green crabs Carcinus maenas. The crabs' shell-breaking behaviour dominated among those fed thin-shelled snails, whereas crabs fed thick-shelled snails mostly winkled flesh through the shell opening without damaging the shell itself (a.k.a. aperture-probing behaviour). Significantly, the size of crab crusher claws grew in proportion to the frequency of shell-crushing behaviour and, for a same shell-crushing frequency, crabs fed thick-shelled snails grew larger crusher claws than those fed thin-shelled snails after two experimental moults. Diet and behaviour had no effect on the growth of the smaller cutter claws of same individuals, providing good evidence that allometric changes to crusher claws were indeed a result of differential use while feeding. Findings indicate that both predation habits and claw sizes are affected by green crabs' diet, supporting the hypothesis that prey-induced phenotypic plasticity contributes to earlier accounts of shell-claw covariance between this predator and its Littorina prey in the wild.     

Influence of predator density on nonindependent effects of multiple predator species

Interactions between multiple predator species are frequent in natural communities and can have important implications for shared prey survival. Predator density may be an important component of these interactions between predator species, as the frequency of interactions between species is largely determined by species density. Here we experimentally examine the importance of predator density for interactions between predator species and subsequent impacts on prey. We show that aggressive interactions between the predatory shore crabs Carcinus maenas and Hemigrapsus sanguineus increased with predator density, yet did not increase as fast as negative interactions between conspecifics. At low density, interactions between conspecific and heterospecific predators had similar inhibitory impacts on predator function, whereas conspecific interference was greater than interference from heterospecifics at high predator density. Thus the impact of conspecific interference at high predator density was sufficient in itself that interactions with a second predator species had no additional impact on per capita predation. Spatial and temporal variability in predator density is a ubiquitous characteristic of natural systems that should be considered in studies of multiple predator species.     

Prey bacteria shape the community structure of their predators

Although predator–prey interactions among higher organisms have been studied extensively, only few examples are known for microbes other than protists and viruses. Among the bacteria, the most studied obligate predators are the Bdellovibrio and like organisms (BALOs) that prey on many other bacteria. In the macroscopical world, both predator and prey influence the population size of the other''s community, and may have a role in selection. However, selective pressures among prey and predatory bacteria have been rarely investigated. In this study, Bacteriovorax, a predator within the group of BALOs, in environmental waters were fed two prey bacteria, Vibrio vulnificus and Vibrio parahaemolyticus. The two prey species yielded distinct Bacteriovorax populations, evidence that selective pressures shaped the predator community and diversity. The results of laboratory experiments confirmed the differential predation of Bacteriovorax phylotypes on the two bacteria species. Not only did Bacteriovorax Cluster IX exhibit the versatility to be the exclusive efficient predator on Vibrio vulnificus, thereby, behaving as a specialist, but was also able to prey with similar efficiency on Vibrio parahaemolyticus, indicative of a generalist. Therefore, we proposed a designation of versatilist for this predator. This initiative should provide a basis for further efforts to characterize the predatory patterns of bacterial predators. The results of this study have revealed impacts of the prey on Bacteriovorax predation and in structuring the predator community, and advanced understanding of predation behavior in the microbial world.     

Cautious cannibals: Behavioral responses of juvenile and adult blue crabs to the odor of injured conspecifics

Blue crabs are cannibalistic, and therefore the scent of injured conspecifics represents both a potential food cue, as well as an indicator of predation risk. We examined the response of blue crabs to conspecific odor alone, as well as in mixtures of attractive cues to determine how animals evaluate and respond to this odor. We explicitly manipulated risk-sensitivity based on either animal size (an indicator of susceptibility to predation) or hunger state (susceptibility to starvation) as ways to evaluate theories of risk-allocation, which suggest that decreases in predation risk, or increases in the risk of starvation, ought to result in diminished responses to sensory cues that signal predator presence or activity. Large and small blue crabs were challenged to locate the source of odor plumes consisting of the scent of injured conspecifics (risk cue), attractive food odors (attractive cue), or their mixture (conflicting cue). Neither large nor small blue crabs tracked aversive cues, but large blue crabs consistently tracked conflicting treatments to their source. Responses to conflicting and aversive treatments also involved diminished movement and reduced tracking speed relative to behaviors displayed in attractive plumes. Thus, even cannibalistic crabs seem to respond more prevalently to the apparent predation risk then to food reward, and risk-sensitive behaviors have a likely cost in terms of reduced food intake. Starved animals were more likely than unstarved animals to track conflicting plumes. Both the ontogenic shift and the response of starved animals support the notion that the cost of risk-aversive behaviors results in this strategy being allocated in proportion to the degree of potential risk. Since risk-aversive responses to chemical cues can produce strong effects in communities, the size-dependent nature of these responses in blue crabs may introduce considerable complexity in interactions between blue crabs, their predators, and their prey.     

