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The effect of experience on the behaviour of cod (Gadus morhua L.) Towards a baited hook
Fisheries Resetrrch. 2 (1983) 19-28 Elsevier Science Publishers B.V., Amsxrdam
19 --Printed
in The Netherlands
THE EFFECT OF EXPERIENCE ON THE BEHAVIOUR MORHUA L.) TOWARDS A BAITED HOOK
ANDERS
FERN6
Institute (Norway)
of
INGVAR Institute
Fisheries
Biology,
University
Technology
Research,
of Bergen,
P.O.
Box
OF COD (GADUS
1839,
N-5011
Bergen
HlJSE+ of Fisheries
(Accepted
6 January
Bergen
ih’orway)
1983)
AFSTRACT Fe&i, J.. and Hue, l., 1983. The effect of expericwe on the behaviour morhua L.) towards a baited Ilook. Fxh. Res.. 2: -3-28.
of cod (Godus
The behaviour of cod towards a baited hook was observed in a ring tank. The intensity of the response was highest initiaiiy, with a modification of the behaviour developing after experience with the baited ho*,k, Irrespective of actual hooking. Hooking occurred less often with time and the hooking probability decreased for consecutive strong responsea of individual cod. The implications of a modification of the behaviour towards baited hooks for !ong line Pishing are discussed. INTRODUCTION
During fishing experiments with hooks and lines, there is a decreased catchability of carp (Beukema, 1970a; Beukema and de Vos, 1974) pike (Beukema, 1970b), largemouth bass (Hackney and Linkous, 1978) and rambow trout (O’Grady and Huges, 1980) during the course of fishing. This is believed to be due to the development of hook avoidance. It is known that pike and perch become negatively conditioned to eating sticklebacks, as the spines hurt the predator’s mouth (Hoogland et al., 1956). and that codfish (Mackay, 1977) and catfish (Little, 1977) can develop a stron.g aversion to food associated with toxicosis. No behaviour studies have, however, been made to investigate the direct modification by experience of response to a hook. In field studies on the behaviour of fish towards long lines (Fern5 et al., 1977; Tilseth et al., 1978), individual fish can seldom be followed for long, *Present N-5392
address: StorebB.
0165-7836/83/$03.00
Institute Norway.
of Marine
0 1983
Research,
Austevoll
E!sevier Science Publishers
Marine
B.V
Aquaculture
Station,
20 and a modification of the behaviour is therefore not easily studied. The present paper describes some laboratory experiments on the behaviour of cod towards a baited hook. Long-lining with baited hooks is one of the major fishing methods in Norway and cod is M important species in this fishery. The aim of the study was to investigate how the behaviour of cod towards a baited hook was influenced by experience. Both the effect of hooking and the effect of experience with the baited hook without hooking could he evaluated in the study. MATERIALS
AND METHODS
Two similar experiments were carried out in 1977. Experiment 1 ran from 24 May-7 June with 10 days of investigation, and Experiment 2 from 9 November-l December with 17 days of investigation. The 15 cod in Experiment 1 had a mean length of 72.1 cm (range 60-83 cm) and a mean condition factor of 1.02. They belonged to the Arcto-Norwegian stock and were caught by trawl in the Barents Sea. During their three-year storage in outdoor concrete tanks they were subject to several bait bag preference tests in the ring tank used for the present study. They spawned for the first time in the spring of 1977. The 20 coastal cod used in Experiment 2 had a mean length of 53.5 cm (range 48-64 cm) and a mean condition factor of 1.03. They were caught in traps two months prior to testing and stored in outdoor tanks. All fish were fed mainly on squid in their home enclosures, but were not fed in the experimental tank. The fish were individually tagged with easily readable slightly buoyant dorsal tags. (The data from four fish who lost their tags during the experiments were included only where it did not bias the analysis, and data from three fish that died or were damaged during the experiments were disregarded.) Length and weight were measured during transportation to the indoor experimental tank. The tank was ring-formed with an outer diameter of 14 m, an inner diameter of 10 m and a depth of 2.3 m. The water temperature was 6--9”C and the light regime was 8 h light and 16 h dark. Testing commenced 10 days (Experiment 1) and 12 days (Experiment 2) after transportation and tagging to allow the fish to become accustomed to the environment. Usually, five trials were made on each experimental day at about the same time each day. A total of 49 and 85 trials were made in Experiments 1 and 2, respectively. A trial involved the placing of one baited hook (a barbless Mustad-Norway No.6) in the tank, and lasted for 10 min, until one fish was hooked or until the bait was lost. The hook was attached to a 2-m piece of long line by a 40 cm snood and placed 50 cm above the tank bottom. Rings of squid were used as bait snd attached to leave the point of the hook exposed. Bait was changed in the 5 min pause between trials. Hooked fish were freed in the tank when possible, but they sometimes
21 came loose of their own accord. If the hook was swallowed the fish was removed from the tank, anaesthetiized, unhooked and returned to the tank. Observations were conducted from the centre of the ring. The behaviour of each cod towards the baited hook was recorded verbally on tape and some of the trials were video-taped for more detailed study. A number of behaviour patterns were defined as follows: -swimming towards the bait while looking at it and turning Approach before touching the bait. -touching the bait with the trailing barbel or lips. If tasting Taste was followed by bite or incomplete bite, it had to last it least two seconds in order to be recorded. -sucking the bait into the mouth. Bite Incomplete bite -differs from bite in that the whole bait is never within *he closed mouth, either because the fish takes only a part of the bait in the mouth or because the mouth is not completely closed. -swimming around with stretched snood with the bait in Pull the mouth. -manipulating the bait in the mouth with chewing moveChew ments. Jerk -a rapid movement of the head with the bait in the mouth, typically directed to the side. Shake -several rapid lateral movements with head and body while the bait is in the mouth. Cod show thii behaviour pattern when seperating the softer part of a mussel from the shell (Brawn, 1969). -swimming rapidly forward with bait in mouth. Rush Bait out of the mouth -the bait is spat or pulled out of the mouth. Hooking -the hook is retained in the mouth for at least 20 E while the fish fights violently.
