Comparative Learning Ability of Selected ~ishes'

Daniel W. Csble Wisconsin Cooperative Fishery Research Unitt2 University of Wisconsin, Stevens Point W / 5448 1, USA

and Gordon B. ~ a r a b e e ~ and Richard 8. Anderson Missouri Cooperative Fishery Research Unit,' University sf Missouri, Columbia, MQ 652 1 1 , USA

Coble, D. W., G . 5. Farabee, and R. 8. Anderson. 1985. Comparative learning ability of selected fishes. Can. ). Fish. Aquat. Sci. 42: 791-796.

Fourteen species of freshwater fish were trained to execute a simple conditioned response in a shuttle box -to move in response to light to avoid an electrical shock. There was no relation between learning ability and phylogenetic position. Better learners included striped bass (Morone saxatjlis), bigmouth buffalo (Bctiobus cyprinellus), common carp (Cyprhus carpd'o), and channel catfish (lctalurus punctatus). Bluegill (hepsmis macrschirus) and northern pike (Esox lucius) were poor learners. Yellow perch (Perca Blavescens) and redbelly tilapia (irilapia sillj) could not be trained. Some fish retained their learned behavior for months, although performance deteriorated with time. Older channel catfish learned better than juveniles, but there was no difference between juvenile and older largemouth bass (Micropterus salmoides). Temperature (18-28OC) and feeding level (ranging from starvation for 25 d to ad libitum) did not affect learning of channel catfish, but the protozoan disease, ichthyophthiriasis, and perhaps our treatment sf fish for the disease retarded it.

O n a entraine quatorne especes de poisson dulqaquicolea executer uwe simple reaction csnditionnee dans le boite a navette c.-3-6. a reagir a la lumiere afin d'eviter une deckarge electrique. HI n'y avait aucune relation entre la capacite d'apprentissage et la position phylogenetique. Le bar raye ( Morone saxatilis) le buffalo B grande bouche (Bctiobus cyprinellus), la carpe (Cyprinus carpio) et la barbue de riviere (Ictalurk~s punctatus) comptaient parmi les especes a apprentissage rapide tandis que Be crapet arlequin (hepomis macrochirus) et %e grand brochet (Esox lucius) n'apprenaient pas vite. La perchaude (Perca favescens) et le tilapia (irijapia zilji) n'ont pu &re entraine. Certains poissons ont retenu Jeur comportement appris pendant piusieurs rnois quoique leur performance se soit deterioree avec %e temps. Les barbues de aivigre agees ont mieux appris que Bes juveniles, mais il n'y avait aucune difference entre les achigans a grande bouche [Micropterus salmoides) juveniles et ages. La temperature (1 8-28°C) et le taux d'alimentation (de la privation complete pendant 25 jours a ad libitum) n'ont pas influe sur ('apprentissage de la barbue de riviere, mais l'ichtyophthiriase (maladie causee par un protozoaire) et peut-&re le traiternent des poissons malades a p u le retarder.

Received December 2, 1982 Accepted December 27, 11984 (57140)

earwing ability of fish has been used to investigate such diverse subjects as sensory perception (literature reviewed by Bull 1953, feeding periodicity and effects o f tem- perature and food nutrient content on feeding (Wozin a+

Mayer 196 f ; Wright and Eastcott 19821, taste preference (Adron et al. B973), and sublethal effects of insecticides and an anesthetic (Jackson et al. 1970; Hatfield and Johmsen 1972; McNicholl and MacKay 1975).

Many aspects of leaning and memory themselves have been extensively studied, including cornaparisons of learning of fish, birds, and mammals (literature reviewed by Gleitman and Rozin

'~aseef in pat on a thesis submitted by G.B.F. to the University of Missouri in partial fulfillment of the requirements for an M. A. degree. 'U . s . Fish and Wildlife Service, Wisconsin Department of Natural

Resources, and University of Wisconsin in Stevens Point cooperating. 3~resent address: Fisheries Management Biologist, Route No. 1 ,

Box 55, Palrnyra, MO 63451, USA. 'u.s. Fish and Wildlife Service, Missouri Department of Conser-

vation, and University of Missouri in Columbia cooperating.

