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Biological Journal of the Linnean Society, 2008, 93, 289–308. With 10 figures

Diversification of coordination patterns during feeding behaviour in cheiline wrasses AARON N. RICE1,2*†, W. JAMES COOPER1,2‡ and MARK W. WESTNEAT1,2 1 2

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA Department of Zoology, Field Museum of Natural History, Chicago, IL 60605, USA

Received 20 December 2006; accepted for publication 22 March 2007

Successful fish feeding often requires the coordination of several complex motor and sensory systems to ensure that food is accurately detected, approached, acquired, and consumed. In the present study, we address feeding behaviour as a coordinated set of multiple, facultatively independent, anatomical systems. We sought to determine whether the patterns of interaction between trophic, locomotor, and oculomotor systems are associated with changes in morphology and ecology within a closely-related, but trophically divergent, group of fishes. We present a quantitative kinematic analysis of skull motion, locomotor behaviour, and oculomotor responses during feeding to assess coordination in three functional systems directly involved in feeding. We use coordination profiles to depict the feeding behaviours of three carnivorous coral reef fishes of the tribe Cheilinini in the family Labridae (the wrasses): Cheilinus fasciatus (a slow-swimming predator of benthic invertebrates), Epibulus insidiator (a slow-stalking predator with extraordinary jaw protrusion), and Oxycheilinus digrammus (a fast-attack predator). Differences were detected in several variables relating to jaw, body, fin, and eye movements. Overall patterns of coordination were more similar between E. insidiator and O. digrammus, which are capable of capturing elusive prey, than between C. fasciatus and E. insidiator, which are the two most closely-related species among the three. Evidence for the evolution of coordination patterns among cheiline fishes suggests that the sensory-motor systems involved in processing stimuli and coordinating a physical response during feeding have changed considerably, even among closely-related species. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 289–308.

ADDITIONAL KEYWORDS: biomechanics – Cheilinini – coral reef fish – functional morphology – kinematics – Labridae – swimming – vision.

INTRODUCTION Coordination is the process of integrating the motions of morphological components of an organism to accomplish a specific objective (Bernstein, 1967; Turvey, 1990; Rice & Westneat, 2005). Because these individual anatomical systems are capable of independent movement, the main objective of coordination during a kinetic process is to synchronize the movement between components to limit possible range of

*Corresponding author. E-mail: [email protected] †Current address: Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA; ‡Current address: Department of Biology, Syracuse University, Syracuse, NY 13244, USA.

motion to a narrower, task-specific range of motion behaviour (Bernstein, 1967; Turvey, 1990). Coordinated behaviour is composed of a combination of sensory inputs synchronized with motor output. During fish feeding, the movements of musculoskeletal systems must be modified throughout the feeding strike so as to coordinate the motions of the jaws, fins, trunk, and eye muscles, permitting accurate targeting of the prey, timing of the bite, and maintenance of visual contact (Rice & Westneat, 2005). These alterations are based on a continuous flow of information that is supplied by a fish’s sensory systems as the strike is taking place. The biomechanics of musculoskeletal systems involved in feeding and locomotion have key consequences for the behaviour, performance, ecology, and

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evolution of fishes (Lauder & Liem, 1989; FerryGraham & Lauder, 2001; Wainwright & Bellwood, 2002; Drucker, Walker & Westneat, 2006; Westneat, 2006). Patterns of coordination among such systems may be an important aspect of structuring complex behaviours such as feeding, and the dynamics of these patterns may also serve as an important predictor of overall feeding performance. The study of coordination during feeding may provide a broader context for this behaviour than observations that have been limited to the actions of the jaws and their associated structures alone (Rand & Lauder, 1981; Webb, 1984; Rice & Westneat, 2005). Although studies of coordination patterns are a promising avenue of approach for addressing questions of behavioural evolution (McLennan, 1994), few studies of fishes have explored coordination within an ecological or evolutionary context (Rand & Lauder, 1981; Borla et al., 2002; Gahtan, Tanger & Baier, 2005; Rice & Westneat, 2005). The coordination of motor systems during fish feeding encompasses skull kinetics, locomotor behaviour, oculomotor function, and their modulation based on incoming sensory input. In the present study, we explore coordination and sensorimotor integration among a closely-related group of three species in the highly diverse fish family Labridae (the wrasses). Wrasses have highly diverse prey-capture morphologies (Wainwright et al., 2004; Westneat et al., 2005) with foods ranging from benthic algae to free swimming fishes (Randall, 1967, 1980; Hobson, 1974; Westneat, 1995a, b). Within the Labridae, the tribe Cheilinini represents a monophyletic clade of four genera and 19 species (Westneat, 1993, 1995a) possessing the highest diversity of feeding morphology, jaw mechanics, and trophic ecology within the Labridae (Wainwright et al., 2004). Three of these genera (Cheilinus, Oxycheilinus, and Epibulus) contain species with jaw morphologies that correspond to different feeding ecologies (Westneat, 1995a). Species in the genera Oxycheilinus and Epibulus are capable of capturing elusive prey, but utilize highly divergent jaw mechanisms and approach behaviours, whereas Cheilinus species (which are more closely related to Epibulus than to Oxycheilinus) prey predominantly upon slow moving, benthic invertebrates (Westneat, 1995a; Westneat et al., 2005). We sought to determine whether the diversification of cheiline trophic habits and morphology has been paralleled by a diversification of behavioural coordination patterns during feeding (sensu Rice & Westneat, 2005). The existing body of work on labrid feeding (Wainwright et al., 2004; Westneat et al., 2005), locomotion (Walker & Westneat, 2002; Thorsen & Westneat, 2005), and phylogenetic relationships (Westneat, 1993; Westneat & Alfaro, 2005), when combined with kinematic analyses of coordination, allows for a comparison

