A Laboratory study on the visual and chemical orientation of the gastropod Nerita Fulgurans Gmelin, 1791

Behavioural responses of the gastropod Nerita fulgurans Gmelin, 1791 to flat black rectangles and intraspecific mucus trails were measured in a circular arena. Snails were tested in water either in the presence or absence of chemicals generated from a predator gastropod, Chicoreus brevifrons (Lamarck, 1822). The test hypothesis was that this snail has different behavioural responses as result of visual and chemical cue integration. Nerita fulgurans has the capacity to orient to solid targets subtending angles larger than 10° and follow its own mucus trails. In water conditioned by the predator C . brevifrons , snails exhibited an avoidance response when 10°, 20° and 45° sectors were presented, demonstrating an integration of chemical and visual information. The simultaneous presentation of two orienting cues (black sectors and mucus trails) was tested to determine the nature of the interaction. When the two cues were oriented in the same direction there was no effect. When the two cues were presented from directions 180° apart a preference for visual cues over mucus trail cues was evident when the visual angle of the visual cue subtended angles greater than 90°. This result demonstrates a hierarchical usage of the orienting references.     

Orientation and Shape Discrimination in Juveniles and Adults of the Mangrove Crab Aratus pisonii (H. Milne Edwards, 1837): Effect of Predator and Chemical Cues

Behavioral responses of juveniles and adults of the mangrove crab Aratus pisonii (H. Milne Edwards, 1837) to black geometric shapes of equal surface area was measured. Crabs were tested either in presence or absence of chemicals generated from two common predator species, the portunid crab Callinectes ornatus Ordway, and the soapfish Haemulon aurolineatum Cuvier, 1830. The present study tested the hypothesis that A. pisonii (1) has the capacity to orient to visual cues; (2) it discriminates between different visual objects based on a combination of chemical and visual information and (3) this behavior changes with age. When presented with single black targets in background water, juveniles oriented toward all shapes. This behavioral response was interpreted as visual orientation toward potential shelter. Among shapes, juveniles showed preference for the vertical rectangle, probably due to the recognition of natural visual elements like mangrove roots. In predator conditioned water, juveniles exhibited a stronger response than in background water. Thus, juveniles were able to detect by odor the potential presence of predators. Change in responsiveness between adults and juveniles was also demonstrated.     

Orientation and Shape Discrimination in Juveniles and Adults of the Mangrove Crab Aratus pisonii (H. Milne Edwards, 1837): Effect of Predator and Chemical Cues

Behavioral responses of juveniles and adults of the mangrove crab Aratus pisonii (H. Milne Edwards, 1837) to black geometric shapes of equal surface area was measured. Crabs were tested either in presence or absence of chemicals generated from two common predator species, the portunid crab Callinectes ornatus Ordway, and the soapfish Haemulon aurolineatum Cuvier, 1830. The present study tested the hypothesis that A. pisonii (1) has the capacity to orient to visual cues; (2) it discriminates between different visual objects based on a combination of chemical and visual information and (3) this behavior changes with age. When presented with single black targets in background water, juveniles oriented toward all shapes. This behavioral response was interpreted as visual orientation toward potential shelter. Among shapes, juveniles showed preference for the vertical rectangle, probably due to the recognition of natural visual elements like mangrove roots. In predator conditioned water, juveniles exhibited a stronger response than in background water. Thus, juveniles were able to detect by odor the potential presence of predators. Change in responsiveness between adults and juveniles was also demonstrated.     

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.     

Predator Inspection Behaviour in a Characin Fish: an Interaction between Chemical and Visual Information?

Recent evidence suggests that predator inspection behaviour by Ostariophysan prey fishes is regulated by both the chemical and visual cues of potential predators. In laboratory trials, we assessed the relative importance of chemical and visual information during inspection visits by varying both ambient light (visual cues) and predator odour (chemical cues) in a 2 × 2 experimental design. Shoals of glowlight tetras (Hemigrammus erythrozonus) were exposed to a live convict cichlid (Archocentrus nigrofasciatus) predator under low (3 lux) or high (50 lux) light levels and in the presence of the odour of a cichild fed tetras (with an alarm cue) or swordtails (Xiphophorus helleri, with an alarm cue not recognized by tetras). Tetras exhibited threat‐sensitive inspection behaviour (increased latency to inspect, reduced frequency of inspection, smaller inspecting group sizes and increased minimum approach distance) towards a predator paired with a tetra‐fed diet cue, regardless of light levels. Similar threat‐sensitive inspection patterns were observed towards cichlids paired with a swordtail‐fed diet cue only under high light conditions. Our data suggest that chemical cues in the form of prey alarm cues in the diet of the predator, are the primary source of information regarding local predation risk during inspection behaviour, and that visual cues are used when chemical information is unavailable or ambiguous.     

