Conspecific and heterospecific alarm substance induces behavioral responses in piau fish Leporinus piau

In ostariophysan fish, the detection of alarm substance released from the skin of a conspecific or a sympatric heterospecific may elicit alarm reactions or antipredator behavioral responses. In this study, experiments were performed to characterize and quantify the behavioral response threshold of Leporinus piau, both individually and in schools, to growing dilutions of conspecific (CAS) and heterospecific skin extract (HAS). The predominant behavioral response to CAS stock stimulation was biphasic for fish held individually, with a brief initial period of rapid swimming followed by a longer period of immobility or reduced swimming activity. As the dilution of skin extract was increased, the occurrence and magnitude of the biphasic alarm response tended to decrease, replaced by a slowing of locomotion. Slowing was the most common antipredator behavior, observed in 62.5% of animals submitted to HAS stimulation. School cohesion, measured as proximity of fish to the center of the school, and swimming activity near the water surface significantly increased after exposure to CAS when compared with the control group exposed to distilled water. Histological analysis of the epidermis revealed the presence of Ostariophysi-like club cells. The presence of these cells and the behavioral responses to conspecific and heterospecific skin extract stimulation suggest the existence of a pheromone alarm system in L. piau similar to that in Ostariophysi, lending further support for the neural processing of chemosensory information in tropical freshwater fish.     

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.     

Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract

Experiments were performed to determine which bundles of the olfactory tracts were essential for mediating alarm reaction in crucian carp (Carassius carassius L.). The fish were maintained in physiological saline after surgery to preserve the remaining tracts and postoperative inspections revealed the functionality of the intact tracts. Operations on the tracts were performed symmetrically on both sides. Sham-operated and non-operated fish showed the typical alarm behaviour of fast swimming to the bottom, dashing movements and aggregation when exposed to skin extract which contain alarm substance. Fish with only the medial bundle of the medial olfactory tract intact also displayed the alarm behaviour upon exposure; however, these fish did not react to the amino acid, L-alanine with either feeding response or alarm reaction. Crucian carp which had the medial bundle of the medial olfactory tract cut, leaving both the lateral bundle of the medial olfactory tract and the lateral olfactory tract intact, did not display any alarm reaction to skin extract; however, these fish reacted to exposure to L-alanine with feeding behaviour. There were statistically significant differences between the behaviour scores for the fish subject to different treatments. The present study demonstrates that the medial bundle of the medial olfactory tract appears to be both necessary and sufficient for mediation of the alarm reaction. The results also show that the sensory neurons which respond to alarm substance terminate and make synaptic connections with the secondary neurons that make up the medial bundle of the medial olfactory tract; thereby demonstrating the specificity of the spatial aspect of olfactory processing. The results are discussed with respect to the spatial aspect of organization within the olfactory system, the pattern of generalization across orders of fish, and the functional implications of the spatial arrangement of information transmission between the peripheral olfactory organ and the brain.     

Anti‐predator response of naïve and experienced common bully to chemical alarm cues

Histological analysis of the skin of common bully Gobiomorphus cotidianus , a New Zealand native eleotrid fish, revealed the presence of club cells in the epidermis. Epidermal club cells are frequently associated with the production of alarm substance (Schreckstoff). The behavioural responses of perch‐naïve and perch‐experienced common bullies to either conspecific skin extract or chemical cues from an introduced predator, perch Perca fluviatilis , were then examined. Both perch‐naïve and perch‐experienced common bullies exhibited a behavioural response when exposed to conspecific skin extract, indicating the probable presence of an alarm substance. In contrast, only perch‐experienced common bullies recognized and exhibited a subsequent behavioural response to the odour of perch. This study is the first to document the presence of epidermal club cells and a behavioural response to a conspecific chemical alarm signal for fishes in the Eleotridae. The results indicate that common bully can learn to recognize perch odour as a threat, and that this ability may be a result of previous predator labelling involving a conspecific alarm substance.     

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.     