R e ~ u le 2 decembre 1982 Accept6 le 27 decembre 1984

197 I ) . Goldfish (Carassius aura t~s) and a tilapia (Ts'lapba macrocephks) are the fish species that have been used most often in these studies. Usually, fish have been trained with a reward system, e.g. receiving food when they press a trigger, or by punishment, e.g. moving in response to Iight to avoid electrical shock.

Objectives of this study were to (1) compare the ability of various fishes, from primitive to more derived, to learn and remember a simple conditioned response, (2) compare learning ability of juvenile and older channel catfish (Pctalurus punc- tatus) and largemouth bass (Micropterus salmoides), and (3) investigate effects of temperature, feeding level, and the disease ichth yophthiriasis (caused by the protozoan Pchthyspthirius rnultijilis) on lemiwg of channel catfish.

Methods

We measured learning by training fish to avoid electric shock in a shuttle box. Large fish were trained in plywood shuttle

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boxes 156 X 35 X 35 cm, and smaller fish in boxes 60 x 25 x 25 cm. Depth of water in the boxes was 28 and 27 em, respectively. Each box was divided in half by a wooden partition, 7.5 cm high or less on the bottom of the box. Electrodes of hardware cloth were affixed to the inside of each half of the boxes. A 7-W light bulb was affixed over each end of each box. Training was carried out in a darkened room; fish were observed through a mirror over the boxes. An automatic timer provided a cycle of light for 20 s, followed by light and shock for 20 s, followed by darkness for 20 s alternately at one end of a box and then the other. The minimum shock needed to elicit a response, 6 V or less, was administered.

A fish was placed in one end of a box and allowed 6 min of darkness to adjust to the box before training began. A training session consisted of six 1-min cycles, 6 min of darkness, and then six more cycles. A correct response was scored each time a fish moved over the wooden partition after the light was turned ow, but before the shock was administered. An incorrect response occurred if a fish did not respond to the light and received the shock. Hence there were 12 chances of a correct response for each fish in a training session. All fish were given two consecutive training sessions (total of twenty-four 1-min cycles) on the first day of training and then one training session on each of the following 4 or 5 d. Some groups of fish were given additional consecutive daily training sessions. Memory was tested for some groups of fish by an additional training session at intervals of 7 d or more after the last consecutive daily training session.

Fish were held in indoor tanks before and between training sessions, The holding tanks were provided with air stones and received a continuous flow of water sufficient to provide one exchange per day, usually at about 20°C. Shuttle boxes were usually filled with water from the holding tacks immediately before each training session. Fish were fed while in the holding tanks. Those tested for memory were held in tanks or ponds after the last consecutive daily training session.

Fish obtained from wild populations or from hatcheries were acclimated to laboratory temperature by holding them for a minimum of the number of days equal to the difference in Celsius degrees between field, transportation, or holding tem- perature and laboratory temperature. Commonly, fish were given a prophylactic treatment for handling stress, or for parasites and diseases, during transportation or holding; treat- ments included solutions of NaCl of 7.5 g/L or less or acriflavin of 3 mg/L, or both, or a 30-9 dip in malachite green of 6.7 mg/L.

Results

The general leming pattern was an irregular increase in correct response in successive training sessions, with values approaching an asymptote in training sessions 4-7 (Table 1). The shuttle box provided a measure of learning for all species except yellow perch (Peaca Javescens) and redbelly tilapia (Tibapia zZilBi), whose correct responses did not increase in successive training sessions (Speman rank correlation, p < 0.05; n = 7).

Fish retained their l emed experience for months; however, retention also deteriorated with time (Table 2). Percent correct response for various species in memory training sessions exceeded percent correct response in the first training session for up to 277 d, but percent correct response also generally decreased with time from values obtained in the last two training

sessions. In our only test in which elapsed time exceeded 1 yr, fathead minnows (Pirnephakes promelas) did not retain their l emed experience after 391 d.

