scholarly journals Fathead minnows learn to recognize predator odour when exposed to concentrations of artificial alarm pheromone below their behavioural-response threshold

2001 ◽  
Vol 79 (12) ◽  
pp. 2239-2245 ◽  
Author(s):  
Grant E Brown ◽  
James C Adrian, Jr. ◽  
Todd Patton ◽  
Douglas P Chivers

Hypoxanthine-3-N-oxide (H3NO) has been identified as the putative alarm pheromone of ostariophysan fishes. Previously we demonstrated a population-specific minimum behavioural-response threshold in fathead minnows (Pimephales promelas) to a H3NO concentration of approximately 0.4 nM. Minnows may, however, perceive low concentrations of H3NO as a predation threat, even though they do not exhibit an overt behavioural response. We conducted a series of laboratory trials to test the hypothesis that minnows can detect the alarm pheromone at concentrations below the minimum behavioural-response threshold. We exposed predator-naïve fathead minnows to H3NO at concentrations ranging from 0.4 to 0.05 nM paired with the odour of a novel predator (yellow perch, Perca flavescens) or distilled water paired with perch odour. We observed significant increases in antipredator behaviour (increased shoal cohesion, movement towards the substrate, a reduction in feeding, and an increase in the occurrence of dashing and freezing behaviour) in shoals of minnows exposed to a combined cue of 0.4 nM H3NO and perch odour (compared with a distilled-water control), but not by shoals exposed to lower concentrations of H3NO paired with perch odour or those exposed to distilled water paired with perch odour. When exposed to perch odour alone 4 days later, minnows initially conditioned to H3NO at concentrations of 0.4–0.1 nM exhibited significant increases in antipredator behaviour. These data demonstrate that minnows attend to the alarm pheromone at concentrations below the minimum behavioural-response threshold and are able to acquire the ability to recognize a novel predator even though they do not exhibit an overt behavioural response.

1995 ◽  
Vol 73 (12) ◽  
pp. 2209-2215 ◽  
Author(s):  
Mark V. Abrahams

Prey species have two fundamental strategies for reducing their probability of being killed by a predator: behavioural modification and morphological defenses. It is hypothesized that prey species which possess morphological defenses should exhibit less behavioural modification in response to predation risk than species lacking such defenses. Experiments were conducted to examine behavioural modification by armoured (brook sticklebacks, Culea inconstans) and unarmoured (fathead minnows, Pimephales promelas) prey species foraging in the presence of a predator (yellow perch, Perca flavescens). Two experiments measured habitat avoidance and reactive distance to an approaching predator. The results of these experiments were consistent with the hypothesis. Compared with fathead minnows, brook sticklebacks exhibited relatively little behavioural modification in response to the presence of a predator, both in terms of avoiding dangerous areas and in their reactive distance to an approaching predator. Sticklebacks, however, graded their reactive distance to an approaching predator in relation to both their body size and group size. These data suggest that the morphology of brook sticklebacks and their behavioural sensitivity to predation risk may allow them to efficiently exploit habitats that contain predators.


Behaviour ◽  
1998 ◽  
Vol 135 (8) ◽  
pp. 1213-1228 ◽  
Author(s):  
Renée Godard ◽  
Catherine Wannamaker ◽  
Bonnie Bowers

AbstractStudies of a limited number of species of fish in the superorder Ostariophysi have shown they they exhibit strong antipredator behaviour to conserved alarm substance in feces and in other byproducts from predatory fish that have consumed ostariophysans. Our experiments examined the ability of a previously untested ostariophysan to recognize chemical cues from two species of snake predators. In Experiment 1, shoals of golden shiners (Notemigonus chrysoleucas) exhibited strong shelter-seeking responses to water which contained waste byproducts from either a sympatric snake or an allopatric snake which had been fed golden shiners but not to a distilled water control. There was no difference in response to the sympatrie snake predator, northern water snakes (Nerodia sipedon), compared to the allopatric snake predator, black-bellied garter snakes (Thamnophis melanogaster). In Experiment 2, individual shiners exhibited vigourous dashing when presented with water which contained waste byproducts from N. sipedon fed golden shiners but exhibited a much weaker response to water which contained waste byproducts from N. sipedon fed green swordtails (Xiphophorus helleri, a non-ostariophysan) or to a water control. These results suggest that the alarm substance produced in the epidermis of the golden shiners is conserved in snake waste byproducts. Experiment 3 showed that there was little difference in shelter-seeking behaviour by shoals of shiners when presented with water in which N. sipedon had soaked, water in which T. melanogaster had soaked, or a distilled water control. Thus it appears that secretions from the skin of these predators may not be chemically labelled.