Size-mediated response to public cues of predation risk in a tropical stream fish

In order to investigate any size-dependent differences between behavioural patterns, wild-caught Hart's rivulus Rivulus hartii of varying sizes were exposed to chemical alarm cues extracted from the skin of conspecifics or heterospecific Poecilia reticulata, or a tank water control, in a series of laboratory trials. In response to conspecific alarm cues, R. hartii subjects of the range of body sizes tested exhibited consistent, size-independent antipredator behaviours that were characterized by decreased locomotory activity and foraging levels and increased refuging behaviour. Conversely, focal R. hartii demonstrated significant size-dependent trends in response to heterospecific alarm cues, with smaller individuals exhibiting antipredator responses and larger individuals shifting their behaviour to increased levels of activity consistent with a foraging, or predatory, response. These results show that the behavioural responses of individual R. hartii to publicly available chemical alarm cues from heterospecifics are mediated by the size of the receiver.     

The ‘club’ cell and behavioural and physiological responses to chemical alarm cues in the Nile tilapia

The alarm response to skin extract has been well documented in fish. In response to skin extract, there is a decline in both locomotion activity and aggressive interactions. Our observation herein of these responses in the cichlid Nile tilapia, Oreochromis niloticus, confirmed the existence of the alarm response in this species. However, so far there has been a paucity of information on the autonomic correlates of this response. In this study, the ventilatory change in response to the chemical alarm cue was evaluated. This parameter was measured 4 min before and 4 min after exposure to 1 mL of either conspecific skin extract or distilled water (extract vehicle). Skin extract induced an increase in the ventilation rate, which suggested an anticipatory adjustment to potentially harmful stimuli. The chemical cue (alarm substance) also interfered with the prioritisation of responses to different environmental stimuli (stimuli filtering); this was suggested by the observation that the Nile tilapia declined to fight after exposure to a cue that indicates a risk of predation. Furthermore, histological analysis of the Nile tilapia skin revealed the presence of putative alarm substance-producing (club) cells.     

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.     

Innate predator recognition and fright response in related populations of Oncorhynchus mykiss under different predation pressure

Innate predator recognition and fright response behaviours were compared in a laboratory study between second generation offspring from two related populations of steelhead trout Oncorhynchus mykiss from Sashin Creek, Alaska. The stream population was anadromous and co-occurred with Dolly Varden Salvelinus malma , a piscivore and salmonid predator. Sashin Lake, formerly fishless, was stocked with fish from the stream population in 1926 and that population has been isolated from heterospecific piscine predation ever since. Fish from the lake population were predicted to show diminished innate fright response to Dolly Varden scent relative to the stream population. The behaviour of 60 individual juvenile O. mykiss from each population was measured and observed in aquaria before and after exposure to chemical cues of Dolly Varden, conspecific skin extract, or a control of distilled water. The alarm substances caused significant behavioural changes in both populations in the amount of time spent motionless, time spent in the lower water column and feeding frequency. No significant differences were observed between the stream and lake populations in the change in behaviour between pre- and post-stimulus observation periods for any of the measured fright responses, indicating that the sequestered lake population has not lost the ability to detect or respond to conspecific alarm substances or Dolly Varden scent.     

Chemical Alarm Signals Enhance Survival of Brook Charr (Salvelinus fontinalis) During Encounters with Predatory Chain Pickerel (Esox niger)

A diversity of aquatic organisms release chemical alarm signals when attacked or captured by a predator. These alarm signals are thought to warn other conspecifics of danger and, consequently, may benefit receivers by increasing their survival. Here we experimentally investigated the differences in behaviour and survival of hatchery-reared juvenile brook charr Salvelinus fontinalis that had been exposed to either brook charr skin extract (experimental treatment) or a control of swordtail skin extract (control treatment). Charr exposed to conspecific skin extract exhibited a significant reduction in movement and/or altered their foraging behaviour in the laboratory when compared with charr exposed to swordtail skin extract. We also exposed charr to either water conditioned by a single brook charr disturbed by a predatory bird model or water conditioned by a single undisturbed brook charr. Charr exposed to disturbance signals reduced activity significantly more than charr exposed to chemical stimuli from undisturbed charr. These results demonstrate the existence of both damage-released alarm signals and disturbance signals in brook charr. Wild brook charr also responded to damage-released alarm cues under natural conditions. Charr avoided areas of a stream with minnow traps labelled with conspecific alarm cues vs. control cues. During staged encounters with chain pickerel Esox niger in the laboratory, predator-naive charr fry were better able to evade the predator if they were previously warned by an alarm signal, thus suggesting a survival benefit to receivers. Collectively, these results demonstrate that the presence of alarm signals in brook charr has important implications for understanding predator–prey interactions.     