between patterns of morphological and behavioural evolution within this lineage. The present study aimed to: (1) provide a quantitative kinematic analysis of the simultaneously recorded trophic, locomotor, and oculomotor movements performed by cheiline wrasses during feeding events and (2) examine how the coordination of these anatomical systems differs among closely-related cheilines that have divergent feeding strategies. These data also allow us to compare the coordination patterns of these carnivorous fishes with those previously published for their herbivorous sister group, the parrotfishes (Rice & Westneat, 2005), and to consider how morphological and behavioural evolution interact during 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 (Lacepède 1801) (N = 4, standard length 17.83 ± 2.21 cm), and Epibulus insidiator (Pallas 1770) (N = 3, standard length 9.75 ± 2.91 cm) were trained to feed on benthic prey items. Cheilinus fasciatus and O. digrammus were collected from the reefs around Lizard Island (Great Barrier Reef, Queensland, Australia) with barrier nets and returned to the aquarium facility at the Lizard Island Research Station. Epibulus insidiator specimens were acquired through the aquarium trade and filmed in the live animal aquarium facility at the Field Museum (IACUC Protocol FMNH04-4). All fishes were fed with a standardized prey presentation consisting of immobilized items (small fishes or crabs) from their normal diet, tethered to the top of a 5-cm high coral skeleton on the left side of the aquaria. Feeding behaviours were filmed with a digital high-speed video camera (Cheilinus and Oxycheilinus: MotionScope, Redlake Imaging; Epibulus: Basler A504k, Basler Vision Technologies) at 250 frames per second in lateral view. A scale bar was placed inside the aquaria to calibrate distance in the field of view. Methods of data analysis follow previously published techniques (Rice & Westneat, 2005) but are summarized briefly below. Digital video footage was exported as an image sequence (Apple QuickTime), and the image sequence was imported into TPSdig (Rohlf, 2003). On each frame of the video sequence, 19 morphological landmarks representing the movement of the jaws, fins, eyes, and body were plotted (Fig. 1A). Landmarks digitized were: (1) tip of premaxilla, (2) tip of dentary, (3) quadrate-articular joint, (4) anterior base of dorsal fin, (5) anterior base of pelvic fin, (6–9) limits of the orbit, (10–13) limits of the pupil, (14) leading edge base of pectoral fin, (15)

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Figure 1. A, morphological landmarks used: 1, tip of premaxilla; 2, tip of dentary; 3, quadrate-articular joint; 4, anterior base of dorsal fin; 5, anterior base of pelvic fin; 6–9, orbit; 10–13, pupil; 14, leading edge base of pectoral fin; 15, trailing edge 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 indicate distances, 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 is 1 cm2.

trailing edge base of pectoral fin, (16) leading edge tip of pectoral fin, (17) trailing edge of median fin ray of the pectoral fin, (18) trailing tip of pectoral fin, and (19) food item. Based on the movement of these landmarks, kinematic variables were calculated (Fig. 1B) using a series of algorithms in a custom kinematics program (CodeWarrior Pascal, Metrowerks Corporation) on an Apple Macintosh G5. Variables relevant to feeding, pectoral fin locomotion, and eye movement were calculated from the morphometric landmarks: distance to prey (linear distance between points 1, 19), body angle of approach (angle created by the line 3, 14, relative to horizontal), gape (distance between points 1 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 the eye (distance between the calculated centres of points 6–9 and 10–13), and pupil angle (angle between the calculated centres of points 6–9 and 10–13, relative to the fish’s horizontal axis). Velocity and acceleration were calculated as the first and second derivatives of the distance to the prey

item using QuickSAND (Walker, 1997, 1998), and smoothed using the predicted mean square error quintic spline (Walker, 1998). Pectoral fin protraction (movement in the anterior–posterior plane) and abduction (movement in the dorsoventral plane) were calculated from the apparent length of the leading edge of the pectoral fin. Once the apparent length of the fin was determined in each feeding sequence, we calculated the projected length (based on the apparent length of the fin ray) into the z-plane as well as the angle relative to the body using the law of cosines (Rice & Westneat, 2005). For comparison, all feeding sequences were temporally 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 of the kinematic parameters were analysed using a nested analysis of variance (ANOVA) to test for potential differences between individuals and species, using the statistical package JMP, version 5.0.1.2 (SAS Institute). Results from the nested ANOVA were corrected with the sequential Bonferroni method (Rice, 1989). Those parameters likely to be affected by

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body size (i.e. gape, jaw protrusion, velocity, etc.) were scaled to the fish’s standard length in statistical analyses to account for the size differences. Stereotypy, a measure of the variability of movement of specific behavioural components (sensu Barlow, 1977; Deban, O’Reilly & Nishikawa, 2001; Reilly, 1995; Schleidt, 1974), can be quantified with a variety of different metrics (Barlow, 1977; Deban et al., 2001; Reilly, 1995). Here, stereotypy was assessed using the coefficient of variation (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 variability decreases, the CV is used as an inversely proportional metric of sterotypy. CV is a relative metric that cannot often be applied across studies or across very different behaviours, but can be a useful assay of sterotypy within a set of similar behaviours. Behaviours may be considered sterotypic (low variation) if the CV ranges from 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 below to indicate relatively stereotypic features of feeding patterns within our data set.

