Anti-predator responses of the intertidal crab Heterozius rotundifrons (Brachyura: Belliidae) in air and water

The intertidal crab Heterozius rotundifrons responds to tactile input, as occurs during a predation attempt, by hyper-extending all of its limbs and remaining in that posture for a variable length of time. We compared the duration of this anti-predator response: (1) in the day versus night (2) in two fluid media (air versus water) (3) after exposure to additional predator cues in one medium (air or water) and testing in the other medium (4) for crabs from different parts of the tidal range and (5) for females with and without eggs on their pleopods.?Crabs showed the posture at night as well as during the day. They also executed the posture when tested in air and extended the duration of the posture in air when they detected an additional predation-risk cue, shadows passing overhead. When crabs experienced input in one medium there was no effect on the duration of behavior shown in the other medium. Crabs from the lower portion of the intertidal showed a markedly longer duration of the limb-extended posture compared to crabs from the higher end of the tidal range of this crab. Berried females responded the same as females without eggs in both air and in water. Thus, crabs show this anti-predator behavior under a wide variety of conditions, but do not appear to transfer information received in one medium to behavior shown in the other media.     

Motion, not Shape, Facilitates Association of Predation Risk with Novel Objects by Fathead Minnows (Pimephales promelas)

Injury‐released chemical cues are reliable indicators of predation risk among many aquatic taxa. When a novel, neutral stimulus is presented in tandem with chemical cues from an injured conspecific, an association is formed between the novel stimulus and apparent risk. Learned recognition of predation risk is well documented for fathead minnows, Pimephales promelas. When minnows detect alarm cues in nature they are also potentially exposed to multiple environmental stimuli, few of which are likely to be relevant indicators of risk. How do minnows discern among candidate stimuli potentially associated with predation risk? Two possibilities are shape and motion. In this study, individual piscivore‐naïve minnows were presented simultaneously with conspecific chemical alarm cues and two stimulus objects. One object was a darkened tube with its long axis in the horizontal plane (fish‐like). The second object was a black disk. Following introduction of chemical alarm cues, one of the objects was raised and lowered repeatedly. After a single conditioning trial, minnows associated risk significantly more with the previously moving object than the previously stationary object, as indicated by reduced activity. Object shape had no significant effect on response intensity in test trials. Our data suggest that minnows have been selected to form aversive responses to moving objects at a site of recent predation because movement is a more predictable indicator of predator identity than shape.     

Alternative tactics and responses to conflicting inputs in the porcellanid crab Petrolisthes elongates

When animals receive stimuli associated with incompatible responses, they either show behaviour patterns relevant to just one input (hierarchical model) or show levels of responses intermediate in intensity (summation model). When animals have alternative responses to one category of input, the summation model can be followed.

Individuals of the porcellanid crab Petrolisthes elongates were exposed to food odours and then to alarm odours and the intensity of feeding behaviours recorded. With their chelipeds intact, crabs exposed to food and alarm odours showed intermediate levels of feeding. Following the induction of cheliped autotomy (thereby eliminating autotomy as an alternative response to predation risk), the crabs exposed to food and alarm odours showed a complete cessation of feeding responses. Thus elimination of an alternative response to elevated predation risk led to a switch from the summation model to the hierarchical model, as predicted.     

Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows ( Pimephales promelas ) and glowlight tetras ( Hemigrammus erythrozonus ) after single simultaneous pairings with conspecific chemical alarm cues

Fathead minnows, Pimephales promelas, and glowlight tetras, Hemigrammus erythrozonus, were tested for their ability to associate predation risk with novel auditory stimuli after auditory stimuli were presented simultaneously with chemical alarm cues. Minnows and tetras gave a fright response when exposed to skin extract (alarm cue) and an artificial auditory sound stimulus, but no response to water (control) and sound, indicating that they did not have a pre-existing aversion to the auditory stimulus. When retested with sound stimuli alone, minnows and glowlight tetras that had previously been conditioned with water and sound showed no response, but those that had been conditioned with alarm cues and sound exhibited antipredator behaviour (reduced activity) in response to the auditory cue. This is the first known demonstration of learned association of an auditory cue with predation risk, and raises questions about the role of sound in mediating predator-prey interactions in fishes.     

