Significant Antipredator Responses Research Articles

Risk-induced neophobia is constrained by ontogeny in juvenile convict cichlids

Recent studies have established that variation in background level of risk has profound effects on antipredator phenotypes. Elevated levels of background risk not only change behaviour, but also physiology, morphology and cognitive function. A variety of prey show neophobic predator avoidance when exposed to short-term elevation in risk. Such phenotypically plastic responses allow prey to balance behavioural trade-offs in the face of uncertain risks. Here, we test the hypothesis that ontogeny functions as a constraining factor in the induction of neophobic predator avoidance. In a series of laboratory trials, we exposed convict cichlids, at three different ontogenetic stages (eggs/wrigglers, juveniles and adults), to conditions of elevated (versus low) risk and tested their response to a novel predator odour (rainbow trout, Oncorhynchus mykiss). When cichlids were exposed as eggs and newly hatched ‘wrigglers’ and tested 21 days later, they showed a significant antipredator response to trout odour. When exposed as ∼18 mm juveniles, cichlids showed a significant avoidance when tested 24 h post-exposure, but not 21 days post-exposure. However, when conditioned as ∼50 mm adults, we found no evidence of induced neophobia. Combined, these results suggest that ontogenetic stage may limit phenotypically plastic neophobia.

Size-based differences determine the contextual value of risky information in heterospecific information use

Behavioural responses to damage-released chemical cues in aquatic species are often examined with emphases on the potential survival benefits accrued by conspecific receivers in accordance with the hypothesis of taxonomic cue conservation. Nevertheless, chemical cues are publically available to any capable receivers in aquatic systems, and therefore convey information on ambient risk levels to unrelated prey species and on the availability of foraging opportunities to potential predators. Many documented alarm response patterns by heterospecific receivers closely match those of conspecifics, suggesting that the contextual value of public information on risk conveyed by alarm cues may be at least as important as their conserved value. To further explore this relationship, we compared the antipredator responses of shoals of three large or three small female Trinidadian guppies, Poecilia reticulata , to conspecific cues or cues from larger or smaller Hart's rivulus, Rivulus hartii , donors to quantify the relative values of publicly available information. Shoals of large female guppies demonstrated functionally similar antipredator responses to damage-released cues from conspecifics and larger heterospecifics, and no response to the damage-released cues from smaller heterospecifics or the kairomones of larger heterospecifics. Shoals of small guppies demonstrated significant antipredator responses to the damage-released cues of size-matched rivulus, but not to those of larger rivulus or to the odours of either size class. Collectively, these results indicate that potential prey assign at least equal importance to conspecific and public chemical cues from unrelated members of the same prey guild indicating elevated levels of predation risk in natural systems.

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

AbstractIntroduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.

Threat-Sensitive Responses to Disturbance Cues in Juvenile Convict Cichlids and Rainbow Trout

We conducted laboratory experiments (1) to confirm the existence of a non-injury released disturbance cue in juvenile convict cichlids and rainbow trout, and (2) to determine if cichlids and trout exhibit a graded threat-sensitive antipredator response to varying concentrations of disturbance cues. The results of our first experiment demonstrate that both cichlids and trout exhibit significant antipredator responses (reductions in time spent moving, foraging rate and area use) to the odour of conspecifics that had been exposed to a realistic predator model but not to the odour of undisturbed conspecifics. The results of our second experiment demonstrate that cichlids and trout exhibit reduced time spent moving and foraging rates proportional to the concentration of disturbance cue detected. Together, these results confirm the presence of disturbance cues in cichlids and trout and demonstrate that disturbance cues provide sufficient information to allow for graded threat-sensitive responses.