RESULTS KINEMATICS

OF FEEDING COORDINATION

The three species of cheiline wrasses displayed consistent patterns of movement and coordination of feeding, locomotor, and oculomotor kinematics during feeding strikes (Fig. 2). Significant differences between species were found in the magnitude and timing of several kinematic variables, including maximum velocity, maximum acceleration, maximum body angle, minimum body angle, gape, gape angle, jaw protrusion, cranial elevation, time to maximum eye movement, and the magnitude of pectoral fin abduction during the braking manoeuvre, as well as the overall order of events during the feeding sequence. Means, standard errors, and results from statistical analyses for all parameters are listed in Table 1. With the exception of size-related differences in C. fasciatus (uncorrected gape, uncorrected jaw protrusion, uncorrected velocity), there were no significant differences between individuals within species for the kinematic parameters; thus, individual effects were not explored further. During the approach (Fig. 3A), velocities for Cheilinus 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 first derivative, velocity (Fig. 3B), was calculated from the changing distance between the tip of the fish’s premaxilla and the food item, the calculated velocity is the sum of the speed of forward body movement and

the speed of jaw protrusion. For all three species, velocity during the strike was substantially higher than during the approach, and all three species had significantly different maximum velocities. Oxycheilinus attained maximum velocity earlier in the strike than Cheilinus and Epibulus. In a pattern similar to maximum velocity, there were significant differences among the three species for maximum acceleration during the strike but, during the approach, all species had low accelerations (Fig. 3C). Cheilinus approached the food at an approximately horizontal body angle, whereas Epibulus and Oxycheilinus approached the food item from above at a negative body angle with the head pointing down; all three body angles were significantly different (Fig. 3D). There was little modulation (typically less than a 10° change) of body angle for each of the species during their respective feeding sequences. Jaw movements differed between the three species during feeding. Gape distance was significantly larger in Oxycheilinus than Cheilinus and Epibulus, and these differences were still significant when gape was scaled by body length (Fig. 4A). Gape angle was higher in Oxycheilinus and Epibulus than Cheilinus (Fig. 4B). Jaw protrusion was significantly higher in Epibulus than in Cheilinus or Oxycheilinus; these differences were also significant when scaled by body length (Fig. 4C). Cranial elevation was significantly higher in Oxycheilinus than Cheilinus and Epibulus (Fig. 4D). There were no differences between the three species for duration and time to maximum displacement of gape, jaw protrusion, or cranial elevation. As with all wrasses (Walker & Westneat, 2002; Westneat et al., 2004; Thorsen & Westneat, 2005), all three species used pectoral fin propulsion during approach to the prey item. For both fin protraction (Fig. 5A) and abduction (Fig. 5B), the three species exhibited similar patterns of pectoral fin movement in magnitude. The duration of the fin cycles during cruising was 0.18 s in Cheilinus, 0.07 s in Oxycheilinus and 0.12 s in Epibulus. All three species employed a large pectoral fin downstroke as a braking manoeuvre. This started immediately after prey capture and produced a large decrease in velocity, assisting the fishes in moving away from the location of the strike. Braking kinematics for the three species show that Cheilinus and Oxycheilinus primarily use fin protraction to change direction (Fig. 5A), whereas Epibulus uses a pronounced pectoral abduction stroke to come to a stop after prey capture (Fig. 5B). Oxycheilinus and Epibulus had significantly larger pectoral fin displacement in abduction during the braking stroke than did Cheilinus. The eyes of the three species were directed towards the prey item (forward and downward) during approach, and then began to shift back to centre

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B

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C

Figure 2. Representative feeding sequences of Cheilinus fasciatus (A), Oxycheilinus digrammus (B) and Epibulus insidiator (C). Timing of events (s) is indicated in each frame. For comparison of scale, the background grid is 1 cm2.

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Table 1. Results of statistical comparisons between Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insidiator for kinematic variables during feeding

Body movements Maximum velocity (BL s-1) Time to maximum velocity (s) Maximum acceleration (cm s-2) Time to maximum acceleration (s) Maximum body angle (°) Minimum body angle (°) Change in body angle (°) Gape Gape (cm) Adjusted gape (cm BL-1) Gape duration (s) Time to maximum gape (s) Gape angle (°) Jaw protrusion Jaw protrusion (cm) Adjusted jaw protrusion (cm BL-1) Jaw protrusion duration (s) Time to maximum jaw protrusion (s) Cranial elevation Cranial elevation (°) Cranial elevation duration (s) Time to maximum cranial elevation (s) Eye movement Maximum eye distance (cm) Eye movement duration (s) Time to maximum eye distance (s) Pectoral fin movement: cruising Protraction magnitude (°) Protraction duration (s) Abduction magnitude (°) Abduction duration (s) Pectoral fin movement: braking Protraction magnitude (°) Protraction onset (s) Protraction duration (s) Abduction magnitude (°) Abduction onset (s) Abduction duration (s)

Cheilinus

Oxycheilinus

Epibulus

F9,26 ratio

P

1.17 ± 0.20 -0.014 ± 0.031 55.73 ± 17.61 -0.062 ± 0.116 -0.002 ± 4.726 -11.6 ± 4.3 -11.6 ± 1.3