TABLE
I
Numerical
values
Behaviour
pattern
Approach Taste Incomplete Bite
bite
assigned
to behaviour Value 1 2 3 4
Jerk Pull Chew
5 5 5
Shake Rush Hooking
5 6 7
patterns
22
Behaviour patterns were given numerical values, whose values increased with increasing intensity of the response (Table I). The defined behaviour patterns could occur individually or in various combinations. A “sequence” was defined as a series of behaviour patterns that terminated when the fish left the field of observation or when another fish reacted to the baited hook. The number of behaviour patterns in a sequence varied from l-12. A strong response was defined to occur when a fish took the bait in the mouth and made one or several of the behaviour patterns with highest intensity, i.e., rush, jerk, shake, chew and pull. A strong response was terminated when the fish was hooked or the bait left the mouth. Several strong responses could occur within one sequence. RESULTS
The frequency of occurrence of the defined hehaviour patterns is given in Table II. Bait out of mouth was a common occurrence in both Experiments 1 and 2. In Experiment 1, bite and rush were observed frequently, whereas in Experiment 2 approach and incomplete bite were more often recorded. Generally speaking, high intensity behaviour patterns were exhibited relatively more often in Experiment 1 than Experiment 2. The sum of behaviour patterns exhibited on a given experimental day varied considerably, but displayed no general trend in Experiment 1. In Experiment 2 there was an overall increase with time. In both experiments there was generally an increase in the relative frequency of low intensity behaviour patterns and a decrease in high intensity hehaviour. The best indicator of the effect of experience is the individual behaviour changes with repeated encounters with the baited hook. To this end, each distinct sequence was given a value as the sum of the numerical values of its behaviour patterns. Successive sequences made by each cod could then be compared. The mean sequence values for the first 20 sequences are given in Table III. Many fish made less than 20 sequences and thus the mean sequence value is based on a decreasing number of fish. In both experiments the mean decreased steadily over time. There was a significant difference between the means of sequence 1 and sequence 2 (Wilcoxon matched-pairs signed-ranks test, P < 0.05) and by the fifth sequence the mean had decreased to approximately one half of the initial value. Sequences 16-20 had means which were only about 35% of the mean of sequence 1. Table III also shows that the means of the sequence values decreased sirnilarly between hooked and not hooked fiih as well as between fish with different condition factors. The category of hooked fish consisted of fish hooked during the first 20 sequences. Most fish (12 out of 15 fish) ware hooked in sequence 1-5. The mean sequence value for the 20 first sequences (grand mean) was
II
617
71
10.1
Sum
%oftotal
30.9
1 4 30 20 22 36 59 39 43 28 16 23 71 32 44 64 65
12
___-~--
Approach
Frequency
4.2
12.1
241
8 4 11 32 10 12 26 6 6 17 11 18 27 38
1 4 6 6 6 3 2
32
6 1 8
0 1 3
121
Taste
9.8
75
10 12 8 6 13 3 2
4 5 12
10 1 10
2
14 18 14 16 11 15 10
23 5 20
12
Bite
328 146 16.4 19.1
19 15 17 35 15 13 19 16 12 23 17 36 41 29
Incomplete bite
97 4.9
4 3 7 2 0 3 6 3 3 4 1 3 2 2
11 23 20
6 2 7 3 8 3 5 4 5 3
12
Jerk
46 6.0
oatterns
1 and 2
of bebaviow
in Experiments
of occunence
pattern occarrence
0 0 4 2 5 12 17 18 13 6
Exp. day 1 2 3 4 5 6 I 8 9 10 11 12 13 14 15 16 17
Experiment
Behaviour pattern
Behaviour
TABLE
126 6.3
0 0 1 0 0 0 0 0 0 0 1 0 1 0 0 1 1 6 5 0.~3 0.3
4.3 10 7 I 50 10 5 0 80 2 0 70 42 6 5 3 7 18 23 20
12
Shake
2 2 3 0 1 1 0 0 3 0 2 0 0 1 0 0 0
8 1 3 1 3 1 1 2 1 0
121
Chew
5 4 5 0 0 2 0 0 0 1 0 2 0 0 1 0 0
18 3 10 13 14 10 9 14 10 10
_~~.
Rush
8 23 13 5 3 5 1 6 9 10 7 1 11 1 7 9 7
2
24 7 31 23 30 22 22 22 17 10
12
18 19 26 21 18 23 37 15 16 23 16 14 26 18 38 43 31
Bait out of mouth
208 402 32 12 21 20 111 126 4.2 0.6 2.8 1.0 14.5 6.3 27.3 20.2
7 3 7 2 2 4 3 2 1 1
1 2 --__.
--~~
Pull
1.2
9
1 3 0 1 0 0 0 1 1 2
12
-p
1.1
21
3 5 4 2 0 1 0 0 0 1 3 1 0 0 1 0 0
Hooking
763
94 30 36 70 96 80 85 93 69 48
1
Sum
1995
68 83 127 84 67 108 174 87 103 118 76 67 156 88 166 210 213
2
.s
III
fish
Conditionfactorz Condition factors
fish
1 2
no.
