Responses of larval dragonflies to conspecific and heterospecific predator cues

Abstract.  1. In cannibalistic populations, smaller individuals are subject to predation by larger conspecifics, and small individuals commonly alter their behaviour in response to cannibals. Little is known, however, about the underlying cues that trigger such responses and how the behavioural responses to conspecific cannibals differ from heterospecific predators.
2. This study tests which cues are used for the detection of conspecific predators in the larva of the dragonfly Plathemis lydia and how the behavioural response to cannibals differed from the response to heterospecific predators.
3. Individuals were exposed to chemical cues, visual cues, and a combination of both cues from conspecifics as well as no predator and heterospecific predator controls during which their activity and feeding rates were observed.
4. Individuals increased their activity, spatial movement and feeding behaviour in response to either visual or chemical cues from conspecific predators, which was opposite to responses displayed with cues from heterospecific predators. Interestingly, the responses to visual and chemical cues from conspecifics combined were weaker than to either cue in isolation and similar to the no cue control.
5. The results clearly indicate that individuals are able to use chemical and visual cues to detect even very subtle differences in phenotype of conspecific predators.
6. The opposite response in behaviour when exposed to conspecific cannibals vs. heterospecific predators suggests that the presence of cannibals will increase the mortality risk of small individuals due to heterospecific predation. This risk-enhancement is likely to have important consequences for the dynamics of predator–prey interactions.     

Predator-induced neophobia in juvenile cichlids

Predation is an important but often fluctuating selection factor for prey animals. Accordingly, individuals plastically adopt antipredator strategies in response to current predation risk. Recently, it was proposed that predation risk also plastically induces neophobia (an antipredator response towards novel cues). Previous studies, however, do not allow a differentiation between general neophobia and sensory channel-specific neophobic responses. Therefore, we tested the neophobia hypothesis focusing on adjustment in shoaling behavior in response to a novel cue addressing a different sensory channel than the one from which predation risk was initially perceived. From hatching onwards, juveniles of the cichlid Pelvicachromis taeniatus were exposed to different chemical cues in a split-clutch design: conspecific alarm cues which signal predation risk and heterospecific alarm cues or distilled water as controls. At 2 months of age, their shoaling behavior was examined prior and subsequent to a tactical disturbance cue. We found that fish previously exposed to predation risk formed more compact shoals relative to the control groups in response to the novel disturbance cue. Moreover, the relationship between shoal density and shoal homogeneity was also affected by experienced predation risk. Our findings indicate predator-induced, increased cross-sensory sensitivity towards novel cues making neophobia an effective antipredator mechanism.     

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

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

Survival Benefit to Antipredator Behavior in the Amphipod Gammarus minus (Crustacea: Amphipoda) in Response to Injury-released Chemical Cues from Conspecifics and Heterospecifics

A wide range of aquatic taxa use environmental chemical cues for the assessment of predation risk. We examined whether Gammarus minus (Crustacea: Amphipoda) exhibit antipredator behavior in response to injury-released chemicals from conspecifics or heterospecifics (Crustacea: Isopoda). We then examined whether behavioral responses to these cues conferred survival benefits to the amphipods. In the first part of this study, we tested the behavioral response of G. minus to the following treatments: 1. water containing injury-released cues of conspecifics; 2. water containing injury-released cues of a sympatric isopod crustacean, Lirceus fontinalis; or 3. water containing no cues (control). Relative to the control, Gammarus responded to the conspecific cue by moving to the substratum and decreasing activity. In contrast, Gammarus responded to the heterospecific cue by moving up into the water column and increasing activity. In the second part of this study, we tested if the behavioral response to these cues confers a survival benefit to Gammarus when exposed to a predator. A green sunfish ( Lepomis cyanellus ) was retained behind a partition in the test tanks. Two minutes after the introduction of the chemical cues in the first test, the barrier was lifted and predation events recorded. Relative to the control, the time to the first attack increased for Gammarus exposed to conspecific cues and decreased for those exposed to heterospecific cues. These data indicate that Gammarus distinguish between chemical cues from conspecific and heterospecific crustaceans, and that the antipredator response to conspecific cues confers a fitness benefit (i.e. increased survival due to increased time to the first attack).     

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.     