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.     

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.     

Is there a fish alarm cue? Affirming evidence from a wild study

Chemical alarm cues released from injured tissue are not released under any other context and therefore reliably inform nearby prey of the presence of a predator. Laboratory and field studies have demonstrated that most aquatic taxa show antipredator responses to chemical alarm cues. Ostariophysan fish (e.g. minnows) possess specialized skin cells that contain an alarm chemical. Magurran et al. (1996, Proceedings of the Royal Society of London, Series B,263, 1551-1556) were the first to use underwater video to carefully document the behavioural response of free-ranging wild populations of minnows to minnow alarm cues. They found no evidence of an antipredator response, and challenged the assumption that the contents of these cells indicate risk in the field. They proposed that alarm responses are context dependent in that they are an artefact of enclosed environments such as laboratory aquaria and field traps. Here, we repeat their experiment on free-swimming field populations of littoral fish and report a significant decrease in the number of fish in areas where chemical alarm cues of blacknose shiners, Notropis heterolepis (Ostariophysi: Cyprinidae) were released. The effect of these chemical cues was equal in magnitude to the effect of the presentation of a model predator. The response to the approach of a model predator (visual cue) was intensified by pre-exposure to chemical alarm cues. We corroborated this interaction between chemical and visual indicators of predation risk in a laboratory study using glowlight tetras, Hemigrammus erythrozonus (Ostariophysi: Characidae). Response to the visual stimulus of a predator was significantly intensified by previous exposure to conspecific chemical alarm cues. We conclude that ostariophysan skin indeed contains an alarm cue that (1) informs nearby prey of imminent predation risk, (2) induces some form of antipredator behaviour in most contexts, and (3) affects subsequent behavioural responses to stimuli in other sensory modalities.     

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, <Emphasis Type="Italic">Umbra limi</Emphasis> (Kirtland 1840)

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory.     

Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues

The ability to accurately assess local predation risk is criticalto prey individuals, as it allows them to maximize threat-sensitivetrade-offs between predator avoidance and other fitness relatedactivities. A wide range of taxonomically diverse prey (includingmany freshwater fishes) relies on chemical alarm cues (alarmpheromones) as their primary information source for local riskassessment. However, the value of chemical alarm cues has beenquestioned due to the availability of additional sensory inputs(i.e., visual cues) and the lack of an overt antipredator responseunder conditions of low perceived risk. In this paper, we testthe hypothesis that chemical alarm cues at concentrations belowthe point at which they elicit an overt behavioral responsefunction to increase vigilance towards other sensory modalities(i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammuserythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide(the putative Ostariophysan alarm pheromone) did not exhibitan overt antipredator response in the absence of secondary visualcues (not different than the distilled water control). However,when exposed to the sight of a visually alarmed conspecific,they significantly increased the intensity of their antipredatorresponse (not different from shoals exposed to the suprathresholdalarm cue). This study demonstrates that prey may benefit fromresponding to low concentration alarm cues by increasing vigilancetowards secondary cues during local risk assessment, even inthe absence of an overt behavioral response. By increasing vigilancetowards secondary risk assessment cues in the presence of alow risk chemical cue, individuals are likely able to maximizethe threat-sensitive trade-offs between predator avoidance andother fitness related activities.     

There must be something in the water: assessing the behavioral responses of rusty crayfish (<Emphasis Type="Italic">Orconectes rusticus</Emphasis>) to fish and amphibian predator kairomones

Animals use chemical cues to find food, locate mates, and detect potential predators. Detecting cues in a risky environment can induce behavioral changes to increase survival. Rusty crayfish (Orconectes rusticus) reduce activity, increase refuge use, and make defensive displays after detecting fish predator cues. However, no studies have introduced amphibian cues. We investigated crayfish responses to hellbender salamander (Cryptobranchus alleganiensis, a dominant predator of crayfish) cues and compared these to responses to largemouth bass (Micropterus salmoides) cues. Largemouth bass occur sympatrically with hellbenders and are known to induce distinct responses in rusty crayfish. We randomly assigned crayfish to predator cue and conspecific alarm cue combinations and recorded frozen behavior, appendage movement, locomotion, and refuge use. We found crayfish increased their proportion of time spent frozen and reduced their proportion of time spent active in the tank when exposed to either predator cue. Moreover, these responses were magnified when crayfish were exposed to predator cues in combination with conspecific alarm cues. Our experiment demonstrates evidence in support of the crayfish’s ability to detect and appropriately respond to predator cues alone and in combination with conspecific alarm cues. Future work should investigate the effects of these behavioral changes on trophic dynamics in a natural system.     

