Z. Tierpsychol., 52,285-290 (1980) @ 1980 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-3573 I ASTM-Coden: ZETIAG

Department of Biological Sciences, The University of Gezira, Sudan

Aquarium Studies on the Ability of Potential Predators to Learn to Avoid Humbug Damselfish,

Dascy ZZus aruanus (Pisces, Pomacentridae) as Prey

By DAVID COATES

With one figure

Received: February 11, 1980

Accepted: March 10, 1980

Abstract

Five species of potential predators of D. aruanus were trained in aquaria using a simple reward versus no-reward training technique in which D. aruanus (no-reward) and a variety of alternative prey species (reward) were pres'ented simultaneously to the former. All the predators tested exhibited an ability to learn to approach the reward species of fish in pre- ference to D.aruanus. Results are discussed in relation to the recently proposed theory that potential predators may learn in the field not to attack D.arrranws but to concentrate on alternative and more easily caught prey.

Introduction

It has been suggested by COATES (1980a) that i t is difficult for certain predators to capture humbug damselfish (Dascyllus aruanus) provided that the latter are aware of the presence of the former. The conspicuous colour-pattern- ing exhibited by D. aruanus and the conspicuous way in which this is display- ed by this species during the presence of a threat has been described and in- vestigated by COATES (1980b). In this work the hypothesis was presented that certain predators may learn not to attack D . aruanus due to this difficulty in capture and thus concentrate on alternative, more easily caught prey; this learning being aided by the conspicuous behaviour and colour-patterning so described. The present work investigates the ability of certain potential pre- dators to learn in the way suggested.

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286 DAVID COATES

With regard to the hypothesis in question i t is interesting to note that GIBSON (1974) has demonstrated the effectiveness of contrasting colour, as opposed to background or matching colour, in “avoidance-image formation” in the star finch (Bathilda ruficauda). This species learned not to attack “apose- matic” seeds but to concentrate on other (“cryptic”) seeds due to a lack of reward with the former. As early as 1901, TRIPLETT showed that perch (Morone americanus) when separated from minnows by a glass screen would, after a period of time, cease to attack this potential prey in that part of the aquarium even when the latter were no longer separated by the intervening glass. They would however again make futile efforts to reach another type of prey, for example worms, when these were placed behind the glass. Essentially similar experiments are listed by WARDEN et al. (1936). HOBSON (1968) states that most predatory fish have large brains (including the Serranidae, possibly the commonest potential predators of D. aruanus) and presumably this factor contributes to their learning ability.

The learning abilities of fish have been studied in some depth and this phenomenon in itself is well documented in the reviews of, for example, THORPE (1963), INGLE (1968) and GLEITMAN and ROZIN (1971). In such works it is shown that fish, in general, are quite capable of learning to solve a variety of problems. Discrimination learning and the discriminatory abilities of fish are also well documented (e.g. MACKINTOSH 1965; SUTHERLAND 1968; INGLE 1971; YAKIMENKO 1975). The present work concerns the simple con- firmation that certain of the potential predators of D. aruanus can learn in the way suggested by COATES (1980 b). The learning ability of predators was investigated in aquaria using a simple reward versus no-reward training tech- nique in which D. aruanus (no-reward) and an alternative species (reward) were presented simultaneously as potential prey.

Method

20 D.aruanus were collected and kept in aquaria. These fish were chosen a t random to serve as no-reward fish. Specimens of D. marginatus, D. trimaculatus, Chromis cueruleus, C. dimidiatus and Anthias squamipinnis were collected within the vicinity of concentrations of social groups of D.aruanus and thus all of these six represent alternative prey species in the field. These fish were also housed within aquaria and one individual (the species being chosen at random) was used to constitute a reward species of test fish. Reward and no-reward fishes had similar size ranges. The colour-patternings of no-reward species differ considerably from that exhibited by D. aruanus (illustrations provided by e. g. CARCASSON 1977).

6 individuals of each of the five predatory species of fish tested by COATES (1980a) were collected within the vicinity of social groups of D . aruanus. These species were Cephalo- pholis argus, Pterois volitans, Gramistes sexlineatus, Parapercis cylindrica and Epinephelus fuscoguttatus. These were housed within individual aquaria measuring 100 X 40 X 40 cm and having opaque sides. An opaque partition served to demarcate the left and right sides of each aquarium and was fixed vertically and in a central position at one end of each aquarium. These partitions extendcd 20 cm into each aquarium and marked the boundary of the left and right “compartments”. Predators were left one week to acclimatise and after that period were not fed except during the training procedure.

Ability of Potential Predators to Learn to Avoid Humbug Damselfish as Prey 287

3 0 Gramis tes s exlineatus

&\ . . . Y

A ., . . . ., , . . ,~ -.L_1

10 20 30 Day Number

Parapercis cylindrica

' O l . . .

