Diversification of coordination patterns during feedingbehaviour in cheiline wrasses
AARON N. RICE1,2*†, W. JAMES COOPER1,2‡ and MARK W. WESTNEAT1,2
1Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA2Department of Zoology, Field Museum of Natural History, Chicago, IL 60605, USA
Received 20 December 2006; accepted for publication 22 March 2007
Coordination is the process of integrating the motionsof morphological components of an organism toaccomplish a specific objective (Bernstein, 1967;Turvey, 1990; Rice & Westneat, 2005). Because theseindividual anatomical systems are capable of inde-pendent movement, the main objective of coordinationduring a kinetic process is to synchronize the move-ment between components to limit possible range of
motion to a narrower, task-specific range of motionbehaviour (Bernstein, 1967; Turvey, 1990). Coordi-nated behaviour is composed of a combination ofsensory inputs synchronized with motor output.During fish feeding, the movements of musculoskel-etal systems must be modified throughout the feedingstrike so as to coordinate the motions of the jaws, fins,trunk, and eye muscles, permitting accurate targetingof the prey, timing of the bite, and maintenance ofvisual contact (Rice & Westneat, 2005). These alter-ations are based on a continuous flow of informationthat is supplied by a fish’s sensory systems as thestrike is taking place.
The biomechanics of musculoskeletal systemsinvolved in feeding and locomotion have key conse-quences for the behaviour, performance, ecology, and
*Corresponding author. E-mail: [email protected]†Current address: Department of Neurobiology andBehavior, Cornell University, Ithaca, NY 14853, USA;‡Current address: Department of Biology, SyracuseUniversity, Syracuse, NY 13244, USA.
Biological Journal of the Linnean Society, 2008, 93, 289–308. With 10 figures
evolution of fishes (Lauder & Liem, 1989; Ferry-Graham & Lauder, 2001; Wainwright & Bellwood,2002; Drucker, Walker & Westneat, 2006; Westneat,2006). Patterns of coordination among such systemsmay be an important aspect of structuring complexbehaviours such as feeding, and the dynamics of thesepatterns may also serve as an important predictor ofoverall feeding performance. The study of coordina-tion during feeding may provide a broader context forthis behaviour than observations that have beenlimited to the actions of the jaws and their associatedstructures alone (Rand & Lauder, 1981; Webb, 1984;Rice & Westneat, 2005). Although studies of coordi-nation patterns are a promising avenue of approachfor addressing questions of behavioural evolution(McLennan, 1994), few studies of fishes have exploredcoordination within an ecological or evolutionarycontext (Rand & Lauder, 1981; Borla et al., 2002;Gahtan, Tanger & Baier, 2005; Rice & Westneat,2005). The coordination of motor systems during fishfeeding encompasses skull kinetics, locomotor behav-iour, oculomotor function, and their modulation basedon incoming sensory input. In the present study, weexplore coordination and sensorimotor integrationamong a closely-related group of three species in thehighly diverse fish family Labridae (the wrasses).
Wrasses have highly diverse prey-capture mor-phologies (Wainwright et al., 2004; Westneat et al.,2005) with foods ranging from benthic algae to freeswimming fishes (Randall, 1967, 1980; Hobson, 1974;Westneat, 1995a, b). Within the Labridae, the tribeCheilinini represents a monophyletic clade of fourgenera and 19 species (Westneat, 1993, 1995a) pos-sessing the highest diversity of feeding morphology,jaw mechanics, and trophic ecology within theLabridae (Wainwright et al., 2004). Three of thesegenera (Cheilinus, Oxycheilinus, and Epibulus)contain species with jaw morphologies that corre-spond to different feeding ecologies (Westneat, 1995a).Species in the genera Oxycheilinus and Epibulus arecapable of capturing elusive prey, but utilize highlydivergent jaw mechanisms and approach behaviours,whereas Cheilinus species (which are more closelyrelated to Epibulus than to Oxycheilinus) prey pre-dominantly upon slow moving, benthic invertebrates(Westneat, 1995a; Westneat et al., 2005). We soughtto determine whether the diversification of cheilinetrophic habits and morphology has been paralleled bya diversification of behavioural coordination patternsduring feeding (sensu Rice & Westneat, 2005). Theexisting body of work on labrid feeding (Wainwrightet al., 2004; Westneat et al., 2005), locomotion (Walker& Westneat, 2002; Thorsen & Westneat, 2005), andphylogenetic relationships (Westneat, 1993; Westneat& Alfaro, 2005), when combined with kinematicanalyses of coordination, allows for a comparison
between patterns of morphological and behaviouralevolution within this lineage.
The present study aimed to: (1) provide a quanti-tative kinematic analysis of the simultaneouslyrecorded trophic, locomotor, and oculomotor move-ments performed by cheiline wrasses during feedingevents and (2) examine how the coordination of theseanatomical systems differs among closely-relatedcheilines that have divergent feeding strategies.These data also allow us to compare the coordinationpatterns of these carnivorous fishes with those previ-ously published for their herbivorous sister group, theparrotfishes (Rice & Westneat, 2005), and to considerhow morphological and behavioural evolution interactduring trophic diversification.