Diet of a polyphagous arthropod predator affects refuge seeking of its thrips prey

Antipredator behaviour of prey costs time and energy, at the expense of other activities. However, not all predators are equally dangerous to all prey; some may have switched to feeding on another prey species, making them effectively harmless. To minimize costs, prey should therefore invest in antipredator behaviour only when dangerous predators are around. To distinguish these from harmless predators, prey may use cues related to predation on conspecifics, such as odours released by a predator that has recently eaten conspecific prey or alarm pheromones released by attacked prey. We studied refuge use by a herbivorous/omnivorous thrips, Frankliniella occidentalis, in response to odours associated with a generalist predatory bug, Orius laevigatus, fed either with conspecific thrips or with other prey. The refuge used by thrips larvae is the web produced by its competitor, the two-spotted spider mite, Tetranychus urticae, where thrips larvae experience lower predation risk because the predatory bug is hindered by the web. Thrips larvae moved into this refuge when odours associated with predatory bugs that had previously fed on thrips were present, whereas odours from predatory bugs that had fed on other prey had less effect. We discuss the consequences of this antipredator behaviour for population dynamics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Effects of Chemical Cues on Foraging in Damselfly Larvae, <Emphasis Type="Italic">Enallagma antennatum</Emphasis>

Animals experiencing a trade-off between predation risk and resource acquisition must accurately predict ambient levels of predation risk to maximize fitness. We measure this trade-off explicitly in larvae of the damselfly Enallagma antennatum, comparing consumption rates in the presence of chemical cues from predators and injured prey. Damselflies distinguished among types of chemical cues based on species of prey injured or eaten. Injured coexisting heterospecific and unknown heterospecific chemical cues did not reduce foraging relative to starved predator cues, while cues arising from predators eating a coexisting heterospecific did decrease foraging. This study shows a cost in terms of reduced foraging in response to chemical cues and further defines the ability of prey to respond discerningly to chemical cues.     

Predation by Pterostichus melanarius (Illiger) (Coleoptera: Carabidae) on immature Rhagoletis mendax Curran (Diptera: Tephritidae) in semi-field and field conditions

Practices that enhance abundance and diversity of generalist predators are often employed with the objective of improving biological control of insect pests. Ground beetles and other predators can prey on blueberry maggot, an important pest of blueberries, when mature larvae pupate in the ground. We conducted mesocosm and field experiments to determine if Pterostichus melanarius, a common predatory ground beetle, lowers maggot numbers in compost mulch or when predator and alternative prey abundances are manipulated. At background (field) densities of alternative prey, increasing densities of P. melanarius did not significantly reduce pest numbers in mesocosms containing compost or soil. When alternative prey were removed from compost, beetles reduced pest numbers by up to 35%. In field experiments, maggot numbers were higher when beetles and other predators were excluded from soil plots, but beetle exclusion had no effect in compost plots where both predator and alternative prey numbers were high. Our results indicate that there can be some reduction of blueberry maggot by P. melanarius and other potential predators when there are few alternative prey. However, despite attracting large numbers of predators compost mulch did not lead to a significant reduction in blueberry maggot; in fact, the high abundance of alternative food associated with compost appeared to interfere with beetle predation on blueberry maggot.     

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.     

Predator (<Emphasis Type="Italic">Carcinus maenas</Emphasis>) nonconsumptive limitation of prey (<Emphasis Type="Italic">Nucella lapillus</Emphasis>) feeding depends on prey density and predator cue type

Predators often have nonconsumptive effects (NCEs) on prey. For example, upon detection of predator cues, prey can reduce feeding activities to hamper being detected by predators. Previous research showed that waterborne chemical cues from green crabs (Carcinus maenas, predator) limit the dogwhelk (Nucella lapillus, prey) consumption of barnacles regardless of dogwhelk density, even though individual predation risk for dogwhelks decreases with conspecific density. Such NCEs might disappear with dogwhelk density if dogwhelks feed on mussels, as mussel stands constitute better antipredator refuges than barnacle stands. Through a laboratory experiment, we effectively found that crab chemical cues limit the per-capita consumption of mussels by dogwhelks at low dogwhelk density but not at high density. The combination of tactile and chemical cues from crabs, however, limited the dogwhelk consumption of mussels at both dogwhelk densities. The occurrence of such NCEs at both dogwhelk densities could have resulted from tactile cues indicating a stronger predation risk than chemical cues alone. Overall, the present study reinforces the notions that prey evaluate conspecific density when assessing predation risk and that predator cue type affects their perception of risk.     