Latent inhibition of predator recognition by embryonic amphibians

To avoid being captured, prey animals need to be able to distinguish predators from non-predators. Recent studies have shown that amphibians can learn to recognize their future predators while in the egg. Here, we investigated whether amphibians would similarly be able to learn to recognize non-predators while in the egg. We exposed newly laid wood frog eggs to the odour of tiger salamander or a water control daily for 5 days. After hatching, the wood frog larvae were raised for two weeks at which time we tried to condition them to recognize the salamander as a predator. Larvae were exposed to injured conspecific cues paired with salamander odour, a well-established mode of learning for aquatic prey. When subsequently tested for their response to salamander odour, the larvae pre-exposed to water as embryos showed significant anti-predator responses. However, larvae pre-exposed to the salamander odour as embryos showed no learning of the predator, indicating that they had already learned to recognize the salamander as a non-predator. These results indicate that amphibian embryos can (i) learn to recognize stimuli as non-threatening and (ii) remember it for at least two weeks. The widespread ability of prey to learn to recognize non-predators might explain the persistence of injured conspecific cues as a reliable mechanism for learned predator recognition.

Antipredator behaviour of naïve Arctic charr young in the presence of predator odours and conspecific alarm cues

Abstract – We investigated how Arctic charr young respond behaviourally to olfactory cues from skin‐damaged conspecifics, charr‐fed pikeperch, and the combination of food‐deprived pikeperch and skin‐damaged conspecific cues in a two‐channel Y‐maze fluviarium test arena. Significant antipredator responses were found to skin‐damaged conspecifics in three behavioural traits, to charr‐fed pikeperch in two traits and to the combination of pikeperch and skin‐damaged conspecific cues in all six behaviours investigated. The combination of predator and conspecific cues significantly increased spatial avoidance and cautiousness to approach the source of scent compared with odours from charr‐fed predators. The results suggest that damage‐released alarm cues exist in charr, and they strengthen the antipredator responses in conspecifics. As the charr used different behaviours and levels of response in the presence of different cues, they seem to have sophisticated skills to distinguish between different odour combinations and be able to adjust their behaviour according to the current predation risk level.

Response to conspecific and heterospecific alarm cues by pumpkinseeds in simple and complex habitats: field verification of an ontogenetic shift

Three focal size classes [small (<40 mm, standard length, LS), medium (40–80 mm LS) and large (>80 mm LS)] of pumpkinseed Lepomis gibbosus were exposed to conspecific or one of three heterospecific chemical alarm cues under one of three levels of habitat complexity (low, intermediate and high). Under low and intermediate habitat complexities, pumpkinseeds <80 mm LS exhibited a significant antipredator response when exposed to the chemical alarm cues of heterospecific prey guild members (largemouth bass Micropterus salmonides and hypoxanthine‐3‐N‐oxide, the putative Ostariophysan alarm ‘pheromone’), while pumpkinseeds >80 mm LS exhibited a foraging response. Under highly complex habitats, pumpkinseeds of all three size classes exhibited an antipredator response. Moreover, under all three habitat conditions, pumpkinseeds of all size classes exhibited an antipredator response to conspecific alarm cues. There was no change in behaviour under any treatment combination in response to an allopatric heterospecific control (swordtails Xiphophorus helleri). These results provide the first field verification of the size dependent use of chemical alarm cues by centrarchids and demonstrate that microhabitat complexity significantly influences the threat‐sensitive use of these cues.

Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions

Under neutral (pH 7·0) conditions, juvenile pumpkinseed Lepomis gibbosus exhibited significant antipredator responses, of similar intensities, to the chemical alarm cues of conspecifics, an allopatric congener the green sunfish Lepomis cyanellus and the artificial alarm cue of a sympatric prey guild member (Cyprinidae, hypoxanthine‐3‐N‐oxide). Under weakly acidic conditions (pH 6·0), however, no increase in antipredator behaviour was seen in response to hypoxanthine‐3‐N‐oxide and a quantitatively weaker response was found in response to conspecific and congener cues, suggesting that the use of chemical alarm cues by some prey fishes may be impaired by acid precipitation.

Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration

Recent studies have shown that juvenile centrachids undergo ontogenetic shifts in their behavioural response towards conspecific and heterospecific chemical alarm cues based on threat-sensitive trade-offs between the benefits associated with predator avoidance and foraging. We conducted laboratory studies to test the hypothesis that the relative concentration of conspecific alarm cues provides relevant information, allowing individuals to maximize these trade-offs. Juvenile (<40 mm standard length) and subadult (>95 mm standard length) pumpkinseed sunfish (Lepomis gibbosus) were exposed to conspecific skin extracts at stock (undiluted) concentration or diluted 1:1 (50%), 1:3 (25%), or 1:7 (12.5%) with distilled water. Juvenile sunfish exhibited significant antipredator responses (relative to the distilled water controls) when exposed to conspecific skin extracts at a concentration as low as 25%. Juveniles exposed to 12.5% skin extract were not significantly different from the distilled water controls. Subadult sunfish exhibited significant antipredator responses only to the two highest concentrations. In response to the two lowest concentrations (25% and 12.5%), however, subadult sunfish exhibited significant foraging responses. These data demonstrate that the relative concentration of chemical alarm cues provides reliable information and allows individuals to accurately assess local predation risk and hence maximize potential trade-offs.

Role of kairomones in feeding interactions between seahorses and mysids

Big-bellied seahorses, Hippocampus abdominalis (Chordata: Syngnathidae), feed predominantly on swarming mysids in southern Tasmania. We tested the possibility that kairomones mediate this predator/prey interaction. ‘Fish water’ was prepared by holding one seahorse in 4 l of seawater for 1 h and using this water within 1 h to test for presence of kairomones. One ml of this water pipetted into a tank containing five mysids, Paramesopodopsis rufa (Arthropoda: Mysidacea), induced a significantly increased number of tailflips (mysid escape response) compared with control seawater. The same effect was seen whether seahorses were fed or starved immediately before the experiment. This effect was not seen when realistic concentrations of excretory products, either ammonium hydroxide or urea, were used instead of fish water. When seahorses were kept in visual contact with mysid prey, but unable to capture them, subsequent testing of the ‘fish water’ in the same way as above did not produce a significant increase of tailflipping in mysids. Thus it appears that, when attacking, seahorses can suppress release of kairomones in order to remain chemically inconspicuous to their prey. This is the first demonstration of this phenomenon. When mysids in a cohesive swarm (65 or 100 individuals) were exposed to ‘fish water’, no significant anti-predator response i.e. decrease in swarm volume, could be detected. We interpret these results to indicate the greater vulnerability of mysids when not in social groupings (swarm or school) and the higher likelihood of an energetic response (particularly tailflipping) to a threat.

RESPONSES OF STRIPED MICE, RHABDOMYS PUMILIO, TO FAECES OF A PREDATORY SNAKE

We investigated the behavioural responses of captive wild-caught striped mice ( Rhabdomys pumilio ) to the faeces of the elapid snake, the rinkhals ( Hemachatus haemachatus ), a striped mouse predator. The rinkhals apparently conceals its presence from potential prey by defecating away from their retreats, and we predicted that R. pumilio recognises this snake's faeces and displays anti-predator responses. We also tested whether R. pumilio is capable of diet-related predator labelling by observing their reactions to faeces of rinkhals fed different meals. Both sexes showed a significant anti-predator response to the presence of rinkhals faeces compared to that of house mouse ( Mus musculus ) bedding, by decreasing activity and investigations of test samples. In addition, R. pumilio showed diet-related predator labelling since its anti-predator response was greater when presented with H. haemachatus faeces containing remains of conspecifics than with those containing remains of house mice. The increased response to faeces with stimuli from conspecifics may function to alert R. pumilio to the presence of a predator. However, the defecation behaviour of H. haemachatus suggests that encounters between R. pumilio and H. haemachatus faeces would not necessarily lead to a predator-prey encounter.