4.30 ± 0.61 -0.095 ± 0.0538 145.86 ± 21.72 -0.089 ± 0.055 -18.78 ± 4.23 -32.7 ± 4.4 -14.0 ± 1.4

13.57 ± 0.65 -0.020 ± 0.008 266.39 ± 25.56 -0.011 ± 0.005 -46.9 ± 3.2 -61.0 ± 3.2 -47.0 ± 3.2

26.7276 0.7639 7.3991 1.2576 7.3991 8.6898 7.3991

0.0001 0.6496 0.0001 0.3053 0.0001 0.0001 0.0001

0.96 ± 0.15 0.060 ± 0.007 0.113 ± 0.023 -0.009 ± 0.006 65.8 ± 7.8

1.76 ± 0.17 0.098 ± 0.009 0.094 ± 0.013 -0.008 ± 0.005 108.3 ± 7.1

0.66 ± 0.080 0.065 ± 0.005 0.084 ± 0.008 -0.005 ± 0.002 103.78 ± 12.08

8.0106 4.7952 1.9437 0.5249 7.2894

0.0001 0.0008 0.0897 0.8430 0.0001

0.7022 ± 0.1010 0.0448 ± 0.0042 0.095 ± 0.010 -0.003 ± 0.006

0.79 ± 0.05 0.045 ± 0.002 0.081 ± 0.008 -0.009 ± 0.005

2.13 ± 0.23 0.213 ± 0.008 0.099 ± 0.010 -0.003 ± 0.002

39.5776 172.2905 1.4952 0.1998

0.0001 0.0001 0.2018 0.9920

9.2 ± 1.5 0.109 ± 0.024 -0.024 ± 0.017

17.0 ± 1.7 0.052 ± 0.004 0.002 ± 0.005

11.91 ± 1.09 0.063 ± 0.012 0.004 ± 0.003

4.6936 1.0835 1.0373

0.0009 0.4073 0.4383

0.17 ± 0.03 0.134 ± 0.037 -0.096 ± 0.016

0.16 ± 0.02 0.076 ± 0.007 -0.027 ± 0.006

0.1014 ± 0.0070 0.103 ± 0.009 -0.036 ± 0.004

1.2621 0.4261 3.1284

0.3030 0.9089 0.0110

25.3 ± 4.0 0.189 ± 0.053 15.6 ± 2.6 0.266 ± 0.065

33.8 ± 4.7 0.077 ± 0.010 24.1 ± 3.3 0.070 ± 0.011

34.2 ± 6.8 0.123 ± 0.028 25.1 ± 2.7 0.129 ± 0.024

1.2822 1.0926 1.3090 1.3488

0.2928 0.4014 0.2797 0.2610

37.2 ± 5.9 0.017 ± 0.026 0.124 ± 0.025 15.8 ± 3.2 0.099 ± 0.023 0.055 ± 0.012

66.7 ± 8.2 0.041 ± 0.012 0.053 ± 0.011 26.5 ± 4.0 0.067 ± 0.014 0.030 ± 0.003

53.4 ± 5.4 0.016 ± 0.013 0.076 ± 0.010 24.6 ± 3.2 0.049 ± 0.010 0.075 ± 0.011

1.5203 0.9683 1.5759 2.5770 2.8963 2.3476

0.1930 0.4874 0.1747 0.0286 0.0163 0.0431

Differences tested for with a nested analysis of variance. Spatial and temporal kinematic values represented by mean ± standard error, taken from individuals and pooled for each species. There were no significant intraspecies differences. P-values in bold indicate significant values after sequential Bonferroni correction (Rice, 1989). Those parameters 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.

immediately before prey capture (Fig. 6A, B). Cheilinus achieved its highest degree of forward direction of the pupil significantly earlier in the strike than either Oxycheilinus or Epibulus (Fig. 6A). There were no differences among the three taxa in either the mag-

nitude or duration of time that the pupil was shifted forward (Fig. 6A). During the approach, the eyes of all three species were directed in a downward orientation towards the prey (Fig. 6B). In Cheilinus, the eyes had almost completely returned to a centred orientation

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Figure 3. Kinematic plots of body movement during the feeding strike in Cheilinus fasciatus, Oxycheilinus digrammus and Epibulus insidiator. A, distance to prey target (cm); B, velocity (body lengths s-1) profile of an individual, representative specimen from each species; C, acceleration (cm s-2) profile of an individual, representative specimen from each species (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 occurs at to, indicated by dashed vertical line. Symbols indicate the mean ± standard error. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 289–308

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Figure 4. Kinematic plots of jaw and head movements during the feeding strike in Cheilinus fasciatus, Oxycheilinus digrammus and Epibulus insidiator. A, gape (cm); B, gape angle (°); C, jaw protrusion (cm); D, cranial elevation (°) versus time for C. fasciatus, O. digrammus, and E. insidiator. Contact with food item occurs at to, indicated by dashed vertical line. Symbols indicate the mean ± standard error. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 289–308

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Figure 5. Angles of pectoral fin movement during the approach and feeding strike in Cheilinus fasciatus, Oxycheilinus digrammus 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 indicate the mean ± standard error.

before the fish reached the prey item, whereas Oxycheilinus and Epibulus still had their eyes directed forward upon reaching the prey (Fig. 6C).