Snail responses to cues produced by an invasive decapod predator

Abstract. Cues released by predators and injured prey often induce shifts in prey behavior that allow prey to evade predators, but also affect prey resource use. I investigated the effects of chemical and mechanical signals produced by injured snails (Physella gyrina) and predatory crayfish (Procambarus clarkii) on microdistributions of P. gyrina. In an initial experiment, I observed snail responses to the presence of a caged crayfish predator, to injured conspecifics, or to both. There were significant effects of time and the treatment × time interaction on the proportion of snails moving above the water line, with greater proportions of snails above the water line at night than during the day and with weak snail crawl‐out behavior being elicited by caged crayfish at night, but not during the day. In a second experiment, I examined snail microdistributions when exposed to crayfish confined to a small cage within each aquarium, crayfish confined to half of each aquarium, and crayfish ranging freely throughout each aquarium. Snails responded most strongly to free‐ranging crayfish by moving above the water line, but also demonstrated significant, but reduced, crawl‐out responses to crayfish confined to half of each aquarium; however, snails did not respond behaviorally to crayfish confined to small cages. In both experiments, there were marginally significant effects of unfed caged crayfish on the proportions of snail populations hiding under benthic shelters, with this response being the strongest at the start of the experiments but weak overall (with only 4–5% of P. gyrina responding in each experiment). These results indicate that cues (e.g., chemical or mechanical) produced by predators altered prey microdistributions, but that the exact prey responses (e.g., moving above the water line or into horizontal or benthic refugia) depended on the intensity and nature of cues.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Hydrodynamic mediation of predator-prey interactions: differential patterns of prey susceptibility and predator success explained by variation in water flow

In most shallow water marine systems, fluid movements vary on scales that may influence local community dynamics both directly, through changes in the abundance of species, and indirectly, by modifying important behaviors of organisms. We examined how differences in current speed affect the outcome of predator-prey interactions for two species of marine benthic predators (knobbed whelks, Busycon carica, and blue crabs, Callinectes sapidus) foraging on two common prey species (bay scallops, Argopecten irradians, and hard clams, Mercenaria mercenaria). The predators differ in their foraging strategies and prey in their potential escape responses. Predation by blue crabs, highly mobile predators/scavengers that rely upon chemical odors transported in the water column to locate prey, could be strongly affected by changes in current speed and turbulent mixing because their foraging strategy relies on a high degree of spatial integration of prey odor plumes. Whelks, slow moving, predatory gastropods that often forage with their bodies buried in the sediment, may be less susceptible to flow-induced distortion of prey odor plumes because their sluggish movements result in a high degree of temporal integration of prey odors. Bay scallops, relatively mobile bivalves capable of rapid short-distance swimming burst, and hard clams, sedentary bivalves, have been shown to respond to varying degrees to predator odors that are dispersed in the water column. Flow regime for the predator-prey experiments was manipulated in situ using large channels. Predation by blue crabs on both juvenile hard clams and bay scallops decreased with increases in water flow (0-12 vs. 0-30 cm s⁻¹). Whelk predation on bay scallops increased with increases in water flow, whereas predation by whelks on hard clams did not differ between flow regimes. For blue crabs movement decreased at periods of high water flow. Because blue crabs locate prey through chemolocation of water-borne cues, which are diluted rapidly at higher flows, decreases in foraging may result from the inability to successfully detect prey at enhanced flows. Differences in predation by whelks could not be explained by a similar mechanism. Visual observations of foraging whelks revealed no differences in whelk behavior between the two flow regimes. The pattern of higher whelk predation on scallops at enhanced flow is likely to be related to a flow-inhibiting ability of scallops to detect predator approach. Thus, flow enhancement interferes with three of the predator-prey systems but the effect on predator success depends on whether the predator or prey is most affected.     

Predation risk perception and food scarcity induce alterations of life-cycle traits of the mosquito Culex pipiens

Abstract.  1. Predators may affect prey populations by direct consumption, and by inducing defensive reactions of prey to the predation risk. Food scarcity frequently has effects on the inducible defences of prey, but no consistent pattern of food–predation risk interaction is known.
2. In this study the combined effect of food shortage and predation-risk perception in larvae of the mosquito Culex pipiens was investigated. Water exposed to the aquatic predator bug Notonecta glauca was used as a source of predation intimidation. Mosquito larvae were reared in three different media containing either no predator cues or the cues of N. glauca that had been fed on either C. pipiens larvae or on Daphnia magna . Food was provided in favourable or limited amount for these set-ups.
3. The results showed that chemical cues from the predators fed with prey's conspecifics caused a decreased survival, delayed pre-imaginal development, and reduction in body size of emerged mosquitoes, whereas chemical cues from predators fed with D. magna caused only delayed development. Food scarcity significantly exacerbates the negative effect of the predator cues on pre-imaginal development of C. pipiens . Effects of the cues on larval development and body size of imagoes are significantly stronger for females than for males.
4. The present study suggests that when food is limited, predators can affect population dynamics of prey not only by direct predation, but also by inducing lethal and sublethal effects due to perception of risk imposed by chemical cues. To understand the effects of predators on mosquito population dynamics, environmental parameters such as food deficiency should be considered.     

Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects

The effects of predators on the density of their prey can have positive indirect effects on the abundance of the preys resource via a trophic cascade. This concept has strongly influenced contemporary views of how communities are structured. However, predators also can transmit indirect effects by inducing changes in prey traits. We show that the mere presence of predator risk cues can initiate a trophic cascade in rocky shore tide pools. In large (mean surface area =9 m²), natural tide pools, we manipulated crab density and their foraging ability to examine the relative importance of lethal (density-mediated) and non-lethal (trait-mediated) predator effects to algal community development. We found that perceived predation risk reduced snail density as much as the direct predation treatment, showing that green crab predation was not an important factor regulating local snail density. Instead, snail emigration away from resident crabs appears to be the most important factor regulating local snail density. As a result, the abundance of ephemeral green algae was similar in the predation risk and direct predation treatments, suggesting that the consumption of snails by crabs plays a minimal role in mediating the trophic cascade. Increased attention to trait-mediated effects that are transmitted by predator-induced changes in prey behavior may change our view of how predators exert their strong influence on community structure.     

Poor phenotypic integration of blue mussel inducible defenses in environments with multiple predators

Aquatic prey encounter an array of threat cues from multiple predators and killed conspecifics, yet the vast majority of induced defenses are investigated using cues from single predator species. In most cases, it is unclear if odors from multiple predators will disrupt defenses observed in single-predator induction experiments. We experimentally compared the inducible defenses of the common marine mussel Mytilus edulis to waterborne odor from pairwise combinations of three predators representing two attack strategies. Predators included the sea star, Asterias vulgaris (= Asterias rubens ), and the crabs Carcinus maenas and Cancer irroratus . The mussels increased adductor muscle mass in response to cues from unfed Asterias (a predatory seastar that pulls mussel shells open) and increased shell thickness in response to unfed Carcinus, a predatory crab that crushes or peels shells. However, the mussels did not express either predator specific response when exposed to the combined cues of Asterias and Carcinus , and mussels did not increase shell thickness when exposed to cues from Cancer alone or any pairwise combination of the three predators. Shell closure or 'clamming up' did not occur in response to any predator combination. These results suggest that predator-specific responses to the Asterias and Carcinus are poorly integrated and cannot be expressed simultaneously. Simultaneous cues from multiple predators affect the integration of predator specific defenses and predator odors from functionally similar predators do not necessarily initiate similar defenses. Ultimately, the degree that prey can integrate potentially disparate defenses in a multiple predator environment may have ecological ramifications and represent a seldom explored facet of the evolution of inducible defenses.     

Temporal variation in behavioral responses to dietary cues from a gape‐limited predator in tadpole prey: A test of the phylogenetic relatedness hypothesis

The ability of prey to recognize and adequately respond to predators determines their survival. Predator‐borne, post‐digestion dietary cues represent essential information for prey about the identity and the level of risk posed by predators. The phylogenetic relatedness hypothesis posits that prey should respond strongly to dietary cues from closely related heterospecifics but respond weakly to such cues from distantly related prey, following a hierarchical pattern. While such responses have mostly been observed in prey at their first encounter with predators, whether prey maintain such hierarchical levels of investment through time remains unclear. We investigated this question by exposing Rhacophorus arboreus tadpoles to the non‐consumptive effect of gape‐limited newt predators Cynops pyrrhogaster that were fed one of five prey diets across a gradient of phylogenetic relatedness: frog tadpoles (Rhacophorus arboreus, Rhacophorus schlegelii, Pelophylax nigromaculatus, and Hyla japonica) and medaka fish (Oryzias latipes). Predators’ diet, time, and their interaction significantly influenced tadpole activity level. We found support for the phylogenetic relatedness hypothesis: Investments in defense were stronger to cues from tadpole diets than to cues from fish diet. However, such a hierarchical response was recorded only in the first four days following predator exposure, then gradually disappear by day 8 on which the tadpoles exhibited similar activity level across all predator treatments. The findings suggest that, at least under the threat of gape‐limited predators, prey use phylogenetic information to evaluate risk and appropriately invest in defense during early encounters with predators; however, energy requirements may prevent prey from maintaining a high level of defense over long exposure to predation risk.