Brook stickleback

Brook stickleback and fathead minnows occupy the same habitat and are vulnerable to common predators. Individuals that detect alarm cues of co-habiting species may benefit by gaining early warning of danger. A field study by Mathis and Smith (1993) demonstrated that skin extract from fathead minnows is effective at inducing avoidance responses by stickleback. Brook stickleback exploit the alarm system of minnows and thus reduce their own risk of predation (Mathis and Smith, 1993 Wisenden et al., 1994). In a trap experiment by Wisenden et al. (1994), the duration of area avoidance by brook stickleback of areas marked with fathead minnow alarm substance was measured. They found that stickleback continued to avoid locations associated with predation risk after the source of the cue was removed, and only after 2-4 hours did the fish resume use of these risky areas. In a follow-up experiment, Wisenden et al. (1995) determined that fishes naive to the association of an area with alarm cue were the first to migrate into the risky area. Fishes present at the time of cue release did not return for 7 to 8 hours after the cue was removed. Perhaps the chief beneficiaries of chemical alarm cues are only those individuals present at the time of cue release. 

McLennan, D. A. (2005). Changes in response to olfactory cues across the ovulatory cycle in brook sticklebacks, Culaeainconstans. Animal Behaviour 69,181-188. 

Mathis, A. and Smith, R.J.F., Intraspecific and cross-superorder responses to chemical alarm signals by brook stickleback, Ecology, 74, 2395, 1993. 

In this paper we review learned recognition of heterospecific alarm cues by prey fishes. We do this by providing a case study of the fathead minnow (Pimephales promelas)/bTOok stickleback Culaea inconstans) alarm systems. Fathead minnows and brook stickleback commonly occur together in a diversity of water bodies. They share a similar suite of predators and consequently cross-species responses to alarm cues should be highly advantageous. 

Pollock et al (2003) were the first to document the ability of minnows to learn to recognize heterospecific cues as an indication of predation. In their study a naturally occurring population of fathead minnows allopatric with brook stickleback did not respond to the skin extract of stickleback with an antipredator response. Stickleback fish were then introduced into the pond with the minnows and the two species were left to coexist for a period of five years. Following the period of co-existence, minnows were tested in the laboratory for a response to stickleback alarm cues. Not only did minnows now respond to stickleback cues, but they did so with the same intensity as they did to their own conspecific cues. A field experiment was also able to document a significant avoidance of stickleback skin extract in the wild. 

A second study by Mirza and Chivers (2001) investigated whether or not minnows could learn to recognize a novel heterospecific cue (stickleback cue) when the cue was associated with a conspecific alarm cue in the diet of an unknown predator. Mirza and Chivers (2001) conditioned fathead minnows with chemical stimuli from a predatory yellow perch (Perea flavescens) fed a mixed diet of either minnows and brook stickleback, or swordtails and stickleback. Minnows were then exposed to chemical alarm cues of injured stickleback alone. Those minnows previously conditioned with perch fed a diet of minnows and stickleback increased their use of shelter. They also froze significantly more often than minnows conditioned with perch fed a diet of swordtails and stickleback or those exposed to distilled water. This study demonstrates another mechanism by which fishes can learn to recognize a novel heterospecific alarm cue as an indication of predation. 

Chivers et al. (2002) tested whether or not learned responses could result in a survival benefit, besides confirming that fish could learn unknown heterospecific cues through the diet or a predator. In a two-part study, fathead minnows were exposed to chemical stimuli collected from rainbow trout (Oncorhynchus mykiss) fed a mixed diet of either minnows and brook stickleback, or swordtail and stickleback. To test if the minnows had acquired recognition of stickleback alarm cues, Chivers et al. (2003) exposed the fish to stickleback alarm cues and introduced an unknown predator, yellow perch or northern pike. 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 show again that fishes are able to learn novel cues through association with known cues in a predator s diet. Furthermore, it shows that anti-predator responses to these newly learned cues could result in a survival benefit. 

Following from the studies on density, Pollock and Chivers (2003) hypothesized that the type of habitat occupied by two species may likewise play a role in the ability to leam heterospecific alarm cues. Brook stickleback were introduced into one of two t) es of outdoor pools containing stickleback-naive fathead minnows and one predatory pike. Fishes were stocked at a ratio known to facilitate learning in the previous study. The two pool types were designed to represent complex habitat, consisting of various types of cover and shelter, and open habitat with no cover present. Fishes were first conditioned... 

Chivers, D. P., and Smith, R. J. F., 1994, Intra- and interspecific avoidance of areas marked with skin extract from brook sticklebacks in a natural habitat, J. Chem. Ecol. 20 1517-1524. 

Pollock, M. S., Chivers, D. P., Mirza, R. S. and Wisenden, B. D., 2003, Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans, Em. Biol. Fish. 66 313-319. 

In the past decade the protocol in most trap experiments has involved the use of distilled water as the sole control treatment. For example, Chivers and Smith (1994c) demonstrated that brook stickleback (Culaea inconstans) avoided conspecific skin extract over distilled water. The stickleback captured in traps marked with skin extract were significantly smaller than those individuals captured in traps marked with water, implicating experience or physiological development as critical factors in the development of anti-predator behavior. 

In summary, most published trap experiments have shown that brook stickleback avoid fathead minnow or stickleback skin extract over distilled water (Wisenden et al., 1994 Chivers and Smith, 1994c Wisenden etal., 1995 Mathis and Smith, 1992, 1993). Similarly, fathead minnows avoid stickleback and minnow cues over distilled water (Wisenden et al., 1995 Mathis and Smith, 1992 Brown et al., 2000). While novel and informative, these studies have the drawback of using distilled water as the only control. 

In an attempt to verify the visual compensation model in the field, a day/night trap experiment was conducted by Kusch et al. (unpublished) on an established community of fathead minnows and brook stickleback. The Kusch et al. study found no interaction between light intensity and treatment. The light level did not affect the avoidance pattern of either species to the various concentrations of fathead minnow alarm cue. 

Chivers, D.P, Brown, G.E. Smith, R.J.F. 1995. Acquired recognition of chemical stimuli from pike, Esox Indus, by brook sticklebacks, Culaea inconstans, (Osteichthyes, Gasterosteidae). Ethology, 99, 234—242. 

Gelowitz, C.M., Mathis, A. Smith, R.J.F. 1993. Chemosensory recognition of northern pike Esox Indus) by brook stickleback Culaea inconstans) population differences and the influence of predator diet. Behaviour, 127y 105-118... 

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