MATERIAL AND METHODS
Three species of cheiline wrasses, Cheilinus fasciatus(Bloch 1791) (N = 4, standard length 15.30 ± 4.31 cm,mean ± SD), Oxycheilinus digrammus (Lacepède1801) (N = 4, standard length 17.83 ± 2.21 cm), andEpibulus insidiator (Pallas 1770) (N = 3, standardlength 9.75 ± 2.91 cm) were trained to feed on benthicprey items. Cheilinus fasciatus and O. digrammuswere collected from the reefs around Lizard Island(Great Barrier Reef, Queensland, Australia) withbarrier nets and returned to the aquarium facility atthe Lizard Island Research Station. Epibulus insid-iator specimens were acquired through the aquariumtrade and filmed in the live animal aquarium facilityat the Field Museum (IACUC Protocol FMNH04-4).All fishes were fed with a standardized prey presen-tation consisting of immobilized items (small fishesor crabs) from their normal diet, tethered to the topof a 5-cm high coral skeleton on the left side ofthe aquaria. Feeding behaviours were filmed with adigital high-speed video camera (Cheilinus and Oxy-cheilinus: MotionScope, Redlake Imaging; Epibulus:Basler A504k, Basler Vision Technologies) at 250frames per second in lateral view. A scale bar wasplaced inside the aquaria to calibrate distance in thefield of view.
Methods of data analysis follow previously pub-lished techniques (Rice & Westneat, 2005) but aresummarized briefly below. Digital video footage wasexported as an image sequence (Apple QuickTime),and the image sequence was imported into TPSdig(Rohlf, 2003). On each frame of the video sequence, 19morphological landmarks representing the movementof the jaws, fins, eyes, and body were plotted(Fig. 1A). Landmarks digitized were: (1) tip of pre-maxilla, (2) tip of dentary, (3) quadrate-articular joint,(4) anterior base of dorsal fin, (5) anterior base ofpelvic fin, (6–9) limits of the orbit, (10–13) limits ofthe pupil, (14) leading edge base of pectoral fin, (15)
trailing edge base of pectoral fin, (16) leading edge tipof pectoral fin, (17) trailing edge of median fin ray ofthe pectoral fin, (18) trailing tip of pectoral fin, and(19) food item.
Based on the movement of these landmarks, kine-matic variables were calculated (Fig. 1B) using aseries of algorithms in a custom kinematics program(CodeWarrior Pascal, Metrowerks Corporation) on anApple Macintosh G5. Variables relevant to feeding,pectoral fin locomotion, and eye movement were cal-culated from the morphometric landmarks: distanceto prey (linear distance between points 1, 19), bodyangle of approach (angle created by the line 3, 14,relative to horizontal), gape (distance between points1 and 2), gape angle (angle 1, 3, 2), jaw protrusion(distance between points 1, 8), cranial elevation(angle 8, 4, 5), pupil distance from the centre of theeye (distance between the calculated centres of points6–9 and 10–13), and pupil angle (angle between thecalculated centres of points 6–9 and 10–13, relative tothe fish’s horizontal axis).
Velocity and acceleration were calculated as thefirst and second derivatives of the distance to the prey
item using QuickSAND (Walker, 1997, 1998), andsmoothed using the predicted mean square errorquintic spline (Walker, 1998). Pectoral fin protraction(movement in the anterior–posterior plane) andabduction (movement in the dorsoventral plane) werecalculated from the apparent length of the leadingedge of the pectoral fin. Once the apparent length ofthe fin was determined in each feeding sequence, wecalculated the projected length (based on the appar-ent length of the fin ray) into the z-plane as well asthe angle relative to the body using the law of cosines(Rice & Westneat, 2005).
For comparison, all feeding sequences were tempo-rally aligned based on the time at prey contact (t0),and all variables are plotted as the mean ± SE.Maximal magnitude, time to maxima and duration ofthe kinematic parameters were analysed using anested analysis of variance (ANOVA) to test for poten-tial differences between individuals and species,using the statistical package JMP, version 5.0.1.2(SAS Institute). Results from the nested ANOVA werecorrected with the sequential Bonferroni method(Rice, 1989). Those parameters likely to be affected by
Figure 1. A, morphological landmarks used: 1, tip of premaxilla; 2, tip of dentary; 3, quadrate-articular joint; 4, anteriorbase of dorsal fin; 5, anterior base of pelvic fin; 6–9, orbit; 10–13, pupil; 14, leading edge base of pectoral fin; 15, trailingedge base of pectoral fin; 16, leading tip of pectoral fin; 17, middle edge of pectoral fin; 18, trailing tip of pectoral fin; 19,food item. B, kinematic variables calculated from morphological landmarks: a, distance to prey; b, body angle of approach;c, gape; d, gape angle; e, jaw protrusion; f, cranial elevation; g, fin abduction; h, fin protraction. Solid lines indicatedistances, dashed lines indicate angles. C, morphological landmarks plotted to estimate the centre of the orbit and pupil,D, pupil vector (distance and angle) measured using calculated centres. For comparison of scale, the background grid is1 cm2.
