Minnow alarm substance

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. 

Alarm substances in fish are extremely potent extract from 1 cm minnow skin creates an active space of over 58 000 liters of water (Smith and Lawrence, 1989). 

In addition to behavior changes, exposure to the alarm odor also has physiological effects. For instance, in pearl dace, Semotilus margarita, the levels of plasma cortisol and glucose increase 15 minutes after the alarm and are back to normal after 5 hours. The brain concentrations of dopamine, norepinephrine, 5-hydroxytryptamine, or tryptophan did not change (Rehnberg et al., 1987). The fish recovered physiologically much sooner than the behavioral activation For example. Von Frisch (1941) observed that minnows avoided the site of their encounter with alarm substance for many hours, even days. 

The alarm substance (Schreckstoff) has served to test Hamilton s selfish-herd theory. Fourteen dace, Leuciscus leuciscus, were habituated to minnow schreckstoff, until they no longer responded. They were then joined by a single, naive minnow. Upon adding schreckstoff to the water, the single minnow was alarmed while the school was not. The single minnow moved into the school and became surrounded by other fish on all sides (Krause, 1993). Among alarmed fish, it is everybody for himself. ... 

The cabbage worm butterfly Pieris rapae crucivora and the sulfur-colored Catopsilia crocale are both found to afford the anticancer component isoxanthopterin (67) (57). In addition, isoxanthopterin (67) from the skin of the European minnow, Phoxinus phoxinus, elicits the fright reaction and hence acts as the alarm substance (52). 

Chivers, D. P., and Smith, R. J. F., 1994a, Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish, Anim. Behav. 48 597-605. 

Mathis, A., and Smith, R. J. F, 1992, Avoidance of areas marked with a chemical alarm substance by fathead minnows Pimephalespromelas) in a natural habitat, Can. J. Zool. 70 1473-1476. 

Wisenden, B. D., and Smith, R. J. F., 1997, The effect of physical condition and shoalmate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows, J. Fish. Biol. 50 799-808. 

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. 

Bernstein, J.W. Smith, R.J.F. 1983. Alarm substance cells in fathead minnows do not affect the feeding preference of rainbow trout. Env. Biol. Fish., 9, 307—311. 

Chivers, D.P Smith, R.J.F. 1995a. Fathead minnows Pimephales promelas) learn to recognize chemical stimuli from high risk habitats by the presence of alarm substance. Behav. Ecol, 6, 155—158. 

Lawrence, B.J. Smith, R.J.F. 1989. The behavioral response of solitary fathead minnows, Pimephales promelas, to alarm substance, J. Chem. Ecol,. 15, 209-219. 

Smith, R.J.F. 1973. Testosterone eliminates alarm substance cells in male fathead minnows (Pimephales promelas). Can. J. Zool, 51, 875-876. 

Two analogous chemical alarm systems have been described in fishes and there is evidence that other comparable systems exist. I will deal primarily with the best known of these systems, the alarm substance or Schreckstoff system found in the ostariophysan fishes (e.g. minnows, suckers, catfish), first described by von Frisch (1938) and recently reviewed by Pfeiffer (1977, 1982) and Smith (1977, 1982a). The terms "alarm substance" and "alarm substance cells" (ASCs) will be used only for the ostariophysan system. The second established alarm system is found in darters of the Family Percidae (Smith, 1979, 1982b). The darter system will be specifically designated when it is described. 

Smith and Lemly (1985) report one situation in which 16% of the individuals in a concentration of fathead minnows, Pimephales promelas, had been injured by piscivorous birds. The fish possessed ASCs, as would be expected in non-breeding fathead minnows. The degree of damage in the fish examined would have been sufficient to release alarm substance since scale loss had occurred and the ASCs lie in the epidermis, outside the scales. 

Since Williams (1964) proposed that the alarm substance acts as a predator deterrent, there has been one direct test of his hypothesis. Bernstein and Smith (1983) treated fathead minnows (Pimephales promelas) with androgen, a process that eliminates ASCs from the skin (Smith, 1973). They then observed the feeding behavior of rainbow trout presented with androgen-treated minnows without ASCs and untreated control minnows with ASCs. The trout showed no significant preference for either type of minnow even though the same test procedure did detect a preference for liver over commercial food pellets. The results indicate that the presence of ASCs in the skin does not act as a deterrent to rainbow trout. This is consistent with the widespread use of minnows, including fathead minnows, as bait fish by sports fishermen. 

Other published statements about the chemical nature of alarm pheromone are not sufficiently precise to provide information on potential non-alarm functions. These include the statement by Ahsan and Prasad (1982) that the alarm pheromone is a polypeptide or protein molecule and the suggestion by Tucker and Suzuki (1972) that the alarm pheromone may be a mixture of peptides, amino acids and derivatives. Similarly Lebedeva et al. (1975) isolated active fractions from minnow skin (Phoxinus phoxinus) but did not identify specific compounds although they found the molecular weight of their active components to be over 950, well above the molecular weight of hypoxanthine-3-oxide. Kasumyan and Lebedeva (1977, 1979) similarly do not provide sufficient detail about the fractions isolated to allow conclusions about other functions for alarm substance. 

Fathead minnow ASC loss remains the most intensively studied case. ASCs dissappear from the skin in response to gonadal androgens (Smith, 1973) and can be eliminated by treatment with 17a-methyltestosterone (Smith, 1973, 1974). Females do not lose their ASCs during normal reproductive cycles but do lose them if treated with 17a-methyltestosterone (Smith, 1974, 1978). Males and females both retain their response to alarm substance throughout the breeding season (Smith, 1976b). 

There is no direct experimental evidence to show that the fright reaction actually improves the survival of the receiver. There are, however, a number of correlations between the fright reactions shown by various fish when they detect alarm substance and their reactions to other indicators of predation. The most general type of reaction in schooling fish is for the school to aggregate and move away from the area of the stimulus. This type of response was first recorded in the European minnow by von Frisch (1938) and has since been observed in many species (Pfeiffer, 1977). 

Smith, J. D., 1982, The control of alarm substance cells in some minnows, M.Sc. Thesis, Biology Dept., University of Saskatchewan,... 

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