Learned Recognition of Intraspecific Predators in Larval Long-Toed Salamanders Ambystoma macrodactylum

The ability of prey to detect predators and respond accordingly is critical to their survival. The use of chemical cues by animals in predator detection has been widely documented. In many cases, predator recognition is facilitated by the release of alarm cues from conspecific victims. Alarm cues elicit anti‐predator behavior in many species, which can reduce their risk of being attacked. It has been previously demonstrated that adult long‐toed salamanders, Ambystoma macrodactylum, exhibit an alarm response to chemical cues from injured conspecifics. However, whether this response exists in the larval stage of this species and whether it is an innate or a learned condition is unknown. In the current study, we examined the alarm response of naïve (i.e. lab‐reared) larval long‐toed salamanders. We conducted a series of behavioral trials during which we quantified the level of activity and spatial avoidance of hungry and satiated focal larvae to water conditioned by an injured conspecific, a cannibal that had recently been fed a conspecific or a non‐cannibal that was recently fed a diet of Tubifex worms. Focal larvae neither reduced their activity nor spatially avoided the area of the stimulus in either treatment when satiated, and exhibited increased activity towards the cannibal stimulus when hungry. We regard this latter behavior as a feeding response. Together these results suggest that an anti‐predator response to injured conspecifics and to cannibalistic conspecifics is absent in naïve larvae. Previous studies have shown that experienced wild captured salamanders do show a response to cannibalistic conspecifics. Therefore, we conducted an additional experiment examining whether larvae can learn to exhibit anti‐predator behavior in response to cues from cannibalized conspecifics. We exposed larvae to visual, chemical and tactile cues of stimulus animals that were actively foraging on conspecifics (experienced) or a diet of Tubifex (naïve treatment). In subsequent behavioral treatments, experienced larvae significantly reduced their activity compared to naive larvae in response to chemical cues of cannibals that had recently consumed conspecifics. We suggest that this behavior is a response to alarm cues released by consumed conspecifics that may have labeled the cannibal. Furthermore, over time, interactions with cannibals may cause potential prey larvae to learn to avoid cannibals regardless of their recent diet.     

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.     

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.

     

Predation Cues in Solitary bee Nests

Predation at the nesting site can significantly affect solitary bees’ reproductive success. We tested female red mason bees’ (Osmia bicornis L.) acceptance of potential nesting sites, some of which were marked with cues coming from predated conspecifics (crushed bees) or from a predator itself (rodent excreta). In our experiment, females did not avoid nests marked with either of the two predator cues. We suggest that bee females do not recognize these two cues as risky. Alternatively, costs of abandoning natal aggregation might be too high compared with any perceived predation risk of staying. Moreover, the presence of crushed bees can provide positive information about the presence of conspecifics and, possibly, information about a nesting aggregation that may be preferred by bees when choosing a nesting site.     

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.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Conspecific and heterospecific information use in bumblebees

Heterospecific social learning has been understudied in comparison to interactions between members of the same species. However, the learning mechanisms behind such information use can allow animals to be flexible in the cues that are used. This raises the question of whether conspecific cues are inherently more influential than cues provided by heterospecifics, or whether animals can simply use any cue that predicts fitness enhancing conditions, including those provided by heterospecifics. To determine how freely social information travels across species boundaries, we trained bumblebees (Bombus terrestris) to learn to use cues provided by conspecifics and heterospecific honey bees (Apis mellifera) to locate valuable floral resources. We found that heterospecific demonstrators did not differ from conspecifics in the extent to which they guided observers'' choices, whereas various types of inorganic visual cues were consistently less effective than conspecifics. This was also true in a transfer test where bees were confronted with a novel flower type. However, in the transfer test, conspecifics were slightly more effective than heterospecific demonstrators. We then repeated the experiment with entirely naïve bees that had never foraged alongside conspecifics before. In this case, heterospecific demonstrators were equally efficient as conspecifics both in the initial learning task and the transfer test. Our findings demonstrate that social learning is not a unique process limited to conspecifics and that through associative learning, interspecifically sourced information can be just as valuable as that provided by conspecific individuals. Furthermore the results of this study highlight potential implications for understanding competition within natural pollinator communities.     