An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni

Mate choice is context dependent, but the importance of current context to interspecific mating and hybridization is largely unexplored. An important influence on mate choice is predation risk. We investigated how variation in an indirect cue of predation risk, distance to shelter, influences mate choice in the swordtail Xiphophorus birchmanni, a species which sometimes hybridizes with X. malinche in the wild. We conducted mate choice experiments to determine whether females attend to the distance to shelter and whether this cue of predation risk can counteract female preference for conspecifics. Females were sensitive to shelter distance independent of male presence. When conspecific and heterospecific X. malinche males were in equally risky habitats (i.e., equally distant from shelter), females associated primarily with conspecifics, suggesting an innate preference for conspecifics. However, when heterospecific males were in less risky habitat (i.e., closer to shelter) than conspecific males, females no longer exhibited a preference, suggesting that females calibrate their mate choices in response to predation risk. Our findings illustrate the potential for hybridization to arise, not necessarily through reproductive "mistakes", but as one of many potential outcomes of a context-dependent mate choice strategy.     

Prey risk assessment depends on conspecific density

In many systems, the number of prey killed by predators increases with prey density. This in turn generates higher levels of the indirect signals that prey use to assess predation risk. A model developed by Peacor (2003) showed that prey that respond to predator cues without accounting for conspecific density will consistently over‐ or under‐estimate risk and therefore invest improperly in anti‐predator defense. We tested this model using Rana temporaria tadpoles as prey and Aeshna cyanea dragonfly larvae as predators. As assumed by the model, prey reduced risky activity with increasing concentrations of predator kairomones and increased activity at high prey density. However, prey did not react to changes in cue or density if the ratio of cue‐to‐density remained constant. Prey therefore monitored their per capita risk, strongly supporting Peacor's model.     

Alarm cue induces an antipredator morphological defense in juvenile Nicaragua cichlids Hypsophrys nicaraguensis

Olfactory cues that indicate predation risk elicit a number of defensive behaviors in fishes, but whether they are sufficient to also induce morphological defenses has receivedlittle attention. Cichlids are characterized by a high level of morphological plasticity during development, and the few species that have been tested do exhibit defensive behaviors when exposed to alarm cues released from the damaged skin of conspecifics. We utilized young juvenile Nicaragua cichlids Hypsophrys nicaraguensis to test if the perception of predation risk from alarm cue (conspecific skin extract) alone induces an increased relative body depth which is a defense against gape-limited predators. After two weeks of exposure, siblings that were exposed to conspecific alarm cue increased their relative body depth nearly double the amount of those exposed to distilled water (control) and zebrafish Danio rerio alarm cue. We repeated our measurements over the last two weeks (12 and 14) of cue exposure when the fish were late-stage juveniles to test if the rate of increase was sustained; there were no differences in final dimensions between the three treatments. Our results show that 1) the Nicaragua cichlid has an innate response to conspecific alarm cue which is not a generalized response to an injured fish, and 2) this innate recognition ultimately results in developing a deeper body at a stage of the life history where predation risk is high [Current Zoology 56 (1): 36-42, 2010].     

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.     

Social Context Influences the Antipredator Behaviour of Fathead Minnows to Chemical Alarm Cues

Prey fishes, like many organisms under fluctuating predation threat, rely on multiple sources of information to accurately gauge current risk. This includes the use of chemical cues such as alarm cues from damaged conspecifics or familiar heterospecifics, as well as the odour of known predators. While each fish is well equipped with its own array of sensory abilities, they should also be alert to the behaviours of nearby neighbours who may have information they lack. In the present study, we tested the ability of fathead minnows to use social cues in combination with the odour of damaged conspecifics and heterospecifics to mediate the assessment of predation risk. Specifically, we tested whether the presence of a shoal of conspecifics or familiar heterospecifics would significantly change a minnow's antipredator behaviour when exposed to the odour of a damage‐release cue from a conspecific or ecologically similar heterospecific. The results of our study showed a significant interaction between the damage‐release cues to which the minnows were exposed and the presence/absence of shoalmates. These findings have important implications for the design of future investigations of antipredator responses because most studies of group‐living prey have been conducted on solitary subjects.     

Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.     

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.     

Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey

The mere presence of predators (i.e., predation risk) can alter consumer physiology by restricting food intake and inducing stress, which can ultimately affect prey‐mediated ecosystem processes such as nutrient cycling. However, many environmental factors, including conspecific density, can mediate the perception of risk by prey. Prey conspecific density has been defined as a fundamental feature that modulates perceived risk. In this study, we tested the effects of predation risk on prey nutrient stoichiometry (body and excretion). Using a constant predation risk, we also tested the effects of varying conspecific densities on prey responses to predation risk. To answer these questions, we conducted a mesocosm experiment using caged predators (Belostoma sp.), and small bullfrog tadpoles (Lithobates catesbeianus) as prey. We found that L. catesbeianus tadpoles adjust their body nutrient stoichiometry in response to predation risk, which is affected by conspecific density. We also found that the prey exhibited strong morphological responses to predation risk (i.e., an increase in tail muscle mass), which were positively correlated to body nitrogen content. Thus, we pose the notion that in risky situations, adaptive phenotypic responses rather than behavioral ones might partially explain why prey might have a higher nitrogen content under predation risk. In addition, the interactive roles of conspecific density and predation risk, which might result in reduced perceived risk and physiological restrictions in prey, also affected how prey stoichiometry responded to the fear of predation.     

