Role of learning in mesh penetration behaviour of haddock (Melanogrammus aeglefinus)

Transcription

1 ICES Journal of Marine Science, 61: 1190e1194 (2004) doi: /j.icesjms Role of learning in mesh penetration behaviour of haddock (Melanogrammus aeglefinus) H. Özbilgin and C. W. Glass Özbilgin, H., and Glass, C. W Role of learning in mesh penetration behaviour of haddock (Melanogrammus aeglefinus). e ICES Journal of Marine Science, 61: 1190e1194. If fish that have passed through the meshes of a fishing net are capable of escaping more easily on subsequent encounters, there may be important implications for the efficiency and selectivity of fishing gears in heavily fished populations. Here we report on the effect of learning on mesh penetration of haddock (Melanogrammus aeglefinus) under laboratory conditions. Ten haddock were trained using a classical conditioning procedure (with food) to race between two alternately flashing light emitting diodes (LEDs) positioned at the ends of a 6-m-long oval swimming pool. Once the fish were conditioned to race between the LEDs, their penetration ratios in netting barriers of 200-mm and 100-mm bar length, square-mesh curtains in their path on each food presentation were calculated. Fish were reluctant to penetrate mesh barriers of 200 mm at the beginning of the experiment, but all the experimental animals did manage to penetrate. The ratio of these fish in penetrating the smaller mesh size of 100 mm decreased in the first two presentations, but then increased again with experience. The potential consequences of these findings in relation to gear efficiency and gear selectivity studies are discussed. Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: haddock, learning, mesh penetration. Received 20 March 2003; accepted 26 April H. Özbilgin: Ege University, Fisheries Faculty, Bornova, Izmir, Turkey. C. W. Glass: Manomet, Center for Conservation Sciences, 81 Stagepoint Road, PO Box 1770, Manomet, MA 02345, USA; glasscw@manomet.org. Correspondence to H. Özbilgin; tel: C ; fax: C ; ozbilginh@yahoo.com. Introduction It has been shown experimentally that fish (as well as higher vertebrates) can readily acquire conditioned reflexes to any external stimulus for which they have corresponding receptors. As early as 1955, Golenchenko raised the possibility that fish could have conditioned responses to active fishing gear; this was further investigated by Kuhorenko (1977) and Pyanov (1993). Pyanov demonstrated conditioned avoidance reactions to trawls which allowed fish to escape from the path of an approaching trawler, and similar reactions have been noted for other species (see Soria et al., 1993; Fréon and Misund, 1999). Fernö and Huse (1983) demonstrated that cod (Gadus morhua), through learning, can adapt their behaviour to avoid hooks. However, despite evidence of avoidance behaviour, fishing gears still capture fish, and in areas where fishing effort is high there is a likelihood that individual fish may encounter fishing nets from time to time. For fish that are able to pass through the meshes of the net there is a strong suite of stimuli that provide the potential for learned responses. It is known that fish can learn quickly, particularly in response to aversive stimuli. Passing through fishing net can be considered as an aversive stimulus, since evidence from both laboratory experiments (Glass et al., 1995) and underwater observations of fish swimming in trawl nets (Glass and Wardle, 1995) indicates that fish avoid penetrating meshes when an alternative path is available. Both fishing gear selectivity experiments and underwater video observations show that significant numbers of fish escape from fishing gears by penetrating the meshes, particularly in small size ranges. As fish grow in size their escape probability decreases, because the mesh opening remains the same. However, prior history of mesh penetration may affect the ability of a fish to escape on the next encounter. If experienced fish can modify their escape behaviour, the implications are important, since in gear efficiency and gear selectivity studies it is assumed that for a given species and size class all fish have an equal probability of being caught. If prior history is important, the efficiency and selectivity of the same gear may not be the same for all individuals. These may vary between a non-fished area (where fish are /$30.00 Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.