Social learning of predators in the dark: understanding the role of visual,chemical and mechanical information

The ability of prey to observe and learn to recognize potential predators from the behaviour of nearby individuals can dramatically increase survival and, not surprisingly, is widespread across animal taxa. A range of sensory modalities are available for this learning, with visual and chemical cues being well-established modes of transmission in aquatic systems. The use of other sensory cues in mediating social learning in fishes, including mechano-sensory cues, remains unexplored. Here, we examine the role of different sensory cues in social learning of predator recognition, using juvenile damselfish (Amphiprion percula). Specifically, we show that a predator-naive observer can socially learn to recognize a novel predator when paired with a predator-experienced conspecific in total darkness. Furthermore, this study demonstrates that when threatened, individuals release chemical cues (known as disturbance cues) into the water. These cues induce an anti-predator response in nearby individuals; however, they do not facilitate learnt recognition of the predator. As such, another sensory modality, probably mechano-sensory in origin, is responsible for information transfer in the dark. This study highlights the diversity of sensory cues used by coral reef fishes in a social learning context.     

Behavioral syndrome over the boundaries of life--carryovers from larvae to adult damselfly

Activity is an important behavioral trait that mediates a trade-offbetween obtaining food for growth and avoiding predation. Activeindividuals usually experience a higher encounter rate withfood items and suffer higher predation pressure than less activeindividuals. I investigated how activity of the damselfly Lestescongener is affected by larval state and predator presence andif larval behavioral type (BT) can be used to predict larvalboldness, foraging success, and adult BT. Activity level ofindividual larvae was studied without predator at 2 differentphysiological states (hungry and fed) and in 2 predator treatments:familiar predator cues and unfamiliar predator cues. Larvaedid not adjust their activity depending on state or when subjectedto unfamiliar predator cues, but a general reduction in activitywas seen in the familiar predator treatment. Hence, active individualsremained active compared with their conspecifics, independentof state or predator treatment. Active individuals were alsobolder and more efficient foragers than their less active conspecifics.Furthermore, both adult activity and boldness were correlatedwith larval BT. The results illustrate that BT of a larvae iscarried over many different situations keeping active larvaeactive even in maladaptive situations, demonstrating how a behavioralsyndrome may constrain behavioral plasticity. Furthermore, resultsshowed that behavioral syndromes can carry over from larvaethrough metamorphosis and dictate the BT of the adult.     

Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish

Chemical cues are of enormous importance in mediating the behaviour of animals, enabling them to navigate throughout their habitats, to detect the presence of predators or prey and for social recognition-identifying and discriminating between conspecifics. In many species of freshwater fish, social recognition is known to be based primarily on chemical cues. Such recognition mechanisms are vulnerable to disruption by the presence of anthropogenic contaminants in the aquatic environment. Here we show that acute exposure to low, environmentally relevant dosages of the ubiquitous contaminant, 4-nonylphenol, can seriously affect social recognition and ultimately social organization in fishes. A 1 hour 0.5 microgl-1 dose was sufficient to alter the response of members of a shoaling fish species (juvenile banded killifish, Fundulus diaphanus) to conspecific chemical cues. Dosages of 1-2 microgl-1 caused killifish to orient away from dosed conspecifics, in both a flow channel and an arena. Given the overall importance of shoaling as an adaptive strategy against predators and for locating food, it is likely that its disruption by anthropogenic contaminants would have serious implications for fishes' fitness.     

Disturbance chemical cues determine changes in spatial occupation by the convict cichlid Archocentrus nigrofasciatus

I studied the effect of disturbance chemical cues on fish that make trade-offs between foraging in an open area and remaining in a safe refuge. I used convict cichlids Archocentrus nigrofasciatus that were either visually exposed to a predator (n = 8) or exposed to water conditioned by chemical cues from disturbed conspecifics (n = 8). Fish visually exposed to a predator decreased their ingestion rate and spent more time in the refuge than in the foraging area, while fish receiving water from frightened conspecifics did not alter their ingestion rate or time spent in the refuge and foraging site, but increased their spatial occupation (i.e., motion). These results suggest that convict cichlids recognized the predator by visual cues. Moreover, disturbance cues are a form of threatening public information that may increase fish spatial occupation due to increased exploring behaviour; but is not sufficiently alarming to alter feeding or increase refuge use.     

Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis

Many species assess predation risk through chemical cues, but the tissue source, chemical nature, and mechanisms of production or action of these cues are often unknown. Amphibian tadpoles show rapid and sustained behavioral inhibition when exposed to chemical cues of predation. Here we show that an alarm pheromone is produced by ranid tadpole skin cells, is released into the medium via an active secretory process upon predator attack, and signals predator presence to conspecifics. The pheromone is composed of two components with distinct biophysical properties that must be combined to elicit the behavioral response. In addition to the behavioral response, exposure to the alarm pheromone caused rapid and strong suppression of the hypothalamo-pituitary-adrenal (HPA) axis, as evidenced by a time and dose-dependent decrease in whole body corticosterone content. Reversing the decline in endogenous corticosterone caused by exposure to the alarm pheromone through addition of corticosterone to the aquarium water (50 nM) partially blocked the anti-predator behavior, suggesting that the suppression of the HPA axis promotes the expression and maintenance of a behaviorally quiescent state. To our knowledge this is the first evidence for aquatic vertebrate prey actively secreting an alarm pheromone in response to predator attack. We also provide a neuroendocrine mechanism by which the behavioral inhibition caused by exposure to the alarm pheromone is maintained until the threat subsides.     