Predator-induced reaction patterns of landlocked <Emphasis Type="Italic">Galaxias maculatus</Emphasis> to visual and chemical cues

Anti-predator behaviour often represents a trade-off between the benefits of reducing predation risk and the drawbacks of limiting access to resources (e.g. food availability, mating and nesting sites). The effectiveness of avoidance behaviour relies on the ability to detect predator cues, which may provide reliable information on predation risk. Using controlled laboratory experiments, we studied the relative importance of visual and chemical cues in the triggering of anti-predator responses in Galaxias maculatus, where Oncorhyncus mykiss was used as the predator. Metabolic cost was also estimated, measured as oxygen consumption. Exposure to different types of predator cue induced diverse behavioural responses in G. maculatus. Detection of the exotic predator, using both visual and chemical stimuli, resulted in reduced G. maculatus swimming activity and changes in respiratory rate.     

Anemonefishes rely on visual and chemical cues to correctly identify conspecifics

Organisms rely on sensory cues to interpret their environment and make important life-history decisions. Accurate recognition is of particular importance in diverse reef environments. Most evidence on the use of sensory cues focuses on those used in predator avoidance or habitat recognition, with little information on their role in conspecific recognition. Yet conspecific recognition is essential for life-history decisions including settlement, mate choice, and dominance interactions. Using a sensory manipulated tank and a two-chamber choice flume, anemonefish conspecific response was measured in the presence and absence of chemical and/or visual cues. Experiments were then repeated in the presence or absence of two heterospecific species to evaluate whether a heterospecific fish altered the conspecific response. Anemonefishes responded to both the visual and chemical cues of conspecifics, but relied on the combination of the two cues to recognize conspecifics inside the sensory manipulated tank. These results contrast previous studies focusing on predator detection where anemonefishes were found to compensate for the loss of one sensory cue (chemical) by utilizing a second cue (visual). This lack of sensory compensation may impact the ability of anemonefishes to acclimate to changing reef environments in the future.

     

Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish?

Carbon dioxide (CO₂) levels in the atmosphere and surface ocean are rising at an unprecedented rate due to sustained and accelerating anthropogenic CO₂ emissions. Previous studies have documented that exposure to elevated CO₂ causes impaired antipredator behavior by coral reef fish in response to chemical cues associated with predation. However, whether ocean acidification will impair visual recognition of common predators is currently unknown. This study examined whether sensory compensation in the presence of multiple sensory cues could reduce the impacts of ocean acidification on antipredator responses. When exposed to seawater enriched with levels of CO₂ predicted for the end of this century (880 μatm CO₂), prey fish completely lost their response to conspecific alarm cues. While the visual response to a predator was also affected by high CO_2, it was not entirely lost. Fish exposed to elevated CO_2, spent less time in shelter than current‐day controls and did not exhibit antipredator signaling behavior (bobbing) when multiple predator cues were present. They did, however, reduce feeding rate and activity levels to the same level as controls. The results suggest that the response of fish to visual cues may partially compensate for the lack of response to chemical cues. Fish subjected to elevated CO₂ levels_, and exposed to chemical and visual predation cues simultaneously, responded with the same intensity as controls exposed to visual cues alone. However, these responses were still less than control fish simultaneously exposed to chemical and visual predation cues. Consequently, visual cues improve antipredator behavior of CO₂ exposed fish, but do not fully compensate for the loss of response to chemical cues. The reduced ability to correctly respond to a predator will have ramifications for survival in encounters with predators in the field, which could have repercussions for population replenishment in acidified oceans.     

Testing the Threat‐Sensitive Hypothesis with Predator Familiarity and Dietary Specificity

In a system with multiple predators, the threat‐sensitive predator avoidance hypothesis predicts that prey respond differently to predators relative to the risks each poses (e.g., degree of dietary specialization). Aquatic animals often rely heavily on detecting predators via chemical cues (kairomones) and respond with a suite of behaviors including detection and avoidance. However, little is known about how animals respond to kairomones of specialist versus generalist predators. In laboratory experiments, we compared behavioral responses of a poorly studied aquatic salamander, the greater siren (Siren lacertina), to cues from specialist and generalist predator snakes to evaluate threat‐sensitive responses. Sirens exhibited a novel behavior (gill‐flushing) most often in the presence of specialist predator cues. Avoidance behavior (reversing direction following cue detection) was higher in response to specialist predator and novel animal control cues and lowest in response to generalist predator cues. An intermediate response to the animal control, an unfamiliar amphibian predator, indicated that sirens respond cautiously to a novel cue. The gradient of observed responses to different snake cues indicates that sirens may be evaluating predation potential of animals based on their foraging specificity and familiarity.     