Not hooked
kamked
Experiment Experiment
sequence
0.95 0.95
17.0 16.7
19.4 13.7
(13) (14)
(15) (12) 12.1 9.9
10.2 11.9
13.1 9.9
23.1 13.4
(9) (18)
2
1
10.8 10.5 9.8 11.4
(13) (14)
11.3 10.3
(15) (12)
(9) (18)
3
(12) (13)
(14) (11)
(9) (16)
8.6 8.1
10.8 5.7
10.1 5.7
4
9.5 7.8
10.1 6.8
(14) (10) (12) (12)
11.0 7.5
(8) (16)
6
(11) (10)
(12) (9)
(7) (14)
Mean Kzquence value for the first twenty sequences. The means are given by Experiments by condition factor. The number of fish is given in parentheses
TABLE
(9) (9)
(7)
6.1 9.6 7.0
(11) (11)
9.2
5.5 5.3
5.0
5.6
11-15 7.1 4.3
(7)
9.3 7.5
B-10
1 and 2, by hooked
(8) (6)
7.9 4.5
(8) 4.8
(4)
(6) (6)
(4)
(7)
(8)
6.8
(5)
(10)
16-20 8.4 4.3
(6)
and not booked
9.3 7.6
10.2 7.4
l-20
fish and
25
higher for fish in Experiment 1 than in Experiment 2 (P < 0.01. t-test) and was also higher for fish with the higher condition factor (P < 0.05). The categories of hooked and not hooked could not be compared this way due to the numerical value of hooking and its subsequent effect on sequence value. There was a considerable variation in number of sequences made by the individual cod. Two fish exhibited no behaviour towards the baited hook. Of the 27 fish that produced at least one sequence, 21 fish made at !cast five sequences and 11 fish more than 20 sequences (Table III). The maximum number of sequences by one fish was 413. No significant difference was found in the proportion of fish in either category that exhibited more than 20 sequences. In Experiments 1 and 2 there were 9 and 21 bookings, respectively (Table II), most of which took place early in the experiments (16 hookings during experimental days l-3). For all fish in both experiments (disregarding the hookmgs of fish that lost their tags), 10 cod were never hooked, 11 cod were hooked once, 2 cod twice, 1 cod three times and 2 cod four times. In Experiments 1 and 2, five and four fish, respectively, were hooked in the oesophagus/stomach while four and 16 fish were hooked in the mouth (one fish was caught in the eye). The difference in hooking position between the experiments was not significant (0.05 < P < 0.10, Fisher exact probability test). When calculating the hooking probability for consecutive contacts with the baited hook, it is essential to know which behaviour patterns led to hooking. The exact moment of hooking is, however, often difficult to determine. A cod was sometimes clearly hooked already when pulling or chewing, but in most cases hooking could not be observed with certainty until after a jerk or rush, albeit these behaviour patterns may sometimes have been more the consequence than the cause of hooking. However, hooking always cccurred in connection with a strong response with one or several of the behaviour patterns rush, jerk, pull, chew, and shake. Seven out of 28 fish (25%) were hooked in their first strong response. Eight fish were hooked on their strong response 2-5 (60 strong responses, 10% hooking) and five fish on strong response 6-10 (58 responses, 8.6% hooking). There was a significant decrease in hooking probability between strong response I. and strong response 2-10 collectively (x*-test, P < 0.05). The hooking probability also seemed to vary with the individual - one fish was hooked four times on four strong responses while another fish was never hooked on 45 strong responses.
The experimental cod showed a decrease in the intensity of the response after experience with a baited hook whether or not the fish was hooked. The aecreased intensity could be caused by conditioning -biting the hook could act as negative reinforcement to the cod in the same way as a stickleback’s
26
spines induce cessation of feeding response in pike or perch (Hoogland et al., 1956) or presentation of electric shock during feeding disturbs the feeding behaviour of sticklebacks (Tugendhat, 1960). It may be argued that aversive stimulation from the hook is not the only cause of a decreased intensity of response. Although a hooked fish also receives handling which may act as negative reinforcement this cannot explain the declining response in not hooked fish. An alternative explanation for the observation could be the general restriction of movement by the mood. However, in experiments with baits attached with a string instead of a hook where the fish movement was similarly restrained, no decrease of response intensity was found (A. Fern& 1977, unpublished). Physical stimulation from the hook is therefore regarded as the main factor behind the decreased response. Analysis of the video tapes also indicated that the fish reacted to the hook while manipulating the bait in the mouth and that this often resulted in incomplete mouth closure. Such incomplete bites were generally not observed on unhooked bait. Even if the hook is the critical stimulus for the negative condtiioning, the fish did not seem to distinguish the hook from the bait. When free bait was put into the tank after the experiment, the fish were at first inhibited by the bait and made several approaches, tastings and incomplete bites before eating the bait. A decrease in the intensity of the response was demonstrated in both Experiments 1 and 2, but responses were generally stronger in Experiment 1. The condition factor of the fish was the same between groups, but length of the fish, earlier holding conditions, and time of the year for the experiments differed. It is probable that the cod in Experiment 1 tested in May-June after the spawr,ing season had a stronger feeding tendency than the cod in Experiment 2 %ested in November. A strong tendency to feed after the spawning season is known for cod (Rae, 1967), and codfish take several times more food in May-June than in November under laboratory conditions (P. Solemdal and S. Tilseth, 1980, personal communication). Another explanation is that previous experience of the tank may have made the cod in Experiment 1 less receptive to frightening stimuli. These cod also swam regularly around the tank, while the cod in Experiment 2 more often stayed in one place. The fish were deprived of food during the experiments, apart from small pieces of bait they picked up, and occ;asional stolen baits. While the food deprivation may have initially increased the feeding tendency in the same way as in sticklebacks (Tugendhat, 1960; Beukema, 1968) and rainbow trout (Ware, 1972), the possibility exists that the feeding tendency .vas negatively affected after some time. In blue-gill sunfish, there is decreased gastric digestion after seven days of starvation, and a more pronounced decrease after longer starvation periods (Windell, 1966). A reduced tendency to feed cannot, however, explain the results of the present study. The rapid decrease in the intensity of the response within the first few contacts with the baited
