In a revision of the original classification system of Breder(1926), Webb (1975) proposed that all possible patterns ofbody–caudal fin propulsion in fishes can be identified as one offour distinct swimming modes: anguilliform, subcarangiform,carangiform and thunniform. The thunniform mode,documented only in the tunas (Fierstine and Walters, 1968;Dewar and Graham, 1994), is believed to be the most efficientbecause of the small amount of lateral undulation along thebody, which minimizes frictional drag (Webb, 1975). Tunasare streamlined, with a tear-drop-shaped body, a narrow caudalpeduncle with lateral keels and a rigid, high-aspect-ratio caudalfin that oscillates rapidly to generate lift-based propulsiveforce. All these properties are considered to increase locomotorefficiency (Lighthill, 1970, 1975; Lindsey, 1978; Magnuson,1978; Blake, 1983; Webb, 1975, 1998). However, thehypothesis that thunniform locomotion is the most efficientmode of body–caudal fin propulsion has not been testedempirically in swimming fishes.

Tunas are the most derived members of the familyScombridae, comprising a monophyletic group (tribe

Thunnini) with several unique characteristics (Collette, 1978;Block et al., 1993; Carpenter et al., 1995; Graham and Dickson,2000). The only other scombrid fishes whose swimming modehas been characterized are the mackerels (tribe Scombrini),which have been classified as carangiform swimmers (Gray,1933; Lindsey, 1978; Videler and Hess, 1984; Shadwick et al.,1998). Bonitos (tribe Sardini), the sister group to the tunas,have been described as carangiform swimmers ‘verging on thethunniform’ (Lindsey, 1978, p. 20), but the only kinematic datawe could find on bonitos (Pyatetskiy, 1970; Altringham andBlock, 1997) do not provide the information needed todetermine swimming mode.

The length of the propulsive wave that travels down thebody during steady swimming and the percentage of the bodythat undergoes lateral undulatory movements are the twocriteria that have been used to distinguish the four modes ofbody–caudal fin locomotion (Webb, 1975; Lindsey, 1978;Videler, 1993). Gray (1933) indicated that propulsivewavelengths are slightly greater than body length incarangiform swimmers, with the exception of the Atlantic

3103The Journal of Experimental Biology 203, 3103–3116 (2000)Printed in Great Britain © The Company of Biologists Limited 2000JEB2852

The swimming kinematics of two active pelagic fishesfrom the family Scombridae were compared to test thehypothesis that the kawakawa tuna (Euthynnus affinis)uses the thunniform mode of locomotion, in which the bodyis held more rigid and undergoes less lateral movement incomparison with the chub mackerel (Scomber japonicus),which uses the carangiform swimming mode. Thisstudy, the first quantitative kinematic comparison of size-matched scombrids, confirmed significantly differentswimming kinematics in the two species. Ten kawakawa(15.1–25.5 cm fork length, FL) and eight chub mackerel(14.0–23.4 cmFL), all juveniles, were videotaped at 120 Hzwhile swimming at several speeds up to their maximumsustained speed at 24 °C. Computerized motion analysiswas used to digitize specific points on the body in sequentialvideo frames, and kinematic variables were quantifiedfrom the progression of the points over time. At a givenspeed, kawakawa displayed a significantly greater tailbeatfrequency, but lower stride length, tailbeat amplitude and

propulsive wavelength, than chub mackerel when sizeeffects were accounted for. Midline curvatures subdividedon the basis of X-rays into individual vertebral elementswere used to quantify axial bending in a subset of the fishstudied. Maximum intervertebral lateral displacement andintervertebral flexion angles were significantly lower alongmost of the body in kawakawa than in chub mackerel,indicating that the kawakawa undergoes less axial flexionthan does the chub mackerel, resulting in lower tailbeatamplitudes. However, lateral movement at the tip of thesnout, or yaw, did not differ significantly interspecifically.Despite these differences, the net cost of transport was thesame in the two species, and the total cost was higher in thekawakawa, indicating that the tuna juveniles are not moreefficient swimmers.

Key words: locomotion, swimming, kinematics, Scombridae, chubmackerel, Scomber japonicus, juvenile, kawakawa tuna, Euthynnusaffinis, thunniform, carangiform.

Summary

Introduction

SWIMMING KINEMATICS OF JUVENILE KAWAKAWA TUNA(EUTHYNNUS AFFINIS) AND CHUB MACKEREL ( SCOMBER JAPONICUS)

JEANINE M. DONLEY AND KATHRYN A. DICKSON*Department of Biological Science, California State University Fullerton, Fullerton, CA 92834, USA

*Author for correspondence (e-mail: kdickson@fullerton.edu)

Accepted 25 July; published on WWW 26 September 2000

3104

mackerel Scomber scombrus, with a propulsive wavelength of93 % of body length (%L), and thunniform swimmers displaypropulsive wavelengths of 100–200 %L (Lindsey, 1978).Lateral undulations confined to the posterior 30 % of the bodycharacterize carangiform locomotion, whereas thunniformswimmers have significant lateral movements confined to thepeduncle and tail region (less than 30 % of the body)(Kishinouye, 1923; Fierstine and Walters, 1968; Webb, 1975;Dewar and Graham, 1994). However, empirical data forscombrid fishes show that these criteria do not clearly andconsistently distinguish the carangiform and thunniformmodes.

The first descriptions of tuna swimming kinematics, whichserved as the basis by which thunniform locomotion wasdefined, were in the kawakawa (Euthynnus affinis) by Fierstineand Walters (1968) and Magnuson (1970). The propulsivewavelengths observed in kawakawa were between 100 %L and200 %L, but the percentage of the body that undergoes lateralundulatory movements was not quantified (Fierstine andWalters, 1968). Those two studies were limited by the use ofbody-outline tracings for frame-by-frame analyses and becausethe fish swam in large circular tanks, making it difficult tomeasure swimming speeds accurately and to control thedirection of travel. More recent studies of mackerel swimmingbetween two points in a large tank (Videler and Hess, 1984)or of tuna and mackerel swimming steadily in a flow tankwith an induced current (Dewar and Graham, 1994; Knower,1998; Shadwick et al., 1998, 1999) have used computerizeddigitizing systems to obtain accurate body outlines and toquantify swimming movements. The mean propulsivewavelength was 98 %L(range 78–106 %) in Atlantic mackerelS. scombrus(Videler and Hess, 1984), and computer-generatedmidline curvatures in both S. scombrusand the chub mackerelS. japonicusshow significant lateral undulations confined tothe posterior third of the body (Videler and Hess, 1984;Shadwick et al., 1998), consistent with the general descriptionof carangiform locomotion. In yellowfin tuna (Thunnusalbacares), Dewar and Graham (1994) reported propulsivewavelengths of 123–129 % of fork length (FL), within therange for thunniform locomotion. However, Knower (1998)reported propulsive wavelengths of only 103 % and 97 %FLin yellowfin and skipjack (Katsuwonus pelamis) tuna,respectively. Dewar and Graham (1994) also reportedsignificant yaw (lateral undulation of the anterior of the fish)and found no position along the body that did not oscillatelaterally. Thus, although all these studies have providedvaluable information about the kinematics of scombrid fishes,they have not led to a quantitative characterization or a clearseparation between the carangiform and thunniform swimmingmodes.

More recently, Knower et al. (1999) proposed differentcriteria, based on electromyographic (EMG) patterns along thelength of the body during steady swimming, to separate thebody–caudal fin swimming modes. In comparing patterns forrepresentative anguilliform, subcarangiform, carangiform andthunniform swimmers, including the Atlantic mackerel and

yellowfin and skipjack tunas, Knower et al. (1999) found lessoverlap in slow, oxidative (red) muscle fiber activation on thetwo sides of the body in the swimming modes characterized byless lateral movement, with the least overlap found in theyellowfin tuna. In the tunas, red muscle EMG bursts begin laterin the tailbeat cycle and EMG offsets coincide more closelywith the time of peak force production. Shadwick et al. (1999)also showed that shortening of the red muscle in the skipjacktuna correlates with body bending at more posterior regions ofthe body and not with local body bending, as it does in all otherfishes that have been studied, including the chub mackerel(Shadwick et al., 1998). This difference has been attributed tothe unique axial, anterior position of the red muscle in tunas,the elongated shape of tunas’ myotomes and differences in thetendons that transfer force from the red muscle to the axialskeleton and caudal fin (Fierstine and Walters, 1968; Westneatet al., 1993; Knower et al., 1999; Graham and Dickson, 2000).All these characteristics are expected to result in differences inswimming kinematics and increased swimming efficiency intunas. What is needed to test these predictions are simultaneousmeasurements of the kinematics and energetics of size-matched individuals of closely related species representing thecarangiform and thunniform swimming modes.

