THE EFFECT OF THE BOTTOM ON THE FAST START OF FLATFISH ClTHARlCHTHYS STIGMAE US

ABSTRACT

Fast starts of the spdckled sanddab. Citharichthys stigmaeus, were initiated by a 1volt per centimeter direct current electjc shock and recorded on movie film at 250 frames per second Observations on kinematics and performance were made for fast starts of fish accelerating in the water column and fmm a grid located at a distance of 0.1.3, or 6 cm above the true bottom. During acceleration the body was bent into a U-shad relative to the bottom. The body sustained a direct push against the grid when accelerating from that grid. The amplitude of propulsive movements of fish accelerating from the grid was larger than acceleration movements offish in the water column away from the bottom, because the potential for energy wastage due to recoil of the body was prevented by the grid. The distance between the grid and the bottom had no effect on fast starts, ruling out any hydrodynamic ground effect. Motion of fish accelerating in the water column was continuous and predominantly in the horizontal plane. There was little motion of fish accelerating from the grid until they started pushing against that grid. Motion was predominantly in the vertical plane. The resultant distance traveled by fish accelerating from the grid, measured at the end of the principal acceleration period exceeded that offish accelerating in the water column. Mlocitiesand acceleration rates were highest for fish accelerating from the grid. It was concluded that contact with the sea bottom would enhance fast-start performance of flatfish.

Fish of the order Pleuronectiformes are unique 1979). Pushing against the substrate is obv )usly because the adults lie on one side. The habit of more energy efficient than pushing against water inclining to one side is common among other because more muscle power is converted into body benthic fish that are normally vertically oriented, motion rather than wasted in acceleratingfluid. It but no other group shows the specialized mor- is utilized by macrurous decapods (Webb 1979). phological adaptations of flatfish. Various obser- The relative importance and effectiveness of these vations on benthic fish suggest that inclining the mechanisms will depend on how flatfish move body or lying on one side is advantageous for their bodies near the ground. camouflage and crypsis (Norman 1966). Large The following experiments were performed to locomotor advantages could also accrue, espe- determine if the sea bottom could influence fast- cially to flatfish orienting their body axis parallel start (acceleration) movements and performance to the ground. of a typical flatfish. Emphasis was placed on fast Improvements in locomotor performance of starts because of their importance in evasion of flatfish could occur through two mechanisms: hy- predators and in catching elusive prey (Eaton and drodynamic ground effect and pushing against a Bombardieri 1978; Webb and Skadsen 1980). rigid substrate. The hydrodynamic ground effect occurs through interaction of the downwash from METHODS propulsive surfaces with the ground (i.e., the sea bottom) and increases effective thrust and de- Fish creases effective drag (Bramwell 1976; Lighthill 1979). It has been described for birds (Withers and Speckled sanddab, Citharichthys stigmaeus Timko 1977) and for pectoral fin propulsion of the Jord8g and Gilbert (family Bothidae) were used. mandarin fish, Synchropus picturatus (Blake Fish were caught in dip nets by divers along the southern California coast, hence avoiding the --_. - 'Southwr-t Fisheries Center La Jolla Laboratory, National damage typical of trawl-caught specimens. Fish Morinr Fidwrtt., Service, NOAA. La .Jolla. Calif: present ad- dw-, SchwJl of Ndcurnl Resources. University ofhlichigan. Anu were held in a 60,000 I tank at 14°C. They were fed Arhot. .\I1 4sl[l!J. twice a week on frozen brine shrimp.