27
hook clearly demonstrates the effect of experience. The fish also responded to the baited hook throughout the experiments, but seemed to be in a conflict between approach and withdrawal (up to seven approaches per sequen?e). Solemdal and Tilseth (1974) found an increased bite actively towards non hooked bait bags in cod during the first experimental week without food. This demonstrates the significance of the hook for the decrease found in the present study. The piece of long line in the laboratory tank was an easily recognizable stimulus and therefore may create an ideal learning situation. The question therefore arises of whether a similar decrease in response occurs after experience with baited hooks in long-line fishing. In field studies on the behaviour of whiting towards a test line, the relationship between the number of fish observed and the number of responses towards the baited hooks indicates that each fish makes relatively few responses, possibly due to a moclification (Ferns et al., 1981). Pike and largemouth bass become more difficult to catch for a second time with hook and line (Beukema, 1970b; Hackney and Linkous, 1978). and one single hooking experience makes carp more difficult to catch for at least a year (Beukema, 1970a). It is therefore probable that cod also show a similar decreased vulnerability. A relatively low intial hooking probability of 25% on the first strong response as found in this study, followed by a rapid modifies&n of the response, could iead to a l&b percentage of cod not being caught during one encounter with a long line. The persistence of this modification in repeated encounters in the variable environment of the sea is difficult to estimate. A monofilament long line catches 40-300% more cod than a multi-twine line (Huse and Karlsen, 1977). It is possible to explain this difference with a learning process in the fish. If both types of lines are attacked equally often initially, the more visible multi-twine line could be more easily recognized by a conditioned fish and therefore more effectively avoided. An alternative explanation would be that a more visible line induces initial avoidance in cod. An initial inhibition towards novel prey has been demonstrated in stickleback and rainbow trout (Beukema, 1968; Ware, 1971). A modification of the behaviour of a fish towards a baited hook may lead the efficiency of a hook to be partly determined by its modificatory effect. In many Pacific types of hooks, the point is bent heavily inwards so that the hook almost forms a circle or a triangle (Stewart, 1977: Forster, 1973). This hook shape may decrease the probability that a fish comes into contact with the point of the hook and thus experiences aversive stimulation when biting which in turn could lead to a greater number of strong responses and higher percentage of hooked fish. Such an effect could combine with a higher hooking probability when fish rush on a bent hook as opposed to a straight hook (Huse, 1979). ACKNOWLEDGEMENTS The authors thank Mr. Per Solemdnl and Mr. Snorre Tilseth for stimulating discussions and remarks on the manuscript. They are also indebted to
28 Mr. Svein Floen for help with the data processing, and Miss Karin PIttman for correcting the English text.
REFERENCES Reukema. J.J.. 1966. Predation by the three-wined stickleback (Gasterosteus aculeotus L.): tie infiuenee of hunger andexperience. Behaviour, 31: l-126. Beukema, J.J., 1970% Angling experiments with carp (Cyptinus carpio L.). II. Decreasing catchability through one-trial learning. Netb. J. Zool., 20: 81-92. Beukema, J.J., 19lOb. Acquired book-avoidance in the pike Esox lucius L. fished with artificial and natural baits. J. Fish Biol., 2: 155-160. Beukoma, J.J. and de Vos, G.J., lSl4. &perimentai tests of a basic assumption of the caoture~ecaoture method in Dond wpulations of carp C~minus car&k L. J. Fish abl.. 6: 317-329. Brawn, V.M.. 1969. Feeding behaviour of cod (Gadus morhua). J. Fish. Res. Board Can., 26: 533-596. FarnG, A., Tilseth, S. and Solemdal, P., 1977. The behaviour of whiting (Gadus merlangus) in relation to long lines. Count. Meet. Int. Counc. Explor. Sea, B: 44. Fern6, A., Solemdal, i’. and Tiheth, 9.. 1981. Factors influencing the altraction and hooking of fish in long line fishing. I.C.E.S. Working Group on reactions of fiih to fishing operations Nantes, 1981. Forster, G.R., 1973. Line fishing on the contiientai slope. The selective effect of different hook patterns. J. Mar. Biol. Assoc. U.K., 53: 749-751. Hackney, P.A. and Linkous, T.E., 1978. Striking behaviour of the largemouth bass and use of the binomial distribution for its analysis. Trans. Am. Fish. Sot., 107: 682-688. Hoogland, R., Morris, D. and Tinbergen, N., 1956. The spines of sticklebacks (Gosteros&us and Pygosteus) as means of defence against predators (Perca and .&ox). Behaviour, 10: 205-236. Huse. I., 1979. Fish behaviour studies as an aid to cod and haddock longline hook design. Count. Meet. Int. Count. Explor. Sea, B: 22. Huse, I. and Karlsen. L., 1977. Further results of Norwegian longline studies. Count. Meet. Intnt.Count. Bxplor. Sea, B: 43. Little, E.E., 1977. Conditioned aversion to amino acid flavors in the catfish, Physiol. Behav., 19: 143-141. Mackay, B., 1911. Visual and flavor cues in toxicosis conditoning of codfish. Bebav. Biol., 19: 01-97. O’Grady, K.T. and Huges. P.C.R., 1980. Factorial analysis of an experimental comparison of three methods of fishing for rainbow trout. Salmo gairdneri Richardson, in still water. J. Fish Biol., 16: 251-264. Rae, B.B., 1967. The food of cod in the North Sea and on west of Scotland grounds. Mar. Res., Solemdal, P. and Tilseth, S., 1914. Reactions of cod (Gadus morhuo L.) to smell stimuli from bait. Count. Meet. Int. Coune. Explor. Sea, F: 40. Stewart, H., 1977. Indian fishing. Early methods on the north-west coast. University of Washington Press, Seattle, 16cpp. Tilseth. S., Solemdal, P. and Fern& A., 1973. Bohaviour studies on t%h reaction to long lines. Count. Meet. Int. Count. Explor. Sea, B: 22. Tugendhat, B., 1960. The disturbed feeding behaviour of the threwpined stickleback. I. Electric shock is administered in the food area. Behaviour, 16: 159-137. Ware, D.M., 1911. Predation by rainbow trout (Salmo goirdneri): The effect of experience. J. Fish. Res. Board Can., 26: 1641-1862. Ware. D.M.. 1912. Predation by rainbow trout (S&no goirdneri): the influence by hunger. prey density, and prey size. J. Fish. Res. Board Can.. 29: 1193-1201. Windell. J.T.. 1966. Rate of digestion in the bluetill sunfish. Invest. Indiana Lakes. Streams, 7: 185-214. -
punetatus.