We examined the kinematics of similar-sized individuals oftwo members of the family Scombridae, one categorized as athunniform swimmer (kawakawa tuna, Euthynnus affinis) andone as a carangiform swimmer (chub mackerel, Scomberjaponicus). We hypothesized that the locomotor characteristicsof E. affinisdiffer from those of S. japonicus, with E. affinisexhibiting less lateral displacement along the body. Themethods of Jayne and Lauder (1995) were used to quantifybody midline bending during steady swimming and to correlatebody bending with vertebral morphology, which has not beenperformed previously with scombrids. Furthermore, bycombining the kinematic data with metabolic cost of transportvalues measured in the same individuals used in the presentstudy (Sepulveda and Dickson, 2000), we have tested thehypothesis that tunas are more efficient swimmers than aremackerels.

Materials and methodsFish, Euthynnus affinis (Cantor, 1849) and Scomber

japonicus (Houttuyn, 1782), were collected and maintainedas described in Sepulveda and Dickson (2000). Followingrespirometry studies that measured maximal sustainedswimming speed and metabolic rate (V˙O2) at each speed up tothat maximum (Sepulveda and Dickson, 2000), each fish wasallowed to swim at a low speed for at least 15 min before videoanalysis was performed to quantify swimming kinematics.These experiments were conducted in a Brett-typetemperature-controlled swimming tunnel containing a totalvolume of 35 l. Individual fish were held within a chamber 13.5cm×13.5 cm×50.8 cm and were forced to swim against watercurrents of known velocities. Because V̇O2, maximal sustainedspeed and kinematic variables were all measured on the same

J. M. DONLEY AND K. A. DICKSON

3105Swimming kinematics of juvenile scombrids

individuals, the swimming tunnel had to have a volume smallenough to allow a significant reduction in oxygenconcentration within a 10 to 15 min period at each swimmingspeed. Corrections for solid-blocking effects were notnecessary because the cross-sectional area of each individualwas less than 10 % of the cross-sectional area of the chamber(Brett, 1964; Webb, 1971). However, wall effects may haveaffected the kinematics relative to fish swimming in nature.Because this effect should be similar for both species, theinterspecific comparisons that are the focus of the present studyshould not be compromised. Furthermore, most recent studiesof scombrid locomotor kinematics have used swimmingtunnels with similar dimensions relative to the size range offish studied. For example, the respirometer used byShadwick et al. (1998) to study S. japonicus22–29 cm intotal length (TL) and 110–185 g had a working section of14.5 cm×14.5 cm×47 cm.

Video analysis

Fish held at 24 °C were videotaped at 120 Hz using a PeakPerformance Technologies high-speed video camera (modelTM640). The camera was positioned in front of a mirrormounted at 45 ° above the lid of the working section of therespirometer to obtain a dorsal view of the fish. Videorecordings were made onto Maxell Professional SVHS tapesover a 2 to 10 min period at each speed at which the fish swamduring its V̇O2 measurements. The speeds at which the fish werevideotaped ranged from the lowest speed of 37–40 cm s−1 toeach individual’s maximum sustainable speed, in incrementsof 7.5 cm s−1 or 10 cm s−1. A total of ten kawakawa(15.1–25.5 cmFL, 43–265 g) and eight chub mackerel(14.0–23.4 cmFL, 26–147 g) were analyzed; all individualswere juveniles.

All speeds on each video tape were analyzed using a PeakPerformance Technologies two-dimensional motion-analysissystem. Video segments in which the fish was swimmingsteadily through 8–10 complete tail beats and was positionedin the center of the chamber, away from the walls and bottomof the chamber, were selected for analysis. Six points along thedorsal midline of each fish were digitized in sequential videofields through 8–10 complete tail beats at each speed. The sixdigitized points were chosen by pinpointing landmarks on thedorsal surface of the fish that are easily observed in bothspecies in sequential video fields: the tip of the snout, the pointalong the dorsal midline between both the anterior and theposterior insertion points of the eyes, the midpoint between theanterior insertions of the pectoral fins, the caudal peduncle andthe tip of the upper lobe of the caudal fin (Fig. 1). A 5 cmsquare grid on the bottom of the flow chamber was used tocalculate a scaling factor in each video tape. The kinematicvariables were calculated for each speed by analyzing theprogression of these digitized points through time.

Kinematic variables

All kinematic variables were calculated at each speed for eachindividual of both species. Tailbeat frequency was calculated

from the two-dimensional display of the progression of the tipof the tail over time by dividing the number of consecutivetailbeat cycles by the time, in seconds, taken for the completionof those beats. One tailbeat cycle is defined as the excursion ofthe tail from one side of the body to the other and back again.Using the same two-dimensional display, tailbeat amplitude, thedistance between the lateral-most positions of the tip of the tailduring one complete tailbeat cycle, was calculated by measuringthe height of each symmetrical tail beat in pixels. These valueswere then converted to centimeters by dividing by the scalingfactor (pixelscm−1) calculated prior to digitizing. Because of adegree of body curvature throughout the tailbeat cycle, it wasnot possible to use the video tapes to obtain accurate estimatesof each fish’s length in pixels. Because the fish were swimmingin the center of the chamber, the calculated tailbeat amplitudesoverestimated the actual tailbeat amplitudes by 0.5–2.0%. The

1 2 3 4 5 6

Fig. 1. A kawakawa (25.5 cmFL, the largest individual studied)swimming in the respirometer, viewed simultaneously from the sideand in dorsal view from the 45 ° mirror placed on top of therespirometer. In sequential video fields at each swimming speed, sixidentifiable points along the fish’s dorsal midline were digitized: 1,the tip of the snout; 2, the anterior insertion point of the eye; 3, theposterior insertion point of the eye; 4, the anterior insertion point ofthe dorsal fin; 5, the base of the caudal peduncle; 6, the tip of theupper lobe of the caudal fin. FL, fork length.

3106

mean tailbeat frequency and tailbeat amplitude at each speedwere used in statistical analyses. Stride length (l), measured incmtailbeat−1, is the distance a fish travels forward with each tailbeat. To calculate l, speed was divided by mean tailbeatfrequency.

Propulsive wave velocity (C), the speed of the wave ofundulation that travels down the length of the body from snoutto the tail during swimming, was calculated by first overlayingthe two-dimensional displays showing the lateral displacementthrough time of the digitized points at the tip of the snout andthe tip of the tail and then measuring the time (in seconds)between the peaks in lateral displacement at the two points(Dewar and Graham, 1994). This represents the time requiredfor the wave of undulation to pass from anterior to posteriorbetween the two points on the fish [a distance equal to fish totallength (TL)]. Measurements were repeated 7–10 times for eachindividual at each speed to calculate a mean progression time.The TL (cm) of each individual (the distance between the twopoints) was divided by the mean progression time to obtain thepropulsive wave velocity (C; in cm s−1) at each speed for eachindividual. Propulsive wavelength (λ) was calculated bydividing C by mean tailbeat frequency.

Body bending analysis

The body bending analysis entailed comparing theintervertebral lateral displacement and bending angle at eachintervertebral joint along the entire length of the axial skeletonsof kawakawa tuna and chub mackerel (see Jayne and Lauder,1995). Three individuals of each species were used, three size-matched pairs that were videotaped at similar speeds: 15.1 and14.0, 21.2 and 21.0, and 23.4 and 24.0 cmFL for kawakawaand chub mackerel, respectively. Each individual wasredigitized swimming at one low and one high speed. Thirty-two approximately equally spaced points along the dorsaloutline were digitized in sequential video fields through onecomplete tail beat, for each individual at each of the twospeeds, using the Peak Performance Technologies analysissystem.

To calculate the relative positions of the vertebral joints, thelateral view of each individual was X-ray photographed at theUniversity of California, Irvine (UCI). The lengths of the skulland each vertebra were determined from the X-rays using aMeasurement TV program in Dr George Lauder’s laboratoryat UCI to digitize points at the tip of the snout, the posterioredge of the neurocranium and all intervertebral joints up to andincluding the posterior tip of the hypural plate. An additionalsegment was added to the digitized midline corresponding tothe length between the posterior edge of the hypural plate andthe tip of the tail. Because of the difference in the number ofvertebrae between the two species (39 in kawakawa comparedwith 31 in chub mackerel), the positions of each joint along thebody were converted to a percentage of total length (%TL),which is the length from the tip of the snout to the posteriortip of the tail.