M.inu*cnyt accepted Scytentber 19~ 271 FIStltRY BULL.ETlN VOL. 79. NO 2. 1981 FISHERY RL'I.I.ErIN VOL i9. SO 2 Procedures length, wetted surface area, location of the center Qf mass, and muscle mass were measured as de- Individual speckled sanddabs were starved for scribed by Webb (1977). 24 h. Each fish was lightly anesthetized (MS-222I2 There were no differences in these morphomet- and a white thread was sewn above the center of ric characteristics among various groups of speck- mass of the stretched-straight body calculated led sanddabs. Combined values were (mean 52 from previous measurements on a subsample of SEI; mass, 28.9623.78 g; length, 13.750.6on; the fish. This reference facilitated later film analysis, center of mass, located 5.2 20.2 cm from the nose; Each fish was then placed in an observation arena wetted surface area, 120510 cm2; muscle mass, and allowed to recover for 24 h overnight. free of skin and scales, 11.7852.28g. The observation arena consisted of a chamber 45 cm long, 30 cm wide, and 40 cm deep. A fast start is Movie film was analyzed frame by frame to ob- a short duration stereotyped activity during serve kinematics and to measure performance. which fish travel short distances but accelerate at Details are given by Webb (1978). Briefly, perfor- high rates to reach large speeds (Eaton et a). 1977; mance was measured for the motion of the center Webb 1978). The size of the arena would not inter- of mass of the stretched-straight body. This point fere with fast-start activity but would prevent sus- approximates the instantaneous center of mass of tained high-speed swimming. This study is con- the flexing body which is the point about which cerned only with the former activity propulsive forces act. Coordinates for motion of the The observation chamber had a false bottom center of mass were measured in the horizontal made from a wire grid (2.5cm squares made from and vertical planes. The resultant motion of the 0.08 cm diameter wire). A solid bottom was located center of mass was calculated. Velocities and ac- beneath the grid and could be set 0,1,3,or 6 cm celeration rates for these three motions (hori- beneath. Comparison of performance during fast zontal, vertical, and resultant) were calculated starts with the grid set at various distances above using moving point linear regression methods. the solid bottom was expected to show the impor- Performance parameters were compared using the tance of the hydrodynamic ground effect as differ- t-test, and significant differences between means ences in performances once physical contact with are declared at the 5% level. the grid had ended. Vertical reinforcers prevented the grid from acting as a spring when a force was RESULTS applied by an accelerating fish. The observation chamber also allowed room for fish to swim in the Kinematics water column for short distances permitting ob- servation of fast starts in the water column remote There were no differences in kinematics of fish from all possible ground interaction. accelerating from the grid set at various distances The bottom was located in one of the four posi- above the solid bottom. Fast-start kinematics for tions beneath the grid while the sanddab became acceleration from the grids (Figure 1) showed the accustomed to the chamber overnight. Next morn- normal three stages originally described by Weihs ing a 1.0 Vlcm d.c. electric shock was used to ini- (1973). During stage 1, the body was bent into a tiate a fast start either from the grid or when the U-posture (0-80 ms in Figure L4) comparable to sanddab was temporarily stationary in the water the C-posture of other teleosts when viewed from column clear of the grid and bottom. All experi- above (Eaton et al.,l977; Webb 1978).The center of ments were performed at 14" C. mass showed some recoil (i.e., lateral movement in Fast starts were recorded on movie film at 250 the opposite direction to the tail, and normal to the framesls. A 45" mirror above the observation fish axis) towards the grid because the fish adopted chamber allowed simultaneous observation of top a posture with the body raised by the median fins and bottom views. A floating lid prevented surface before a fast start (Stickney et al. 1973). The body ripples distorting the top-view image. was always bent away from the bottom. Each fish was killed after an experiment. The During stage 2 (80-120 ms in Figure lA), the body outline was traced on paper. Mass, total body was bent in the direction opposite to that of stage 1 as the body curvature traveled caudally *Reference to trade names does not imply endorsement by the along the body. Some point of the body remained in National Marine Fisheries Service, NOAA. contact with the grid almost to the end of stage 2. 272 I

WEBB: EFFECT OF BOTTOM ON FAST START OF A FLATFISH

A

I IO cm 1

B

FIGURE 1.-Tracings ofthe body center-linecseen from theside) at 20 ms intervals toshow the acceleration movementsduritig fast stnrtsofCitharichthyssti~nracus: AI Acceleration from contact with thegrid. BI Acceleration in the water column. Dots show the location of the center of mass of the stretched-straight body. The extended and variable stage 3 following the major acceleration strokes has been omitted for clarity