1: 1+X.
Ictalurus
19 --Printed
in The Netherlands
THE EFFECT OF EXPERIENCE ON THE BEHAVIOUR MORHUA L.) TOWARDS A BAITED HOOK
ANDERS
FERN6
Institute (Norway)
of
INGVAR Institute
Fisheries
Biology,
University
Technology
Research,
of Bergen,
P.O.
Box
OF COD (GADUS
1839,
N-5011
Bergen
HlJSE+ of Fisheries
(Accepted
6 January
Bergen
ih’orway)
1983)
AFSTRACT Fe&i, J.. and Hue, l., 1983. The effect of expericwe on the behaviour morhua L.) towards a baited Ilook. Fxh. Res.. 2: -3-28.
of cod (Godus
The behaviour of cod towards a baited hook was observed in a ring tank. The intensity of the response was highest initiaiiy, with a modification of the behaviour developing after experience with the baited ho*,k, Irrespective of actual hooking. Hooking occurred less often with time and the hooking probability decreased for consecutive strong responsea of individual cod. The implications of a modification of the behaviour towards baited hooks for !ong line Pishing are discussed. INTRODUCTION
During fishing experiments with hooks and lines, there is a decreased catchability of carp (Beukema, 1970a; Beukema and de Vos, 1974) pike (Beukema, 1970b), largemouth bass (Hackney and Linkous, 1978) and rambow trout (O’Grady and Huges, 1980) during the course of fishing. This is believed to be due to the development of hook avoidance. It is known that pike and perch become negatively conditioned to eating sticklebacks, as the spines hurt the predator’s mouth (Hoogland et al., 1956). and that codfish (Mackay, 1977) and catfish (Little, 1977) can develop a stron.g aversion to food associated with toxicosis. No behaviour studies have, however, been made to investigate the direct modification by experience of response to a hook. In field studies on the behaviour of fish towards long lines (Fern5 et al., 1977; Tilseth et al., 1978), individual fish can seldom be followed for long, *Present N-5392
address: StorebB.
0165-7836/83/$03.00
Institute Norway.
of Marine
0 1983
Research,
Austevoll
E!sevier Science Publishers
Marine
B.V
Aquaculture
Station,
20 and a modification of the behaviour is therefore not easily studied. The present paper describes some laboratory experiments on the behaviour of cod towards a baited hook. Long-lining with baited hooks is one of the major fishing methods in Norway and cod is M important species in this fishery. The aim of the study was to investigate how the behaviour of cod towards a baited hook was influenced by experience. Both the effect of hooking and the effect of experience with the baited hook without hooking could he evaluated in the study. MATERIALS
AND METHODS
Two similar experiments were carried out in 1977. Experiment 1 ran from 24 May-7 June with 10 days of investigation, and Experiment 2 from 9 November-l December with 17 days of investigation. The 15 cod in Experiment 1 had a mean length of 72.1 cm (range 60-83 cm) and a mean condition factor of 1.02. They belonged to the Arcto-Norwegian stock and were caught by trawl in the Barents Sea. During their three-year storage in outdoor concrete tanks they were subject to several bait bag preference tests in the ring tank used for the present study. They spawned for the first time in the spring of 1977. The 20 coastal cod used in Experiment 2 had a mean length of 53.5 cm (range 48-64 cm) and a mean condition factor of 1.03. They were caught in traps two months prior to testing and stored in outdoor tanks. All fish were fed mainly on squid in their home enclosures, but were not fed in the experimental tank. The fish were individually tagged with easily readable slightly buoyant dorsal tags. (The data from four fish who lost their tags during the experiments were included only where it did not bias the analysis, and data from three fish that died or were damaged during the experiments were disregarded.) Length and weight were measured during transportation to the indoor experimental tank. The tank was ring-formed with an outer diameter of 14 m, an inner diameter of 10 m and a depth of 2.3 m. The water temperature was 6--9”C and the light regime was 8 h light and 16 h dark. Testing commenced 10 days (Experiment 1) and 12 days (Experiment 2) after transportation and tagging to allow the fish to become accustomed to the environment. Usually, five trials were made on each experimental day at about the same time each day. A total of 49 and 85 trials were made in Experiments 1 and 2, respectively. A trial involved the placing of one baited hook (a barbless Mustad-Norway No.6) in the tank, and lasted for 10 min, until one fish was hooked or until the bait was lost. The hook was attached to a 2-m piece of long line by a 40 cm snood and placed 50 cm above the tank bottom. Rings of squid were used as bait snd attached to leave the point of the hook exposed. Bait was changed in the 5 min pause between trials. Hooked fish were freed in the tank when possible, but they sometimes
21 came loose of their own accord. If the hook was swallowed the fish was removed from the tank, anaesthetiized, unhooked and returned to the tank. Observations were conducted from the centre of the ring. The behaviour of each cod towards the baited hook was recorded verbally on tape and some of the trials were video-taped for more detailed study. A number of behaviour patterns were defined as follows: -swimming towards the bait while looking at it and turning Approach before touching the bait. -touching the bait with the trailing barbel or lips. If tasting Taste was followed by bite or incomplete bite, it had to last it least two seconds in order to be recorded. -sucking the bait into the mouth. Bite Incomplete bite -differs from bite in that the whole bait is never within *he closed mouth, either because the fish takes only a part of the bait in the mouth or because the mouth is not completely closed. -swimming around with stretched snood with the bait in Pull the mouth. -manipulating the bait in the mouth with chewing moveChew ments. Jerk -a rapid movement of the head with the bait in the mouth, typically directed to the side. Shake -several rapid lateral movements with head and body while the bait is in the mouth. Cod show thii behaviour pattern when seperating the softer part of a mussel from the shell (Brawn, 1969). -swimming rapidly forward with bait in mouth. Rush Bait out of the mouth -the bait is spat or pulled out of the mouth. Hooking -the hook is retained in the mouth for at least 20 E while the fish fights violently.