The effects of reduced pH on chemical alarm signalling in ostariophysan fishes

Under laboratory conditions, we examined the effects of acute exposure to weakly acidic conditions (pH 6.0) on the ability of fathead minnows (Pimephales promelas) and finescale dace (Phoxinus neogaeus) to detect and respond to conspecific and artificial alarm pheromones. Initially, minnows and dace exhibited normal antipredator responses when exposed to conspecific alarm pheromones under normal (pH 8.0) conditions. When retested at pH 6.0, we observed no significant antipredator response. However, when returned to normal pH conditions, both exhibited normal antipredator responses. Minnows exposed to the putative ostariophysan alarm pheromone (hypoxanthine-3-N-oxide) exhibited a similar trend in behavioural response. Finally, we manipulated the pH of minnow skin extract and hypoxanthine-3-N-oxide to determine the chemical mechanism responsible for this observed loss of response. Minnows exhibited significant antipredator responses to natural and artificial alarm pheromones at normal pH conditions, but did not respond to either stimulus once they had been buffered to pH 6.0 or acidified and rebuffered to pH 7.5. These data suggest that the ability of minnows and dace to detect and respond to alarm pheromones is impaired under weakly acidic conditions and that this loss of response is due to a nonreversible covalent change to the alarm pheromone molecule itself.

Ostariophysan Alarm Pheromones: Laboratory and Field Tests of the Functional Significance of Nitrogen Oxides

In laboratory and field-trapping studies, we exposed fathead minnows (Pimephales promelas) and finescale dace (Chrosomus neogaeus) to hypoxanthine-3-N-oxide and a suite of structurally and functionally similar compounds in order to determine if: (1) hypoxanthine-3-N-oxide functions as a chemical alarm signal in ostariophysan fishes and (2) the purine skeleton, a structural component, or the nitrogen oxide, a functional component, or both act as the molecular trigger in this chemical alarm signaling system. Minnows and dace exhibited significant antipredator responses when exposed to conspecific skin extract or hypoxanthine-3-N-oxide (increased shoaling and decreased area use) and the functionally similar pyridine-N-oxide (increased shoaling) but not to structurally similar molecules lacking a nitrogen oxide functional group or to a swordtail skin extract control. Field-trapping studies revealed similar results. Traps labeled with fathead minnows skin extract, hypoxanthine-3-N-oxide, or pyridine-N-oxide caught significantly fewer fish than did those labeled with distilled water. These data strongly suggest that the nitrogen oxide functional group acts as the chief molecular trigger in the Ostariophysan alarm pheromone system and that, contrary to previous research, hypoxanthine-3-N-oxide may be one of several possible molecules that function as a chemical alarm signal. Here we report the first example of a single functional group capable of eliciting a suite of behavioral responses.

Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss)

We investigated, under laboratory conditions, the presence of chemical alarm signals in juvenile rainbow trout (Oncorhynchus mykiss). In an initial experiment, we exposed trout to a whole-body extract from conspecifics or a distilled-water control. When exposed to whole-body extract, trout significantly (i) decreased time spent swimming, (ii) increased time taken to resume foraging, and (iii) decreased the number of food items eaten. These data indicate a significant chemically mediated antipredator response. A second experiment was conducted to determine (i) if this is a generalized response to injured fish or a specific response to injured conspecifics, and (ii) if the chemical signal is localized in the skin. We exposed juvenile trout to one of three chemical stimuli: (1) trout skin extract, (2) trout body extract, or (3) swordtail (Xiphophorus helleri) skin extract. Significant antipredator responses were observed in trout exposed to conspecific skin extract, but responses of those exposed to conspecific body extract or swordtail skin extract did not differ from those of distilled-water controls. These data strongly suggest that juvenile rainbow trout possess a chemical alarm signal, localized in the skin, that elicits antipredator behaviour when detected.by conspecifics.