The dorsal outline point-coordinate data were converted tocomplete curves using a cubic spline function as described by

Jayne and Lauder (1995). A computer algorithm was then usedto calculate a dorsal midline for each video field from thedorsal outlines. Each calculated midline was then divided intosegments that represent the various skeletal elements, using therelative lengths of each vertebral element. This was carried outfor all fields comprising a full tailbeat cycle for each of thesix fish swimming at both speeds. Intervertebral lateraldisplacement and intervertebral bending angle were thencalculated using an Excel macro written by Jayne and Lauder(1995).

Maximum intervertebral lateral displacement (D) wasdetermined for each of the joints along the axial skeleton. Forstatistical analysis, lateral displacement was converted to unitsof relative length (%TL), and the mean maximum lateraldisplacements at specific positions along the body (as %TL) foreach species were compared. Lateral displacements arecalculated from the midline; thus, the maximum lateraldisplacement at the tip of the tail is equivalent to half thetailbeat amplitude as defined above, and twice the maximumlateral displacement at the tip of the snout is equivalent to yaw.

The angle of bending between vertebral elements (β) wasdetermined for each joint along the axial skeleton, beginningwith the joint between the posterior edge of the neurocraniumand the first vertebra and ending at the joint between the lastcaudal vertebra and the anterior edge of the hypural plate. Theangle calculated is that angle subtended to the position of theadjacent anterior skeletal segment at the same point intime. For statistical analysis, the maximum angle at eachintervertebral joint was determined, and mean maximumangles at specific positions along the body (as %TL) for eachspecies were compared.

Statistical analyses

Because speed and size covary and both may have an effecton each kinematic variable, it was necessary to use amultivariate analysis to quantify the effects of speed and sizeand to assess their relative influences on each kinematicvariable. We addressed the question of whether there was asignificant difference between chub mackerel and kawakawain the relationship between speed and each kinematic variablewhen size has been accounted for. In most published kinematicstudies, it has been common practice to account for differencesin size between individuals by dividing the kinematic variableby a unit of length or testing the significance of a regressionof a kinematic variable versusspeed expressed inbody lengths s−1 rather than cm s−1. Those methods of adjustingfor fish size assume that size has a linear effect on thekinematic variable and on speed. However, the effect of sizemay not be linear; in this case, this assumption is incorrectbecause it introduces a different size effect to the data (Hunterand Zweifel, 1971; Packard and Boardman, 1999). Therefore,we have used the more accurate and appropriate method ofaccounting for both size and speed effects by using a multipleregression analysis.

Statistical analyses were performed with Minitab (version10.5) and SAS (version 6.12). Using Minitab, it was determined

J. M. DONLEY AND K. A. DICKSON

3107Swimming kinematics of juvenile scombrids

that the kinematic data were normally distributed and did nottherefore require transformation prior to analysis. A statisticalmodel was then created for each kinematic variable in SAS usinga repeated-measures multiple regression analysis. Each multipleregression equation represents a plane in three-dimensionalspace, and takes the form y=γ0+γ1x1+γ2x2+γ3x1x2, where yis thekinematic variable, x1, x2 and x1x2 are explanatory variables forspeed, fork length and a speed×fork length interaction, and theγ values are numerical coefficients that represent the magnitudeof the effect of each variable. The statistical program tests if eachγ value is significantly different from zero (P=0.05). If not, thenthe corresponding variable makes no significant contribution tothe relationship, and the variable is dropped from the model anda new regression is calculated. The final models used to describethe actual fish kinematics were derived through this backwardsstep-wise reduction process in which insignificant terms weredropped from the model one by one until only significant termsremained.

To test for significant interspecific differences, each multipleregression equation for chub mackerel was used as a baselinewith which the corresponding regression for kawakawa wascompared. If there are significant interspecific differences inthe slopes in either or both the x1 and x2 dimensions, then thesedifferences are best described by two separate planes withdifferent orientations in three-dimensional space. If there is nodifference in the slope in either the x1 or x2 dimension but they-intercepts (γ0 values) are significantly different, then thespecies differences are best represented by two parallel planes,one above the other in three-dimensional space. Eachkinematic variable was tested for the effects of species, speedand fish size in terms of both mass and length. Interaction terms

were created in Minitab and included interactions of specieswith speed, mass and fork length and of speed with mass andfork length.

The body bending data were subjected to analysis ofvariance (ANOVA) using SuperANOVA (version 1.11). Athree-way ANOVA was performed on the maximumintervertebral lateral displacement and maximumintervertebral bending angle data for each species to determinewhether there were any significant effects of position, species,speed or position×species interactions. In all statisticalanalyses, a significance level of P=0.05 was used.

ResultsKinematics

Several swimming kinematic variables were comparedbetween E. affinis and S. japonicusto characterize theirrespective swimming modes. The multiple regression equationsfor each kinematic variable described by the final statisticalmodels are shown in Table 1. Whenever both size and speedeffects were significant, the maximum and minimum values forboth size and speed were used to solve the equation for the fourcorners of a plane, which was then plotted, along with the datafor all individuals, in three-dimensional space in which the x1,x2 and y axes are speed, fork length and the kinematic variable,respectively. When a kinematic variable varied with only speedor size, two-dimensional plots were used.

Tailbeat frequencySpeed effects

When the effects of fish size were accounted for, tailbeat

Table 1.The equations for the three-dimensional planes representing the final models of the repeated-measures multipleregression analysis for each kinematic variable (see text for details)

Kinematic variable,y Species Multiple regression equation

Tailbeat frequency (Hz) Scomber japonicus y=(4.18±0.84)+(0.050±0.002)U+(−0.118±0.041)FLEuthynnus affinis y=(7.66±1.89)+(0.050±0.002)U+(−0.251±0.094)FL

Tailbeat amplitude (cm) S. japonicus y=(−0.060±0.528)*+(0.010±0.002)U+(0.137±0.026)FLE. affinis y=(−0.060±0.528)*+(−0.002±0.004)*U+(0.137±0.026)FL

Tailbeat amplitude (%FL) S. japonicus y=(13.46±0.48)+(0.052±0.008)UE. affinis y=(13.46±0.48)+(−0.008±0.001)U

Stride length, l (cm) S. japonicus y=(−1.82±1.36)+(0.086±0.006)U+(0.462±0.066)FLE. affinis y=(−3.69±1.75)+(0.086±0.006)U+(0.462±0.066)FL

Stride length, l (%FL) S. japonicus y=(73.92±10.12)+(0.413±0.028)U+(−1.782±0.500)FLE. affinis y=(19.99±2.62)+(0.413±0.028)U+(0.395±0.136)FL

Propulsive wavelength, λ (cm) S. japonicus y=(−7.93±4.31)*+(1.745±0.269)FL+(−0.0438±0.0131)ME. affinis y=(−9.90±5.03)+(1.745±0.269)FL+(−0.0438±0.0131)M

Propulsive wavelength, λ (%TL) S. japonicus y=(24.70±22.95)*+(6.524±1.684)FL+(−0.532±0.129)ME. affinis y=(24.70±22.95)*+(4.711±1.318)FL+(−0.213±0.045)M

In each equation, means ±S.E.M. are given for each coefficient, speed (U) is in cm s−1, fork length (FL) is in cm, mass (M) is in g. An asterisk indicates a coefficient that is not significantly different from zero (P>0.05).TL, total length.

3108

frequency increased significantly with speed in both species(P=0.0001) (Fig. 2). There was no significant differencebetween the slopes of the regressions of tailbeat frequencyversusspeed for kawakawa and chub mackerel (Table 1).

Size effects

When the effects of speed were accounted for, there was asignificant effect of fork length on tailbeat frequency(P=0.0055); at the same speed, smaller individuals had highertailbeat frequencies than did larger individuals. The pattern ofdecrease in tailbeat frequency with length was significantlydifferent between the two species (P=0.0135). With a givenincrease in FL, tailbeat frequency decreased more in kawakawathan it did in chub mackerel. When the effects of speed and FLwere accounted for, mass had no significant effect on tailbeatfrequency.

Species effects

Because both speed and size had a significant effect ontailbeat frequency, the data sets of the two species wererepresented as planes in three-dimensional space (Fig. 2). They-intercepts for the two species differed significantly(P=0.0014), with the plane for E. affinisbeing above that forS. japonicus, indicating that tailbeat frequency was greater inkawakawa than in chub mackerel when speed and size effects

are accounted for. Although both speed and size had an effecton tailbeat frequency in both species, the size effects were notas great in E. affinis, whereas speed effects were the same inboth species (Fig. 2). Mean tailbeat frequency in the kawakawaand the chub mackerel were, respectively, 4.57 and3.82 tailbeat cycles s−1 (Hz) at the lowest swimming speeds(approximately 40 cm s−1) and 7.03 and 6.57 Hz at the highestswimming speeds (approximately 80–100 cm s−1).