STEREOTYPY

AND COORDINATION PROFILES OF FEEDING

Many of the different kinematic components of the feeding strike for the three species displayed low levels of variability (Fig. 7, Table 2). Almost all kinematic parameters had a coefficient of variation (CV) of less than 1.0, but the more variable features in all three species were associated with the time that elapsed from the beginning of the strike until the achievement of maximum for velocity, maximum body angle, maximum gape, maximum jaw protrusion, and maximum pectoral fin protraction during braking. Most parameters were characterized by a relatively low CV, suggesting a similar degree of stereotypy during the feeding strike for Cheilinus, Oxycheilinus, and Epibulus, despite differences in coordination patterns.

The timing patterns of multiple variables during the feeding sequence were consistent within each species but different among the three species. Cheilinus began to rotate its eyes back to a centred position at the onset of mouth opening (Fig. 8B, C), whereas Oxycheilinus and Epibulus maintained the eyes directed forward until after peak gape was attained and the jaws began to close (Figs 9B, C , 10B, C). Cheilinus began its pectoral fin braking stroke when it achieved peak gape, and as it protracted its fins, and pectoral fin movement was predominantly in the anterior-posterior plane (Fig. 8B, D), with little dorsoventral movement (Fig. 8E). Oxycheilinus and Epibulus initiated their pectoral fin braking stroke at the 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 by Epibulus (Fig. 10D, E). However, all three species demonstrated an increase in velocity at the onset of the strike that was timed with jaw opening (Figs 8A, B, 9A, B, 10A, B).

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Figure 6. Kinematic plots of eye movements during feeding strike in Cheilinus fasciatus, Oxycheilinus digrammus and Epibulus insidiator. A, pupil distance from the centre of the eye (cm) versus time; B, pupil angle (°) versus time; C, pupil distance from the centre of the eye (cm) versus distance from prey item (cm) for C. fasciatus, O. digrammus, and E. insidiator. Schematic eye above figures represents the overall trend of eye movement and angle during the feeding strike. Pupil distances were smoothed with a three-point running average. Dashed line indicates contact with prey item. Symbols indicate the mean ± standard error.

DISCUSSION Analysis of the feeding kinematics of C. fasciatus, E. insidiator, and O. digrammus revealed stereotypical patterns of coordination between the jaws, fins

and eyes in all three species (Fig. 11). Examination of these patterns suggests several components of this behaviour that are important for describing wrasse feeding. Some aspects of the observed feeding behaviours are shared between all of these species, and may

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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 larger CV represents higher variability.

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Table 2. Coefficient of variation values for Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insidiator of the kinematic variables during feeding

Body movements Maximum velocity Time to maximum velocity Maximum acceleration Time to maximum acceleration Maximum body angle Minimum body angle Change in body angle Gape Gape Gape duration Time to maximum gape Gape angle Jaw protrusion Jaw protrusion Jaw protrusion duration Time to maximum jaw protrusion Cranial elevation Cranial elevation Cranial elevation duration Time to maximum cranial elevation Eye movement Maximum eye distance Eye movement duration Time to maximum eye distance Pectoral fin movement: cruising Protraction magnitude Protraction duration Abduction magnitude Abduction duration Pectoral fin movement: braking Protraction magnitude Protraction onset Protraction duration Abduction magnitude Abduction onset Abduction duration

Cheilinus

Oxycheilinus

Epibulus

0.454 ± 0.145 2.747 ± 0.838 0.685 ± 0.050 1.320 ± 0.319 0.907 ± 0.505 1.540 ± 1.177 0.290 ± 0.150

0.493 ± 0.100 1.386 ± 0.202 0.530 ± 0.129 2.163 ± 0.481 1.241 ± 0.573 0.514 ± 0.223 0.262 ± 0.085

0.168 ± 0.049 0.997 ± 0.424 0.175 ± 0.062 1.186 ± 0.283 0.226 ± 0.108 0.161 ± 0.103 0.297 ± 0.082

0.358 ± 0.072 6.652 ± 2.331 0.512 ± 0.139 0.304 ± 0.033

0.264 ± 0.159 3.142 ± 1.848 0.334 ± 0.083 0.194 ± 0.054

0.052 ± 0.023 1.058 ± 0.674 0.256 ± 0.089 0.139 ± 0.019

0.333 ± 0.060 0.184 ± 0.032 7.666 ± 1.978

0.243 ± 0.037 0.329 ± 0.075 3.657 ± 2.062

0.043 ± 0.007 0.133 ± 0.043 1.443 ± 0.289

0.362 ± 0.064 0.598 ± 0.164 1.473 ± 0.048

0.326 ± 0.066 0.264 ± 0.070 3.622 ± 0.614

0.267 ± 0.067 0.348 ± 0.134 1.670 ± 0.211

0.490 ± 0.086 0.309 ± 0.055 0.504 ± 0.127

0.368 ± 0.039 0.320 ± 0.043 1.067 ± 0.268

0.180 ± 0.028 0.310 ± 0.067 0.409 ± 0.115

0.736 ± 0.109 1.714 ± 0.156 0.835 ± 0.154 0.479 ± 0.190

0.562 ± 0.100 0.409 ± 0.101 0.409 ± 0.185 0.522 ± 0.155

0.532 ± 0.171 0.817 ± 0.434 0.381 ± 0.117 0.332 ± 0.107

0.633 ± 0.173 0.736 ± 0.109 1.714 ± 0.156 0.835 ± 0.154 0.479 ± 0.190 0.657 ± 0.103