Species Cornpaison

Species are listed in Table 1 in decreasing order of leming ability, measured by the area under the curve that would be obtained if percent correct response were plotted against training sessions 1 -7. Striped bass (Morone sresrabi/is), big- mouth buffalo (Hetiobus cyprineklus), common carp (Cygrinus earpis), and channel catfish were the better learners in the shuttle box; bluegill (Lepomis macrochkrus) and northern pike (Essx lueius) were the two poorest of those that lemed.

There was no relation between leming ability and phyloge- netic position. The two more primitive holsstean species. shortnose gar (Lepisssfeus pkatostomus) and bowfin (Amiw cakva), were intermediate in leming ability; the phylogesmeti- cally intermediate Cyprinidae sand Ictaluridae were better learners; and the more derived Centrarchidae, and a more primitive teleost , northern pike, were poor learners.

Juveniles and Older Fish

We obtained contradictory results in comparing learning of juvenile and older fish of two species. Percent correct response of older channel catfish (channel catfish 1, apparently disease- free) was significantly greater (Wilcoxon paired-sample test, p < 0.05; n = 7) than that of juveniles (channel catfish 4-9 combined, apparently disease-free; Table 1 ; Fig. I). In contrast there was no significant difference in percent correct response between juvenile and older largemouth bass (largemouth bass B vs. largemouth bass 2 and 3 combined).

Temperature and Feeding Level, Channel Catfish

Temperature did not affect learning of channel catfish over the range tested. Channel catfish groups 4, 5, and 6 (Table 1) were acclimated and trained at 18, 22, and 28"C, respectively. There was no significant difference in percent correct response among the groups (Wilcoxon paired-sample test, p < 0.05; BZ = 7).

Feeding probably did not affect learning of channel catfish. Charnel catfish groups 7, 8, and 9 (Table 1) were starved, poorly fed: and well fed, respectively. Percent correct response was significantly greater for the poorly fed group than for the well-fed group (Wilcoxorn paired-sample test, p < 0.05; n = 7). However, there was no significant difference between the starved and well-fed gmup or between the starved and poorly fed group. Therefore, the significant difference was probably fortuitous.

Disease

The disease ichthyophthiriasis, and perhaps our treatment of fish for the disease, appeared to reduce learning ability of channel catfish. We saw the white spots of ichthyophthiriasis on fish at the time of the third training session of channel catfish in group 3 (Fig. 1). After the seventh training session, fomalin and acriflavin hydrochloride were added to the water in the holding tanks for this group to provide concentrations of 25 and 10 mg/L, respectively. Percent correct response increased in the eighth training session on the following day, but 1 d later all but one fish had died. The percent correct response of channel catfish in group 3 was significantly smaller (Wilcsxon paired-

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TABLE 1. Learning of various species 6% correct response in sslccessive training sessions), number and lengths (mm) of fish trained, and temperatures and training dates (1968-71) far various species.

Training session Length mean ( s ~ ) Temperature

Species and group No. 1 2 3 4 5 6 7 Number orrange ("@I Date

Striped bass (Mororae s&x;catilis)

Bigmouth buffalo (Ietiobus cyprinsllus)

Cornon c q (Cyprinus carpio)

B 2

Channel catfish

Aug. 3-7

Apa. 15-20

A u ~ . 4-9 June 8- 12

(Pctalurus pusactatus) 1 M a . 3-14

Mar. 24 - Apr. 7 Jan. 5-1 1 Jan. 24-29 Jan. 24-29 Jan. 24-29 k c . 28 -Jm. 2 Dec. 28 - Jan. 2 Dec. 28 - Jan. 2

2b.c 3 b,c

4 5 6 7 'j 8 9

E3swfinb (Arnia celva)

Inland silverside (Mesaidia bevllina) Sept. 8- 13,4 fish;