Tailbeat amplitudeSpeed effects

Tailbeat amplitude, measured both in centimeters and as apercentage of fish fork length (%FL), increased significantlywith speed in the chub mackerel (P=0.0001), but not in thekawakawa (Table 1).

Size effects

When the effects of speed were accounted for, tailbeatamplitude (in cm) increased with FLin both species (Fig. 3).There was no significant effect of mass on tailbeat amplitudewhen FL effects were accounted for. To attempt to remove sizeeffects, as other investigators have done, tailbeat amplitudewas converted into relative units (%FL). There was no

J. M. DONLEY AND K. A. DICKSON

2

3

4

5

6

7

8

9

1416

1820

2224

26

4060

80100

120

Tai

lbea

t fre

quen

cy (

Hz)

Fork length (c

m)

Speed (cm s-1)

Fig. 2. The dependence of tailbeat frequency on both swimmingspeed and fish fork length in kawakawa (red plane and red symbols)and chub mackerel (blue plane and blue symbols). Each symbolindicates the tailbeat frequency versusspeed data for an individual.The maximum and minimum values of speed and fork length wereused to solve the multiple regression equations (Table 1) for the fourcorners of each plane. At a given size, the kawakawa uses asignificantly greater tailbeat frequency than does the chub mackerelto swim at a given speed. The increase with speed is similar in thetwo species, but tailbeat frequency decreases more with fork lengthin the kawakawa than it does in the chub mackerel.

1

2

3

4

5

1416

1820

222426

40 60 80 100 120

Tai

lbea

t am

plitu

de (

cm)

Fork length (c

m)

Speed (cm s-1)

Fig. 3. The dependence of tailbeat amplitude on both swimmingspeed and fish fork length in kawakawa (red plane and red symbols)and chub mackerel (blue plane and blue symbols). Each symbolindicates the tailbeat amplitude versusspeed data for an individual.The maximum and minimum values of speed and fork length wereused to solve the multiple regression equations (Table 1) for the fourcorners of each plane. The y-intercepts of the two planes are similar,and the effects of fork length on tailbeat amplitude are similar inboth species. However, tailbeat amplitude does not vary significantlywith speed in the kawakawa, but increases with speed in the chubmackerel; thus, the two species have similar tailbeat amplitudes atlow speeds, but tailbeat amplitude is greater in the chub mackerel atthe higher speeds.

3109Swimming kinematics of juvenile scombrids

significant effect of size on tailbeat amplitude when expressedas %FL(Table 1), indicating that using tailbeat amplitude inrelative units of fish length was an appropriate adjustment forsize differences.

Species effects

Differences in the data sets of the two species are bestrepresented in three-dimensional space (Fig. 3). The y-intercepts of the two planes are similar, and the effects of FLon tailbeat amplitude (cm) are similar in the two species,but the effect of speed on tailbeat amplitude differsinterspecifically (P=0.0001). As speed increased, therelationship between tailbeat amplitude and speed for the twospecies diverged, with E. affinishaving lower amplitudesthan S. japonicusat high speeds (Fig. 3). This is because4

6

8

10

12

14

16

18

20

1416

18 2022

2426

40 60 80 100120

Stri

de le

ngth

(cm

)

Fork length (cm)

Speed (cm s-1)

Fig. 4. The dependence of stride length on both swimming speed andfish fork length in kawakawa (red plane and red symbols) and chubmackerel (blue plane and blue symbols). Each symbol indicates thestride length versusspeed data for an individual. The maximum andminimum values of speed and fork length were used to solve themultiple regression equations (Table 1) for the four corners of eachplane. At a given size and speed, the chub mackerel has asignificantly greater stride length than does the kawakawa. Theincrease in stride length with both fork length and speed is similar inthe two species.

10

15

20

25

30

35

Mea

n pr

opul

sive

wav

elen

gth

(cm

)

10 15 20 25 30

Fork length (cm)

Fig. 5. Mean propulsive wavelength versus fork length inkawakawa (red circles; N=9) and chub mackerel (blue squares;N=8). Because there was no significant effect of speed onpropulsive wavelength, the mean of the propulsive wavelengths atall swimming speeds was calculated for each individual. Error barsrepresent ± 1 S.D. Mean propulsive wavelength is significantlygreater in the chub mackerel than in the kawakawa when the effectsof size are accounted for.

0

2.5

5.0

7.5

10.0

12.5

0 25 30 35 40 45 50 55 60 65 70 75 80 85 90 100

0

1.5

3.0

4.5

6.0

0 25 30 35 40 45 50 55 60 65 70 75 80 85 90 100

Relative position along the body (%TL)

A

B

Mea

n m

axim

um in

terv

erte

bral

angl

e (d

egre

es)

Mea

n m

axim

um in

terv

erte

bral

late

ral d

ispl

acem

ent (

%T

L)

Fig. 6. Mean maximum intervertebral lateral displacement (A) andmean maximum intervertebral bending angle (B) versus positionalong the body (%TL) in kawakawa (red) and chub mackerel (blue).In both species, there was no significant effect of swimming speedon either variable, but there were significant effects of body positionand species. Minimum lateral displacement occurred atapproximately 35–40 %TLand minimum bending occurred atapproximately 40 %TLin both species. Both maximum intervertebrallateral displacement and maximum intervertebral bending angle weresignificantly greater in the chub mackerel than in the kawakawa.Values are means ±S.D. (N=3). TL, total length.

3110

tailbeat amplitude did not vary significantly with speed in thekawakawa, but increased with speed in the chub mackerel(Table 1). Maximum tailbeat amplitude ranged from 12 to14.5 %FL in kawakawa and from 14 to 20.5 %FLin chubmackerel.

Stride lengthSpeed effects

When size effects were accounted for, stride length lincreased significantly with speed (P=0.0001). There was nosignificant difference in the slopes of the regressions of l versusspeed for the two species (Table 1).

Size effects

When speed effects were accounted for, both speciesshowed a significant increase in l(in cm) with fish fork length(P=0.0001). There was no significant difference in the slopesof the regressions of l versus FLfor the two species. There wasno significant effect of mass on l when FL effects wereaccounted for (Table 1). Because other studies have usedrelative stride lengths, we also analyzed stride length convertedto %FL. However, a significant effect of FLwas evident (Table1), indicating that the effects of FL were not removed by usingrelative l values.

Species effects

The l data are represented as two parallel planes in three-dimensional space, with the plane for S. japonicusbeing higherthan that for E. affinis(Fig. 4). The y-intercepts of the planesdiffer, but the slopes in both the x1 and x2 dimensions are equalfor the two species. Thus, stride lengths increase similarly withspeed and with FLin E. affinisand S. japonicusbut, at a givenspeed and size, the length of each stride is significantly lowerin E. affinis(P=0.0001).

Propulsive wavelengthSpeed effects

When size effects were accounted for, there was no significantrelationship between propulsive wavelength λ (cm) and speed.

Size effects

When speed effects were accounted for, both mass and forklength had a significant effect on λ (Table 1). As FLincreased,there was a significant increase in λ(P=0.0001). When theeffects of FLwere taken into account, there was a significantdecrease in λwith mass (P=0.0013). Thus, if a three-dimensional plane were to be drawn, unlike those for the othervariables, the two xvalues would be mass and FL, with nospeed axis (Table 1).

Propulsive wavelength as a percentage of body length is oneof the criteria used to determine swimming mode. Thus, thestatistical analyses included an assessment of λexpressed as apercentage of fish total length (%TL). However, this sizeadjustment in λdid not completely account for differences insize, as indicated by the presence of significant size effects inthe final models for both λ (cm) and λ(%TL) (Table 1).

Species effects

There was a significant effect of size, but not speed, onpropulsive wavelength, so differences between species wererepresented by plotting mean λversus FL(Fig. 5). When theeffects of fish size are accounted for, the propulsivewavelengths (cm) of E. affiniswere significantly lower thanthey were for S. japonicus(P=0.0081). Mean relativepropulsive wavelengths ranged from 89 to 96 %TL inkawakawa and from 98 % to 120 %TLin chub mackerel. Thesepropulsive wavelengths were then translated into the numberof propulsive waves on the body: 1.04–1.12 in the kawakawaand 0.84–1.02 in the chub mackerel.

Body bending

Body bending analysis was performed on three size-matchedindividuals of each species swimming at one low and one highspeed. Intervertebral lateral displacement and intervertebralbending angle at each joint along the axial skeleton weredetermined. Each of these variables was assessed separately forthe effects of species, position along the body, speed andspecies×position and species×speed interactions using a three-way ANOVA in SuperANOVA (version 1.11). Position alongthe body was represented in relative units, or percentage oftotal length (%TL).