Overriding the oddity effect in mixed-species aggregations: group choice by armored and nonarmored prey

Because "odd" individuals often suffer disproportionately highrates of predation, solitary individuals should join groupswhose members are most similar to themselves in appearance.We examined group-choice decisions by individuals in armoredand nonarmored species and predicted that either (1) the oddityeffect would result in preference for conspecific groups forsolitary individuals of both species, or (2) individuals inthe armored species would prefer to associate with groups containingindividuals of the more vulnerable species. Armored brook sticklebacks(Culaea inconstans) and nonarmored fathead minnows (Pimephalespromelas) have the same predators and often occur together instreams. In mixed-species shoals, yellow perch (Perca flavescens)attacked minnows earlier and more often than sticklebacks. Wetested whether solitary minnows and sticklebacks preferred toassociate with conspecific or heterospecific shoals under conditionsof both low and high predation risk. When predation risk washigh, minnows preferred to associate with conspecifics overheterospecifics, as predicted by the oddity effect. In contrast,sticklebacks preferentially associated with groups of minnowsover groups of conspecifics when predation risk was high. Whenpredation risk was low, solitary individuals of both speciespreferentially associated with conspecific over heterospecificshoals. Stickleback shoal choices under low-risk conditionsmay have been influenced by interspecific competition for food.In feeding experiments, minnows were more efficient foragersthan sticklebacks, so it should benefit sticklebacks to avoidminnows unless predation risk is high. Therefore, for armoredprey, the benefits of associating with more vulnerable preyappear to override the costs of both the oddity effect and foodcompetition when predation risk is high.     

Innate responses to conspecific and heterospecific alarm cues in the endangered eastern cape redfin Pseudobarbus afer

We examined innate responses to conspecific and heterospecific alarm cues in a small cyprinid minnow, the Eastern Cape redfin Pseudobarbus afer. We found that redfins respond to conspecific skin extract, which contains alarm chemicals, and showed that their preferred response is to hide in refugia. Redfins also respond to skin extract from an allopatric, distantly related minnow species, the chubbyhead barb Enteromius anoplus indicating that neither sympatry nor close phylogenetic relationships are necessary for recognition of heterospecific alarm cues. Although both conspecific and heterospecific alarm cues induced similar responses, the response to heterospecific cues was less intense. This may be explained by a trade-off between selection to maximise threat recognition and selection to avoid the costs of responding to irrelevant cues, or by differences in chemical structures of alarm cues between species. These findings have implications for the conservation of this Endangered fish species and for freshwater fishes throughout Africa.     

Non-additivity among multiple cues of predation risk: a behaviorally-driven trophic cascade between owls and songbirds

Non-lethal effects of predators on prey are initiated in the form of responses to direct and indirect cues of predation risk. Like their lethal equivalents, non-lethal effects may affect species further down the food web initiating a behaviorally-driven trophic cascade. I presented a direct cue of predation risk, owl vocalizations, to white-footed mice ( Peromyscus leucopus ) during either a new or full moon (indirect cue). Mice reduced their activity in space by nearly two-thirds in response to playbacks of owl vocalizations during a full moon. However, neither moonlight (full vs new) nor the presence/absence of owl calls had an effect on space use when each cue varied singly. Previous studies have demonstrated a tight correlation between spatial activity in mice as used in the current experiment and nest predation rates on ground-nesting birds. Because moonlight is a ubiquitous deterrent of activity in nocturnal rodents I used of long-term nesting records the veery ( Catharus fuscescens ) to test whether nest predation rates were correlated negatively with moonlight. For half the lunar cycle (∼full moon to new moon) predation rates decreased with moonlight as predicted. During the second half of the lunar cycle predation and moonlight did not correlate as expected, but this was likely due to the depletion of vulnerable nests after a period of in which predation rates were at their maximum near the full moon. These studies suggest that the non-lethal effects of predatory risk on mice (i.e. changes in space use) cascade to affect their prey. Through the mechanism of reduced space use by rodents, perceived predation risk has the potential to significantly and indirectly affect songbird nest predation rates.     