1998 ◽  
Vol 55 (3) ◽  
pp. 611-617 ◽  
Author(s):  
Grant E Brown ◽  
R Jan F. Smith

In this study, we exposed predator-naive, hatchery-reared juvenile rainbow trout (Oncorhynchus mykiss) to the chemical stimuli from northern pike (Esox lucius) and either trout skin extract (a chemical alarm signal) or a distilled water control to test for acquired recognition of a novel predator. Trout exposed to conspecific skin extract and pike odour significantly increased antipredator behaviour (i.e., decreased foraging and area use and increased shoaling and freezing), while those exposed to distilled water and pike odour did not. Conditioned trout were exposed to pike odour alone (versus a distilled water control) either 4 or 21 days later. When presented with pike odour 4 days postconditioning, trout significantly increased antipredator behaviour (i.e., decreased foraging and area use and increased time under cover and freezing). Trout tested 21 days postconditioning still exhibited a significant increase in antipredator behaviours when presented with pike odour alone (i.e., decreased foraging and increased freezing). These data are the first to demonstrate that hatchery-reared trout can be conditioned to recognize the chemical cues of a predator and suggest that this may serve as a strategy to train hatchery-reared fish to recognize predators prior to stocking into natural waterways.


1995 ◽  
Vol 73 (5) ◽  
pp. 955-960 ◽  
Author(s):  
Douglas P. Chivers ◽  
Grant E. Brown ◽  
R. Jan F. Smith

We exposed groups of four fathead minnows (Pimephales promelas) that were familiar to each other and had been taken from naturally occurring shoals, and groups of four fish unfamiliar to each other, taken from four separate shoals, to either chemical stimuli from pike or a model fish predator (northern pike, Esox lucius). In response to both chemical stimuli from pike and the pike model, minnows from familiar groups showed greater shoal cohesion than those from unfamiliar groups. Tighter shoal cohesion should result in a higher probability of surviving an encounter with a predator. Fish in familiar shoals also exhibited more dashing, a known antipredator response, than those in unfamiliar groups. In addition, groups of familiar fish showed less freezing behaviour than unfamiliar groups. In response to the model fish predator, familiar shoals exhibited a greater number of predator inspections, and the number of inspectors per inspection visit was greater, than those in unfamiliar groups. These results suggest that preferential shoaling with familiar conspecifics leads to an increase in cooperative antipredator behaviour and may thereby lower a minnow's risk of predation.


1992 ◽  
Vol 70 (8) ◽  
pp. 1473-1476 ◽  
Author(s):  
Alicia Mathis ◽  
R. Jan F. Smith

If chemical alarm pheromones warn individuals of nearby predation on conspecifics, then individuals should avoid areas where alarm pheromone is present. This hypothesis was tested in a natural stream habitat by exposing fathead minnows (Pimephales promelas) to minnow traps that had been marked with either conspecific alarm pheromone or with a control substance (glass-distilled water). The minnows exhibited significant avoidance of traps marked with the alarm pheromone: less than 4% of the minnows that were captured were found in the experimental traps. There was a nonsignificant tendency for minnows in control traps to be larger than those caught in experimental traps, suggesting a possible role of experience or developmental factors in determining the response to alarm pheromone. There was no apparent difference in overall body condition (i.e., length-specific mass) between the minnows that were caught in control versus experimental traps. Detection of the alarm pheromone may allow receivers to avoid areas where risk of predation is high.