Intervertebral lateral displacement

Speed effects. There was no significant effect of swimmingspeed on maximum lateral displacements in either species.

Position effects. Intervertebral lateral displacementD variedsignificantly with axial position (P=0.0001), but the pattern ofmaximum lateral displacement with position along the bodywas similar in both species (Fig. 6A). Minimum lateralamplitudes occurred at 35–40 %TL in both species, andmaximum D occurred at the tip of the caudal fin (100 %TL).

Species effects. Mean maximum lateral displacements weresignificantly greater in the chub mackerel than in thekawakawa (P=0.0001) (Fig. 6A).

To determine whether there are interspecific differences inyaw, twice the mean maximum lateral displacement at the tipof the snout (0 %TL) for the two species was compared usinga two-tailed t-test. There was no significant effect of speed onthe yaw values within each species (P>0.30), so values forboth low and high speeds were grouped together in theanalysis. Mean yaw was 3.5±1.2 %TL in the kawakawa and3.8±1.5 %TL(means ±S.D.) in the chub mackerel; these valuesdo not differ significantly (P=0.684).

Mean maximum lateral displacement at the tip of the tail was6.7±1.5 %TLin the kawakawa and 8.9±1.6 %TL (means ±S.D.)in the chub mackerel. These values are similar to half thetailbeat amplitude values for the same individuals.

Intervertebral bending angle

Speed effects. There was no significant effect of speed onmean maximum intervertebral bending angles in either species.

Position effects. Intervertebral bending angleβ variedsignificantly with position along the body (P=0.0001). The

J. M. DONLEY AND K. A. DICKSON

3111Swimming kinematics of juvenile scombrids

positions of minimum and maximum bending angle weresimilar for the two species, occurring at approximately 40 %TLand 85 %TL, respectively (Fig. 6B). However, β increasedsignificantly more near the posterior end of the body in chubmackerel than it did in kawakawa (Fig. 6B), as indicated by asignificant species×position interaction term (P=0.0448).

Species effects. Mean maximum intervertebral angles rangedfrom 0.67 to 3.6 ° in chub mackerel and from 0.53 to 1.48 ° inkawakawa; there was a significant species effect, with greaterangles in the chub mackerel (P=0.0001).

DiscussionThe specific goal of this study was to create a more complete

quantitative description of the swimming kinematics of twoscombrid fishes to test the hypothesis that the kawakawa tunauses a different locomotor mode from the chub mackerel, inwhich the body is held more rigid with less lateral undulation,and thus swims more efficiently. Taken together, the kinematicdata show that the kawakawa does display less lateralmovement of the body than does the chub mackerel whileswimming at the same speeds. The most direct measures ofbody flexure, maximum intervertebral lateral displacement andbending angle, were significantly lower in the kawakawa thanin the chub mackerel (Fig. 6). To maintain the same swimmingspeed, kawakawa beat their tails at a higher frequency than dochub mackerel but use lower tailbeat amplitudes and move asmaller distance per tail beat. However, despite less lateralmovement in the kawakawa, the maximal sustainable speedsand net cost of transport did not differ significantly betweenthe two species (Sepulveda and Dickson, 2000). Thus, we havenot provided evidence that thunniform locomotion is moreefficient than the carangiform swimming mode.

Kinematics and comparisons with previous studies

At sustainable speeds, most fishes that utilize body–caudalfin propulsion increase their swimming speed primarily byincreasing tailbeat frequency. Previous research hasdocumented linear increases in tailbeat frequency with speedin a number of teleost species, including scombrids (Magnusonand Prescott, 1966; Yuen, 1966; Pyatetskiy, 1970; Hunter andZweifel, 1971; Webb, 1971; Magnuson, 1978; Videler andHess, 1984; Fierstine and Walters, 1968; Dewar and Graham,1994; Jayne and Lauder, 1995), as was found for both E. affinisand S. japonicus in the present study (Fig. 2). Tailbeatfrequency also varied with fish length in the juvenilescombrids, with larger individuals having a lower tailbeatfrequency than smaller individuals swimming at the samespeed (Fig. 2), as has been shown in other teleosts (Bainbridge,1958; Magnuson, 1963; Magnuson and Prescott, 1966; Yuen,1966; Pyatetskiy, 1970; Hunter and Zweifel, 1971; Videler andHess, 1984; Fierstine and Walters, 1968; Webb, 1975; Webbet al., 1984; Dewar and Graham, 1994).

The effect of speed on tailbeat amplitude differed betweenthe two species; tailbeat amplitude increased significantly withspeed in chub mackerel, but did not vary with speed in

kawakawa (Fig. 3; Table 1). The maximum amplitudesrecorded in the present study (14.5 %FL in kawakawa and20.5 %FL in chub mackerel) are consistent with the range ofamplitudes recorded for yellowfin Thunnus albacares(Dewarand Graham, 1994) and bluefin Thunnus thynnus(Wardle etal., 1989) tunas, dace Leuciscus leuciscus, trout Salmo irideusand goldfish Carassius auratus(Bainbridge, 1958) and troutOncorhynchus mykiss (Webb et al., 1984). However, the meantailbeat amplitude values for similar-sized chub mackerel(approximately 23–26 cmTL) in the present study areconsistently lower than those measured at similar speeds in athree-dimensional kinematic study by Gibb et al. (1999),possibly because of differences in the methods used in the twostudies.

Relationships between tailbeat amplitude and speed fromprevious studies are less consistent than are trends in tailbeatfrequency. Previous results in the three species studied byBainbridge (1958), the jack mackerel Trachurus symmetricus(Hunter and Zweifel, 1971), and bluefish Pomatomus saltatrixand gray mullet Mugil cephalus (Pyatetskiy, 1970) indicatedthat tailbeat amplitude remains constant with changes in speedabove a minimum steady swimming speed. In the chubmackerel in the study of Gibb et al. (1999), tailbeat amplitudeincreased significantly with speed. In previous studies of tunas,amplitudes did vary with speed in kawakawa (Fierstine andWalters, 1968), but did not change with speed in yellowfin(Dewar and Graham, 1994). Thus, the tailbeat amplitudeversusspeed relationships in the present study are generallyconsistent with previous studies, even though there was a greatdeal of variability in these data (Fig. 3).

At a given speed and size, relative stride length l wassignificantly lower in kawakawa than in chub mackerel(Fig. 4). Relative stride lengths observed at the highestswimming speeds ranged from 50 to 85 %TL in kawakawa andfrom 60 to 85 %TLin chub mackerel, both of which encompassthe range predicted by Videler (1993) for maximum l. Stridelengths greater than 80 %TLhave also been reported for bluefintuna (Wardle et al., 1989). However, because we found asignificant effect of FLon l, comparisons among species basedon relative l(as a percentage of fish length) may be misleading.

The significant increase in lwith speed found in bothkawakawa tuna and chub mackerel in the present study isconsistent with stride length relationships observed in otherteleost fishes, including scombrids (Fierstine and Walters,1968; Hunter and Zweifel, 1971; Webb et al., 1984; Dewar andGraham, 1994). As swimming speed increases, the kawakawaand chub mackerel may recruit more red muscle fibers topower the tail beat, and this may result in an increase in thedistance swum per tail beat. Alternatively, adjustments inswimming kinematics and in the angle of attack of the tail,which was not quantified in the present study, may alter l. Bychanging gait as speed increases, fish may also be able to varyl (Webb, 1998).

Videler (1993) suggested that fish may utilize their extendedpectoral fins as a braking system while swimming at lowspeeds and, thereby, reduce their stride lengths at these speeds;

3112

at higher swimming speeds, fish adduct their pectoral fins,resulting in an increase in stride length. Scombrids have alsobeen observed to orient the body at an angle to the flow togenerate lift at low speeds (He and Wardle, 1986), a behaviorthat may reduce l. However, the fish in the present study swamcontinuously with their pectoral fins adducted and appeared toorient the body parallel to the flow in all video sequencesanalyzed at all speeds studied. Thus, the increased stride lengthcannot be attributed to variations in the use of the pectoral fins,body ‘tilting’ or different gaits.

