THE OPTOMOTOR REACTION OF SCHOOLING CARANCID FISHES*

BY EVELYN SHAWDepartment of Animal Behavior, The American Museum of Natural History,

AND ARLENE TUCKERInstitute of Animal Behavior, Rutgers University .

IntroductionMany schooling fishes maintain parallel

orientation with some set range of distancesbetween them, as has been discussed by manyauthors beginning with Parr (1927) . A usualfeature of fishes in schools is their constantswimming and forward movement . As the entireschool moves, the individual fish remain essen-tially parallel, but change position with relationto one another and also alter their velocitieswithout interrupting the smooth forward move-ment of the school .

The sensory stimuli which maintain consistentparallel orientation of the fish during forwardmovement and changing velocities are apparent-ly of such nature that the fish are stimulatedsimilarly whether they are at the head, themiddle, the rear end or on the sides of the school .In exploring the nature of these stimuli, Parr'soriginal work (1927) and the work of manyinvestigators since (reviewed by Morrow, 1948 ;Atz, 1953 ; Breder, 1959) have shown that visionis the important sensory system . Nevertheless,the specific way in which the visual system medi-ates this behaviour is not known . In our studieswe are investigating the optomotor reflex offish as a possible mechanism by which the fishcan shift positions in the school, change velo-city and maintain their parallel orientation,(Shaw, 1965) . This study is concerned only withthe behaviour of a school once formed and notwith the mechanisms of initial school formation .

MethodThe optomotor apparatus consisted of a

cylindrical lucite aquarium surrounded by aconcentric motor-driven rotating steel drum .Both the aquarium and the drum rested insidea child's plastic swimming pool. The pool wasfilled with sea water to the top of the apparatus,as seen in Fig. 1, Plate VII . The dimensions are

Research supported, in part, by NSF G-10832 and inpart by a contract between The American Museum ofNatural History and the Office of Naval Research,Contract No. ONR 552 (09) . This work was carried outat the Lerner Marine Laboratory, Bimini, Bahamas .

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given in Fig . 2. The drum could be rotated ineither direction at speeds ranging from 3 .5 to38 . 5 revolutions per minute. The lucite aquariumhad its own inflow-outflow system. Waterentered into the bottom of the aquarium througha small hole, 8 mm. in diameter. The waterflowed out by spilling over the top of theaquarium. The water did not create currentsaround the aquarium, but moved upwards fromthe inflow to the top .

Three different stimuli, lining the interior ofthe drum, from top to bottom, were used . Thesestimuli consisted of (1) a field of alternatingblack and white vertical stripes, made by pastingblack tape on white styrene sheets ; (2) a panelof alternating black and white vertical stripes,subtending an area of 60° with the remainingarea white and (3) as a control, a plain whitestyrene sheet.

The following procedure was used in testing .After a fish was permitted a period of adaptation,up to one half hour, tests were started with aone-minute observation of the swimming activ-ity of the fish, while the drum was not moving .The drum was then rotated at the lowest speedfor one minute and the speed was graduallyincreased, in step fashion, from the lowest tothe highest speeds. At each speed a minute ofobservation was made on the qualitative be-haviour of the fish, and the total number ofcomplete revolutions made by the subject wasrecorded . The initial direction of rotation ineach series was assigned randomly .

The species studied were Caranx ruber (Bloch),the bar jack (6 to 9 inches long), and Selarcrumenophthalmus (Bloch), the bigeye scad(6 to 8 inches long) . Both species were veryfragile when kept under laboratory conditions .Handling caused lesions on the side of the bodywhich resulted in death of the fish within a fewdays . Occasionally the transparent cornea be-came cloudy while the fish were in storage tanksor in the apparatus . The results reported herewere obtained on those few recently-caughtindividuals which showed little or no damage

Stationary aquarium

Rotating drum

Fig . 2 . Dimensions of the optomotor apparatus .

SHAW & TUCKER : THE OPTOMOTOR REACTION OF SCHOOLING CARANGID FISHES

331

under our conditions . The number of fish ob-served is indicated on the graphs .

Results and InterpretationQualitative Observations

In the observations, taken while the drum wasnot moving, two kinds of behavioural activitywere noted . Fish remained quiescent with thelong axis radial to the aquarium wall or movedin either direction, circling the container . Fishremained near the bottom or centre of theaquarium and rarely moved to the top .

When fish were exposed to the fully stripedfield, the most common behaviour was con-tinuous and regular movement in the samedirection as the drum and normal to the radiusof the aquarium . This is the typical optomotorresponse observed by Trinckner (1952) inCarassius, the goldfish, and Hortsmann (1959)in Mugil, the mullet, and Harden Jones (1963)in a number of other species .