30 1 Pterois volitans

1 . . . . 10 20 30

D a y Number

30 Epinephelus fuscoguttutus

L J 10 20 30

Day Number

10

I 10 20 30

Day Number

Fig . 1: The total number of non-approach (.. .... ), approaches to the no-reward fish (- - . - ..) and approaches to the reward fish (- ) made by the various species of pre- datory fish tested, throughout the training

procedure

288 DAVID COATES

Individual test fish were housed within individual and identical transparent perspex boxes (6cm tubes) the front section of which could be raised by using a length of cotton thread allowing remote operation thereby providing the predator with access to the test fish. Presentation consisted of suspending the boxes in a compartment by using clips. Reward and no-reward test fish were presented simultaneously, the former in the right or left compart- ment at random, the latter in the alternative compartment.

A trial consisted of the following. When a predator was’ at the opposite end of the aquarium to the partition the test fish were presented. If a predator approached the reward fish this was released into the aquarium and usually immediately eaten. If the predator approached the no-reward fish this was not released. An “approach” was defined as a predator entering either of the compartments. The test apparatus was always removed (including any test fish) 2min after presentation irrespective of an approach by a predator. A predator’s initial choice of compartment only was recorded.

Five trials were undertaken, at intervals of 15 min, each day for each predator. Each predator was trained with this procedure over a period of 30 days.

Results

All the predators tested exhibited an ability to learn the problem set. Over the training period there was firstly, an increase in approaches towards the reward fish and secondly, there was a decrease in approaches towards the no-reward fish (Fig. 1).

The last 15 training days were considered statistically. Significantly (sign test p < 0.05) more approaches were given towards the reward fish compared to the no-reward fish on 14 of these days for C. argus and Pt. volitans; 15 days for G. sexlineatus; 9 days for Pa. cylindrica and 12 out of the 15 training days for E. fuscoguttatus.

No comparisons between species will be attempted here although it must be stressed that such differences are not necessarily due to any differences in generic or specific learning ability. For example, Pa. cylindrica does not adapt well to aquarium life and being a bottom living species only moving occasion- ally to lunge a t its prey from a distance (pers. obs.; HIATT and STRASBURG 1960; RANDALL 1967; HOBSON 1974) the training technique used is not that most suitable for studying the abilities of this species. The relatively “poor” performance of the latter species may be due to these factors as witnessed by the high proportion of non-approaches recorded (Fig. 1). In contrast, G. sex- lineatus showed very good learning in this situation. This species adapts very easily to aquarium life (pers. obs.).

Discussion

All of the species of predators tested demonstrated an ability to learn to approach other species in preference to D. aruanus. It is reasonable to assume that this was due to the lack of reward when approaching the latter species or, conversely, due to the reward obtained on approaching the alternative species. A learning ability has been demonstrated in these potential predators of D. aruanus that is considered beyond that required in order to support the

Ability of Potential Predators to Learn to Avoid Humbug Damselfish as Prey 289

hypothesis presented by COATES (1980 b). That is, that certain predators may learn to avoid this species in order to concentrate on more easily caught prey. Of course it remains to be shown that this type of learning actually occurs in the field situation. Studies on learning in the field are not easy. FRICKE (1975) has reported studies on a predatory coral-reef fish (Balistes ~ U S C U S ) preying on urchins, demonstrating the importance of learning in this situation.

It is generally accepted that predators will tend to concentrate on those prey that are vulnerable or those that are most easily caught (e.g. KREBS 1973; MURDOCH and OATEN 1975). Taking this accepted fact to its logical con- clusion it must be assumed that a certain amount of learning must take place by some predators of the prey that are most easily available to them. Such a phenomenon has been observed in many species, for example, great tits (TIN- BERGEN 1960), bluegill sunfish (REED 1969), wood pigeons (MURTON 1971) and coal tits (TULLOCK 1971). Whether or not such examples are truly learn- ing phenomena is discussed by MURDOCH and OATEN (1975) but in each case the behaviour of the predators towards different prey was modified by experience.

O n a coral-reef the density of fish is high and a number of piscivorous fishes exhibit a degree of variation in their individual diets (HIATT and STRAS- BURG 1960; RANDALL 1967; HOBSON 1968, 1974). The effects of experience on the relative effort that such predators devote to capturing different prey species may be considerable. Anti-predator adaptations by prey co-evolve with predator hunting strategies (GILBERT and RAVEN 1975) and the ap- propriate reciprocal effects of such hunting on the behaviour of prey species of fishes on the reef can be expected. For example, certain prey species have an ability to recognise predatory and non-predatory fishes and react accord- ingly (HURLEY and HARTLINE 1974; COATES 1980a), and behaviour and colour-patternings may assist the appropriate learning processes in the poten- tial predators concerned (COATES 1980 b). The situation is undoubtedly complex.

Acknowledgements

I would like to thank R. F. G. ORMOND, P. J. VINE and T. A. REDDING-COATES for their most useful comments on various manuscripts. I am indebted to the Department of Zoology, University of Khartoum for thc use of their Marine Research Laboratory a t Suakin. Financial assistance was gratefully received from the University of Gezira.

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FRICKE, H. W. (1975): Losen einfacher Probleme bei einem Fisch (Freiwasserversuche an Bulistcs fuscus). Z. Tierpsychol. 38, 18-33.

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Author’s address: David COATES, Department of Biological Sciences, The University of Gezira, P. 0. Box 20, Wad Medani, Sudan.