Nov. 29 - Dec. 4, 10 fish Shoatnose gar

(Lepbsosteus pketostornus) SmdIrnouth b a s

(Micropterus dolornieui) Spotted bass

(Mieropterus pmetulatus) Black bullhead

(Ictelurus melas) Fathead mimow

(Pirnepkles promelas) Largemouth bass

(Micropterus se~rn~ides ) 1 2b 3

Bluegill (Lepomis macrochirus)

Northern pike (ESOX ~ U C ~ U S )

Yellow perch (Perca flavescens)

1 2

Redbelly tilapia (Tilapa'a ailli)

Aug. 17-21

June 23-28

Aug. 19-24

Jan. 23-31

Sept. 8-13 Sept. 16-27 A u ~ . 7-29

July 23-28

Sept. 4-9

Dec. 4-9 June 22-26

June 29 - July 3

"Percent correct response in seventh training session was extrapolated. b~raining was continued beyond seven sessions. Percent correct response in sessions 8-13 for channel catfish group 1 was 91, 91, 96, 94, 97,

100; sessions 8- 16 for channel catfish group 2 was 58,57,49,59, 73, 71,87, 83,94; session 8 for channel catfish group 3 was 56; session 8 for bowfin was 53; session 8-1 1 for fathead minnow was 42, 41, 49, 46; sessions 8-13 for largemouth bass group 2 was 23, 36, 43, 56, 60, 58.

'Fish were infected with Ichthyophthirius rnult$lis. %hannel catfish groups 7, 8, and 9 were fed at different levels - starved, fed 8.75% of body weight per day, and fed ad libitum,

respectively - for 20 d before and during training.

sample test, p < 0.05; n = 79 than that of the apparently running water to their holding tanks was stopped and fomalin disease-free channel catfish in groups 4-9, combined. md acriflavin hydrochloride were added, as before (Fig. 1).

Ichthysphthiriasis was seen on channel catfish in group 2 Those fish remained in the treatment solution for the next 6 Q during the fifth training session, md immediately thereafter, except for the short time daily when they were in fresh water in

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TABLE 2. For fish species tested for memoy, percent correct response in the first and in the last two training sessions and after various periods fsllowing the last training session.

Sessions Days after lase training session Species and group No. First Last two '7 37 39 42 56 126 157 189 277 391

Striped bass Common carp

2 Channel catfish

1 7 8 9

Shortnose gar Fathead minnow Largemouth bass

2

70 .........=

20---

3 A- 49 H........

2 4 6 8 10 12 14 16 TRAINING SESSION

FIG. 1. Percent correct response for channel catfish groups 1,2,3, and 4-9 combined (Table 8 ) . IS, Ich seen; T, treatment with formalin (25 rng/L) and acriflavira hydrochloride (10 mg/L); TSC, treatment solution changed.

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the shuttle boxes. Again, percent correct response increased in the first training session after treatment, but then declined to a lower level for 5 d. After the 1 Ith training session, when correct response was 5996, the treatment solution in the holding tanks was removed and replaced with fresh mnning water to which NaCl was added to provide a concentration of 5 g/L. Percent correct response increased irregularly to a high level in the next five training sessions.

The effect sf the treatment solution on learning is difficult to discern in the results of these two experiments. In both, percent correct response increased in the first training session after treatment, suggesting no effect of treatment. In contrast, the improved leming after removal of the treatment solution for channel catfish in group 2 suggests that the treatment impaired leming .

The inland silverside (Menidia beryllina) was the only other species that did not seem to be healthy duPing training. The fish suffered continual mortality during a 28-6% holding period indoors before training, and therefore were given a malachite green dip, and salt (<5 g/L) was added to the mnning water of the holding tanks. Mortalities continued through the training perid; we do not know if their poor physical condition affected their response.