0.479 ± 0.083 0.892 ± 0.068 0.623 ± 0.063 0.241 ± 0.102 0.682 ± 0.147 0.398 ± 0.028

0.346 ± 0.024 1.155 ± 0.598 0.200 ± 0.041 0.453 ± 0.118 0.758 ± 0.111 0.415 ± 0.068

Data are mean coefficient of variation ± standard error.

represent ancestral conditions for the cheilines, whereas those patterns of coordination that are particular to individual species help describe the diversification of feeding tactics that has occurred within this lineage. Combining this behavioural data with the body of information already available on the skull morphology and dietary habits of these animals suggests that the radiation of cheiline trophic morphology has occurred in conjunction with a diversification of feeding behaviour (Westneat, 1995a; Ferry-Graham et al., 2002), which is reflected in the coordination profiles presented here (Fig. 11).

COORDINATION

OF THE FEEDING STRIKE

All three species maintained a downward-pointing body angle with a relatively constant velocity during their approach to the prey. Their eyes were consistently orientated forward towards the food item, suggesting that visual input is important guiding the fish to the prey (Collin & Shand, 2003). Once the fishes were within less than one body length of the prey, the jaws rapidly opened and closed, the eyes rotated back to a centred position (no longer looking at the original position of the prey), and the

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Figure 8. Selected Cheilinus fasciatus coordination variables, showing the kinematic relationships between different functional 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, indicated by dashed vertical line.

pectoral fins were swept forward and down as a braking manoeuvre (Fig. 11). Cheiline species exhibited several differences in their feeding behaviours. Cheilinus approaches food at a relatively slow and steady rate, whereas Oxycheilinus employs a fast-start-like lunge (cf. Schriefer & Hale, 2004) to initiate an explosive ram-feeding strike. The approach speed of Epibulus is intermediate, until the rapid and extreme protrusion of their jaws (up to two-thirds of the fish’s head length; Westneat & Wainwright, 1989) creates a sudden decrease in the distance between the fish and the food item. As this occurs, the remainder of the body remains nearly stationary. Oxycheilinus had an early onset of peak gape, a large gape angle, and a very rapid gape cycle whereas Cheilinus had the longest gape cycle, smallest gape angle, did not achieve maximal gape until the point of

prey contact, and exhibited the smallest degree of jaw protrusion (Fig. 4). During the approach, Epibulus had patterns of onset times for the different feeding kinematics that were similar to Cheilinus (Fig. 4). However, upon beginning the strike, Epibulus had very rapid changes in gape angle, jaw protrusion, cranial elevation, and exhibited the shortest duration for these variables among the three species. Magnitudes of gape angle and cranial elevation were similar between Epibulus and Oxycheilinus. The approach and strike patterns of Epibulus represents shared features of the feeding components with Cheilinus, as it maintains a slow cruising speed while foraging and positioning itself relative to the food item, but then a rapid strike (initiated at a relatively closer distance to the prey than Oxycheilinus), comparable to other ram-feeding predatory fishes (Westneat & Wainwright, 1989).

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Figure 9. Selected Oxycheilinus digrammus coordination variables, showing the kinematic relationships between different functional 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, indicated by dashed vertical line.

In fish feeding, higher attack speed and larger suction are thought to correlate with an ability to capture more elusive prey (Liem, 1978; Nemeth, 1997a, b), and this association is seen amongst the cheiline wrasses. We suggest that the observed differences between degrees of strike speed, jaw protrusion, and gape correlate with an ability to prey upon evasive animals such as some shrimps and fishes. Cheilinus fasciatus feeds on a diversity of benthic invertebrates including ophiuroids, gastropods (Cerithiidae, Mitridae, Trochidae, Turridae, Triphoridae Epitoniidae, Columbellidae, Strombidae), decapod crustaceans (Paguridae, Xanthidae), and bivalves (Pectinidae, Pteriidae); Oxycheilinus mostly feeds on decapod crustaceans (Portunidae, Xanthidae), stomatopods, and teleosts; Epibulus feeds on decapod crustaceans (Galatheidae, Palaemonidae, Portunidae,

Xanthidae), teleosts, and some gastropods (Cerithiidae, Epitonniidae) (Randall, 1980; Sano, Shimizu & Nose, 1984; Westneat, 1995b, unpubl. data). The main difference in diet composition between these three taxa is that Epibulus and Oxycheilinus have expanded their feeding niche to include predation on fishes and evasive crustaceans (Hobson, 1974; Randall, 1980; Westneat & Wainwright, 1989; Westneat, 1991, 1995a, b; Connell, 1998; Ferry-Graham et al., 2001). The marked differences in jaw protrusion among these three species (Fig. 4C, Table 1) may demonstrate the effect of jaw kinesis in coordinating other processes of overall feeding behaviour. Most importantly, the magnitude of jaw protrusion determines the maximum distance between the predator and the food item at which prey capture can occur (Motta,

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Figure 10. Selected Epibulus insidiator coordination variables, showing the kinematic relationships between different functional 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, indicated by dashed vertical line.