TABLE
I
Numerical
values
Behaviour
pattern
Approach Taste Incomplete Bite
bite
assigned
to behaviour Value 1 2 3 4
Jerk Pull Chew
5 5 5
Shake Rush Hooking
5 6 7
patterns
22
Behaviour patterns were given numerical values, whose values increased with increasing intensity of the response (Table I). The defined behaviour patterns could occur individually or in various combinations. A “sequence” was defined as a series of behaviour patterns that terminated when the fish left the field of observation or when another fish reacted to the baited hook. The number of behaviour patterns in a sequence varied from l-12. A strong response was defined to occur when a fish took the bait in the mouth and made one or several of the behaviour patterns with highest intensity, i.e., rush, jerk, shake, chew and pull. A strong response was terminated when the fish was hooked or the bait left the mouth. Several strong responses could occur within one sequence. RESULTS
The frequency of occurrence of the defined hehaviour patterns is given in Table II. Bait out of mouth was a common occurrence in both Experiments 1 and 2. In Experiment 1, bite and rush were observed frequently, whereas in Experiment 2 approach and incomplete bite were more often recorded. Generally speaking, high intensity behaviour patterns were exhibited relatively more often in Experiment 1 than Experiment 2. The sum of behaviour patterns exhibited on a given experimental day varied considerably, but displayed no general trend in Experiment 1. In Experiment 2 there was an overall increase with time. In both experiments there was generally an increase in the relative frequency of low intensity behaviour patterns and a decrease in high intensity hehaviour. The best indicator of the effect of experience is the individual behaviour changes with repeated encounters with the baited hook. To this end, each distinct sequence was given a value as the sum of the numerical values of its behaviour patterns. Successive sequences made by each cod could then be compared. The mean sequence values for the first 20 sequences are given in Table III. Many fish made less than 20 sequences and thus the mean sequence value is based on a decreasing number of fish. In both experiments the mean decreased steadily over time. There was a significant difference between the means of sequence 1 and sequence 2 (Wilcoxon matched-pairs signed-ranks test, P < 0.05) and by the fifth sequence the mean had decreased to approximately one half of the initial value. Sequences 16-20 had means which were only about 35% of the mean of sequence 1. Table III also shows that the means of the sequence values decreased sirnilarly between hooked and not hooked fiih as well as between fish with different condition factors. The category of hooked fish consisted of fish hooked during the first 20 sequences. Most fish (12 out of 15 fish) ware hooked in sequence 1-5. The mean sequence value for the 20 first sequences (grand mean) was
II
617
71
10.1
Sum
%oftotal
30.9
1 4 30 20 22 36 59 39 43 28 16 23 71 32 44 64 65
12
___-~--
Approach
Frequency
4.2
12.1
241
8 4 11 32 10 12 26 6 6 17 11 18 27 38
1 4 6 6 6 3 2
32
6 1 8
0 1 3
121
Taste
9.8
75
10 12 8 6 13 3 2
4 5 12
10 1 10
2
14 18 14 16 11 15 10
23 5 20
12
Bite
328 146 16.4 19.1
19 15 17 35 15 13 19 16 12 23 17 36 41 29
Incomplete bite
97 4.9
4 3 7 2 0 3 6 3 3 4 1 3 2 2
11 23 20
6 2 7 3 8 3 5 4 5 3
12
Jerk
46 6.0
oatterns
1 and 2
of bebaviow
in Experiments
of occunence
pattern occarrence
0 0 4 2 5 12 17 18 13 6
Exp. day 1 2 3 4 5 6 I 8 9 10 11 12 13 14 15 16 17
Experiment
Behaviour pattern
Behaviour
TABLE
126 6.3
0 0 1 0 0 0 0 0 0 0 1 0 1 0 0 1 1 6 5 0.~3 0.3
4.3 10 7 I 50 10 5 0 80 2 0 70 42 6 5 3 7 18 23 20
12
Shake
2 2 3 0 1 1 0 0 3 0 2 0 0 1 0 0 0
8 1 3 1 3 1 1 2 1 0
121
Chew
5 4 5 0 0 2 0 0 0 1 0 2 0 0 1 0 0
18 3 10 13 14 10 9 14 10 10
_~~.
Rush
8 23 13 5 3 5 1 6 9 10 7 1 11 1 7 9 7
2
24 7 31 23 30 22 22 22 17 10
12
18 19 26 21 18 23 37 15 16 23 16 14 26 18 38 43 31
Bait out of mouth
208 402 32 12 21 20 111 126 4.2 0.6 2.8 1.0 14.5 6.3 27.3 20.2
7 3 7 2 2 4 3 2 1 1
1 2 --__.
--~~
Pull
1.2
9
1 3 0 1 0 0 0 1 1 2
12
-p
1.1
21
3 5 4 2 0 1 0 0 0 1 3 1 0 0 1 0 0
Hooking
763
94 30 36 70 96 80 85 93 69 48
1
Sum
1995
68 83 127 84 67 108 174 87 103 118 76 67 156 88 166 210 213
2
.s
III
fish
Conditionfactorz Condition factors
fish
1 2
no.