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

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

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.     

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.     

Larval behavioral syndrome does not affect emergence behavior in a damselfly (<Emphasis Type="Italic">Lestes congener</Emphasis>)

Activity is a key behavioral trait that often mediates a trade-off between finding food for growth and evading predation. We investigated how activity of the damselfly Lestes congener is affected by larval state and predator presence and if larval behavioral type (BT) can be used to predict larval emergence behavior. Activity level of individual larvae was studied without predators at two different physiological states (hungry, fed) and in two predator treatments (familiar or unfamiliar predator cues). Larvae did not adjust their activity depending on state or when subjected to unfamiliar predator cues but a general reduction in activity was seen in the familiar predator treatment. Hence, active individuals remained active compared to their conspecifics, independent of state or predator treatment illustrating the presence of a behavioral syndrome. However, we found no correlation between larval BT and emergence behavior. Active individuals did not differ from less active individuals in any emergence characteristics. The results illustrate that the larval BT occurs in many situations keeping active larvae active even in maladaptive situations. Furthermore, we show that damselfly emergence behavior can be completely decoupled from larval BT, indicating a loss of stability in individual BT during critical stages in ontogeny.     

水生生态环境中捕食信息素的生态学效应

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

Perception of infection: disease-related social cues influence immunity in songbirds

While avoidance of sick conspecifics is common among animals, little is known about how detecting diseased conspecifics influences an organism''s physiological state, despite its implications for disease transmission dynamics. The avian pathogen Mycoplasma gallisepticum (MG) causes obvious visual signs of infection in domestic canaries (Serinus canaria domestica), including lethargy and conjunctivitis, making this system a useful tool for investigating how the perception of cues from sick individuals shapes immunity in healthy individuals. We tested whether disease-related social information can stimulate immune responses in canaries housed in visual contact with either healthy or MG-infected conspecifics. We found higher complement activity and higher heterophil counts in healthy birds viewing MG-infected individuals around 6–12 days post-inoculation, which corresponded with the greatest degree of disease pathology in infected stimulus birds. However, we did not detect the effects of disease-related social cues on the expression of two proinflammatory cytokines in the blood. These data indicate that social cues of infection can alter immune responses in healthy individuals and suggest that public information about the disease can shape how individuals respond to infection.     

Juvenile western toads, Bufo boreas, avoid chemical cues of snakes fed juvenile, but not larval, conspecifics

Previous investigations have demonstrated the importance of predator diet in chemically mediated antipredator behaviour. However, there are few data on responses to life-stage-specific predator diets, which could be important for animals like amphibians that undergo metamorphosis and must respond to different suites of predators at different life-history stages. In laboratory choice tests, we investigated the chemically mediated avoidance response of juvenile western toads, Bufo boreas, to four different chemical stimuli: (1) live conspecific juveniles; (2) live earthworms; (3) snakes fed juvenile conspecifics; and (4) snakes fed larval conspecifics (tadpoles). Juvenile toads avoided chemical cues from snakes that had eaten juvenile conspecifics, but did not respond to the other three stimuli, including chemical cues from snakes fed larval conspecifics. In addition, the response to cues from snakes fed juveniles differed significantly from that of snakes fed larvae. To our knowledge, this is the first study to demonstrate the importance of diet in predator avoidance of juvenile anurans and the ability of juvenile toads to distinguish between chemical cues from predators that have consumed larval versus juvenile conspecifics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social Context Modulates Predator Evasion Strategy In Guppies

Social context is a powerful mediator of behavioral decisions across animal taxa, as the presence of conspecifics comes with both costs and benefits. In risky situations, the safety conferred by the presence of conspecifics can outweigh the costs of competition for resources. How the costs and benefits of grouping influence decisions among alternative antipredator behaviors remains largely unexplored. We took advantage of the Trinidadian guppy (Poecilia reticulata) to examine the influence of social context on alternative behavioral responses to threats. We compared the frequency of active (startle) versus passive (freeze) responses to sudden acoustic stimuli in the presence and absence of conspecifics. We found that fish were relatively less likely to startle and more likely to freeze when in a group than when alone, indicating that immediate social context modulates predator evasion strategy in guppies. We suggest that these social context‐dependent changes reflect trade‐offs between survival and energy expenditure. To our knowledge, an effect of immediate social environment on startle probability has not been previously demonstrated in a teleost.