Other activities, not of this typical form, wereoccasionally seen in individual fish . Sometimes,at low speeds, the subject remained with the longaxis of its body perpendicular to the wall of theaquarium and, maintaining this orientation,it pivoted in the same direction as the drum .While in this position, a right and left lateralmovement of the head and anterior part of thebody was also seen . Since the speed of headmovement in each direction was the same (no

fast and slow compon-ent could be distin-guished) this behaviour

Striped stimulus panel was clearly not thehead mystagmus whichTrinckner (1952) des-cribed in goldfish andwhich we have also ob-served in Menidia, thesilversides .In the situation

where only a panel wasstriped, the orientationof the animal to diff-erent areas could beobserved . Through dir-ect observation and byanalysis of films takenof this behaviour, itwas noted that the an-imal's approach to syn-chrony with the stripedpanel was closest at

intermediate speeds as seen in graph 3, (Fig . 5) .At slow speeds, the fish position was slightlyahead of the panel, at fast speeds, slightly be-hind. Initial position was rarely maintained forseveral consecutive drum rotations and theanimal swam behind or ahead of the stripes . Thefish then accelerated or decelerated and a posit-ion near the panel was re-established . At themiddle range of speeds, the animals tended tostay opposite the panel, although again, the fishwas rarely in exactly the same place relative toany given stripes for many consecutive rotations .However, when the drum stopped the animalstopped circling immediately and remained nearthe striped portion of the field . Thus it becameapparent that the animal oriented to the panelof stripes, was moving because of the move-ment of the stripes, but swam at a variablespeed even when the drum speed was constant .Hortsmann (1959) found that mullet, if placedinside of a drum where a third is covered withstripes, moved sometimes with and sometimesagainst the movement of the drum. This obser-vation differs from that reported here, but theresults cannot be compared because Hortsmanndid not present data on the speed of drumrotation .

When the entire drum was white the fishesremained still, moved circularly, swam erratic-ally up and down the side wall, or movedalternately in clockwise and counter-clockwisedirections in short bursts of speed .

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ANIMAL BEHAVIOUR, XIII, 2-3

GRAPH I BAR JACKS3

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SHAW & TUCKER: THE OPTOMOTOR REACTION OF SCHOOLING CARANGID FISHES

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GRAPH 2 BIGEYE SCADS

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RPM of drumFig. 4. ReNolutions per minute, at various drum speeds and in various stimuli, are compared in the bigeye scads .

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ANIMAL BEHAVIOUR, XIII, 2-3

Quantitative ObservationsGraphs 1 and 2 (Fig . 3 & 4) show the relation-

ship between revolutions per minute (r.p.m .) ofthe drum and that of the fish when exposed tothe various stimuli . A comparison of the differ-ent conditions for both species reveals this :only a field containing vertical stripes produceda following response which increased regularlyin speed with increase in r .p.m. of the field .This response is not obtained with rotation ofthe entirely white field, and it is clear that move-ment of the animals is because of the movingstriped field and not to artifacts such as themoving overhead struts which held the drum

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GRAPH 3 PARTLY STRIPED

suspended .In Graph 3 (Fig. 5) when only a small part of

the field is striped the r .p.m. of both speciesis alike and similar to the r.p.m. of the drum. Apossible explanation is suggested by the qualita-tive observations given above. Observations offish in the panel situation show that the fishmaintain the position relative_ to the panel withinbroad limits. It does so by changes in acceler-ation and only the average r.p.m. is the same asthat of the field ; the animal's orientation to thepanel and his swimming velocity, relative to it,vary. In Graph 4, (Fig . 6), where the entire fieldis striped, there is a uniformity of stimuli and no