body size (i.e. gape, jaw protrusion, velocity, etc.) werescaled to the fish’s standard length in statistical analy-ses to account for the size differences. Stereotypy, ameasure of the variability of movement of specificbehavioural components (sensu Barlow, 1977; Deban,O’Reilly & Nishikawa, 2001; Reilly, 1995; Schleidt,1974), can be quantified with a variety of differentmetrics (Barlow, 1977; Deban et al., 2001; Reilly, 1995).Here, stereotypy was assessed using the coefficient ofvariation (CV, standard deviation divided by the mean)for each individual, and then pooled by species(Barlow, 1977; Rice & Westneat, 2005; Schleidt, 1974).Because behaviours are more sterotypic as variabilitydecreases, the CV is used as an inversely proportionalmetric of sterotypy. CV is a relative metric that cannotoften be applied across studies or across very differentbehaviours, but can be a useful assay of sterotypywithin a set of similar behaviours. Behaviours may beconsidered sterotypic (low variation) if the CV rangesfrom 1.0 (e.g. Barlow, 1977; Masahiro, Takashi &Masafumi, 1991) down to 0.3 or below (e.g., Barimo &Fine, 1998). In this study we used a CV of 1.0 or belowto indicate relatively stereotypic features of feedingpatterns within our data set.
RESULTSKINEMATICS OF FEEDING COORDINATION
The three species of cheiline wrasses displayed con-sistent patterns of movement and coordination offeeding, locomotor, and oculomotor kinematics dur-ing feeding strikes (Fig. 2). Significant differencesbetween species were found in the magnitude andtiming of several kinematic variables, includingmaximum velocity, maximum acceleration, maximumbody angle, minimum body angle, gape, gape angle,jaw protrusion, cranial elevation, time to maximumeye movement, and the magnitude of pectoral finabduction during the braking manoeuvre, as wellas the overall order of events during the feedingsequence. Means, standard errors, and results fromstatistical analyses for all parameters are listed inTable 1. With the exception of size-related differencesin C. fasciatus (uncorrected gape, uncorrected jawprotrusion, uncorrected velocity), there were nosignificant differences between individuals withinspecies for the kinematic parameters; thus, individualeffects were not explored further.
During the approach (Fig. 3A), velocities for Cheili-nus and Epibulus ranged from 0–2 body lengths s-1,and 2–3 body lengths s-1 for Oxycheilinus (Fig. 3B).Because the time-distance curve (Fig. 3A), and its firstderivative, velocity (Fig. 3B), was calculated from thechanging distance between the tip of the fish’s pre-maxilla and the food item, the calculated velocity isthe sum of the speed of forward body movement and
the speed of jaw protrusion. For all three species,velocity during the strike was substantially higherthan during the approach, and all three species hadsignificantly different maximum velocities. Oxycheili-nus attained maximum velocity earlier in the strikethan Cheilinus and Epibulus. In a pattern similar tomaximum velocity, there were significant differencesamong the three species for maximum accelerationduring the strike but, during the approach, all specieshad low accelerations (Fig. 3C). Cheilinus approachedthe food at an approximately horizontal body angle,whereas Epibulus and Oxycheilinus approached thefood item from above at a negative body angle with thehead pointing down; all three body angles were sig-nificantly different (Fig. 3D). There was little modu-lation (typically less than a 10° change) of body anglefor each of the species during their respective feedingsequences.
Jaw movements differed between the three speciesduring feeding. Gape distance was significantly largerin Oxycheilinus than Cheilinus and Epibulus, andthese differences were still significant when gapewas scaled by body length (Fig. 4A). Gape angle washigher in Oxycheilinus and Epibulus than Cheilinus(Fig. 4B). Jaw protrusion was significantly higher inEpibulus than in Cheilinus or Oxycheilinus; thesedifferences were also significant when scaled by bodylength (Fig. 4C). Cranial elevation was significantlyhigher in Oxycheilinus than Cheilinus and Epibulus(Fig. 4D). There were no differences between the threespecies for duration and time to maximum displace-ment of gape, jaw protrusion, or cranial elevation.
As with all wrasses (Walker & Westneat, 2002;Westneat et al., 2004; Thorsen & Westneat, 2005), allthree species used pectoral fin propulsion duringapproach to the prey item. For both fin protraction(Fig. 5A) and abduction (Fig. 5B), the three speciesexhibited similar patterns of pectoral fin movement inmagnitude. The duration of the fin cycles duringcruising was 0.18 s in Cheilinus, 0.07 s in Oxycheili-nus and 0.12 s in Epibulus.
All three species employed a large pectoral fin down-stroke as a braking manoeuvre. This started immedi-ately after prey capture and produced a large decreasein velocity, assisting the fishes in moving away fromthe location of the strike. Braking kinematics for thethree species show that Cheilinus and Oxycheilinusprimarily use fin protraction to change direction(Fig. 5A), whereas Epibulus uses a pronounced pecto-ral abduction stroke to come to a stop after preycapture (Fig. 5B). Oxycheilinus and Epibulus had sig-nificantly larger pectoral fin displacement in abductionduring the braking stroke than did Cheilinus.
