Heczko, E. J. and B. H. Seghers

Env. Biol. Fish. Vol. 6, No. 1, pp. 25-29, 1981

Effects of alarm substance on schooling in the common shiner (Notropis corm&m, Cyprinidae)

Eva J. Heczko & Benoni H. Seghers

Department of Zoology, University of Western Ontario, London, Ontario N6A 5B7, Canada

Keywords: Schreckstoff, Fright reaction, Pheromone, Antipredator mechanisms, Cover-seeking, Fish

Synopsis

The behavioral responses of common shiners (Notropis corntctus) to ‘Schreckstoff (alarm pheromone produced in the epidermis) were quantified in laboratory experiments. Schreckstoff increased cohesion and polarization, and decreased the variability in overall school dimensions. There was also a positive correlation between size of fish and their distance to the center of the school. Furthermore, the tendency to seek cover increased in the presence of Schreckstoff. The greater organization in school structure appears to be an adaptive response to aquatic predators, whereas increased cover seeking may be an adaptive response to aerial predators.

Introduction panied by bradycardia (Pfeiffer & Lamour 1976) and increased visual alertness (Pfeiffer & Riegel- ‘Schreckstoff is an alarm pheromone (von Frisch bauer 1978). 1938, in Pfeiffer 1962, Smith 1977) released from Schreckstoff and the Schreckreaktion appear to club cells in the epidermis (Pfeiffer & Lemke 1973) be confined to the Ostariophysi (Pfeiffer 1977). The when dalmaged (e.g. when a fish is captured by a exact molecular structure of the alarm substance is predator). Other fish will respond to this water- not yet known O>feiffer 1975, 1978), but it seems borne phleromone with a ‘Schreckreaktion’ (fright similar in all species, since it is effective interspeci- reaction), which may consist of cover seeking, fically with the strongest reaction between closely closer crowding, rapid swimming or immobility related species (Pfeiffer 1963a, Smith 1977). Most (von Frisch 1938, 1941, in Pfeiffer 1962, Verheijen authors usually ascribe an antipredator function to 1962a, 1963). Detection of the pheromone is only this pheromone, through inhibition of cannibalism olfactory (Pfeiffer 1963b), but the fright reaction (Verheijen 1962b, Pfeiffer 1963a, Verheijen & Reu- may be visually transmitted to other fish’(Verheijen ter 1969, Marusov 1976) repulsion of predators 1956). The initial reaction involves increased res- (Williams 1964) or by warning others in a school piration rate (Pfeiffer 1962) which may be accom- (Pfeiffer 1962). This study tested the third hypothesis, that it functions as an advance alert mechanism. We attempted to quantify the structural changes in Received 30.1.1980 Accepted 31.7.1980 schools of shiners upon addition of Schreckstoff,

~0 Dr. W. Junk b.v. Publishers, The Hague. Printed in The Netherlands. 037%1909/81/061-025 $01.00. following the suggestion for more objective quan- grid divided into 1 cm squares. The X-Y coor- tilicati.on of the alarm response (Aoki & Kuroki dinates of each fish’s snout were plotted, and the 1975). center of the school determiped by calculating the mean X-Y coordinates. The mean of the distances Materials and methods of individual fish from the center of the school was used as a measure of overall cohesion (Thines & Pretreatment and preparation of Schreckstoff Vandenbussche 1966). A decrease in mean distance to center of the school indicated an increase in Common shiners were seined from Medway Creek, overall cohesion. A measure of school polarization a tributary of the Thames River, near London, was obtained by -determining the heading of each Ontario. They were held in 200 1tanks at 19 - 22” C, fish with a protractor, and calculating the mean on a lo:14 h light: dark photoperiod, and fed dry heading for the school. The deviation of each fish fish food (Tetramin) to satiation each morning. from the mean heading was calculated, and a mean Schreckstoff was freshly prepared before each obtained for the school (Van Olst & Hunter 1970). experiment by decapitating a shiner (6 cm total length), eviscerating the body, removing the scales Effect of Sihreckstoff on cover-seeking behavior (to release Schreckstoff), and cutting the skin 10 times (to a depth of 1 mm) on both sides. After A white, circular pool (1.2 1 m diameter) was lined soaking the body in 75 ml of aged water for 5 min with a polyethylene plastic sheet and filled with the solution was filtered (0.1 cm pore size). The aged water to a depth of 15 cm. A clump of filtrate was a potent stimulus for the fright reaction. submerged vegetation approximately 15 cm in diameter was placed near the edge. A second pool Effect of Schreckstojj’ on school structure (control) was left with only water and vegetation, while Schreckstoff extract was poured into the Although we observed shiners in schools of up to experimental pool and mixed thoroughly. Six com- several hundred in Medway Creek, we used only six mon shiners were then placed into either pool and fish in each test school so behavior could be recordings of their behavior begun immediately. monitored for individuals. A ,white, circular pool The number of fish in vegetation over a 1 min (1.82 m (diameter) was filled with aged water to a period was recorded (from behind a blind) with one depth of 10 cm, well within the range observed in channel of an event recorder (Esterline-Angus) for Medway Creek, but shallow enough to make the each fish, every 5 min over a 1 hour period. school vntually two-dimensional (Williams 1964, Van Olst & Hunter 1970). A clear plastic (poly- Results and discussion ethylene) liner in the pool was discarded’with the water after each use. An overhead 400 watt incan- Schreckstoff caused a significant increase (Mann- descent bulb provided illumination. Whitney U-test, p x0.05) in cohesion among shiner Six fish. of equal length (A 0.3 cm) were placed schools (Fig. 1). This result concurs with the in- into the pool and left undisturbed for 1 hour. Then creased cohesion among schools of Rasbora hetero- either 2 1 of aged water (control) or 75 ml of morpha in response to Schreckstoff (Thines & Schreckstoff extract followed by 2 1 aged water was Vandenbussche 1966). Significantly less variation poured in through a hose near the edge of the pool. (F-test, p ~0.01) was found in the mean distance of Immediately after the introduction of this water, school center in the presence of Schreckstoff extract five photographs were taken, without flash at 1 min (Fig. 1). In addition, a significant positive corre- intervals with black and white film (ASA 400). This lation (p ~0.05) was found between size of fish and was repeated for 20 different schools (10 control, 10 mean distance to center (Fig. 2). It is to be expected Schreckstoff). A minimum of three photographs that larger fish have a greater mean distance to from each lschool were used for analyses. school center for physical reasons. This relationship Each negative was projected on a 18 y\ 24 cm was not found for control groups, so the treated