1999 ◽  
Vol 77 (4) ◽  
pp. 562-570 ◽  
Author(s):  
Grant E Brown ◽  
Jean-Guy J Godin

We investigated the presence and possible function of chemical alarm signals (alarm pheromones) in wild Trinidadian guppies (Poecilia reticulata) using laboratory, trapping, and direct field observational methods. In laboratory experiments, female guppies from a population exposed to high predation significantly increased their shoaling, dashing, and freezing behaviours and significantly reduced area use when exposed to the skin extract of sympatric female guppies. When exposed to the skin extract of females from a low-predation population, female guppies from a high-predation population exhibited significant, though smaller, increases in antipredator behaviour. No significant differences in antipredator behaviours were noted when females were exposed to swordtail (Xiphophorus helleri) skin extract, which lacks any known alarm pheromone. We conducted two field experiments to confirm these laboratory results. In a trapping experiment, significantly more guppies were caught in funnel traps labelled with distilled water than in paired traps labelled with sympatric guppy skin extract. In a final experiment, a realistic model of a natural predator (pike cichlid, Crenicichla alta), paired with either sympatric guppy skin extract or distilled water, was presented to groups of free-ranging guppies in pools of a high-predation river. Significantly fewer guppies were observed within a 50-cm radius of the predator model and significantly fewer guppies inspected the model when it was paired with guppy skin extract versus distilled water. Taken together, our results strongly suggest the presence of a chemical alarm signal (alarm pheromone) in the Trinidadian guppy, establish the validity of laboratory and trapping studies in the investigation of chemical alarm signalling, and demonstrate that alarm pheromones may function to mediate predation risk under natural conditions in the guppy.


2002 ◽  
Vol 59 (8) ◽  
pp. 1331-1338 ◽  
Author(s):  
Grant E Brown ◽  
James C Adrian, Jr. ◽  
Michael G Lewis ◽  
Jon M Tower

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.


Behaviour ◽  
2004 ◽  
Vol 141 (10) ◽  
pp. 1235-1248 ◽  
Author(s):  
Reehan Mirza ◽  
Grant Brown ◽  
Ellie Roh

AbstractMuch study has been devoted to the function of chemical alarm cues in predator-prey relationships in aquatic environments, but little is known about the production of these valuable sources of chemosensory information. Recent studies have demonstrated that donor (cue sender) condition may play an important role in the production of chemical alarm cues in juvenile convict cichlids (Archocentrus nigrofasciatus). In laboratory experiments, we conducted trials to test for the effect of donor body condition on the minimum behavioural response threshold and/or intensity of antipredator response to conspecific chemical alarm cues. Chemical alarm cue donors were sampled from high or low condition populations. Pairs of juvenile cichlids were exposed to the skin extracts of high condition versus low condition donors, across a range of relative concentrations (200, 100, 50, 25, and 12.5%), and a distilled water control. We found that cichlids exhibited overt antipredator behaviour beginning at a concentration of 25% for the high condition cue, while a minimum response threshold concentration of 50% was seen for low condition cue. The intensity of antipredator response was greater following exposure to the alarm cues of high condition stimulus versus low condition donors. Taken together, these findings suggest that the damage-released chemical alarm cues from high condition donors are qualitatively and quantitatively greater than those of low condition donors.


Behaviour ◽  
2002 ◽  
Vol 139 (7) ◽  
pp. 929-938 ◽  
Author(s):  
Douglas Chivers ◽  
Reehan Mirza ◽  
Jeffery Johnston

AbstractNumerous species of aquatic animals release chemical cues when attacked by a predator. These chemicals serve to warn other conspecifics, and in some cases heterospecifics, of danger, and hence have been termed alarm cues. Responses of animals to alarm cues produced by other species often need to be learned, yet mechanisms of learned recognition of heterospecific cues are not well understood. In this study, we tested whether fathead minnows (Pimephales promelas) could learn to recognize a heterospecific alarm cue when it was combined with conspecific alarm cue in the diet of a predator. We exposed fathead minnows to chemical stimuli collected from rainbow trout, Oncorhynchus mykiss, fed a mixed diet of minnows and brook stickleback, Culaea inconstans, or trout fed a mixed diet of swordtails, Xiphophorous helleri, and stickleback. To test if the minnows had acquired recognition of the heterospecific alarm cues, we exposed them to stickleback alarm cues and introduced an unknown predator, yellow perch (Perca flavescens) or northern pike (Esox lucius). Both perch and pike took longer to initiate an attack on minnows that were previously exposed to trout fed minnows and stickleback than those previously exposed to trout fed swordtails and stickleback. These results demonstrate that minnows can learn to recognize heterospecific alarm cues based on detecting the heterospecific cue in combination with minnow alarm cues in the diet of the predator. Ours is the first study to demonstrate that behavioural responses to heterospecific chemical alarm cues decreases the probability that the prey will be attacked and captured during an encounter with a predator.


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