The eyes of the three species were directed towardsthe prey item (forward and downward) duringapproach, and then began to shift back to centre
Figure 2. Representative feeding sequences of Cheilinus fasciatus (A), Oxycheilinus digrammus (B) and Epibulusinsidiator (C). Timing of events (s) is indicated in each frame. For comparison of scale, the background grid is 1 cm2.
immediately before prey capture (Fig. 6A, B). Cheili-nus achieved its highest degree of forward direction ofthe pupil significantly earlier in the strike than eitherOxycheilinus or Epibulus (Fig. 6A). There were nodifferences among the three taxa in either the mag-
nitude or duration of time that the pupil was shiftedforward (Fig. 6A). During the approach, the eyes of allthree species were directed in a downward orientationtowards the prey (Fig. 6B). In Cheilinus, the eyes hadalmost completely returned to a centred orientation
Table 1. Results of statistical comparisons between Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insid-iator for kinematic variables during feeding
Cheilinus Oxycheilinus Epibulus F9,26 ratio P
Body movementsMaximum velocity (BL s-1) 1.17 ± 0.20 4.30 ± 0.61 13.57 ± 0.65 26.7276 0.0001Time to maximum velocity (s) -0.014 ± 0.031 -0.095 ± 0.0538 -0.020 ± 0.008 0.7639 0.6496Maximum acceleration (cm s-2) 55.73 ± 17.61 145.86 ± 21.72 266.39 ± 25.56 7.3991 0.0001Time to maximum acceleration (s) -0.062 ± 0.116 -0.089 ± 0.055 -0.011 ± 0.005 1.2576 0.3053Maximum body angle (°) -0.002 ± 4.726 -18.78 ± 4.23 -46.9 ± 3.2 7.3991 0.0001Minimum body angle (°) -11.6 ± 4.3 -32.7 ± 4.4 -61.0 ± 3.2 8.6898 0.0001Change in body angle (°) -11.6 ± 1.3 -14.0 ± 1.4 -47.0 ± 3.2 7.3991 0.0001
Differences tested for with a nested analysis of variance. Spatial and temporal kinematic values represented bymean ± standard error, taken from individuals and pooled for each species. There were no significant intraspeciesdifferences. P-values in bold indicate significant values after sequential Bonferroni correction (Rice, 1989). Thoseparameters likely to be affected by body size were scaled by the fish’s standard length (e.g. adjusted jaw protrusion,adjusted gape).BL, body length.
Figure 3. Kinematic plots of body movement during the feeding strike in Cheilinus fasciatus, Oxycheilinus digrammusand Epibulus insidiator. A, distance to prey target (cm); B, velocity (body lengths s-1) profile of an individual, represen-tative specimen from each species; C, acceleration (cm s-2) profile of an individual, representative specimen from eachspecies (Cheilinus and Oxycheilinus data correspond to the left y-axis, Epibulus data correspond to the right y-axis);D, body angle of approach (°) versus time for C. fasciatus, O. digrammus, and E. insidiator. Contact with food item occursat to, indicated by dashed vertical line. Symbols indicate the mean ± standard error.
Figure 4. Kinematic plots of jaw and head movements during the feeding strike in Cheilinus fasciatus, Oxycheilinusdigrammus and Epibulus insidiator. A, gape (cm); B, gape angle (°); C, jaw protrusion (cm); D, cranial elevation (°) versustime for C. fasciatus, O. digrammus, and E. insidiator. Contact with food item occurs at to, indicated by dashed verticalline. Symbols indicate the mean ± standard error.
before the fish reached the prey item, whereas Oxy-cheilinus and Epibulus still had their eyes directedforward upon reaching the prey (Fig. 6C).
STEREOTYPY AND COORDINATION PROFILES
OF FEEDING
Many of the different kinematic components of thefeeding strike for the three species displayed lowlevels of variability (Fig. 7, Table 2). Almost all kine-matic parameters had a coefficient of variation (CV) ofless than 1.0, but the more variable features in allthree species were associated with the time thatelapsed from the beginning of the strike until theachievement of maximum for velocity, maximum bodyangle, maximum gape, maximum jaw protrusion, andmaximum pectoral fin protraction during braking.Most parameters were characterized by a relativelylow CV, suggesting a similar degree of stereotypyduring the feeding strike for Cheilinus, Oxycheilinus,and Epibulus, despite differences in coordinationpatterns.
The timing patterns of multiple variables duringthe feeding sequence were consistent within eachspecies but different among the three species. Cheili-nus began to rotate its eyes back to a centred positionat the onset of mouth opening (Fig. 8B, C), whereasOxycheilinus and Epibulus maintained the eyesdirected forward until after peak gape was attainedand the jaws began to close (Figs 9B, C , 10B, C).Cheilinus began its pectoral fin braking stroke whenit achieved peak gape, and as it protracted its fins,and pectoral fin movement was predominantly in theanterior-posterior plane (Fig. 8B, D), with littledorsoventral movement (Fig. 8E). Oxycheilinus andEpibulus initiated their pectoral fin braking stroke atthe completion of the gape cycle (Figs 9B, D, 10B, D);fin movement was predominantly in the anterior–posterior direction after the strike for Oxycheilinus(Fig. 9D, E), but was directed dorsoventrally byEpibulus (Fig. 10D, E). However, all three speciesdemonstrated an increase in velocity at the onset ofthe strike that was timed with jaw opening (Figs 8A,B, 9A, B, 10A, B).