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SHAW & TUCKER: THE OPTOMOTOR REACTION OF SCHOOLING CARANGID FISHES

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ANIMAL BEHAVIOUR, XIII, 2-3

one pair of stripes or one fixation point shouldbe distinguishable from any other . Therefore,if the fish does not synchronize its speed ofmovement with that of the initial fixation pointit cannot alter its velocity to re-establish theinitial fixation point, because that point is in-distinguishable from any other . The behaviourof the fish in the uniformly striped field is prob-ably the following : the animal adopts a fixationpoint, swims with it in view for a period oftime, loses it, picks up a new fixation point,remains with it for a period, etc . Thus the movingfield is "stopped" in the perception of the animalfor successive periods. Precise synchrony ofanimal with drum is not necessary in order toobtain perceptuality a stationary field for suc-cessive short periods of time . To maintain theseperiods of time as the invariant, however, re-quires an average increase in r .p.m. which isproportional to the increase in r.p.m. of thedrum. The average velocity of the animal forany given velocity of the drum is probablypartially determined by drum speed and par-tially by the natural swimming habits of theanimal. Harden Jones (1963) also found speciesdifferences in the velocities of various fish . Thebar jack circles more times per minute, for anygiven drum speed, than the bigeye scads . Wehave observed that bar jacks are much fasterswimming than bigeye scads under natural con-ditions. When many fixation points are possible,rather than a few, the influence of naturalswimming speeds can be more pronounced with-out disrupting the basic perceptual function, thatof "stopping" the moving field .

Discussion and Application to the SchoolingProblem

The previous section shows that in the opto-motor response : (1) the fish moves in the samedirection as the moving field and parallel to it ;(2) the fish changes its speed as the speed of themoving field changes ; (3) the fish alters itsposition relative to the field, that is, it is notalways opposite the same area of the stimulus .

The similarity between this behaviour andcertain features of schooling is striking . In aschool : (1) fish are all moving in the same direc-tion ; (2) a fish changes speed as the fish sur-rounding it change speed ; (3) a fish changes itsposition relative to other fish, but nonethelessremains parallel to them and in the school . Theentire group moves forward while members ofthe group may be making changes in theirpositions .Therefore, by exposing a fish to a stimulus

consisting of a series of moving black and whitevertical stripes, important features of schoolingbehaviour have been reproduced . Fish in theschool may be providing for other fish in theschool a series of successive contrasts which aregreatly enhanced because the fish are moving .Baylor & Shaw (1962) have suggested that theteleost eye is capable of perception of smallmovements with concommittant enhanced con-trast . This may be highly adaptive in schoolingand the optomotor reflex may play an importantrole in the features of schooling mentionedabove. Such a possibility is also implied byProtasov & Altukov (1961) in their study ofoptomotor reactions in schooling fish, youngfish and river "rheophilic fish .

SummaryCarangid fishes were tested in an optomotor

apparatus and their orientation to different kindsof stimuli was observed . The fish did not orientto any particular region of the stimulus con-sisting of uniform black and white verticalstripes . The r .p.m. of the fish was generallygreater than the r .p.m. of the drum . On the otherhand, the fish oriented to the panel stimulus andtended to remain near it during the entire rangeof revolutions . The r .p.m. of the fish closelyfollowed the r .p.m. of the drum .

Certain features of the behaviour of the fishin an optomotor apparatus are compared withcertain features of schooling under natural con-ditions .

REFERENCESAtz, J . W. (1953) . Orientation in schooling fishes . Proc.

Conf. Orientation in Animals, ONR, 103-130.Baylor, E. R. & Shaw, E. (1962) . Refractive error and

vision in fishes . Science, 136, 157-158 .Breder, C. M. (1959) . Studies of social groupings in

fishes . Bull. Amer. Mus. Nat . Hist ., 117, 397-481 .Harden Jones, F. R . (1963) . The reaction of fish to mov-

ing backgrounds . J. exp. Biol., 40, 437-446 .Hortsmann, E . (1959) . Schwarmstudienunter Ausnutzung

einer Optomotorischen Reaktion bei Mugilcephalus (Cuv .) . Pubbl. Staz. Zool. Napoli, 31,25-35 .

Morrow, J. E. (1948) . Schooling behaviour in fishes .Quart. Rev. Biol., 23, 27-38 .

Parr, A . E . (1927) . A contribution to the theoreticalanalysis of schooling behavior of fishes . Occ. Pap .Bingham Oceanogr . Coll ., No . 1, 1-32 .

Protasov, V . R . & Altakov, U. P . (1961). The possibilityof using the optomotor reaction for controllingthe movement of fishes . Plynoe . Khoz. 2, 29-32.(Referat . Zhur . Biol., 1961, 200412) .

Shaw, E . (1965). The optomotor response and theschooling of fish . ICNAF Spec . Publ. (in press) .

Trincker, D . (1952) . Reafferenz-Princip and Anpassung .Die Naturwiss ., 39, 115-116 .

(Accepted for publication 19th February, 1965 ;Ms. number : 461).

ANIMAL BEHAVIOUR, XIII, 2-3

PLATE VII

Fig . 1 . The optornotor apparatus . The fish can be seen in the circular aquarium .

Shaw & Tucker, Anim . Behav., 13, 2 -3