Zebra finches are bolder in an asocial, rather than social, context

Despite an expanding interest in animal personalities, the influence of social interactions and sex differences on individual differences in behaviour remains poorly understood. Using the social zebra finch (Taeniopygia guttata), we tested for behavioural differences in exploration of a novel environment and objects, between individuals of both sexes in relation to a social context; the presence of three male companions, three female companions or no companion birds. We predicted that the presence of conspecific companions should result in focal birds reacting to novelty by exploring more extensively because the companion birds contribute to anti-predator vigilance behaviour and because social isolation often causes behavioural inhibition in social species. We found that exploratory behaviour of focal individuals was significantly reduced in the presence of conspecific companions, irrespective of the companion's sex. Moreover, we found a weak trend towards females being more exploratory than males, irrespective of the social context. These results demonstrate the importance of considering the social context in animal personality studies and of exploring sex differences in personalities.     

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.     

Ontogenetic Changes in the Response of Largemouth Bass (Micropterus salmoides, Centrarchidae, Perciformes) to Heterospecific Alarm Pheromones

Juvenile largemouth bass ( Micropterus salmoides ) undergo an ontogenetic niche shift from invertebrate feeding members of the cyprinid prey guild to piscivory during their first year of growth. We conducted laboratory and field trials to determine whether juvenile bass show a similar ontogenetic shift in their response to the alarm pheromone of finescale dace ( Phoxinus neogaeus , Cyprinidae). When exposed to dace skin extract (with alarm pheromone), juvenile bass exhibited a significant positive relationship between standard length and horizontal and vertical area use and time spent moving. Small bass (< 50 mm standard length) tended to reduce area use and time spent moving (indicative of an anti-predator response), while larger bass (> 50 mm standard length) increased area use and time spent moving (indicating a foraging response). Bass exhibited no change in behaviour when exposed to swordtail ( Xiphophorus helleri ) skin extract, which lacks Ostariophysan alarm pheromone. During field trials, small (30–45 mm standard length) and medium (46–60 mm standard length) bass actively avoided areas labelled with dace alarm pheromone and exhibited a significant increase in dashing behaviour. Large bass (61–80 mm standard length) were attracted to such areas and exhibited a significant increase in approach behaviour. These data suggest that largemouth bass undergo an ontogenetic shift in response to heterospecific chemical alarm signals.     

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.     

Consequences of temperature and temperature variability on swimming activity,group structure,and predation of endangered delta smelt

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Role of olfaction and vision cues in feeding behavior and alarm reaction in the catfish pintado, Pseudoplatystoma corruscans

Experiments were performed to investigate senses that are essential for mediating fright reaction and food behavior in Pseudoplatystoma corruscans, pintado. The dilemma “to feed or to flee” was also analyzed in fishes with intact and sectioned olfactory tracts, stimulated by alarm substance extracts and food. Fishes were arranged into five groups: fish with intact lateral olfactory tracts (LOT), fish with intact medial olfactory tract (MOT), fish with tracts totally sectioned (TOTAL, both LOT and MOT), sham operated, and nonoperated fish. The five groups were submitted to either alarm substance extract and food stimulus or to distilled water (control) and food stimulus. Fish reacted to food independently of which tract (LOT, MOT or TOTAL) was sectioned; vision seems necessary and elemental to detect and deflagrate food response. Latency of the responses to each reaction was different between groups. None of the fish with sectioned tracts reacted to alarm substance extract, while sham- and nonoperated fish showed the typical alarm behavior response, leading to the conclusion that olfaction is essential for mediating alarm response. These results indicate that others sense systems (e.g., vision) are sufficient to trigger and elicit feeding behavior and that olfaction is not necessary to fully maintain food detection to qualitative and quantitative extent. However, olfactory tract integrity seems to be required for mediation of alarm reaction in P. corruscans.     