Figure 5. Angles of pectoral fin movement during the approach and feeding strike in Cheilinus fasciatus, Oxycheilinusdigrammus and Epibulus insidiator. A, protraction angle (°); B, abduction angle (°) versus time for C. fasciatus,O. digrammus, and E. insidiator. Contact with food item occurs at to, indicated by dashed vertical line. Symbols indicatethe mean ± standard error.
Analysis of the feeding kinematics of C. fasciatus,E. insidiator, and O. digrammus revealed stereotypi-cal patterns of coordination between the jaws, fins
and eyes in all three species (Fig. 11). Examination ofthese patterns suggests several components of thisbehaviour that are important for describing wrassefeeding. Some aspects of the observed feeding behav-iours are shared between all of these species, and may
Figure 6. Kinematic plots of eye movements during feeding strike in Cheilinus fasciatus, Oxycheilinus digrammus andEpibulus insidiator. A, pupil distance from the centre of the eye (cm) versus time; B, pupil angle (°) versus time; C, pupildistance from the centre of the eye (cm) versus distance from prey item (cm) for C. fasciatus, O. digrammus, andE. insidiator. Schematic eye above figures represents the overall trend of eye movement and angle during the feedingstrike. Pupil distances were smoothed with a three-point running average. Dashed line indicates contact with prey item.Symbols indicate the mean ± standard error.
Figure 7. Stereotypy of the different components of the feeding strike for Cheilinus fasciatus, Oxycheilinus digrammus,and Epibulus insidiator as a function of the coefficient of variation (CV). A, body movement and position;B, jaw movement; C, fin movement; D, eye distance, represented by mean CV ± standard error for each species. A largerCV represents higher variability.
represent ancestral conditions for the cheilines,whereas those patterns of coordination that are par-ticular to individual species help describe the diver-sification of feeding tactics that has occurred withinthis lineage. Combining this behavioural data withthe body of information already available on theskull morphology and dietary habits of these animalssuggests that the radiation of cheiline trophicmorphology has occurred in conjunction with a diver-sification of feeding behaviour (Westneat, 1995a;Ferry-Graham et al., 2002), which is reflected in thecoordination profiles presented here (Fig. 11).
COORDINATION OF THE FEEDING STRIKE
All three species maintained a downward-pointingbody angle with a relatively constant velocity duringtheir approach to the prey. Their eyes were consis-tently orientated forward towards the food item,suggesting that visual input is important guidingthe fish to the prey (Collin & Shand, 2003). Oncethe fishes were within less than one body length ofthe prey, the jaws rapidly opened and closed, theeyes rotated back to a centred position (no longerlooking at the original position of the prey), and the
Table 2. Coefficient of variation values for Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insidiator of thekinematic variables during feeding
Cheilinus Oxycheilinus Epibulus
Body movementsMaximum velocity 0.454 ± 0.145 0.493 ± 0.100 0.168 ± 0.049Time to maximum velocity 2.747 ± 0.838 1.386 ± 0.202 0.997 ± 0.424Maximum acceleration 0.685 ± 0.050 0.530 ± 0.129 0.175 ± 0.062Time to maximum acceleration 1.320 ± 0.319 2.163 ± 0.481 1.186 ± 0.283Maximum body angle 0.907 ± 0.505 1.241 ± 0.573 0.226 ± 0.108Minimum body angle 1.540 ± 1.177 0.514 ± 0.223 0.161 ± 0.103Change in body angle 0.290 ± 0.150 0.262 ± 0.085 0.297 ± 0.082
pectoral fins were swept forward and down as abraking manoeuvre (Fig. 11).
Cheiline species exhibited several differences intheir feeding behaviours. Cheilinus approaches foodat a relatively slow and steady rate, whereas Oxy-cheilinus employs a fast-start-like lunge (cf. Schriefer& Hale, 2004) to initiate an explosive ram-feedingstrike. The approach speed of Epibulus is intermedi-ate, until the rapid and extreme protrusion of theirjaws (up to two-thirds of the fish’s head length; West-neat & Wainwright, 1989) creates a sudden decreasein the distance between the fish and the food item. Asthis occurs, the remainder of the body remains nearlystationary.
Oxycheilinus had an early onset of peak gape, alarge gape angle, and a very rapid gape cycle whereasCheilinus had the longest gape cycle, smallest gapeangle, did not achieve maximal gape until the point of
prey contact, and exhibited the smallest degree of jawprotrusion (Fig. 4). During the approach, Epibulushad patterns of onset times for the different feedingkinematics that were similar to Cheilinus (Fig. 4).However, upon beginning the strike, Epibulus hadvery rapid changes in gape angle, jaw protrusion,cranial elevation, and exhibited the shortest durationfor these variables among the three species. Magni-tudes of gape angle and cranial elevation were similarbetween Epibulus and Oxycheilinus. The approachand strike patterns of Epibulus represents sharedfeatures of the feeding components with Cheilinus, asit maintains a slow cruising speed while foraging andpositioning itself relative to the food item, but then arapid strike (initiated at a relatively closer distanceto the prey than Oxycheilinus), comparable toother ram-feeding predatory fishes (Westneat &Wainwright, 1989).