2 Mesh penetration behaviour of haddock 1191 naive) and a heavily fished area (where fish may already have experienced mesh penetration). In other words, experienced fish may have a higher probability of survival than naive fish. This information can have important implications for population surveys and whole net selectivity data. The effect of learned avoidance behaviour in fishing operations has been discussed by Fréon et al. (1993) and Soria et al. (1993), who concluded that there could be a long-term decrease of catchability in exploited stocks where fish are relatively more experienced than fish of an unexploited stock. This paper reports on an experiment carried out to investigate the role of learning in modification of avoidance responses of fish as a means of understanding the process of net penetration. A group of 10 haddock (Melanogrammus aeglefinus) was conditioned to race between two alternately flashing light emitting diodes (LEDs) associated with food reward, and their progress in penetrating first 200-mm and then 100-mm bar length mesh barriers is reported. The study was not designed as a classical study of learning in fish; the primary aim was to find out if prior history of a fish affects subsequent behaviour and to discuss this in terms of the potential effects on whole gear selectivity. Although the research described here is at a preliminary stage, some results are presented with possibly wide applications. Material and methods The experiment was carried out at the Fish Behaviour Unit of the Marine Laboratory in Aberdeen in March A group of 10 haddock was used with an average total length of approximately 30 cm. The fish were caught using barbless hooks and held in the laboratory for more than six months. Water temperature varied between 7(C and 8(C during the course of the experiment. Tank design The experiment was carried out in an oval swimming pool (6.1! 3.6! 1.2 m) with 0.9-m water depth (Figure 1). The tank room was illuminated with a diurnal light cycle using overhead white bulbs adjusted by a computer to simulate sunrise and sunset. A video camera (Panasonic, WV CL 350) was mounted on the ceiling above the tank to record the behaviour of the fish during the experiment. Two feeding stations, with LEDs and feeding pipes (Özbilgin, 1998), were established in both ends of the experimental tank. A mesh curtain, opened and closed by means of a pulley system, was used as a barrier in the middle of the tank, between the two feeding stations. Two 3.6! 1.2-m mesh curtains were made with 200-mm and 100-mm bar length square meshes using 1.8-mm diameter white twine. The bottom lines of these curtains were rigged with white leaded rope. The intention in choosing these mesh sizes was to create a situation where the fish could easily pass through the meshes, as in the case of juvenile fish in commercial fishing. Experimental protocol A week before the experiment started, experimental animals were put into the experimental tank and conditioned to swim towards flashing LEDs associated with a food reward (chopped sandeel) at a feeding station. The amount of food provided was limited to a maximum of 3% of fish weight per day, using at least 100 pieces of food in each session. Only one session with 5e10 food presentations was performed each day. Each session was completed within 2e5 min and the experiments were carried out at different times of the day to prevent an anticipation effect. In the first presentation of each day the mesh curtain remained open (termed as the control presentation ), LEDs on one side of the tank were switched on, food reward was given, and fish were gathered on one side of the tank. When the fish were eating the food reward, the 200- mm mesh curtain was closed. As soon as the food was eaten, the LEDs were switched off. The LEDs on the opposite feeding station were then switched on and food reward was given about 2 s later. The LEDs remained flashing for only 10 s. When the majority of the fish did not penetrate, another control presentation without mesh curtain was done to gather them all in one feeding station. After achievement of a consistently high percentage of mesh penetration (O60% on repeated trials), the 200-mm mesh curtain was replaced by a 100-mm mesh curtain. Data analysis All the sessions were video-recorded and the recordings were analysed frame by frame. In the control presentations, the numbers of fish reacting to the flashing LEDs (arriving at the feeding station) were counted. When the mesh curtain was closed, the number of reacting fish ( penetrating the mesh barrier and reaching the feeding station) and the total numbers on that side before any reaction had taken place were counted to yield an estimate of the fraction of fish successfully passing through the mesh. Results In 29 of 34 control responses, prior to closure of the mesh curtain, 100% of the fish responded to the LEDs (Figure 2). There was only one trial with a 60% response, one with 80% response, and three with 90% response. When the 200-mm mesh curtain was closed, the penetration percentages were zero in the first five presentations. The main behaviour pattern of the fish during these presentations was to swim in a circle and keep away from the mesh barrier. On some occasions fish swam towards the LEDs at the far end but turned away before reaching the barrier. These fish did not complete their