1984; Osse, 1985). By protruding its jaws, a fish adds a component to their overall attack speed that is independent of any locomotor limitations. Jaw protrusion reduces the time that elapses between the onset of an attack and prey contact, and extensive protrusion, especially if it occurs rapidly, can reduce this time dramatically. Increased protrusion allows for a sudden ambush-style strike to surprise and capture the prey, as the prey may base its escape response on the predator’s initial approach speed (Liem, 1978). The extreme jaw protrusion seen in Epibulus, the greatest reported for any fish species (Westneat & Wainwright, 1989; Westneat, 1991), may demonstrate some of the adaptive advantages in the evolution of this morphology, including decreasing the time to prey capture, increasing the time in which the food item remains in the binocular visual field (Motta, 1984; Osse, 1985), and enabling the fish to acquire food items from interstitial

spaces into which the jaws can fit, but not the entire head.

OCULOMOTOR

AND LOCOMOTOR KINEMATICS IN VISUAL PREDATORS

By simultaneously recording coincident locomotor and oculomotor data, we are able to place the patterns of jaw movement within a larger context so as to present a more comprehensive description of feeding behaviour. Vision is one of the dominant sources of sensory input 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 diurnal coral reef fishes, these cheiline wrasses used visual input to guide their approach to the prey item. During the approach, and before the strike, all three species directed the eyes forward, presumably focusing on the

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Figure 11. Schematic representation of kinematic variables representing jaw, fin and eye movements during feeding behaviour in Cheilinus fasciatus, Oxycheilinus digrammus, and Epibulus insidiator. Time period of activity for the variables 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.

prey item (Fernald, 1990; Easter & Nicola, 1997; Collin & Shand, 2003). This is different from the parrotfishes, which do not focus their eyes on the food item at the moment of prey capture, but shift them back to a centred position (Rice & Westneat, 2005); the cheilines’ eyes do not shift back to a centred position until after prey capture occurs (Fig. 6A, C). For parrotfishes feeding on immobile algae, the nonevasive nature of their food may obviate the need for visual input during the last moments of an approach and a more centred position for the pupils may aid in predator detection (Rice & Westneat, 2005). Because the snout may block the binocular visual field at very close ranges (Tamura, 1957; Osse, 1985; Rice & Westneat, 2005), Cheilinus and Oxycheilinus may rely on lateral line input during the final moments of prey capture (Janssen & Corcoran, 1993; New & Kang, 2000; New, Alborg Fewkes & Khan, 2001; New, 2002). However, the extreme jaw protrusion of Epibulus may allow for prey capture to occur when both the prey and the jaws are within the binocular visual field, perhaps allowing for increased accuracy. Because piscivorous fishes are known to use their lateralis system to guide them during the moments of prey capture (Montgomery et al., 2002), it is possible that their braking manoeuvre is delayed until after prey capture so as to avoid excess hydro-

dynamic noise (Higham et al., 2005). Additionally, the braking stroke with the pectoral fins of these predators may delayed until after the feeding strike so as to minimize the visual and hydrodynamic profile apparent to the prey, and decrease their apparent looming threshold (Domenici, 2002). The patterns of fin movement differed among the three species (Figs 5, 8–10), reflective of significant differences related to the coordination of feeding behaviour. Cheilinus used slow and steady propulsive pectoral fin beats to manoeuvre towards its food, whereas Oxycheilinus primarily used a fast-start to lunge towards its food, and employed smaller pectoral fin movements for positioning during the strike. Both Oxycheilinus and Cheilinus displayed a dramatic forward braking stroke that may help prevent collision with the substrate, similar to braking seen in centrarchids and parrotfishes (Higham, 2007; Rice & Westneat, 2005). Epibulus used its pectoral fins for precise manoeuvreing before extending its jaws once it reached an appropriate strike distance, and used a more dorsoventral downstroke after prey capture to retain postural control due to a change in its centre of mass, rather than change directions due to swimming. During these benthic prey capture events, many components of the feeding strike were stereotypical (Fig. 7, Table 2). For almost all parameters investi-

© 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 289–308

CHEILINE WRASSE FEEDING COORDINATION gated (except for fin protraction), Epibulus had the lowest levels of variation. It is likely that the highly derived jaws of Epibulus are stereotypic due to their predation almost exclusively upon evasive prey such as fishes and mobile crustaceans (Hobson, 1974; Randall, 1980; Westneat, 1995b). Conversely, the least consistent behaviours were the onset times for several jaw movement parameters of Cheilinus and Oxycheilinus (Fig. 7B). For Oxycheilinus, this variation might be due to the fast lunge they make towards the food item. The variable modulation of jaw activity may be necessary when there is little time to adjust the targeting of the entire body. The stereotyped benthic feeding behaviour seen in the cheilines may be because the benthic prey items, although varied, do not present dramatically different functional demands for feeding (sensu Bout, 1998) compared to prey 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 the cheilines and those of previously analysed parrotfishes (Rice & Westneat, 2005) have several implications for the evolution of coordination patterns within wrasses as a family. The sister taxon relationship between cheiline wrasses and parrotfishes (Westneat & Alfaro, 2005) requires that all members of both clades evolved from a single ancestor possessing its own patterns of coordination during feeding. From this starting point, the coordination patterns of the cheilines and the parrotfishes diverged to develop two very different feeding ecologies: carnivory and herbivory. This example demonstrates that, in fishes, coordination patterns among multiple functional systems are adaptable and capable of evolving to exploit different ecological niches. The increase in the diversity of feeding behaviours in this radiation provides an example of how the adaptation of coordination patterns may play an important part in trophic evolution. The differences in coordination patterns between the cheilines and scarines may be due to associated consequences of the basic biomechanics of prey capture (e.g., Alfaro, Janovetz & Westneat, 2001; Alfaro & Westneat, 1999; Ferry-Graham et al., 2001; FerryGraham et al., 2002). There is a well-known tradeoff between speed and force in musculoskeletal systems that has powerful implications for morphological design (Alexander, 1968; McMahon, 1984; Vogel, 2003), particularly in fish jaws (Barel, 1983; Westneat, 2003, 2004). Predatory wrasses will often use fast jaw opening to create high suction to dislodge benthic prey (Ferry-Graham et al., 2002), whereas parrotfishes can only remove food from the substrate by applying high forces alone (Bellwood & Choat, 1990; Alfaro & West-