Antipredator Behaviour and Suppressed Aggression by Convict Cichlids in response to Injury-released Chemical Cues of Conspecifics but not to those of an Allopatric Heterospecific

In aquatic environments, chemical cues serve as an important source of information for the detection of predation risk. Here, we investigate the response of convict cichlids, Cichlasoma nigrofasciatum, to injury-released chemical cues. We exposed pairs of juvenile convict cichlids first to dechlorinated tap water (control), then later to one of two test stimuli: 1. chemical cues from injured convict cichlids; or 2. chemical cues from injured mosquito fish, Gambusia affinis. Gambusia are allopatric and phylogenetically unrelated to convict cichlids. Gambusia skin was used to control for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of test aquaria and time under a shelter object. In response to Gambusia skin, convict cichlids tended to increase time spent near the tank bottom but did not increase use of the shelter object. There was a trade-off between antipredator and agonistic behaviours. In response to convict cichlid cues, there was a significant reduction in the frequency of approaches and bites. Gambusia skin extract had no significant effect on aggressive behaviour. These data suggest a species-specific antipredator response to conspecific alarm pheromones in a New World cichlid fish and demonstrate a trade-off between predator avoidance and intraspecific aggression. Further, the presence of an alarm response in this model species sets the stage for the use of chemical cues as a research tool to manipulate predation risk in studies of the interaction between predation risk and reproductive behaviour.     

Predator recognition learning in rainbow darters Etheostoma caeruleum: specific learning and neophobia

This study investigated whether rainbow darters Etheostoma caeruleum can learn to recognize unfamiliar predators through the process of classical conditioning. Etheostoma caeruleum were conditioned by exposing them simultaneously to their chemical alarm cues (a known fright stimulus) and either chemical cues from larval ringed salamanders Ambystoma annulatum (unfamiliar predator) or to a blank water cue (control). Conditioning could result in either specific learning of the A. annulatum cue or increased wariness in response to any novel cue (neophobia). To distinguish between these possibilities, E. caeruleum in both groups were exposed to either A. annulatum cues alone or to chemical cues from western rat snakes Pantherophis obsoletus (novel cue) 2 days after conditioning. Treatment (A. annulatum‐conditioned) E. caeruleum, but not control E. caeruleum, showed a fright response when they were exposed to both the conditioned (A. annulatum) and novel (P. obsoletus) cues, indicating increased sensitivity to new stimuli. When E. caeruleum were retested after an additional 32 days, however, the fright response occurred only following exposure to the conditioned (A. annulatum) stimulus, indicating that specific learning of the A. annulatum cue had been retained whereas the neophobia to novel stimuli was temporary.     

Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges

The threat sensitivity hypothesis assumes that multiple cues from a predator should contribute in an additive way to determine the degree of risk-sensitive behaviour. The ability to use multiple cues in assessing the current level of predation risk should be especially important to prey exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds or mammals by hiding inside rock crevices, where they may encounter another predator, the smooth snake, Coronella austriaca. We investigated in the laboratory whether chemical cues may be important to wall lizards for detection of snakes. The greater tongue-flick rate and shorter latency to first tongue-flick in response to predator scents indicated that lizards were able to detect the snakes' chemical cues. We also investigated the use of different predatory cues by lizards when detecting the presence of snakes within refuges. We simulated successive predator attacks and compared the propensity of lizards to enter the refuge and time spent within it for predator-free refuges, refuges containing either only visual or chemical cues of a snake, or a combination of these. The antipredatory response of lizards was greater when they were exposed to both visual and chemical cues than when only one cue was presented, supporting the threat sensitivity hypothesis. This ability may improve the accuracy of assessments of the current level of predation risk inside the refuge. It could be especially important in allowing lizards to cope with threats posed by two types of predators requiring conflicting prey defences.     