3 1192 H. Özbilgin and C. W. Glass Figure 1. Experimental tank. Feeding pipes and LEDs are set at both ends of the tank. response to the light flashing beyond the mesh barriers but raced to the LEDs in the following control presentation. From the sixth closure of the 200-mm mesh curtain, penetration percentages were approximately 30 in the following three presentations and with the exception of one occasion more than 50 in the following 14 presentations. Mesh penetration reached 100% in the 15th closure of the mesh barrier. When the 200-mm mesh curtain was replaced with the 100-mm mesh curtain after the 22nd presentation, the penetration percentage of the fish dropped dramatically to between 20 and 40. However, in the third presentation with 100-mm mesh, penetration reached 100% and did not fall below 60% in the following 21 presentations. Discussion The results of this study show that although the mesh openings were at least several times larger than the crosssection of the fish, they did not penetrate the meshes at the beginning of the experiment. This is in good agreement with observations of fish in fishing gears (Glass et al., 1995), where fish are seen to avoid the meshes of netting surrounding them. This, in turn, results in reduced selectivity of many fishing gears. It can be concluded from the results of this experiment that prior history in haddock can have an effect on their mesh penetration. During the course of the experiment, previous experience of mesh penetration usually resulted in a faster penetration in the following food presentation. Brown and Warburton (1999) reported a similar observation for rainbowfish (Melanotaenia duboilai) in shoals of five displaying a significant decrease in escape latencies over a series of five model trawls. Moreover, once some of the fish in a group experienced mesh penetration, usually a higher percentage penetrated in the following food presentations. Fish seemed to follow each other, which may be regarded as social learning (Noakes and Baylis, 1990). One fast-learning fish can be an example to the other fish and so encourage them to react to the LEDs. Similar observations were made by Hunter and Wisby (1964), who found that carp trained to avoid a moving net learned faster when in groups rather than as individuals. Brown and Warburton (1999) also reported that rainbowfish in shoals of five found and escaped through a hole in the oncoming net more quickly than fish in pairs. These observations may be summarized as follows: (1) if a fish has previous experience in responding to a stimulus, it can process the same information faster in the next encounter, and (2) mesh penetration behaviour of a fish in a group may be socially transmitted to the rest of the group. Gear selectivity studies indicate that a significant proportion of the juvenile fish entering codends pass through the meshes of the netting, that is, they experience what we term here mesh penetration. If what has been demonstrated in these laboratory experiments occurs in commercial fishing operations, it could be expected that juveniles that have already experienced mesh penetration may have a lower probability of capture than fish entirely naive to the stimulus given by the fishing gear. Pyanov (1993) argues that fish learn to avoid the trawl in a single encounter with a net. His evidence is that the fish caught by a trawl in an area previously never fished and later tracked by the means of Pinger transmitters always avoided the trawler in the subsequent tows from about 50-m distance. On the other hand, tagged fish that were originally caught with gillnets demonstrated a herding reaction to the approaching trawler and were caught by the gear.

4 Mesh penetration behaviour of haddock Response percentage Number of food presentations Figure 2. Percentage of the reaction completed in less than 10 s by haddock (Melanogrammus aeglefinus). Circles are control trials, blank squares are trials with 200-mm mesh barriers, and black squares are trials with 100-mm mesh barriers. It was not within the scope of this study to estimate the number of fishing gear encounters of a given size and species of fish. Despite the present experiment, it is not known how many gear avoidance experiences or mesh penetrations are needed in the wild for fish to learn effective capture evasion behaviour. Probability of gear encounter and probability of mesh penetration are expected to vary significantly between the fishing grounds and speed of learning of an individual fish. However, some fishing effort studies may provide a rough estimate of the probability of a given area being fished by a specific category of fishing gear. For example, total area