Interacting Effects of Leg Autotomy and Exposure to Predator Cues on Survival in A Wolf Spider (<Emphasis Type="Italic">Pardosa valens</Emphasis>)

Chemical cues from predators (kairomones) are used by many aquatic and terrestrial animals when deciding on behavioral responses to predation threats. These responses may also be affected by the animal’s physiological state (e.g., nutrition level, parasitism, or prior injury), which could alter normal responses to kairomones. In this study, we examined effects of leg autotomy (the voluntary sacrifice of a leg) on subsequent responses to predator chemical cues in females of the riparian-zone wolf spider Pardosa valens. In a fully-crossed design, spiders with all legs intact or with one leg removed were exposed to one of two cue treatments for 90 min: a control (no predator cue) or one with chemical cues (silk and excreta) from a larger sympatric wolf spider, Rabidosa santrita. We then introduced an R. santrita into each container, and recorded subsequent survival of P. valens. Survivorship was significantly higher for individuals previously exposed to predator cues than for those in the control group; however, autotomy had no effect on survivorship, which was similar for both intact and autotomized spiders in both the predator-cue and control treatments. In addition, although P. valens were more likely to be found off the substrate than on it when the predator was added in each of the four treatment pairings, this initial position did not influence survivorship. These results therefore indicate that P. valens can behaviorally respond to predator kairomones in ways that reduce their risk of predation, but that this response is unaffected by the prior sacrifice of a leg.     

Effects of Sibship and the Presence of Multiple Predators on the Behavior of Green Frog (Rana clamitans) Tadpoles

In nature, prey are exposed to multiple predators simultaneously. We examined the effects of the cues of two potential predators, mosquitofish and odonate larvae, individually and in combination on the behavior of green frog (Rana clamitans) tadpoles. In addition to examining the behavioral response of green frog tadpoles to multiple predators, we examined variation in behavior among tadpoles from different egg masses (i.e. different sibships). Sibships differed in activity level and there was a significant predator cue by sibship interaction. Two sibships were relatively more active in the control and odonate predator cue treatments but showed reduced activity in treatments containing mosquitofish cues, whereas the remaining sibships showed consistently low levels of activity in all predator cue treatments, including the control. The use of the vegetated side of the aquarium did not differ between tadpoles exposed to the different predator cues. Sibship had no effect on tadpoles’ use of the vegetated side of the aquarium, and there was no interaction between sibship and predator cue. Our results suggest that green frogs did not respond to simultaneous exposure to multiple predator cues any differently than they did to exposure to individual predator cues. More importantly, our results suggest variation, possibly genetically based, in behavioral responses of tadpoles to predators, and thus selection on these behaviors is possible. Of particular interest is that there was variation in behavioral responses to a non‐native predator (Gambusia affinis), suggesting an evolutionary response to an invasive predator is possible.     

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.     

Eastern bluebirds Sialia sialis do not avoid nest boxes with chemical cues from two common nest predators

Chemodetection of common nest predators may be advantageous for nesting birds; however, few studies have examined the ability of songbirds to detect chemical odors from predators. Thus, in 2002, we presented eastern bluebirds Sialia sialis with pairs of nest boxes; one box in the pair was regularly scented with chemical cues from a common nest predator, the black rat snake Elaphe obsoleta , and the other with a neutral cue. In 2004, we again presented bluebirds with pairs of boxes, one scented with chemical cues from a different nest predator, the deer mouse Peromyscus maniculatus , and the other with a neutral scent. Although human females were able to correctly distinguish paper laced with predator cues from paper with neutral cues, bluebirds were as likely to lay eggs in boxes with predator cues as in boxes with neutral cues. While it remains possible that bluebirds may detect scent from potential nest predators, it appears that the presence of these chemical cues does not ultimately influence selection of nest sites.     

Differences in cue-dependent spatial navigation may be revealed by in-depth swimming analysis

Several factors can influence allocentric navigation in the Morris water maze (MWM), including the number of available distal visual cues. Using in-depth analytical measures investigating platform-based and swimming behaviour, we examine and compare animals exposed to either one or three distal visual cues during MWM acquisition. We demonstrate that, although animals exposed to one cue can acquire the task as well as those in a multiple cue condition, several subtle differences between the groups’ swimming behaviours are noted. Both groups actively use cues to guide them to the platform, but changing the number of cues alters the animals’ patterns of behaviour, wherein exposure to a single cue leads to a simpler strategy in which the cue appears to act as a beacon for navigation.