Acquired Recognition of Chemical Stimuli from Pike,Esox lucius,by Brook Sticklebacks,Culaea inconstans (Osteichthyes,Gasterosteidae)

In this study we test whether brook sticklebacks (Culaea inconstans) can acquire predator recognition through releaser-induced recognition learning, i.e. simultaneous exposure to aversive ('releasing') stimuli and neutral stimuli causing learned aversion to the neutral stimuli. We exposed wild-caught pike-naive brook sticklebacks (collected from a creek containing fathead minnows, Pimephales promelas, but not pike, Esox lucius) to chemical stimuli from pike that were mixed with brook stickleback skin extract, fathead minnow skin extract, or a control of distilled water. In subsequent tests 2 d later, when only pike stimuli were presented, sticklebacks conditioned with stickleback skin extract and fathead minnow skin extract exhibited antipredator behaviour (i.e. increased schooling and movement toward the substrate), while those conditioned with distilled water did not. Sticklebacks conditioned with stickleback skin extract responded to pike with a more intense response, in terms of movement toward the substrate, than those conditioned with fathead minnow skin extract, suggesting that conspecific skin extract may be a stronger stimulus than heterospecific skin extract for learning recognition of predators. To our knowledge this is the first study to demonstrate that an acanthopterygian fish can acquire predator recognition through the pairing of conspecific alarm pheromone with the cue of a predator. Furthermore, our results are the first to demonstrate that fish can acquire predator recognition through the pairing of a heterospecific alarm pheromone with the cue of a predator. These results suggest that brook sticklebacks will benefit by being in close proximity to fathead minnows. Acquired predator recognition has long-term consequences in mediating predator-prey interactions.     

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.     

Sensitivity and selectivity of neurons in the medial region of the olfactory bulb to skin extract from conspecifics in crucian carp,Carassius carassius

To examine the functional subdivision of the teleost olfactory bulb, extracellular recordings were made from the posterior part of the medial region of the olfactory bulb in the crucian carp, Carassius carassius. Bulbar units classified as type I or type II were frequently and simultaneously encountered at a recording site. Type I units displayed a diphasic action potential (AP) with a relatively small amplitude, a short duration (rise time approximately 1 ms) and high spontaneous activity (2.5 per s). Type II units exhibited an AP with a rise time of approximately 1.8 ms and low spontaneous activity (1.5 per s). The AP of this latter unit was nearly always followed by a slow potential, a characteristic diphasic wave with a rise time of approximately 5 ms. Chemical stimulation of the olfactory organ with a graded series of conspecific skin extract induced an increased firing of the type I units. During the period of increased activity of the type I units, the activity of the type II units was suppressed. Stimulation with nucleotides, amino acids and taurolithocholic acid did not induce firing of the type I units of the posterior part of the medial region of the olfactory bulb. These results indicate that the posterior part of the medial region of the olfactory bulb is both sensitive to and selective for skin extract from conspecifics, which has been shown to be a potent stimulus inducing alarm behaviour. The results of the present study indicate that recording single unit activity from a particular region of the olfactory bulb is a suitable method for isolating pheromones or other chemical signals that induce specific activity in the olfactory system. The projection of the neurons categorized as type II was determined by antidromic activation of their axons by electrical stimulation applied to the medial bundle of the medial olfactory tract. The anatomical basis of the type I and type II units in the fish olfactory bulb is discussed.     

No evidence for emotional empathy in chickens observing familiar adult conspecifics

The capacity of animals to empathise is of high potential relevance to the welfare of group-housed domestic animals. Emotional empathy is a multifaceted and multilayered phenomenon which ranges from relatively simple processes such as emotional matching behaviour to more complex processes involving interaction between emotional and cognitive perspective taking systems. Our previous research has demonstrated that hens show clear behavioural and physiological responses to the mild distress of their chicks. To investigate whether this capacity exists outside the mother/offspring bond, we conducted a similar experiment in which domestic hens were exposed to the mild distress of unrelated, but familiar adult conspecifics. Each observer hen was exposed to two replicates of four conditions, in counterbalanced order; control (C); control with noise of air puff (CN); air puff to conspecific hen (APC); air puff to observer hen (APH). During each test, the observer hens' behaviour and physiology were measured throughout a 10 min pre-treatment and a 10 min treatment period. Despite showing signs of distress in response to an aversive stimulus directed at themselves (APH), and using methodology sufficiently sensitive to detect empathy-like responses previously, observer hens showed no behavioural or physiological responses to the mild distress of a familiar adult conspecific. The lack of behavioural and physiological response indicates that hens show no basis for emotional empathy in this context.