Discussion Species Comparison

Although fish l emed in the shuttle box - percent correct response increased with s~accessive training sessions - our determination of relative leming ability of the various species may have been influenced by intrinsic behavior as well as by leming ability. Evidence that some measure of comparative leming ability was obtained is provided by comparison of the results of this study with those of others in which learning was assessed by different methods. Common carp were among the better lemers in this study. Carp are commonly considered to be "mat fish," and there is experimental evidence that they learn quickly. Beukema ( 1 978) and Beukema and de Vos (1 974) found that carp lemed to avoid capture by angling after a single exposure to angling. Moreover, goldfish, close relatives of the carp, are widely used in experimental psychology, in part because of their good leming ability (Agranoff and Davis 1968).

We know of only one other published study in which leming of some of the same species was compared; results of that study are in accord with ours. Hunter and Wisby (1964) placed fish in a tank, moved a net with holes from one end of the tank to the other, and measured the ability of various species to l e m to escape confinement at the end of the tank by swimming through the holes. Four species were common to both studies. Ranked in decreasing order of Beaming ability were common carp, largemouth bass, bluegill, and northern pike, and the latter was the lowest of all species tested, in both studies. Beukema and de Vos (1944) found that common c a p in ponds lemed to avoid a seine.

Wild catfish and bluegills exhibited the same relative leming ability as in this study when 'Vemand" feeders were placed in a Wisconsin lake. Raked in decreasing order on the basis of speed and extent to which fish learned to press a lever that released food pellets were channel catfish, unidentified bull- heads (brta&elurus sp,), and bluegills, and the channel catfish were far superior to bluegills (T. Larson, Fish Management Biologist, Wisconsin Department of Natural Resources, pers. comm. ) .

Evidence that something other than leaning ability may have influenced our results is provided by correlations between intrinsic behavior s f various species and their performance in the shuttle box. The latter is influenced by the propensity of each species to flee in response to a stimulus, or not to flee but to react in other ways such as darting about or remaining motionless. Because yellow perch and redbelly tilapia reacted to light and electrical shock by remaining motionless, the shuttle box did not provide a measure of learning for these species, Probably there is a gradation of reaction to stimuli between the extremes sf immediately fleeing versus remaining motionless.

Species that are mobile or limnetic should tend to flee readily in response to a stimulus or perceived threat. This characteristic would tend to make such species appear to be better learners in a shuttle box. Of three such species tested, striped bass, bigmouth buffalo, and inland silverside, two were the two best lemers. The common carp was also among the better lemers. Pflieger ( 1 9'75, p. 127) stated "Carp are extremely w a y and charge away rapidly at the slightest disturbance."

Species that are primarily benthic or that associate with cover might tend to seek immediate cover rather than to flee when stimulated. Some fish of various species in early training sessions moved, but not necessarily over the barrier, in response to shock. Although electric shock, being such an unpleasant stimulus, would tend to override a proclivity not to Wee, such a tendency could make a species appear to be a poorer l emer than those whose first reaction is to flee rather than hide. Most of the species tested are primarily benthic or associate with cover, and their learning ability appeared to be less than that of striped bass, bigmouth buffalo, and common carp.

Comparisons of pairs of some of the species also suggest that characteristics of the species may have influenced their perfor- mance. Because anatomy of fish is related to their life habits, the slender channel catfish with a deeply forked tail should be more active or mobile than the chubby black bullhead with its nearly square tail. If more active fish tend to perform better in a shuttle box, the channel catfish should appear to lean better than the black bullhead, and it did. Comparing escape tactics from a predator, Moody et al. (1983) stated that fathead minnows remained in open water whereas bluegills sought cover. On the basis of the reasoning expressed above, the fathead minnow should appear to l e m better than the bluegill in a shuttle box, and it did.

Relative leming ability of the species tested cannot be explained entirely by correlations between intrinsic behavior and performance in the shuttle box. For example, the benthic channel catfish would not be expected to be among the four best lemers in a shuttle box,

To overcome the problem of characteristics of a species interfering with detemination of relative leming ability among species, a variety of methods of assessing leming should be used. We recommend methods based both on punishment and reward, and that the methods require performance of more complicated tasks than reflex and simple flight reactions - as has been done extensively with goldfish. However, a single method can be adequate to test leming within a species, e.g. to assess effects of environmental or physiological factors on leming.