In previous studies, propulsive wavelength (λ) has been usedto classify swimming mode (see Introduction). On the basis ofcharacterizations of thunniform and carangiform swimming,the kawakawa was predicted to have higher λ values than thechub mackerel. However, the opposite was found to be true(Fig. 5). This may be due to the greater number of vertebraein the kawakawa, because λduring steady swimming has beenhypothesized to be inversely proportional to vertebral number(see Videler, 1985; Jayne and Lauder, 1995; Long and Nipper,1996). When size effects were taken into account, there wasno significant relationship between λ and speed in eitherkawakawa or chub mackerel. This result confirms thepropulsive wavelength trends seen in some studies (Webb etal., 1984), but is not consistent with others (Jayne and Lauder,1995). However, there were significant effects on λ of massand fork length, measured both in absolute terms (in cm) andas a percentage of total length, in both species in the presentstudy. Thus, differences in size were not correctly accountedfor by dividing by fish length. This implies that many previouscomparisons of propulsive wavelengths among species and infish of different sizes are confounded by mass and lengtheffects and cannot accurately be made by expressing λ as apercentage of fish length. Furthermore, other studies haveshown λ to vary with axial position (Blight, 1977) and withina fish species (Long and Nipper, 1996). Thus, it is unclearwhether propulsive wavelength can or should be used as acriterion for distinguishing swimming modes in fishes (see alsoLong and Nipper, 1996). Instead, the body bendingcharacteristics were focused on, because they are more directmeasures of body flexure.

Body bending

Many previous kinematic studies of fish bending patternshave quantified body midline curvature but have not analyzedbending along the axial skeleton at each intervertebral joint.The latter is more meaningful because it relates body bendingto the morphological characteristics of the fish that allowbending. Prior to the present study, such studies had beencompleted on anguilliform and subcarangiform swimmers(Jayne and Lauder, 1995; Gillis, 1998; Lauder, 2000), but noton carangiform or thunniform swimmers. We have shown thatthis type of analysis can distinguish the swimming patterns ofthe kawakawa and chub mackerel (Fig. 6). Both maximumintervertebral lateral displacement and maximumintervertebral bending angle were significantly lower in thekawakawa than in the chub mackerel, supporting the

hypothesis that the kawakawa is a more stiff-bodied swimmerthan is the chub mackerel.

There was no significant relationship between speed andmaximum intervertebral lateral displacement or bending anglein either kawakawa or chub mackerel, but body bendingcharacteristics did vary with vertebral position. The position ofboth minimum lateral displacement and minimumintervertebral angle occurred at approximately 35–40 %TLinboth species. These data are consistent with previous studiesof other teleosts, in which the position of minimum lateraldisplacement occurred posterior to the neurocranium at thecenter of mass, with amplitudes increasing from that pointcaudally (Videler and Hess, 1984; Dewar and Graham, 1994;Jayne and Lauder, 1995; Shadwick et al., 1998). Maximumlateral displacement occurred at the tail tip (Fig. 6A), butmaximum intervertebral bending angle occurred just anteriorto the caudal fin (Fig. 6B). The relationship between bendingangle and body position differed between the two species. Inthe middle and posterior regions of the body, the angles werehigher in chub mackerel than in kawakawa. The greaterbending angles caused the greater lateral displacement andtailbeat amplitudes in the chub mackerel.

The intervertebral lateral displacement data allowed us toestimate yaw, or twice the maximum lateral displacement thatoccurs at the tip of the snout. On the basis of the predicteddifferences between thunniform and carangiform locomotion,thunniform swimmers should display less yaw because theanterior of the body should be held more rigid. However, asignificant amount of yaw (2.3–5 %FL) was found in akinematic study of yellowfin tuna (Dewar and Graham, 1994).That range encompasses the values of 3.0–3.6 % of body lengthin Atlantic mackerel Scomber scrombusreported by Videlerand Hess (1984). In the present study, yaw values for bothspecies fell within the range for yellowfin tuna, and yaw didnot differ significantly between the kawakawa and the chubmackerel (3.5±1.2 %TLand 3.8±1.5 %TL, respectively; means± S.D.). Thus, any contributions to drag made by the side-to-side movements of the snout should be similar in the twospecies.

Because neither intervertebral lateral displacement norintervertebral bending angle varied significantly with speed ineither kawakawa or chub mackerel, but did differ between thetwo species, the properties that determine the degree of axiallateral flexion must vary interspecifically and with positionalong the body in both species, but remain constant withchanges in swimming speed. This suggests that morphologicalproperties, such as the degree of articulation between adjacentvertebrae, the number, length and diameter of vertebrae,characteristics of the intervertebral joints, red muscleplacement and/or the placement and strength of tendonattachments to the axial skeleton, are important determinantsof intervertebral flexion. These characteristics will not changewith swimming speed but may vary along the length of thebody and are known to vary between tunas and mackerels(Collette, 1978; Graham et al., 1983; Westneat et al., 1993;Graham and Dickson, 2000).

J. M. DONLEY AND K. A. DICKSON

3113Swimming kinematics of juvenile scombrids

Videler (1985) suggested that the bony appendages betweenvertebrae (pre- and post-zygapophyses) did not restrict lateralflexion, but rather that the nature of the intervertebral joints(the tightness of collagenous connection and the cross-sectional diameter of vertebrae) determined lateral flexibilityin the Atlantic mackerel (Scomber scombrus). The diametersof the vertebrae in S. scombrusare very similar down thelength of the body up to the twenty-fourth vertebra and thendecrease caudally. This observation led Videler (1985) tosuggest that mackerel have limited flexibility throughout muchof their body, but increased flexibility near the peduncle, whichis reflected both in the midline curvatures reported for thisspecies and in the body bending data in the present study(Fig. 6). However, other studies have suggested that thezygapophyses are important determinants of lateral flexion (seebelow). Furthermore, the distribution of the myotomal musclemay also affect lateral displacement.

Differences in lateral bending properties with position alongthe body were also seen in Hebrank’s (1982) study of themechanical properties of isolated backbones of the skipjacktuna Katsuwonus pelamis, a species similar in body shape andvertebral number (40–41) to the kawakawa (Kishinouye, 1923;Godsil and Byers, 1944; Fierstine and Walters, 1968). Hebrank(1982) found three distinct regions of differing flexibility alongthe axial skeleton of skipjack tuna. All intervertebral jointsalong the body from the cranium to the intervertebral jointanterior to the thirty-fourth vertebra were similar in theirbending properties. There was significantly less flexibility inthe intervertebral joints between vertebrae 34, 35 and 36.Hebrank (1982) attributed this limited flexibility to thepresence of the bony processes on those vertebrae that formthe caudal keel (located at approximately 81–88 %TL in K.pelamis). The intervertebral joints posterior to the keel withinthe caudal fin complex had greater flexibility, suggesting thatthe majority of thrust-producing lateral movements wererestricted to the tail region in skipjack (Hebrank, 1982). Asimilar morphology has been described in the little tunnyEuthynnus alletteratus(Nursall, 1956) and in E. affinis, inwhich the keel is on vertebrae 33, 34 and 35 (Godsil, 1954; seeX-ray photograph in Fig. 7). Magnuson (1970) reported thatthe peduncular vertebrae of E. affinisare fused, the vertebraeanterior to the prepeduncular joint have long interlockingzygapophyses that would restrict lateral flexion and thatvertebrae 30, 31 and 32, which form the two joints immediatelyanterior to the caudal keel, have poorly developedzygapophyses which would allow more lateral bending at thesejoints.

The pattern of less flexibility at the caudal keel relative tointervertebral joints located more anteriorly and posteriorly isconsistent with the ‘double-jointed’ system described byFierstine and Walters (1968), which has been suggested to bea characteristic of the unique thunniform locomotor mode oftunas (Fierstine and Walters, 1968; Dewar and Graham, 1994).However, the intervertebral angle data for the kawakawa in thepresent study do not support this view. In contrast to whatwould be predicted from Hebrank (1982), the bending angles

at the vertebrae containing the caudal keel were not unusuallylow. The maximum bending angles for the intervertebral jointsbetween vertebrae 33 and 35 (anterior to vertebrae 34 and 35)were higher than for more anterior joints (Fig. 7). Themaximum bending angles were even higher for the jointsanterior to vertebrae 36 and 37, but declined for the moreposterior joints within the caudal fin complex (Fig. 7). Perhapsin steadily swimming tunas, flexion at the intervertebral jointsis not influenced so much by the presence of the keel or thedegree of articulation of the vertebrae along the axial skeletonas it appeared to be in the isolated vertebral columns studiedby Hebrank (1982). In the intact body of a tuna, other featuresthat may affect axial bending, such as the distribution of thelocomotor muscle and muscle–tendon connections to thevertebrae, may be more important than the presence of thebony keel in determining the degree of bending that occurs atdifferent positions along the body during sustained swimming(Videler, 1985; Westneat et al., 1993; McHenry et al., 1995;Shadwick et al., 1999; Graham and Dickson, 2000).

The unusual anterior, axial red muscle position in tunas andthe anterior displacement of the entire myotomal muscle mass

Fig. 7. Mean maximum intervertebral bending angles for theintervertebral joints anterior to vertebrae 28–39, the last vertebra, inthe kawakawa and an X-ray of the caudal region (lateral view) of a260 mm fork length kawakawa. The bony lateral keel is on vertebrae33, 34 and 35, indicated by the lines. Values are means ±S.D. (N=3).