The center of mass was propelled vertically away The timing of various fast-start events was simi- from the ground. lar among groups of fish (Table 1). The duration of Fast start stage 3, occurring after the major stage 1 showed a slight but nonsignificant tend- acceleration period, was variable, ranging from an ency to decrease as the distance between the grid unpowered glide to continued swimming with and the solid bottom increased. The fish accelerat- caudal propagation of propulsive waves sustained ing from the grid lost contact after 112 ms, before from the starting curvature in stage 2. the completion of stage 2 in 124 ms (Table 1). A typical fast start of a sanddab in the water column away from the bottom is illustrated in Fast-Start Performance Figure 1B. Fast starts in the water column showed the same stages as fast starts from the grid. The The distance between the solid bottom and the amplitude of body movements was usually smaller grid had no significant effect on vertical and hori- than those of fish accelerating from the grid. zontal distances traveled by the center of mass of Center of mass recoil, reduced during acceleration speckled sanddabs during fast starts (Figure 2) from thegrid, was observed for fish accelerating in including distances traveled after losing contact the water column, as seen in other teleosts. with the grid. This showed that no measurable

TABLEL-Fksults for the duration offast-start events for Citharichthys stigmaeus accelerating from a grid at various distances above a solid bottom and accelerating in the water column. Mean 22 SE are shown, n = 10. Distance between the grd and the Sdid Acceleration in bnom (cm) Combtned dala lor Tmmg me water cdumn 0 1 3 6 acceleration lrom the grd

~~~ ~~ ~ ~~~ ~ Ouration of stage I ms 58 -8 65r6 65x14 62-8 60-8 63x5 Duration 01 stages t plus 2. ms to5s12 136~18 118~13 149~40 113-9 124~7 Tme to end of ground contact. ms - 116~19 108-9 116~15 11319 11226 \ -. - 273 6t 't t

FIGURE 2.-Relationships between the distance traveled by the center of mass Ithe point about which propulsive forces 14 act)and elapsed time during fast starts of Cifhon'chfhys stigrnoeus. The motion of L the center of mass was resolved into the distance traveled in the horizontal (A. 91 and vertical IC, D1 planes. These data were used to calculate the rt!sulLm~tdis- tance traveled (E.Ft. Fast-start perfor- mance is shown for fish accelerating in the water column IA, C. El and from the grid (9. D, F1. The dotted lines in B. D. and F show the motions of the center of mass of fish accelerating in the water col- umn from A, C. and E to facilitate com- parison with fast starts from the qid. Ver- tical bars shown 22 SE.

TIME - ms

hydrodynamic ground effect influenced speckled ms at the end of stage 1, compared with 1.920.4 cm sanddab fast starts. All data for fish accelerating in the same time for fish accelerating in the water from the grid were therefore combined for sub- column. By the end ofstage 2 fish starting from the sequent analysis and for comparison with fish ac- grid had moved forward 3.920.9 cm in 124 ms. celerating in the water column. This was an improvement over stage 1, but still The performance of fish accelerating from the less than that of fish in the water column which grid differed from that of fish accelerating in the moved forward 6.8-cO.9 cm in the same time. The water column. The differences were seen in hori- small initial displacement of fish in contact with zontal and vertical motions and in the net (resul- the grid was probably due to frictional interac- tant) motion. In the horizontal plane, fish ac- tions between the fish and the grid (Arnold and celerating from the grid traveled 0.820.2 cm in 63 Weihs 1978). The normal force at the point of con- 274 U'ERR EFFECT OF BUTTOSI ON FAST START OF A FLATFISH tact would also have been augmented by recoil DISCUSSION forces generated by the tail and head tending to displace the fish downwards. These experimtnts show that the bottom (grid) The motion of the center of mass in the vertical does influence fast starts in speckled