The physical configuration of our shuttle boxes probably did not interfere with our determination of relative leming ability. Agranoff and Davis (8974) stated that height of water over the barrier is important for goldfish. We adjusted bmier heights after observing reaction to shock to foster attainment of correct

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response. Also, we used boxes of different sizes to accommo- date different sizes of fish.

In summary, fish Iemed a simple conditioned response, and our determination of comparative Beaming ability was consis- tent with other assessments of lemiwg of some of the same species. Yet, intrinsic behavior of the various species may have influenced our determination of relative leming. Assessment of the extent of that influence requires comparisons sf learning of the species with more than one method.

Memosy , Age, Temperature, Feeding Level, Disease

Long-term memory that deteriorated with time (Table 2) has also been found in other studies. Tarrant (1964) reported retention of a conditioned response in juvenile sockeye salmon (Onesrhynchus nerka) for more than a year, with loss sf some of the conditioned response after the 18 1st day. Common carp (Beukema 1970; Beukema and de Vos 1 974) and largemouth bass (Anderson and Heman 1969) became less vulnerable to being caught after exposure to angling. Catchability of the common carp was reduced 1 yr after exposure to angling, although there was evidence of fading of the acquired hook avoidance. Some sf the largemouth bass lost their reduced catchability after 6 mo. A&on et al. (8973) reported retention for 3 mo for rainbow trout (Salmo gairdnert); Gleitman and Rozin (1971) and Wensch and Diicker (1966) reported deteriora- tion in retention of goldfish over a period of 1-3 mo.

The importance of age or maturity on leming is not well established. Not only did we obtain contrasting results with two species, but also, Shashoua (1973) and Agranoff and Davis (1974) reported seasonal variation in learning ability of goldfish in which acquisition and retention scores were high in February md March and low in July. They thought the variation might be related to age, condition, physiological state, hormonal levels, or biogenic amine levels in the brain. In contrast, Fjerdingstad (1974) did not find such seasonal variation in goldfish. We could not investigate seasonal variation in leming kcaalse when we trained different groups of a single species, we did so at the same time of the y e s . However, because seasonal variation has been reported, we included dates of training in Table 1 .

Our lack of an effect of temperature on leming of channel catfish in the range of 18-28°C agrees with results of other studies with other species at similar temperature ranges. Prosser and Fuhi (1 965) acclimated and conditioned goldfish at 5, f 5, 25, and 30°C. The percent conditioned (7 1-83) did not decrease with decreased temperature, in the range of 30-15°C. French (1 942) held goldfish at 4, 16, and 28°C before training them to negotiate a maze at 22OC. Those tested at 16°C did not make more errors than those tested at 28OC. Rozin (1965) found no difference between groups of goldfish tested at 20 and 30°C to discriminate time when pressing a lever for a reward.

Temperatures of 1 11°C or less, however, have been found to affect leming. When Hunter and Wisby (1964) acclimated and trained groups of common carp to escape a net at 11 and 24"C, more escapes occurred at the higher temperature. Hw the experiments of hosser and Farhi (1965) and French (1942), goldfish conditioning was poorer and errors greater at the lowest temperatures than at the higher temperatures.

We found no study of effects of disease or feeding Bevel on leming sf fish. Degree of satiation obviously could influence conditioning that is based on a food reward system. Such systems can also be influenced by factors other than hunger; Razin and Mayer (1961) found that some goldfish became

anorexic, and some, after pressing a lever releasing food pellets, left the pellets uneaten. Our results suggest that low feeding levels would have little effect as long as fish are not stawed to the point that behavior is impaired.

Acknowledgements

We thank E. McEain and J . Maenner for helping to conduct experiments, 6. Vaughaua and members of the Missouri Department of Conservation for collecting fish, F. Hilbert (University of Wisconsin - Stevens Point) for preparing a computer program, and J. R. Heaton and W. H. EeGrmde for reading the manuscript.

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