Not hooked
kamked
Experiment Experiment
sequence
0.95 0.95
17.0 16.7
19.4 13.7
(13) (14)
(15) (12) 12.1 9.9
10.2 11.9
13.1 9.9
23.1 13.4
(9) (18)
2
1
10.8 10.5 9.8 11.4
(13) (14)
11.3 10.3
(15) (12)
(9) (18)
3
(12) (13)
(14) (11)
(9) (16)
8.6 8.1
10.8 5.7
10.1 5.7
4
9.5 7.8
10.1 6.8
(14) (10) (12) (12)
11.0 7.5
(8) (16)
6
(11) (10)
(12) (9)
(7) (14)
Mean Kzquence value for the first twenty sequences. The means are given by Experiments by condition factor. The number of fish is given in parentheses
TABLE
(9) (9)
(7)
6.1 9.6 7.0
(11) (11)
9.2
5.5 5.3
5.0
5.6
11-15 7.1 4.3
(7)
9.3 7.5
B-10
1 and 2, by hooked
(8) (6)
7.9 4.5
(8) 4.8
(4)
(6) (6)
(4)
(7)
(8)
6.8
(5)
(10)
16-20 8.4 4.3
(6)
and not booked
9.3 7.6
10.2 7.4
l-20
fish and
25
higher for fish in Experiment 1 than in Experiment 2 (P < 0.01. t-test) and was also higher for fish with the higher condition factor (P < 0.05). The categories of hooked and not hooked could not be compared this way due to the numerical value of hooking and its subsequent effect on sequence value. There was a considerable variation in number of sequences made by the individual cod. Two fish exhibited no behaviour towards the baited hook. Of the 27 fish that produced at least one sequence, 21 fish made at !cast five sequences and 11 fish more than 20 sequences (Table III). The maximum number of sequences by one fish was 413. No significant difference was found in the proportion of fish in either category that exhibited more than 20 sequences. In Experiments 1 and 2 there were 9 and 21 bookings, respectively (Table II), most of which took place early in the experiments (16 hookings during experimental days l-3). For all fish in both experiments (disregarding the hookmgs of fish that lost their tags), 10 cod were never hooked, 11 cod were hooked once, 2 cod twice, 1 cod three times and 2 cod four times. In Experiments 1 and 2, five and four fish, respectively, were hooked in the oesophagus/stomach while four and 16 fish were hooked in the mouth (one fish was caught in the eye). The difference in hooking position between the experiments was not significant (0.05 < P < 0.10, Fisher exact probability test). When calculating the hooking probability for consecutive contacts with the baited hook, it is essential to know which behaviour patterns led to hooking. The exact moment of hooking is, however, often difficult to determine. A cod was sometimes clearly hooked already when pulling or chewing, but in most cases hooking could not be observed with certainty until after a jerk or rush, albeit these behaviour patterns may sometimes have been more the consequence than the cause of hooking. However, hooking always cccurred in connection with a strong response with one or several of the behaviour patterns rush, jerk, pull, chew, and shake. Seven out of 28 fish (25%) were hooked in their first strong response. Eight fish were hooked on their strong response 2-5 (60 strong responses, 10% hooking) and five fish on strong response 6-10 (58 responses, 8.6% hooking). There was a significant decrease in hooking probability between strong response I. and strong response 2-10 collectively (x*-test, P < 0.05). The hooking probability also seemed to vary with the individual - one fish was hooked four times on four strong responses while another fish was never hooked on 45 strong responses.
The experimental cod showed a decrease in the intensity of the response after experience with a baited hook whether or not the fish was hooked. The aecreased intensity could be caused by conditioning -biting the hook could act as negative reinforcement to the cod in the same way as a stickleback’s
26
spines induce cessation of feeding response in pike or perch (Hoogland et al., 1956) or presentation of electric shock during feeding disturbs the feeding behaviour of sticklebacks (Tugendhat, 1960). It may be argued that aversive stimulation from the hook is not the only cause of a decreased intensity of response. Although a hooked fish also receives handling which may act as negative reinforcement this cannot explain the declining response in not hooked fish. An alternative explanation for the observation could be the general restriction of movement by the mood. However, in experiments with baits attached with a string instead of a hook where the fish movement was similarly restrained, no decrease of response intensity was found (A. Fern& 1977, unpublished). Physical stimulation from the hook is therefore regarded as the main factor behind the decreased response. Analysis of the video tapes also indicated that the fish reacted to the hook while manipulating the bait in the mouth and that this often resulted in incomplete mouth closure. Such incomplete bites were generally not observed on unhooked bait. Even if the hook is the critical stimulus for the negative condtiioning, the fish did not seem to distinguish the hook from the bait. When free bait was put into the tank after the experiment, the fish were at first inhibited by the bait and made several approaches, tastings and incomplete bites before eating the bait. A decrease in the intensity of the response was demonstrated in both Experiments 1 and 2, but responses were generally stronger in Experiment 1. The condition factor of the fish was the same between groups, but length of the fish, earlier holding conditions, and time of the year for the experiments differed. It is probable that the cod in Experiment 1 tested in May-June after the spawr,ing season had a stronger feeding tendency than the cod in Experiment 2 %ested in November. A strong tendency to feed after the spawning season is known for cod (Rae, 1967), and codfish take several times more food in May-June than in November under laboratory conditions (P. Solemdal and S. Tilseth, 1980, personal communication). Another explanation is that previous experience of the tank may have made the cod in Experiment 1 less receptive to frightening stimuli. These cod also swam regularly around the tank, while the cod in Experiment 2 more often stayed in one place. The fish were deprived of food during the experiments, apart from small pieces of bait they picked up, and occ;asional stolen baits. While the food deprivation may have initially increased the feeding tendency in the same way as in sticklebacks (Tugendhat, 1960; Beukema, 1968) and rainbow trout (Ware, 1972), the possibility exists that the feeding tendency .vas negatively affected after some time. In blue-gill sunfish, there is decreased gastric digestion after seven days of starvation, and a more pronounced decrease after longer starvation periods (Windell, 1966). A reduced tendency to feed cannot, however, explain the results of the present study. The rapid decrease in the intensity of the response within the first few contacts with the baited