Figure 8. Selected Cheilinus fasciatus coordination variables, showing the kinematic relationships between differentfunctional systems. A, velocity (body lengths s-1); B, gape (cm); C, eye distance (cm); D, fin protraction (°); E, fin abduction(°) versus time to prey contact (s) represented as the mean ± standard error. Contact with food item occurs at to, indicatedby dashed vertical line.
In fish feeding, higher attack speed and largersuction are thought to correlate with an ability tocapture more elusive prey (Liem, 1978; Nemeth,1997a, b), and this association is seen amongst thecheiline wrasses. We suggest that the observed dif-ferences between degrees of strike speed, jaw protru-sion, and gape correlate with an ability to prey uponevasive animals such as some shrimps and fishes.Cheilinus fasciatus feeds on a diversity of benthicinvertebrates including ophiuroids, gastropods(Cerithiidae, Mitridae, Trochidae, Turridae, Triph-oridae Epitoniidae, Columbellidae, Strombidae),decapod crustaceans (Paguridae, Xanthidae), andbivalves (Pectinidae, Pteriidae); Oxycheilinus mostlyfeeds on decapod crustaceans (Portunidae, Xanthidae),stomatopods, and teleosts; Epibulus feeds on decapodcrustaceans (Galatheidae, Palaemonidae, Portunidae,
Xanthidae), teleosts, and some gastropods (Cerithi-idae, Epitonniidae) (Randall, 1980; Sano, Shimizu& Nose, 1984; Westneat, 1995b, unpubl. data). Themain difference in diet composition between thesethree taxa is that Epibulus and Oxycheilinus haveexpanded their feeding niche to include predationon fishes and evasive crustaceans (Hobson, 1974;Randall, 1980; Westneat & Wainwright, 1989; West-neat, 1991, 1995a, b; Connell, 1998; Ferry-Grahamet al., 2001).
The marked differences in jaw protrusion amongthese three species (Fig. 4C, Table 1) may demon-strate the effect of jaw kinesis in coordinating otherprocesses of overall feeding behaviour. Most impor-tantly, the magnitude of jaw protrusion determinesthe maximum distance between the predator and thefood item at which prey capture can occur (Motta,
Figure 9. Selected Oxycheilinus digrammus coordination variables, showing the kinematic relationships between dif-ferent functional systems. A, velocity (body lengths s-1); B, gape (cm); C, eye distance (cm); D, fin protraction (°); E, finabduction (°) versus time to prey contact (s) represented as the mean ± standard error. Contact with food item occurs atto, indicated by dashed vertical line.
1984; Osse, 1985). By protruding its jaws, a fish addsa component to their overall attack speed that isindependent of any locomotor limitations. Jaw pro-trusion reduces the time that elapses between theonset of an attack and prey contact, and extensiveprotrusion, especially if it occurs rapidly, can reducethis time dramatically. Increased protrusion allowsfor a sudden ambush-style strike to surprise andcapture the prey, as the prey may base its escaperesponse on the predator’s initial approach speed(Liem, 1978). The extreme jaw protrusion seen inEpibulus, the greatest reported for any fish species(Westneat & Wainwright, 1989; Westneat, 1991),may demonstrate some of the adaptive advantagesin the evolution of this morphology, includingdecreasing the time to prey capture, increasing thetime in which the food item remains in the binocularvisual field (Motta, 1984; Osse, 1985), and enablingthe fish to acquire food items from interstitial
spaces into which the jaws can fit, but not the entirehead.
OCULOMOTOR AND LOCOMOTOR KINEMATICS IN
VISUAL PREDATORS
By simultaneously recording coincident locomotor andoculomotor data, we are able to place the patterns ofjaw movement within a larger context so as to presenta more comprehensive description of feeding behav-iour. Vision is one of the dominant sources of sensoryinput mediating prey capture behaviour in fishes(Pankhurst, 1989; Pettigrew, Collin & Fritsches,2000; Gahtan et al., 2005; McElligott & O’Malley,2005; Lisney & Collin, 2006). As with most diurnalcoral reef fishes, these cheiline wrasses used visualinput to guide their approach to the prey item. Duringthe approach, and before the strike, all three speciesdirected the eyes forward, presumably focusing on the
Figure 10. Selected Epibulus insidiator coordination variables, showing the kinematic relationships between differentfunctional systems. A, velocity (body lengths s-1); B, gape (cm); C, eye distance (cm); D, fin protraction (°); E, fin abduction(°) versus time to prey contact (s) represented as the mean ± standard error. Contact with food item occurs at to, indicatedby dashed vertical line.
prey item (Fernald, 1990; Easter & Nicola, 1997;Collin & Shand, 2003). This is different from theparrotfishes, which do not focus their eyes on the fooditem at the moment of prey capture, but shift themback to a centred position (Rice & Westneat, 2005);the cheilines’ eyes do not shift back to a centredposition until after prey capture occurs (Fig. 6A, C).For parrotfishes feeding on immobile algae, the non-evasive nature of their food may obviate the need forvisual input during the last moments of an approachand a more centred position for the pupils may aid inpredator detection (Rice & Westneat, 2005).