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neat, 1999). Oxycheilinus uses a lunge of the whole body to quickly capture its food, and then uses its small pectoral fins to steer away from the capture site to prevent collision, though there is no change in trajectory. In the slower moving parrotfishes and Cheilinus, there is a slow, deliberate approach, and they use their large pectoral fins to reverse direction to prevent collision with the substrate. For Epibulus, there is little risk in substrate collision, due to their prey capture from a proportionately greater distance and a slower body speed than either the other cheilines or parrotfishes, and thus the pectoral fins are predominantly used for positioning the fish relative to the food item. Oxycheilinus thus provides an example of the coordination patterns during a very fast attack, whereas Cheilinus and the parrotfishes provide examples of coordination patterns that are used during slower prey capture events. Although their diet is more restricted than many other wrasses, the parrotfishes also display an array of feeding strategies and behaviours that are associated with their different dietary preferences (Bellwood & Choat, 1990; Alfaro & Westneat, 1999; Choat, Robbins & Clements, 2002, 2004; Rice & Westneat, 2005). Despite differences in the timing of jaw and body movements, parrotfishes exhibit an extended bite cycle compared to the cheilines, with the mouth achieving peak gape well before contact with the prey item (Rice & Westneat, 2005). Additionally, the parrotfish fins engage in their braking manoeuvre at the point of prey contact, synchronized with jaw closing (Rice & Westneat, 2005), whereas the cheiline fins begin the braking manoeuvre well after the gape cycle completes (Figs 8, 9, 10). The differences in coordination behaviour between the parrotfishes and the cheilines are likely due to the underlying functional requirements for scraping and excavating hard substrate as opposed to capturing evasive or attached prey in a complex environment. For carnivores, the challenge in feeding is in initial procurement and food handling, whereas prey processing after capture is relatively straightforward. Conversely for herbivores, the challenge is not in food procurement but food processing, as many of the ingested materials are indigestible (Choat, 1991; Choat et al., 2002, 2004). The biomechanical tradeoff between food capture and food processing may be incorporated in the resulting coordination patterns of these fishes while feeding. Carnivorous fishes pursuing prey that are fast and mobile must attack quickly to be successful, as they may have only one attempt at a particular potential food item: thus their behaviour is constructed around the acute prey detection and a rapid bite cycle. For herbivores, the primary concern is being able to access stationary food on a stable platform using their fins to assist

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in precise orientation (Choat, 1991). As the parrotfishes do not have to deal with an escaping food item, their eyes are released from focusing on the food and are used in monitoring the surroundings for predators after food is located (Krause & Godin, 1996; Overholtzer & Motta, 2000; Rice & Westneat, 2005), while they execute many repeated bites during a feeding bout (Bellwood & Choat, 1990; Alfaro & Westneat, 1999; Rice & Westneat, 2005). Comparison of parrotfishes and carnivorous cheilines may provide an excellent system in which to continue evolutionary studies of coordination (sensu Choat, 1991). Behaviour is ultimately a combination of many coordinated components within the body of the organism (Bernstein, 1967; Turvey, 1990), and this has important implications for the many studies of functional morphology. Coordination itself is not the principal goal of an organism (Weiss & Jeannerod, 1998), but rather the successful completion of a task such as mating, predator avoidance or food acquisition. Many previous analyses that examined the functioning of individual motor systems in isolation, overlooked the supporting, and often more subtle, contributions of accessory systems to the successful performance of the observed behaviour (Cordo & Gurfinkel, 2003; Massion, Alexandrov & Frolov, 2003). As organisms interact with their environments in multiple ways while performing complex tasks, the functioning of individual physiological systems does not occur in isolation, and it is therefore difficult to understand the functioning of these separate systems without knowing how they are coordinated. We have attempted to integrate functional studies of the visual system and two motor systems in order to achieve a more comprehensive understanding of how complex behaviours are generated and evolve (Lauder, 1986; Lauder & Liem, 1989; McLennan, 1994). Quantitatively analysing and comparing kinematic patterns of coordination between age classes, populations, species, or families will allow for clear demonstrations of how complex ethological units such as feeding behaviour at the organismal level change along ecological 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. Morano and J. G. New for substantive and helpful comments on the manuscript. This project was made possible by grants from the University of Chicago Hinds Fund (A.N.R.), American Society of Ichthyologists and Herpetologists Raney Fund Award (A.N.R.), the LernerGray Memorial Fund for Marine Research (A.N.R.), a

Grant-in-Aid of research from the Society of Integrative and Comparative Biology (A.N.R.), the Chicago chapter of the ARCS Foundation (W.J.C.), a National Science Foundation Doctoral Dissertation Improvement Grant IBN-0308977 (W.J.C., M.W.W.), and grants IBN-0235307 from the National Science Foundation and N000149910184 from the Office of Naval Research (M.W.W.).

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