Behavioral plasticity in an invaded system: non-native whelks recognize risk from native crabs

Inducible defenses have the potential to affect both invasion success and the structure of invaded communities. However, little is known about the cues used for risk-recognition that influence the expression of inducible defenses in invasive prey, because they involve a novel threat. In laboratory experiments, we investigated behavioral defenses induced by a native crab on two invasive oyster drills (marine whelks Urosalpinx cinerea and Ocinebrina inornata). Both drills hid more often and reduced their feeding rates when they detected predators consuming conspecific prey. Examination of the responses of U. cinerea to specific cue sources (predator kairomones, conspecific alarm cues) indicated that this species had the strongest responses to cues from injured conspecifics, but that it did recognize the novel crab predator. Our observation of native predator (per se) recognition by an invasive marine prey is novel. In addition, we observed that neither species of drill reduced their defensive behavior to reflect predation risk shared by a group of prey. The lack of density dependence in risk-assessment could cause populations of invasive prey to transmit both quantitatively and qualitatively different community effects over the course of an invasion as abundance changes. Together, these findings demonstrate several ways that the risk-assessment strategies could be important in establishment and post-establishment dynamics of invasive prey.     

Attracted to the enemy: Aedes aegypti prefers oviposition sites with predator-killed conspecifics

Oviposition habitat choices of species with aquatic larvae are expected to be influenced by both offspring risk of mortality due to predation, and offspring growth potential. Aquatic predators may indirectly influence growth potential for prey by reducing prey density and, for filter-feeding prey, by increasing bacterial food for prey via added organic matter (feces, partially eaten victims), creating the potential for interactive effects on oviposition choices. We tested the hypothesis that the mosquito Aedes aegypti preferentially oviposits in habitats with predatory Toxorhynchites larvae because of indirect effects of predation on chemical cues indicating bacterial abundance. We predicted that A. aegypti would avoid oviposition in sites with Toxorhynchites, but prefer to oviposit where bacterial food for larvae is abundant, and that predation by Toxorhynchites would increase bacterial abundances. Gravid A. aegypti were offered paired oviposition sites representing choices among: predator presence; the act of predation; conspecific density; dead conspecific larvae; and bacterial activity. A. aegypti preferentially oviposited in sites with Toxorhynchites theobaldi predation, and with killed conspecific larvae, but failed to detect preferences for other treatments. The antibiotic tetracycline eliminated the strongest oviposition preference. Both predation by Toxorhynchites and killed larvae increased bacterial abundances, suggesting that oviposition attraction is cued by bacteria. Our results show the potential for indirect effects, like trophic cascades, to influence oviposition choices and community composition in aquatic systems. Our results suggest that predators like Toxorhynchites may be doubly beneficial as biocontrol agents because of the attraction of ovipositing mosquitoes to bacterial by-products of Toxorhynchites feeding.     

Macro- and micro-habitat selection of small rodents and their predation risk perception under a novel invasive predator at the southern end of the Americas

Invasive predators are responsible for the extinction of numerous island species worldwide. The naïve prey hypothesis suggests that the lack of co-evolutionary history between native prey and introduced predators results in the absence of behavioral responses to avoid predation. The lack of terrestrial mammal predators is a core feature of islands at the southern end of the Americas. Recently, however, the American mink (Neovison vison) established as a novel terrestrial predator, where rodents became a main portion of its diet. Here, we investigated on Navarino Island, Chile, macro- and micro-habitat selection of small rodents using Sherman traps. Additionally, we experimentally tested behavioral responses of small rodents to indirect cues of native raptorial predation risk (vegetation cover) and direct cues of novel mink predation risk (gland odor) using Sherman traps and foraging trays (giving-up density (GUD)). At the macro-habitat level, we detected native rodents of the species Abrothrix xanthorhinus and Oligoryzomys longicaudatus and the exotic Mus musculus. In general, rodents preferred scrubland habitats. At the micro-habitat level, we only captured individuals of A. xanthorhinus. They preferred covered habitats with tall vegetation. GUD increased in opened areas (riskier for raptorial predation) regardless of the presence or not of mink odor. These results suggest that A. xanthorhinus can perceive predation risk by raptors, but not by mink, results that accord with the hypothesis that co-evolutionary history is important for rodents to develop antipredator behavior. Given that these rodents represent an important proportion of mink diet, the low abundances together with the apparent lack of antipredator response raise conservation concerns for the small rodent populations inhabiting the southernmost island ecosystems of the Americas.