3114

may act to reduce axial flexibility and may affect themechanical advantage, force generation and kinematics at thetail (Nursall, 1956; Westneat et al., 1993; Shadwick et al.,1999; Graham and Dickson, 2000). The anterior location of thered muscle and the relatively long posterior oblique tendonsconnecting to the backbone in tunas allow red musclecontraction at one position to cause bending at a positionlocated more posteriorly; this focuses red muscle contractileforce towards the tail and allows the anterior regions toundergo less lateral movement (Shadwick et al., 1999). Thismorphology also results in a lower mechanical advantage(input motion/output motion) and a higher velocity ratio (theinverse of mechanical advantage) in tunas compared withmackerels (Westneat et al., 1993), which is reflected in thelower tailbeat amplitudes and higher tailbeat frequencies in thekawakawa in the present study. Axial stiffness may also beaffected by the nature of red muscle activation patterns inswimming fish (Knower et al., 1999) or may be increased ifthe axial muscles perform negative work (Long and Nipper,1996). However, the latter is unlikely in tunas during steadysustained swimming, because recent studies of the skipjacktuna have shown that the red aerobic muscle fibers generateonly positive work, with the force of muscle contraction beingtransferred to the caudal fin viastiff posterior tendons (Knoweret al., 1999; Shadwick et al., 1999).

Using models based on the morphology of the tendons thatattach the red muscle to the axial skeleton, and assumingmuscle shortening of 10 %, Westneat et al. (1993) estimatedintervertebral bending angles of 3.6 ° for the little tunny(Euthynnus alletteratus) and of 3.3 ° for the king mackerel(Scomberomorus cavalla). The maximum intervertebral anglesfor both species in the present study did not exceed 2 ° exceptfor the value of 3.5 ° at 85 %TL in S. japonicus (Fig. 6B),which implies that red muscle shortening is less than 10 % atthe sustained speeds studied or that the models areoversimplified. Muscle shortening was not measured in thepresent study, but Shadwick et al. (1998, 1999) measured redmuscle strain of ±8 % of resting length in a 23 cmFL chubmackerel swimming at 1.75FL s−1 (40 cm s−1) and of ±5–8 %of resting length in 40–49 cmFL skipjack tuna swimming1.1–2.3FL s−1.

Implications for the evolution of thunniform locomotion andendothermy in tunas

The interspecific differences in body bending patternsdocumented in the present study show that the kawakawaswims with less lateral movement than does the chub mackereland support the hypothesis that the kawakawa and chubmackerel use different modes of locomotion. An increase inswimming efficiency has been postulated as the selectiveadvantage of the thunniform locomotor pattern unique to tunas(Lighthill, 1970, 1975; Lindsey, 1978; Magnuson, 1978;Blake, 1983; Webb, 1975, 1998; Graham and Dickson, 2000).Thus, the kawakawa would be predicted to be a more efficientswimmer than the chub mackerel. However, the maximumsustainable swimming speeds and net cost of transport are the

same for these two species, and the total cost of transport isgreater in the kawakawa, when the effects of fish size areaccounted for (Sepulveda and Dickson, 2000). Thus, improvedswimming performance seems not to be a consequence ofreduced lateral flexion during sustained swimming, at least inthe juvenile scombrids in the present study. It is possible thatincreases in efficiency may be manifested in the tunas whenthey reach larger sizes or during voluntary swimming in vivo.However, there may be trade-offs to the thunniform mode oflocomotion that have not previously been considered. Forexample, we found that the reduced lateral displacement in thekawakawa results in a lower tailbeat amplitude than in the chubmackerel at the same speed. The kawakawa thus requires agreater tailbeat frequency to swim a given speed, and thisshould increase locomotor costs because each beat of the tailrequires energy for muscle contraction. We also found that theamount of yaw, which is assumed to lead to the production ofdrag, did not differ significantly between the kawakawa andchub mackerel. There would, however, be some reduction indrag in the posterior regions of the body because of the reducedlateral displacement. The combination of this with the addedcost of higher tailbeat frequencies may result in a net cost oftransport that is similar in the kawakawa and the chubmackerel.

Rather than swimming efficiency acting as a selective forcein the evolution of thunniform locomotion, the locomotor styleof tunas may simply be a consequence of their ability toconserve metabolic heat to maintain elevated muscletemperatures (i.e. they are endothermic). The anterior and axialred myotomal muscle placement has been hypothesized to havecontributed to the evolution of endothermy in tunas because itresults in reduced conductive heat loss across the body surface(Carey, 1973; Block et al., 1993). The higher tailbeatfrequencies at a given speed observed for the kawakawa mayresult in higher heat production rates within the red muscle andthereby contribute to endothermy.

Future studies of similar-sized bonitos, members of the sistertaxon to tunas, and of the slender tuna Allothunnus fallai, themost basal member of the tuna clade (Graham and Dickson,2000), may resolve these questions and help to ascertainwhether thunniform locomotion evolved before or after theevolution of endothermy. The bonitos have many charactersrelated to swimming performance that are intermediatebetween those of mackerels and tunas, but they are notendothermic (Kishinouye, 1923; Godsil, 1954; Collette, 1978).Using the only known kinematic data on bonitos swimming atcontrolled speeds (Pyatetskiy, 1970), we made a preliminarycomparison between one (16.0 cmTL) Atlantic bonito (Sardasarda) and individuals of approximately the same size from thepresent study. Since chub mackerel and kawakawa weredistinguished on the basis of their tailbeat frequency versusspeed relationships, these data were extracted for the Atlanticbonito from Pyatetskiy (1970). Because temperature mayaffect the swimming kinematics of these fishes, chub mackerelkinematic data at 18 °C (J. M. Donley, unpublished results),the temperature at which the Pyatetskiy (1970) study was

J. M. DONLEY AND K. A. DICKSON

3115Swimming kinematics of juvenile scombrids

conducted, were also examined. The relationship betweentailbeat frequency and swimming speed has a similar slope butlower y-intercept in the bonito than in the chub mackerel at thesame temperature, which is opposite to the relationship foundbetween the kawakawa and chub mackerel. This suggests thatthe bonito may be more similar to the chub mackerel and thusmight utilize the carangiform swimming mode. However,because this comparison is based on very limited data, it doesnot shed much light on the question of when thunniformlocomotion first appeared within the family Scombridae. Amore comprehensive study of bonito swimming kinematics,including a quantitative body-bending analysis, is needed tocharacterize the swimming mode of the bonitos and to assesslocomotor adaptations among the scombrids.

We thank Chugey Sepulveda and Alice Gibb for assistancewith videotaping, Rich Brill, Rob Dollar and R. MichaelLaurs for support at the National Marine Fisheries ServiceKewalo Basin laboratory in Hawaii, Gary Hunt and DaveParsons for the design and construction of the respirometer,Jim Degen for constructing the mirror used in videotaping,Hexcel and Plascore, Inc., for donating supplies used in therespirometer, Karen Messer for help with statistical analysisand two anonymous reviewers for their comments on themanuscript. We are indebted to George Lauder for thecomputer programs used in the body-bending analyses, and heand Gary Gillis for assistance with those analyses. Specialthanks go to Dale Simmons for his expertise in catchingjuvenile tunas in Hawaii, without which this work would nothave been possible. We also thank Dave Itano, ChuckHolloway and Kim Holland for help in locating a source ofjuvenile tunas. Funding was provided by the CSUFDepartment of Biological Science and the National ScienceFoundation (no. IBN-9318065).

ReferencesAltringham, J. D. and Block, B. A. (1997). Why do tuna maintain

elevated slow muscle temperatures? Power output of muscleisolated from endothermic and ectothermic fish. J. Exp. Biol.200,2617–2627.

Bainbridge, R. (1958). The speed of swimming of fish as related tosize and to the frequency and amplitude of the tail beat. J. Exp.Biol. 35, 109–133.

Blake, R. W. (1983). Fish Locomotion. Cambridge: CambridgeUniversity Press.

Blight, A. R. (1977). The muscular control of vertebrate swimmingmovements. Biol. Rev. 52, 181–218.

Block, B. A., Finnerty, J. R., Stewart, A. F. R. and Kidd, J.(1993).Evolution of endothermy in fish: Mapping physiological traits on amolecular phylogeny. Science260, 210–214.

Breder, C. M., Jr (1926). The locomotion of fishes. Zoologica4,159–256.

Brett, J. R. (1964). The respiratory metabolism and swimmingperformance of young sockeye salmon. J. Fish. Res. Bd Can. 21,1183–1226.