swept in 1989 in the North Sea by towed fishing gears in contact with the seabed (including beam trawl, otter trawl, industrial pair trawl, industrial single trawl, pair trawl and seine) was km 2 year ÿ1 (ICES, 1995). Because the area of the North Sea is approximately km 2, we can expect that, on average, an area equivalent in size to the entire North Sea was fished by demersal towed gears at least once in Furthermore, fishing effort shows significant concentrations on particular fishing grounds. For example, the hours fished by demersal otter trawls in different ICES statistical rectangles may vary by as much as several hundredfold (Jennings et al., 1999). If the avoidance of areas where gear may be lost in these rectangles is taken into account, the numbers indicating the concentration of fishing effort in certain grounds would be even greater. The current study demonstrates that haddock can modify their behaviour based on prior experience. Although they are reluctant to penetrate the mesh barriers in a laboratory setting (as they are in commercial trawling situations), one mesh penetration tends to increase the probability of penetration in the next encounter. Fish that encounter a trawl gear on more than one occasion may be capable of escaping more effectively on subsequent encounters, and, perhaps more importantly, may help facilitate learned responses in naive fish. However, it has to be remembered that the results presented here were obtained using food as reinforcement, which is different from the situation in field, where freedom is the reinforcer. The true nature and effect of the learning abilities of fish in codend mesh penetration behaviour during commercial fishing operations remains to be investigated. Acknowledgements Thanks are extended to Ben Williamson, Ally Findlay, and Witek Mojsiewicz for looking after the fish and helping to set up the experimental tank, to Dr Clem Wardle and Dr Monty Priede for their discussions, and to L. Kasal and G. Gökçe for drawing the experimental tank. H.Ö. acknowledges the Ministry of National Education of the Turkish Republic for support during his studies at the Marine Laboratory in Aberdeen. References Brown, C., and Warburton, K Social mechanisms enhance escape responses in shoal of rainbowfish, Melanotaenia duboilai. Environmental Biology of Fishes, 56: 455e459. Fernö, A., and Huse, I The effect of experience on the behaviour of cod, Gadus morhua, towards a baited hook. Fisheries Research, 2: 19e28. Fréon, P., Gerlotto, F., and Misund, O. A Consequences of fish behaviour for stock assessment. ICES Marine Science Symposia, 196: 190e195. Fréon, P., and Misund, O. A Dynamics of Pelagic Fish Distribution and Behaviour: Effects on Fisheries and Stock Assessment. Blackwell Science, Oxford. 348 pp. Glass, C. W., and Wardle, C. S Studies on the use of visual stimuli to control fish escapes from cod-ends. II. The effect of a black tunnel on the reaction behaviour of fish in otter trawl cod-ends. Fisheries Research, 23: 165e174. Glass, C. W., Wardle, C. S., Gosden, S. J., and Racey, D. N Studies on the use of visual stimuli to control fish escapes from cod-ends. I. Laboratory studies on the effect of a black tunnel on mesh penetration. Fisheries Research, 23: 157e164. Golenchenko, A. P Speech. In Proceedings of the Conference on Fish Behavior and Searching, pp. 53e54. Ichthyological Commission, 5, Academy of Science, URSS, Moscow. 236 pp. (in Russian)

5 1194 H. Özbilgin and C. W. Glass Hunter, J. R., and Wisby, W. J Net avoidance behaviour of carp and other species of fish. Journal of the Fisheries Research Board of Canada, 21: 613e633. ICES Report of the Study Group on Ecosystem Effects of Fishing Activities. ICES Cooperative Research Report, No pp. Jennings, S., Alsvag, J., Cotter, A. J., Ehrich, S., Greenstreet, S. P. R., Jarre-Teichmann, A., Mergardt, N., Rijnsdorp, A. D., and Smedstad, O Fishing effects in northeast Atlantic shelf seas: patterns in fishing effort, diversity and community structure. III. International trawling effort in the North Sea: an analysis of spatial and temporal trends. Fisheries Research, 40: 125e134. Kuhorenko, K. G Formation of defense conditioned reflex to fishing gears in Atlantic mackerel. In Fish Behaviour Studying in Connection with Fishing Gear Perfecting, pp. 91e97. Proceedings of the Institute for Animal Evolution, Morphology and Ecology, Moscow. 177 pp. (in Russian). Noakes, D. L. G., and Baylis, J. R Behaviour. In Methods for Fish Biology, pp. 555e583. Ed. by C. B. Schreck, and P. B. Moyle. American Fisheries Society, Bethesda, Maryland. 704 pp. Özbilgin, H The seasonal variation of trawl cod-end selectivity and the role of learning in mesh penetration behaviour of fish. PhD thesis, University of Aberdeen, Scotland, UK. 206 pp. Pyanov, A. I Fish learning in response to trawl fishing. ICES Marine Science Symposia, 196: 12e16. Soria, M., Gerletto, F., and Fréon, P Study of learning capabilities of tropical clupeoids using an artificial stimulus. ICES Marine Science Symposia, 196: 17e20.