Antipredator Behavior in Desmognathus ochrophaeus: Threat‐Specific Responses to Chemical Stimuli in a Foraging Context

Prey species may reduce the likelihood of injury or death by engaging in defensive behavior but often incur costs related to decreased foraging success or efficiency. To lessen these costs, prey may adjust the intensity or type of antipredator behavior according to the nature of the perceived threat. We evaluated the potential for threat‐sensitive responses by Allegheny Mountain dusky salamanders (Desmognathus ochrophaeus) exposed to chemical stimuli associated with predation by asking three questions: (1) Do individual D. ochrophaeus respond to chemical cues in a threat‐sensitive manner? (2) Do salamanders exhibit the same pattern of behavioral response while foraging? and (3) Is foraging efficiency reduced when focal individuals are exposed to stimuli from predators or predation events? In our first experiment, we evaluated salamander chemosensory movements (nose‐taps), locomotor activity (steps), and edge behavior in response to chemical stimuli from disturbed and injured conspecifics as well as predatory Gyrinophilus porphyriticus and found that individual D. ochrophaeus show a significant graded increase in nose‐taps when exposed to cues from conspecifics and a reduction in activity when exposed to the predator. In our second experiment, we again observed salamander responses to the same chemical stimuli but in this instance added five Drosophila prey to the test dishes. We found that salamanders exhibited a similar pattern of response to the chemical stimuli in the presence of prey, showing a graded increase in nose‐taps to cues from conspecifics and a reduction in activity when exposed to the predator. However, foraging efficiency (i.e. the proportion of successful strikes) did not vary significantly among treatments. Our data show that individual D. ochrophaeus detect and differentially respond to chemical stimuli associated with predation, but do not significantly reduce foraging efficiency. Overall, the type and relative intensity of these responses is largely unaffected by the presence of potential prey.     

Contingencies in the behaviour of the crab Heterozius rotundifrons

We recorded the responses of individual intertidal crabs, Heterozius rotundifrons, to stimuli presented singly and in combinations in the laboratory. Undisturbed crabs did not respond to the introduction of odour from a crushed conspecific but did respond strongly to food odour. Undisturbed crabs responded equally to food odour alone and a combination of food and odour from a crushed conspecific. When tactile stimulation was applied, as when the crab is grasped by a predator, individual H. rotunidfrons assumed a rigid, appendage-extended posture for several minutes. Tests with predatory fish showed that this catatonic posture is a very effective predator-defence mechanism. The duration of the catatonic state was decreased by the addition of food odour but increased by the addition of alarm odour (crushed conspecific) or the combination of alarm and food odours. Thus, which chemical stimulus was dominant was reversed by tactile input (i.e. dominance was contingent upon context). The effect of alarm odour on food odour responses lasted 4 h. Visual input in the form of a shadow passing over the crabs, either before or after tactile induction of the catatonic state, also increased the duration of that state. However, the duration of the catatonic state following exposure to both cues associated with danger (shadow+alarm odour) was similar to that of the control level. The crabs appeared to switch strategies when three cues associated with danger (tactile grasping, alarm odour and shadows) were detected, either simultaneously or over a 4-h period. The results illustrate the highly contingent nature of the behaviour of these crabs. Copyright 2000 The Association for the Study of Animal Behaviour.     