Because the snout may block the binocular visualfield at very close ranges (Tamura, 1957; Osse, 1985;Rice & Westneat, 2005), Cheilinus and Oxycheilinusmay rely on lateral line input during the finalmoments of prey capture (Janssen & Corcoran, 1993;New & Kang, 2000; New, Alborg Fewkes & Khan,2001; New, 2002). However, the extreme jaw protru-sion of Epibulus may allow for prey capture to occurwhen both the prey and the jaws are within thebinocular visual field, perhaps allowing for increasedaccuracy. Because piscivorous fishes are known to usetheir lateralis system to guide them during themoments of prey capture (Montgomery et al., 2002), itis possible that their braking manoeuvre is delayeduntil after prey capture so as to avoid excess hydro-
dynamic noise (Higham et al., 2005). Additionally, thebraking stroke with the pectoral fins of these preda-tors may delayed until after the feeding strike so as tominimize the visual and hydrodynamic profile appar-ent to the prey, and decrease their apparent loomingthreshold (Domenici, 2002).
The patterns of fin movement differed among thethree species (Figs 5, 8–10), reflective of significantdifferences related to the coordination of feedingbehaviour. Cheilinus used slow and steady propulsivepectoral fin beats to manoeuvre towards its food,whereas Oxycheilinus primarily used a fast-start tolunge towards its food, and employed smaller pectoralfin movements for positioning during the strike. BothOxycheilinus and Cheilinus displayed a dramaticforward braking stroke that may help prevent collisionwith the substrate, similar to braking seen in cen-trarchids and parrotfishes (Higham, 2007; Rice &Westneat, 2005). Epibulus used its pectoral fins forprecise manoeuvreing before extending its jaws once itreached an appropriate strike distance, and used amore dorsoventral downstroke after prey capture toretain postural control due to a change in its centre ofmass, rather than change directions due to swimming.
During these benthic prey capture events, manycomponents of the feeding strike were stereotypical(Fig. 7, Table 2). For almost all parameters investi-
Figure 11. Schematic representation of kinematic variables representing jaw, fin and eye movements during feedingbehaviour in Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insidiator. Time period of activity for thevariables is indicated by a horizontal coloured bar. The maximum for each parameter is indicated by a solid black bar.Contact with food item occurs at to, indicated by dashed vertical line.
gated (except for fin protraction), Epibulus had thelowest levels of variation. It is likely that the highlyderived jaws of Epibulus are stereotypic due to theirpredation almost exclusively upon evasive prey suchas fishes and mobile crustaceans (Hobson, 1974;Randall, 1980; Westneat, 1995b). Conversely, theleast consistent behaviours were the onset times forseveral jaw movement parameters of Cheilinus andOxycheilinus (Fig. 7B). For Oxycheilinus, this varia-tion might be due to the fast lunge they make towardsthe food item. The variable modulation of jaw activitymay be necessary when there is little time to adjustthe targeting of the entire body. The stereotypedbenthic feeding behaviour seen in the cheilines maybe because the benthic prey items, although varied,do not present dramatically different functionaldemands for feeding (sensu Bout, 1998) compared toprey items in the water column (Ferry-Graham et al.,2001; Ferry-Graham et al., 2002).
EVOLUTIONARY TRENDS IN LABRID COORDINATION
Comparisons between the coordination patterns of thecheilines and those of previously analysed parrotfishes(Rice & Westneat, 2005) have several implications forthe evolution of coordination patterns within wrassesas a family. The sister taxon relationship betweencheiline wrasses and parrotfishes (Westneat & Alfaro,2005) requires that all members of both clades evolvedfrom a single ancestor possessing its own patterns ofcoordination during feeding. From this starting point,the coordination patterns of the cheilines and theparrotfishes diverged to develop two very differentfeeding ecologies: carnivory and herbivory. Thisexample demonstrates that, in fishes, coordinationpatterns among multiple functional systems areadaptable and capable of evolving to exploit differentecological niches. The increase in the diversity offeeding behaviours in this radiation provides anexample of how the adaptation of coordination pat-terns may play an important part in trophic evolution.
The differences in coordination patterns between thecheilines and scarines may be due to associated con-sequences of the basic biomechanics of prey capture(e.g., Alfaro, Janovetz & Westneat, 2001; Alfaro &Westneat, 1999; Ferry-Graham et al., 2001; Ferry-Graham et al., 2002). There is a well-known tradeoffbetween speed and force in musculoskeletal systemsthat has powerful implications for morphologicaldesign (Alexander, 1968; McMahon, 1984; Vogel,2003), particularly in fish jaws (Barel, 1983; Westneat,2003, 2004). Predatory wrasses will often use fast jawopening to create high suction to dislodge benthic prey(Ferry-Graham et al., 2002), whereas parrotfishes canonly remove food from the substrate by applying highforces alone (Bellwood & Choat, 1990; Alfaro & West-
neat, 1999). Oxycheilinus uses a lunge of the wholebody to quickly capture its food, and then uses its smallpectoral fins to steer away from the capture site toprevent collision, though there is no change in trajec-tory. In the slower moving parrotfishes and Cheilinus,there is a slow, deliberate approach, and they use theirlarge pectoral fins to reverse direction to preventcollision with the substrate. For Epibulus, there islittle risk in substrate collision, due to their preycapture from a proportionately greater distance and aslower body speed than either the other cheilines orparrotfishes, and thus the pectoral fins are predomi-nantly used for positioning the fish relative to the fooditem. Oxycheilinus thus provides an example of thecoordination patterns during a very fast attack,whereas Cheilinus and the parrotfishes provideexamples of coordination patterns that are used duringslower prey capture events.