sanddabs. plane also differed between speckled sanddabs ac- Fast starts from the bottom were associated with celerating from the grid and in the water column large amplitude motions that would normally (Figure 2C, D). For fish accelerating from the grid cause substantial recoil of the center of mass be- there was little vertical movement during fast- cause the bottom prevents that recoil. Motions of start stage 1 because of the presence of that grid. fish accelerating from bottom contact were pre- During stage 2, however, the center of mass was dominantly vertical compared with horizontal accelerated vertically upwards moving 6.022.4 motions of fish accelerating in the water column. cm in 124 ms. Fish accelerating in the water col- The relative magnitude of vertical and horizontal umn showed little vertical motion, except that due displacements of sanddab accelerating from the to recoil (Figure 2C). f grid are comparable with those observed in The resultant motion of the center of mass of the crayfish under similar circumstances (Webb 1979). fish showed differences between acceleration in For both speckled sanddab and crayfish the the water column and from the grid, but these marked vertical motion is caused by prolonged differences were less marked than motions in the contact between the body and the ground. Unfor- hot.i/.ontal and vertical planes (Figure 2E, F). The tunately, these large vertical displacements in increase in distance covered with time was ini- speckled sanddabs preclude anj significant hy- tially greater for fish accelerating in the water drodynamic interaction with the ground after con- column. They traveled a total of 3.720.6 cm in 63 tact is lost. ms compared with 2.920.4 cm for fish accelerating Withers and Timko (1977) give a succinct expla- froni the grid. However, once fish pushed against nation of this hydrodynamic ground effect, where the grid in stage 2, performance improved. By the the ground influences the flow, increasing lift end of stage 2, they had traveled a cumulative (thrust) and decreasing drag. Hydrodynamic distance of 10.221.2 cm in 124 ms, greater than ground effect rapidly declines as the ratio, yls, that of 8.7 21.3 cm achieved by fish accelerating in increases, where y is the gap between the surface the water column. generating thrust and the ground, and s is the Velocities calculated for the center of mass span (width) of that surface. Blake (1979) found reached maximum values close to the end of stage that 80-9W0 of the ground effect vanished by the 2. Maximum values were significantly greater for timeyls reached unity in hovering mandarin fish. fish accelerating from the grid compared with fish The mean maximum span of speckled sanddab, accelerating in the water column (Table 2). Mean located at the center of mass, was 6.750.2 cm. For acceleration rates would, of course, follow similar this span, yls = 1 after about 130 ms, 18 ms after trends to velocities. Maximum acceleration rates the end of physical contact with the bottom (Fig- only showed significantly improved performance ure 2D). The caudal fin had a maximum span of for resultant motion of fish accelerating from the 2.4?0.3cm,and avalueofyls = lisreached within grid (Table 2). about 16 ms after the tail loses contact with the bottom (Figure 1A). Thus, the vertical accelera- tion rapidly lifts the speckled sanddab out of the hydrodynamic influence of the ground so that TABLE?.-Results of maximum acceleration rates and maxi- there is insufficient time for any interaction to mum velocities for Citharichthys stlgrnaeus accelerating from thegn ':~ndinthewatercolumn.Datacmran 52SE;n = lolare affect performance. However, the absence of this shown li~rmotion of the center of mass effect during a fast start does not preclude hydro- Fast starts Fasl starts dynamic ground interactions from improving from in the water Item the ard column steady swimming close to the sea floor.