Carey, F. G. (1973). Fishes with warm bodies. Scient. Am. 228,36–44.

Carpenter, K. E., Collette, B. B. and Russo, J. L.(1995). Unstableand stable classifications of scombroid fishes. Bull. Mar. Sci.56,379–405.

Collette, B. B.(1978). Adaptations and systematics of mackerels andtunas. In The Physiological Ecology of Tunas(ed. G. D. Sharp andA. E. Dizon), pp. 7–39. New York: Academic Press.

Dewar, H. and Graham, J. B. (1994). Studies of tropical tunaswimming performance in a large water tunnel. III. Kinematics.J.Exp. Biol. 192, 45–59.

Fierstine, H. L. and Walters, V. (1968). Studies in locomotion andanatomy of scombroid fishes. Mem. South. Calif. Acad. Sci. 6,2–30.

Gibb, A. C., Dickson, K. A. and Lauder, G. V. (1999). Tailkinematics of the chub mackerel, Scomber japonicus: testing thehomocercal tail model of fish propulsion. J. Exp. Biol. 202,2433–2447.

Gillis, G. B. (1998). Environmental effects on undulatory locomotionin the American eel (Anguilla rostrata): kinematics in water and onland. J. Exp. Biol.201, 949–961.

Godsil, H. C. (1954). A descriptive study of certain tuna-like fishes.Calif. Dept Fish Game Fish Bull. 97, 1–188.

Godsil, H. C. and Byers, R. D.(1944). A systematic study of thePacific tunas. Calif. Dept Fish Game Fish Bull.60, 1–131.

Graham, J. B. and Dickson, K. A. (2000). The evolution ofthunniform locomotion and heat conservation in scombrid fishes:New insights based on the morphology of Allothunnus fallai. Zool.J. Linn. Soc. 129, 419–466.

Graham, J. B., Kohern, F. J. and Dickson, K. A. (1983)Distribution and relative proportions of red muscle in scombridfishes: Consequences of body size and the relationships tolocomotion and endothermy. Can. J. Zool. 61, 2087–2096.

Gray, J. (1933). Studies in animal locomotion. I. The movements offish with special reference to the eel. J. Exp. Biol. 10, 88–104.

He, P. and Wardle, C. S.(1986). Tilting behaviour of the Atlanticmackerel, Scomber scombrus, at low swimming speeds. J. FishBiol. 29, 223–232.

Hebrank, M. R. (1982). Mechanical properties of fish backbones inlateral bending and in tension. J. Biomech.15, 85–89.

Hunter, J. R. and Zweifel, J. R.(1971). Swimming speed, tail beatfrequency, tail beat amplitude and size in jack mackerel, Trachurussymmetricusand other fishes. US Fish Wildl. Serv. Fish Bull.69,253–266.

Jayne, B. C. and Lauder, G. V.(1995). Speed effects on midlinekinematics during steady undulatory swimming of largemouth bass,Micropterus salmoides. J. Exp. Biol. 198, 585–602.

Kishinouye, K. (1923). Contributions to the comparative study of theso-called scombroid fishes. J. Coll. Agric. Tokyo Imperial Univ.8,293–475.

Knower, A. T. (1998). Biomechanics of thunniform swimming:electromyography, kinematics and caudal tendon function in theyellowfin tuna Thunnus albacaresand the skipjack tunaKatsuwonus pelamis. PhD dissertation, University of California,San Diego. 136pp.

Knower, T., Shadwick, R. E., Katz, S. L., Graham, J. B.and Wardle, C. S. (1999). Red muscle activation patterns inyellowfin (Thunnus albacares) and skipjack (Katsuwonuspelamis) tunas during steady swimming. J. Exp. Biol. 202,2127–2138.

Lauder, G. V. (2000). Function of the caudal fin during locomotionin fishes: kinematics, flow visualization and evolutionary patterns.Am. Zool.40, 101–122.

3116

Lighthill, J. (1970). Aquatic animal propulsion of highhydromechanical efficiency. J. Fluid Dynamics 44, 265–301.

Lighthill, J. (1975). Mathematical Biofluiddynamics. Philadelphia:Society for Industrial and Applied Mathematics.

Lindsey, C. C.(1978). Form, function and locomotory habits in fish.In Fish Physiology, vol. VII (ed. W. S. Hoar and D. J. Randall),pp. 1–13. New York: Academic Press.

Long, J. H., Jr and Nipper, K. S. (1996). Body stiffness inundulating vertebrates. Am. Zool. 36, 678–694.

Magnuson, J. J. (1963). Tuna behavior and physiology, a review(Methodology paper No. 5). Proceedings of the World ScientificMeeting on the Biology of Tunas and Related Species, La Jolla,California, 2–14 July 1962, vol. 3, 1057–1066.

Magnuson, J. J. (1970). Hydrostatic equilibrium of Euthynnusaffinis, a pelagic teleost without a swim bladder. Copeia1970,56–85.

Magnuson, J. J. (1978). Locomotion by scombrid fishes:Hydromechanics, morphology and behavior. In Fish Physiology,vol. VII (ed. W. S. Hoar and D. J. Randall), pp. 240–315. NewYork: Academic Press.

Magnuson, J. J. and Prescott, J. H.(1966). Courtship, locomotion,feeding and miscellaneous behaviour of Pacific bonito (Sardachiliensis). Anim. Behav. 14, 54–67.

McHenry, M. J., Pell, C. A. and Long, J. H.(1995). Mechanicalcontrol of swimming speed: stiffness and axial wave form inundulating fish models. J. Exp. Biol.198, 2293–2305.

Nursall, J. R. (1956). The lateral musculature and the swimming fish.Proc. Zool. Soc., Lond.126, 127–143.

Packard, G. C. and Boardman, T. J.(1999). The use of percentagesand size-specific indices to normalize physiological data forvariation in body size: wasted time, wasted effort? Comp. Biochem.Physiol.122A, 37–44.

Pyatetskiy, V. Y. (1970). Kinematic swimming characteristics ofsome fast marine fish. In Hydrodynamic Problems in Bionics,Bionika, vol. 4, Kiev (translated from Russian, JPRS 52605, pp.12–23. Natl. Tech. Inf. Serv., Springfield, Virginia, 1971).

Sepulveda, C. and Dickson, K. A.(2000). Maximum sustainablespeeds and cost of swimming in juvenile kawakawa tuna(Euthynnus affinis) and chub mackerel (Scomber japonicus). J.Exp. Biol.203, 3089–3101.

Shadwick, R. E., Katz, S. L., Korsmeyer, K. E., Knower, T. andCovell, J. W. (1999). Muscle dynamics in skipjack tuna: timing ofred muscle shortening in relation to activation and body curvatureduring steady swimming. J. Exp. Biol.202, 2139–2150.

Shadwick, R. E., Steffensen, J. F., Katz, S. L. and Knower, T.(1998). Muscle dynamics in fish during steady swimming. Am.Zool. 38, 755–770.

Videler, J. J. (1985). Fish swimming movements: A study of oneelement of behaviour. Neth. J. Zool. 35, 470–485.

Videler, J. J. (1993). Fish Swimming. London: Chapman & Hall.Videler, J. J. and Hess, F.(1984). Fast continuous swimming of two

pelagic predators saithe (Pollachius virens) and mackerel (Scomberscombrus): a kinematic analysis. J. Exp. Biol. 109, 209–228.

Wardle, C. S., Videler, J. J., Arimoto, T., Franco, J. M. andHe, P. (1989). The muscle twitch and the maximum swimmingspeed of giant bluefin tuna, Thunnus thynnus. J. Fish Biol. 35,129–137.

Webb, P. W.(1971). The swimming energetics of trout. I. Thrust andpower output at cruising speeds. J. Exp. Biol. 55, 489–520.

Webb, P. W. (1975). Hydrodynamics and energetics of fishpropulsion. Bull. Fish. Res. Bd Can. 190, 1–159.

Webb, P. W.(1998). Swimming. In The Physiology of Fishes, secondedition (ed. D. Evans), pp. 1–24. Boca Raton, FL: CRC Press.

Webb, P. W., Kostecki, P. T. and Stevens, D. E.(1984). The effectof size and swimming speed on locomotor kinematics of rainbowtrout. J. Exp. Biol. 109, 77–95.

Westneat, M. W., Hoese, W., Pell, C. A. and Wainwright, S. A.(1993). The horizontal septum: Mechanisms of force transfer inlocomotion of scombrid fishes (Scombridae, Perciformes). J.Morph. 217, 183–204.

Yuen, H. S. H.(1966). Swimming speeds of yellowfin and skipjacktuna. Trans. Am. Fish. Soc. 95, 203–209.

J. M. DONLEY AND K. A. DICKSON