26 20 hesion has been reported in response to predators in sticklebacks, Gasterosteus aculeatus, and guppies, z } ‘-ISE *lSD Poecilia veticulata (Keenleyside 1955, Seghers 1974). I 1 Shiners exposed to Schreckstoff extract spent more time hidden in vegetation than did controls (Fig. 4). The initial response of shiners provided with vegetation is to seek cover. The presence of Schreck- stoff causes the fish to remain hidden and not begin exploratory movements as they would normally. This minimizes movement, and so may further decrease detection by predators (Edmunds 1974). But when does the fright reaction consist of cover seeking and when does it produce increased structural organization of the school? If schooling is simply a form of cover seeking !j (Williams 1964), the answer is obvious. In the absence of other kinds of cover, fish take cover among themselves (i.e. increased school cohesion). Another possibility is that cover seeking may occur

Cl - mainly in shallow water. Remains of shiners have

COntrOt Schrecksfoff been found in the stomachs of a number of pisci-

Fig. 1. The effect of Schreckstoff on school cohesion (as vorous birds which feed in shallow water (Salyer & measured bg the mean distance to the centre of school, Control Lagler 1940,1946, Kushlan 1978). Moving a dark ob- N=lO, Schreckstoff N=lO). schools not only exhibited greater cohesion but alsq seemed to pack together as closely as thtir size would permit. Furthermore, Schreckstoff treated schools were significantly more polarized than’ controls (Fig. 3). The, changes in the Schreckstoff treated schools mean the:y were more uniform or structured (Shaw 1978, p. 66). This decreases the probability of spatially odd individuals, such individuals being more susceptible to predation (Mueller 1971, Mi- linski 1977). The greater organization of the school should also enhance communication through’ a variety of sensory channels. This enhanced structural organization supports the theory of schooling as an antipredator mechan- 5_y:-‘-- ism (Hobson 1968). The confusion effec?‘ from a . number of closely-spaced fish suggests that predators are unable to fixate on several moving f/ targets simultaneously, but must isolate a single 4 5 6 7 fish. Rock bass, Ambloplites uupestris, prey on Mean total length (Cm) schools of common shiners by itriking at the school Fig. 2. The relationship of distance to centre of school with mean size of shiner. Schools exposed to Schreckstoff exhibit a to scatter the individuals, and then feeding on significant positive correlation (r=0.724, p <0.05, regression isolated prey (Heczko 1980). Increased school co- line of best fit).

27 ject over an experimental pool, to simulate an aerial defense mechanism (Edmunds 1974), and increased predator, always elicited cover-seeking behavior cohesion the secondary mechanism (avoidance of in the shiners. But shiners never entered vegetation being captured once detected). when a rock bass was present in the pool (Heczko 19’80). Thus, cover seeking may be the primary Acknowledgements

This paper is based on an M.Sc. thesis at The

E +- ISE University of Western Ontario, supported by a N.S.E.R.C. research grant to B.H. Seghers. Many thanks to Brian Bietz, Helene Dupuis and Graham Sudbury for help in collection of the fish, John Englert for encouragement and assistance dur- -ing the course of the study, Roger Green for statis- ” tical guidance and Jean-Guy Godin for critical reading of the initial draft.

References cited

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