Although their diet is more restricted than manyother wrasses, the parrotfishes also display an arrayof feeding strategies and behaviours that are associ-ated with their different dietary preferences (Bell-wood & Choat, 1990; Alfaro & Westneat, 1999; Choat,Robbins & Clements, 2002, 2004; Rice & Westneat,2005). Despite differences in the timing of jaw andbody movements, parrotfishes exhibit an extendedbite cycle compared to the cheilines, with the mouthachieving peak gape well before contact with the preyitem (Rice & Westneat, 2005). Additionally, the par-rotfish fins engage in their braking manoeuvre at thepoint of prey contact, synchronized with jaw closing(Rice & Westneat, 2005), whereas the cheiline finsbegin the braking manoeuvre well after the gape cyclecompletes (Figs 8, 9, 10). The differences in coordina-tion behaviour between the parrotfishes and thecheilines are likely due to the underlying functionalrequirements for scraping and excavating hard sub-strate as opposed to capturing evasive or attachedprey in a complex environment.
For carnivores, the challenge in feeding is ininitial procurement and food handling, whereas preyprocessing after capture is relatively straightfor-ward. Conversely for herbivores, the challenge is notin food procurement but food processing, as many ofthe ingested materials are indigestible (Choat, 1991;Choat et al., 2002, 2004). The biomechanical trade-off between food capture and food processing may beincorporated in the resulting coordination patternsof these fishes while feeding. Carnivorous fishes pur-suing prey that are fast and mobile must attackquickly to be successful, as they may have only oneattempt at a particular potential food item: thustheir behaviour is constructed around the acute preydetection and a rapid bite cycle. For herbivores, theprimary concern is being able to access stationaryfood on a stable platform using their fins to assist
in precise orientation (Choat, 1991). As the parrot-fishes do not have to deal with an escaping fooditem, their eyes are released from focusing on thefood and are used in monitoring the surround-ings for predators after food is located (Krause &Godin, 1996; Overholtzer & Motta, 2000; Rice &Westneat, 2005), while they execute many repeatedbites during a feeding bout (Bellwood & Choat,1990; Alfaro & Westneat, 1999; Rice & Westneat,2005). Comparison of parrotfishes and carnivorouscheilines may provide an excellent system in whichto continue evolutionary studies of coordination(sensu Choat, 1991).
Behaviour is ultimately a combination of manycoordinated components within the body of the organ-ism (Bernstein, 1967; Turvey, 1990), and this hasimportant implications for the many studies of func-tional morphology. Coordination itself is not the prin-cipal goal of an organism (Weiss & Jeannerod, 1998),but rather the successful completion of a task such asmating, predator avoidance or food acquisition. Manyprevious analyses that examined the functioning ofindividual motor systems in isolation, overlooked thesupporting, and often more subtle, contributions ofaccessory systems to the successful performance ofthe observed behaviour (Cordo & Gurfinkel, 2003;Massion, Alexandrov & Frolov, 2003).
As organisms interact with their environments inmultiple ways while performing complex tasks, thefunctioning of individual physiological systems doesnot occur in isolation, and it is therefore difficult tounderstand the functioning of these separate systemswithout knowing how they are coordinated. We haveattempted to integrate functional studies of the visualsystem and two motor systems in order to achieve amore comprehensive understanding of how complexbehaviours are generated and evolve (Lauder, 1986;Lauder & Liem, 1989; McLennan, 1994). Quantita-tively analysing and comparing kinematic patternsof coordination between age classes, populations,species, or families will allow for clear demonstrationsof how complex ethological units such as feedingbehaviour at the organismal level change along eco-logical and evolutionary trajectories.
ACKNOWLEDGEMENTS
We would like to thank A. Hoggett, L. Vail, B. Lamb,and T. Lamb for their assistance while at L.I.R.S.We thank M. E. Hale, M. LaBarbera, J. L. Moranoand J. G. New for substantive and helpful commentson the manuscript. This project was made possible bygrants from the University of Chicago Hinds Fund(A.N.R.), American Society of Ichthyologists and Her-petologists Raney Fund Award (A.N.R.), the Lerner-Gray Memorial Fund for Marine Research (A.N.R.), a
Grant-in-Aid of research from the Society of Integra-tive and Comparative Biology (A.N.R.), the Chicagochapter of the ARCS Foundation (W.J.C.), a NationalScience Foundation Doctoral Dissertation Improve-ment Grant IBN-0308977 (W.J.C., M.W.W.), andgrants IBN-0235307 from the National Science Foun-dation and N000149910184 from the Office of NavalResearch (M.W.W.).
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