Alarm pheromones fishes

FIGURE 2.1 Hypoxanthine oxide, a fish alarm pheromone. 

Some taxa may possess pheromone-producing tissues, while others have similar tissues but without pheromones. At the cellular level, extensive comparative studies of fish alarm responses show that cyprinids possess club cells, which release an alarm odor when ruptured by a predator attack. Polypteriformes have... 

Predatory fish may also be affected by alarm pheromones (Section 7.2) of the prey, both directly and indirectly. The alarm odor may act as defense compoimd that inhibits predator attack or reduces capture rate by inducing predator avoidance in school members of the prey species. 

Fish avoid more vigorously the odor of predators that have fed on members of their species than that of those on different diets. For example, young Arctic chart avoid water from brown trout fed on Arctic chart and are less wary of that from pellet-fed trout (Hirvonen et ah, 2000). Prey fish also reduce their predator inspection behavior vis-a-vis predators that have eaten members of their own species. For instance, finescale dace, Phoxinus neogaeus, dash toward predators such as yellow perch, Percaflavescens, and withdraw. Dace inspect perch models less often if the model is accompanied by water from perch that had eaten dace than if accompanied hy water from perch on a swordtail, Xiphophorus hdleri, diet. Dace produce alarm pheromone, while swordtails do not. The Central American swordtails do not cooccur with finescale dace (Brown etal, 2001). 

In minnows, taste is not sufficient for predator recognition. Anosmic fathead minnows, P. pmmelas, did not show the flight reaction to the odor of northern pike, Esox lucius (Chivers and Smith, 1993). Naive European minnows, Phoxinus phoxinus, do not exhibit a fright reaction when first exposed to a predator odor, such as that of pike, E. lucius. They develop a conditioned fright response only after experiencing the predator odor in dangerous circumstances, such as when accompanied by schreckstoff (alarm pheromone) of conspecifics. Responses to the odor of non-piscivorous fishes such as tilapia, Tilapia mariae, can also be conditioned in this fashion but the responses are much weaker (Magurran, 1989). 

Alkylpyrazines occur frequently as flavour constituents in foodstuffs that undergo heating, e.g. coffee and meat. They are probably formed by a Maillard reaction between amino acids and carbohydrates. Alkylpyrazines also act as alarm pheromones in ants. Coelenterazine 35, a bioluminiscent natural product isolated from a jelly fish, is used in bioassays [159]. 

Williams (1964, 1992), however, argued that there are considerable problems in explaining the evolution of an alarm pheromone. It was assumed that individuals produced alarm substance to warn their school or species of danger, but schools of fish are not composed of closely related individuals (Naish et al. 1993). Magurran et al. (1996) further demonstrated that fright responses in fish were elicited in a context-dependent manner. The alarm responses were likely exaggerated in the laboratory condition where the opportunities for escape were largely reduced. In the natural environment, alarm substances did not produce adaptive behaviors. In crustaceans, behaviors similar to the alarm response in fish can be elicited by the reception of injured conspecifics (Hazlett, Chap. 18). 

Brown GE, Adrian JC Jr, Kaufman IH, Erickson JL, Gershaneck D (2001) Responses to nitrogen-oxides by chariciform fishes suggest evolutionary conservation in Ostariophysian alarm pheromones. In Marchlewska-Koj A, Lepri J, Muller-Schwarze D (eds) Chemical signals in vertebrates. Plenum, New York, pp 305-312... 

Magurran AE, Irving PW, Henderson PA (1996) Is there a fish alarm pheromone A wild study and critique. Proc R Soc Lond B 263 1551-1556... 

Brown, G. E., Adrian, J. C. Jr., Kaufinan, L H., Erickson, J. L., and Gershaneck, D, 2001b, Responses to nitrogen-oxides by Characiforme fishes suggest evolutionary conservation in Ostariophysan alarm pheromones, in Chemical Signals in Vertebrates, Vol. 9, A. Marchlewska-Koj, J.J. Lepri, and D. MOller-Schwarze, eds.. Plenum Press, New York, pp. 305-312. 

The aim of this paper is to provide some speculative discussion and propose some hypotheses about the multiple possible functions and interactions, both within a species and between species, that could influence the evolution of chemical alarm signals in fishes. Fish alarm pheromones have been reviewed by Smith (1992) and Chivers Smith (in press) but I will provide basic background information with a few examples. 

In most families of the Superorder Ostariophysi (e.g., minnows, suckers, catfish, characins and loaches), individuals show antipredator responses when they detect chemicals released from injured conspecifics. This response is absent in some armoured catfish, pencilfishes and ostariophysans with electric organs (Pfeiffer 1977). In ostariophysan fishes the alarm pheromone is contained in epidermal club cells, or alarm substance cells, that have no pores to the exterior, and have no proven function except the production and storage of the alarm substance that triggers antipredator behavior in conspecific receivers. 

Alarm pheromones may act directly on predators as repellants (Williams 1964). Although there is no good evidence for this in fish, it is still a possibility. Obviously some-... 

Johnston (1998) gives several examples of how combinations of neurophysiology and behavioral analysis can sort out the differences between classical pheromones, pheromone-like signals and odor quality signals composed of a mixture of several active compounds. Application of these techniques to fish alarm substances might reveal patterns in the evolution of these chemical signals. 

Taxonomic Comparisons. Obviously there are many variations on the basic injury released alarm pheromone theme in fishes and other organisms. A more comprehensive examination of the distribution and variations of this phenomenon might reveal patterns. For example, are there alarm substances that are predator attractants and others that are predator repellants Are some ecological niches more amenable to chemical alarm signaling than others Electrical ostariophysans, for example, seem to lack the alarm pheromone system (Pfeiffer 1977) but may use their electrical signals in some comparable manner. 

Brown, G.E., Chivers, D.P. Smith, R.J.F. 1995b. Fathead minnows avoid conspecific and heterospecific alarm pheromones in the faeces of northern pike. J. Fish Biol., 47, 387—393. 

---