Avoidance behavior in two sympatric planaria species: effects of conspecific and heterospecific chemical alarm cues

In many aquatic animals, predator avoidance can be stimulated by chemical cues, including those released by injured prey (alarm cues). Alarm cues of both conspecific and heterospecific origin have been identified within several fish taxa, where phylogenetic conservation of the cue-response complex is common. Turbellarian flatworms (planaria) are among the simplest animals known to respond to chemical cues released by injured conspecifics. We examined how two locally sympatric planaria species respond to conspecific and heterospecific chemical cues using macerated tissue suspensions. Brown (Girardia tigrina) and black (Dugesia dorotocephala) planaria both exhibited avoidance behavior when presented conspecific cues. Despite a significant twofold difference in body size (black > brown), stimulus prepared from a single (1×) individual of either species elicited avoidance. Increasing brown planaria cue concentration by macerating two individuals (2×) produced a significant increase in conspecific avoidance. Heterospecific stimuli produced asymmetric results. Black planaria avoided the brown planaria stimulus, but only in the higher concentration (2×) trials. Brown planaria did not consistently exhibit avoidance of the black planaria stimulus and some brown subjects approached and consumed black planarian tissues. Our results expand the demonstrated occurrence of alarm cues among planaria and suggest that avoidance behavior can be mediated by multiple environmental and intrinsic factors in freshwater Turbellaria.     

The behavioural responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels

• 1 Experiments were designed to determine the relative importance of chemical and visual stimuli in eliciting predator avoidance behaviour in juvenile freshwater crayfish Pacifastacus leniusculus (Dana).
• 2 Crayfish placed in visual and/or chemical contact with one of two predators exhibited marked avoidance behaviour, spending less time walking and climbing and more time within shelters.
• 3 The combined effects of both visual and chemical stimuli increased crayfish shelter use and reduced walking and climbing activity to a greater degree than either stimulus when presented alone.
• 4 Crayfish exhibited avoidance behaviour in response to chemical stimuli during periods of light and darkness. Visual detection of predators elicited avoidance behaviour during the day.
• 5 It is suggested that the behavioural response of P. leniusculus to chemical stimuli reduces the likelihood of being detected by visual predators, and that chemical stimuli lower the response threshold for avoidance behaviour in crayfish reacting to visual stimuli. The adaptiviry of using chemical cues to detect predators is emphasized.

     

Larvae of cryptic species of Anopheles gambiae respond differently to cues of predation risk

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Acoustic stimuli from predators trigger behavioural responses in aggregate caterpillars

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

Detection of substrate-associated odour cues versus prey-associated cues by the oral veil in Tritonia diomedea

Our goal was to test two potential sensory roles for the oral veil in the nudibranch Tritonia diomedea (now synonymous with T. tetraquetra). First, we hypothesized this cephalic sensory organ could detect substrate-associated odours left behind by an odour plume flowing across sediment. In two experiments in a laboratory flow tank, however, T. diomedea did not show consistent crawling headings in response to either prey or predator odours associated with sediment substrate. In one of the experiments, the slugs did significantly decrease crawling speed in response to prey odours. Although slugs could thus detect at least some substrate-associated odours, these results suggest such cues are not used for navigation. We next considered the oral veil’s potential role in behaviours requiring responses to nearby cues. Our observations of animals before and after denervation of the oral veil suggest that, unsurprisingly, predatory bite-strikes do rely on sensory input from the oral veil. Overall, these data, combined with the results of earlier studies, are consistent with the oral veil detecting cues primarily from nearby stimuli (including both chemical and mechanical modalities), while having little or no role in detecting and responding to odour cues originating from distant sources used for navigation behaviour.     

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.     

Predatory fish sounds can alter crab foraging behaviour and influence bivalve abundance

The risk of predation can have large effects on ecological communities via changes in prey behaviour, morphology and reproduction. Although prey can use a variety of sensory signals to detect predation risk, relatively little is known regarding the effects of predator acoustic cues on prey foraging behaviour. Here we show that an ecologically important marine crab species can detect sound across a range of frequencies, probably in response to particle acceleration. Further, crabs suppress their resource consumption in the presence of experimental acoustic stimuli from multiple predatory fish species, and the sign and strength of this response is similar to that elicited by water-borne chemical cues. When acoustic and chemical cues were combined, consumption differed from expectations based on independent cue effects, suggesting redundancies among cue types. These results highlight that predator acoustic cues may influence prey behaviour across a range of vertebrate and invertebrate taxa, with the potential for cascading effects on resource abundance.     