27
hook clearly demonstrates the effect of experience. The fish also responded to the baited hook throughout the experiments, but seemed to be in a conflict between approach and withdrawal (up to seven approaches per sequen?e). Solemdal and Tilseth (1974) found an increased bite actively towards non hooked bait bags in cod during the first experimental week without food. This demonstrates the significance of the hook for the decrease found in the present study. The piece of long line in the laboratory tank was an easily recognizable stimulus and therefore may create an ideal learning situation. The question therefore arises of whether a similar decrease in response occurs after experience with baited hooks in long-line fishing. In field studies on the behaviour of whiting towards a test line, the relationship between the number of fish observed and the number of responses towards the baited hooks indicates that each fish makes relatively few responses, possibly due to a moclification (Ferns et al., 1981). Pike and largemouth bass become more difficult to catch for a second time with hook and line (Beukema, 1970b; Hackney and Linkous, 1978). and one single hooking experience makes carp more difficult to catch for at least a year (Beukema, 1970a). It is therefore probable that cod also show a similar decreased vulnerability. A relatively low intial hooking probability of 25% on the first strong response as found in this study, followed by a rapid modifies&n of the response, could iead to a l&b percentage of cod not being caught during one encounter with a long line. The persistence of this modification in repeated encounters in the variable environment of the sea is difficult to estimate. A monofilament long line catches 40-300% more cod than a multi-twine line (Huse and Karlsen, 1977). It is possible to explain this difference with a learning process in the fish. If both types of lines are attacked equally often initially, the more visible multi-twine line could be more easily recognized by a conditioned fish and therefore more effectively avoided. An alternative explanation would be that a more visible line induces initial avoidance in cod. An initial inhibition towards novel prey has been demonstrated in stickleback and rainbow trout (Beukema, 1968; Ware, 1971). A modification of the behaviour of a fish towards a baited hook may lead the efficiency of a hook to be partly determined by its modificatory effect. In many Pacific types of hooks, the point is bent heavily inwards so that the hook almost forms a circle or a triangle (Stewart, 1977: Forster, 1973). This hook shape may decrease the probability that a fish comes into contact with the point of the hook and thus experiences aversive stimulation when biting which in turn could lead to a greater number of strong responses and higher percentage of hooked fish. Such an effect could combine with a higher hooking probability when fish rush on a bent hook as opposed to a straight hook (Huse, 1979). ACKNOWLEDGEMENTS The authors thank Mr. Per Solemdnl and Mr. Snorre Tilseth for stimulating discussions and remarks on the manuscript. They are also indebted to
28 Mr. Svein Floen for help with the data processing, and Miss Karin PIttman for correcting the English text.
REFERENCES Reukema. J.J.. 1966. Predation by the three-wined stickleback (Gasterosteus aculeotus L.): tie infiuenee of hunger andexperience. Behaviour, 31: l-126. Beukema, J.J., 1970% Angling experiments with carp (Cyptinus carpio L.). II. Decreasing catchability through one-trial learning. Netb. J. Zool., 20: 81-92. Beukema, J.J., 19lOb. Acquired book-avoidance in the pike Esox lucius L. fished with artificial and natural baits. J. Fish Biol., 2: 155-160. Beukoma, J.J. and de Vos, G.J., lSl4. &perimentai tests of a basic assumption of the caoture~ecaoture method in Dond wpulations of carp C~minus car&k L. J. Fish abl.. 6: 317-329. Brawn, V.M.. 1969. Feeding behaviour of cod (Gadus morhua). J. Fish. Res. Board Can., 26: 533-596. FarnG, A., Tilseth, S. and Solemdal, P., 1977. The behaviour of whiting (Gadus merlangus) in relation to long lines. Count. Meet. Int. Counc. Explor. Sea, B: 44. Fern6, A., Solemdal, i’. and Tiheth, 9.. 1981. Factors influencing the altraction and hooking of fish in long line fishing. I.C.E.S. Working Group on reactions of fiih to fishing operations Nantes, 1981. Forster, G.R., 1973. Line fishing on the contiientai slope. The selective effect of different hook patterns. J. Mar. Biol. Assoc. U.K., 53: 749-751. Hackney, P.A. and Linkous, T.E., 1978. Striking behaviour of the largemouth bass and use of the binomial distribution for its analysis. Trans. Am. Fish. Sot., 107: 682-688. Hoogland, R., Morris, D. and Tinbergen, N., 1956. The spines of sticklebacks (Gosteros&us and Pygosteus) as means of defence against predators (Perca and .&ox). Behaviour, 10: 205-236. Huse. I., 1979. Fish behaviour studies as an aid to cod and haddock longline hook design. Count. Meet. Int. Count. Explor. Sea, B: 22. Huse, I. and Karlsen. L., 1977. Further results of Norwegian longline studies. Count. Meet. Intnt.Count. Bxplor. Sea, B: 43. Little, E.E., 1977. Conditioned aversion to amino acid flavors in the catfish, Physiol. Behav., 19: 143-141. Mackay, B., 1911. Visual and flavor cues in toxicosis conditoning of codfish. Bebav. Biol., 19: 01-97. O’Grady, K.T. and Huges. P.C.R., 1980. Factorial analysis of an experimental comparison of three methods of fishing for rainbow trout. Salmo gairdneri Richardson, in still water. J. Fish Biol., 16: 251-264. Rae, B.B., 1967. The food of cod in the North Sea and on west of Scotland grounds. Mar. Res., Solemdal, P. and Tilseth, S., 1914. Reactions of cod (Gadus morhuo L.) to smell stimuli from bait. Count. Meet. Int. Coune. Explor. Sea, F: 40. Stewart, H., 1977. Indian fishing. Early methods on the north-west coast. University of Washington Press, Seattle, 16cpp. Tilseth. S., Solemdal, P. and Fern& A., 1973. Bohaviour studies on t%h reaction to long lines. Count. Meet. Int. Count. Explor. Sea, B: 22. Tugendhat, B., 1960. The disturbed feeding behaviour of the threwpined stickleback. I. Electric shock is administered in the food area. Behaviour, 16: 159-137. Ware, D.M., 1911. Predation by rainbow trout (Salmo goirdneri): The effect of experience. J. Fish. Res. Board Can., 26: 1641-1862. Ware. D.M.. 1912. Predation by rainbow trout (S&no goirdneri): the influence by hunger. prey density, and prey size. J. Fish. Res. Board Can.. 29: 1193-1201. Windell. J.T.. 1966. Rate of digestion in the bluetill sunfish. Invest. Indiana Lakes. Streams, 7: 185-214. -
punetatus.
1: 1+X.
Ictalurus