Maximum acce!era!lon rates. mis2. Thus, the observations on fast starts of speckled Hrmzontal 37Z7 48110 sanddab from the bottom show that a single Vertical 54~10 44f9 Resultant 66~12 46~12 kinematic pattern is used, which sustains bottoni Maximum velocities. mis contact for most ofa fast start, but which prevents Horizontal 66-11 92-10 Veri~cji 92- 12 1714 deve 1o pme n t of any sign i ficant h yd rotly na rn ic Resultant 104-17 76114 ground effect. However, a direct push against :I 275 FISIiEIplaice (Pleuronectesplafesxa Ll J. Exp. Biol. 75147-169. example, the small initial displacement of the BLAKE.R. W center of mass of fish accelerating from the ground 1979. The energetics of hovering in the mmd;irin fish might be disadvantageous in some circumstances, cSyrchrupi,rrs pictunitus). J. Exy. Biol. 82.25-33. such as escaping from predators. However, sig- RRAMWELL. A. R. S. nificant protection is achieved by camouflage and 1976. Helicopter dynamics.' Edward Arnold. Lond.. 408 p. cryptic behavior in pleuronectiform fishes, render- EATON.R. c.. AND R. A. BOMB.4RDIERL ing this contingency unlikely. 1978. Behavioral functions of the 3Ltuthner neuron. In The influence of the bottom is clearly advan- E. Faher and H. Korn Irditoral, Neurobiology of the tageous in the capture of elusive prey, a second Mauthner cell, p. 221-224. Raven Press. N.Y. EATON,R. C.. R. A. BOMBARDIERI.AND D. L. 11EYER. behavior in which fast starts play a key role 1977. The Mauthner-initiated startle re3pon.e in teleost (Eaton and Bombardieri 1978; Webb and Skadsen fish. J. Exp. Biol. 66:65-81. 1980). Elusive prey, e.g., fish and crustacea, are HOBSON. E. s. common dietary items for pleuronectiform fishes 1979. Interactions between piscivorus fishes and their in the families Psettodidae, Bothidae, and prey. In H. Clepper ceditorl. Predator-prey systems in fisheries management, p. 231-142. Sport Fish. Inst.. Pleuronectidae (Liem and Scott 1966; Norman \Va.sh.. D.C. 1966). The bottom eliminates recoil so that the fish LEIM. A. H.. AND \V B. SCOrr. can rapidly accelerate the head vertically (Figure 1966. Fishes of the Atlantic coast of Canada. Fish. Res. 1). Continued rapid vertical acceleration is facili- Board Can., Bull. 155.4% p. LICHTHILL.J. tated by prolonged bottom contact through the 1979. A simple fluid-flow model ofground effect on hover- major acceleration period of a fast start. Bottom ing. J. Fluid .\lech. 93:781-797. contact also results in the acquisition of a superior NORMAN.J. R. final speed that would be advantageous in a con- 1966. A systematic monograph of the flatfishes I Heterw tinued attack. The time taken to accelerate from somata). Johnson Reprint Corp.. Lond.. 459 p. STICKNEY. R. R.. D. B. WHITE. AND D. MILLER. the bottom and reach maximum speed could also 1973. Observations of fin use in relation to feeding and be reduced by resting in sand in a curved U-shaped resting behavior in flatfishes I Pleuronectiformesl. posture. This may occur since flatfish often dig into Copeia 1973:154-156. sand with the eyes and tail at the surface, but the WEBB.I? W. body buried, implying a curved posture (Hobson 1977. Effects of median-fin amputation on fast-start per- formance of rainbow trout cSoImo garrdneril. J. Exp. 1979). Thus, the morphology and behavior of the Biol. 68:123-135. benthic sanddab appear to be adaptive in improv- 1978. Fast-start pekormance and body form in seven ing fast-start performance, as well as for camou- species of teleost fish. J. Esp. Biol. 51:211-226. flage. Such advantages undoubtedly apply equally 1979. Mechanics of. escape respones in craylish 10m to other members of the pleuronectiformes and nectes vinlis). J. Exp. Biol. 59245-263. WEBB, E! w.. AND J. >%.SdADSEN. therefore provide an additional functional expla- 1980. Strike tactics ofEsox. Can. J. 2001. 58:1462-1469. nation of the unique flatfish body form and habits. WEIHS, D. 1973. The mechanism of rapid starting of slender fish. ACKNOWLEDGMENTS Biorheology 10:343-350. WITHERS,I? C.. .4hn p. L. TI%iKo. 1977. The significance of ground effect to the aero- This work was completed during the tenure of dynamic cost of flight and energetics of the black skim- an NRClNOAA Research Associateship. Fish mer IRhyncops nigra). J. Exp. Biol. 70:13-26.