Predation risk assessment by olfactory and visual cues in a coral reef fish

Assessment of predation risk is vital for the success of an individual. Primary cues for the assessment include visual and olfactory stimuli, but the relative importance of these sources of information for risk assessment has seldom been assessed for marine fishes. This study examined the importance of visual and chemical cues in assessing risk for the star goby, Asterropteryx semipunctatus. Visual and chemical cue intensities were used that were indicative of a high threat situation. The behavioural response elicited by both the visual cues of a predator (the rock cod, Cephalopholis boenak) and the chemical alarm cues from conspecifics were similar in magnitude, with responses including a decrease in feeding strikes and moves. A bobbing behaviour was exhibited when the predator was visible and not when only exposed to the chemical alarm cue. When visual and chemical cues were presented together they yielded a stronger antipredator response than when gobies were exposed solely to conspecific alarm cues. This suggests additivity of risk assessment information at the levels of threat used, however, the goby’s response is also likely to depend on the environmental and social context of the predator–prey encounter. This study highlights the importance of chemical cues in the assessment of predation risk for a coral reef fish.     

Are behavioural responses to predation cues linked across life cycle stages?

1. Prey organisms can perceive cues to predation hazard and adopt low‐risk behaviours to increase survival. Animals with complex life cycles, such as insects, can exhibit such anti‐predatory behaviours in multiple life stages. 2. Cues to predation risk may induce ovipositing females to choose habitats with low predation risk. Cues to predation risk may also induce larvae to adopt facultative behaviours that reduce risk of predation. 3. One hypothesis postulates that anti‐predation behaviours across adult and larval stages may be negatively associated because selection for effective anti‐predator behaviour in one stage leads to reduced selection for avoidance of predators in other stages. An alternative hypothesis suggests that selection by predation favours multi‐component defences, with both avoidance of oviposition and facultative adoption of low‐risk behaviours by larvae. 4. Laboratory and field experiments were used to determine whether defensive responses of adult and larval mosquitoes are positively or negatively associated. The study tested effects of waterborne cues from predatory Toxorhynchites theobaldi on oviposition choices and larval behaviours of three of its common prey: Culex mollis, Limatus durhamii and Aedes albopictus. 5. Culex mollis shows strong anti‐predator responses in both life stages, consistent with the hypothesis of a multi‐component behavioural defence. The other two species showed no detectable responses to waterborne predator cues in either adult or larval stages. Larvae of these unresponsive species were significantly more vulnerable to this predator than was C. mollis. 6. For these mosquitoes, species appear either to have been selected for multi‐component defences against predation or to act in ways that could be called predator‐naïve.     

Population Differences in Responses of Fathead Minnows (Pimephales promelas) to Visual and Chemical Stimuli from Predators

Fathead minnows (Cyprinidae: Pimephales promelas) from a population that is sympatric with predatory northern pike (Esocidae: Esox lucius) exhibited a fright reaction to the visual stimulus of a live northern pike significantly more often than minnows from a population that is allopatric with pike. The fright response included increased use of shelter, dashing and freezing. Minnows from the pike-sympatric population also exhibited a significantly greater fright response, measured as a reduction in activity, following exposure to chemical stimuli from pike (i.e. water from a tank that had contained a pike) than did minnows from the pike-allopatric population. There was no significant change in activity by minnows from either population following exposure to chemical stimuli from nonpiscivorous peacock gudgeons (Eleotridae: Tateurndina ocellicauda), suggesting that the difference between the two populations is specific to stimuli from pike rather than a general difference in response to chemical stimuli from heterospecific fishes. Fathead minnows apparently utilize at least a two-tiered predator recognition system that incorporates both visual and chemical cues.     

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.