Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda)

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ZOOLOGY Zoology 111 (2008) 16–29 www.elsevier.de/zool

Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda) Justin R. Grubicha,1, Aaron N. Ricea,b,, Mark W. Westneata a

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

b

Received 2 April 2007; received in revised form 10 May 2007; accepted 11 May 2007

Abstract The great barracuda, Sphyraena barracuda, is a voracious marine predator that captures fish with a swift ram feeding strike. While aspects of its ram feeding kinematics have been examined, an unexamined aspect of their feeding strategy is the bite mechanism used to process prey. Barracuda can attack fish larger than the gape of their jaws, and in order to swallow large prey, can sever their prey into pieces with powerful jaws replete with sharp cutting teeth. Our study examines the functional morphology and biomechanics of ‘ram-biting’ behavior in great barracuda where the posterior portions of the oral jaws are used to slice through prey. Using fresh fish and preserved museum specimens, we examined the jaw mechanism of an ontogenetic series of barracuda ranging from 20 g to 8.2 kg. Jaw functional morphology was described from dissections of fresh specimens and bite mechanics were determined from jaw morphometrics using the software MandibLever (v3.2). High-speed video of barracuda biting (1500 frames s1) revealed that prey are impacted at the corner of the mouth during capture in an orthogonal position where rapid repeated bites and short lateral headshakes result in cutting the prey in two. Predicted dynamic force output of the lower jaw nearly doubles from the tip to the corner of the mouth reaching as high as 58 N in large individuals. A robust palatine bone embedded with large dagger-like teeth opposes the mandible at the rear of the jaws providing for a scissor-like bite capable of shearing through the flesh and bone of its prey. r 2007 Elsevier GmbH. All rights reserved. Keywords: Prey capture strategy; Bite force; Jaw biomechanics; Ram biting; Teeth

Introduction The great barracuda, Sphyraena barracuda, is an apex predator common throughout the world’s tropical seas, Corresponding author. Present address: Department of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853-2702, USA. Tel.: +1 607 254 4373; fax: +1 607 254 1303. E-mail address: [email protected] (A.N. Rice). 1 Present address: Bureau of Oceans and International Environmental and Scientific Affairs, U.S. Department of State, Washington, DC 20520, USA.

0944-2006/$ - see front matter r 2007 Elsevier GmbH. All rights reserved. doi:10.1016/j.zool.2007.05.003

among coral reefs, sea grass beds, mangrove estuaries, and pelagic environments. Its diet consists almost entirely of fishes (97% of stomach contents) and adults can grow over 2 m in length (Gudger, 1918; de Sylva, 1963; Randall, 1967; Blaber, 1982; Schmidt, 1989; Barreiros et al., 2002). S. barracuda is a swift piscivore that uses its acute visual and olfactory senses to locate prey (Sinha, 1987). It attacks prey with rapid swimming speed (12 m s1; Walters, 1966) and captures prey with its long serrated jaws, slicing into the flesh with a multitude of sharp caniniform teeth. While attacks on

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humans are rare (Wright, 1948; de Sylva, 1963) de Sylva (1963) documented 29 barracuda attacks on humans between 1873 and 1962, some of which resulted in limb amputations and even death. In contrast to most shark attacks, these ferocious barracuda attacks are perpetrated by considerably smaller fish (o40 kg) (Wright, 1948), a fact that underscores the potentially tremendous cutting forces in their bite. Indeed, large barracuda can quickly dispatch large prey by severing them in two (Yasuda, 1960; de Sylva, 1963; Randall, 1967; Porter and Motta, 2004). Examination of the stomach contents and prey items of the barracuda suggests that its feeding habits may be unique in comparison to other fishes: there are numerous reports of only ‘‘back-halves’’ of prey items found in barracuda stomachs (de Sylva, 1963; Randall, 1967). However, the dynamics and mechanisms of great barracuda feeding have received little attention. The kinematics of the strike of S. barracuda has been described in small juvenile fish (o200 mm) (Porter and Motta, 2004), and the feeding morphology has been investigated (Gudger, 1918; Gregory, 1933; de Sylva, 1963); yet, no study has examined the functional morphology and biomechanics of their powerful cutting jaws. Biomechanical models can provide important insight into the force and motion involved in animal behavior (e.g., Alexander, 2003; Koehl, 2003; Westneat, 2003). Recent theoretical models for the lever mechanics of the lower jaw have incorporated muscle contraction kinetics to analyze jaw mechanisms as a dynamic (rather than static) system by including the geometry and properties of the adductor muscles that power jaw closing (Westneat, 2003). Lever models in fish skulls have great potential for testing hypotheses of mechanical design in a diversity of fishes and for developing ideas of functional transformation during growth and development (Westneat, 2004; Alfaro et al., 2005). Recent studies of jaw modeling (e.g., Wainwright et al., 2004; Westneat et al., 2005) have generally cited Barel (1983) and Westneat (1994) as early applications of lever mechanics for fish jaws. However, we note here that in fact it was Gregory (1933, p. 414) who apparently first identified the third class lever arrangement in the lower jaws of fishes, using an illustration of S. barracuda as his example. Our study expands on Gregory’s original work by exploring the ontogeny and functional morphology of the great barracuda feeding mechanism and generating predictions of its bite force and jaw kinetics based on lever mechanics. We have three primary goals with this study: (1) to qualitatively describe the jaw morphology and kinematics of the unusual ‘ram-biting’ feeding behavior in S. barracuda; (2) to examine scaling patterns in the jaw musculature, lever mechanics, and bite forces of barracuda ranging from newly settled juveniles to adult body sizes; and (3) to dynamically model the

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theoretical bite performance of barracudas from jaw morphometrics to elucidate the underlying mechanics of their prey severing ability.

Materials and methods Specimen collection and dissection Seven great barracudas (S. barracuda) across a large range of body sizes (20–8200 g; Table 1) were dissected to describe scaling of jaw functional morphology and bite mechanics. Four specimens were collected live in the Florida Keys by hook and line, and three were analyzed from the fish collection at the Field Museum of Natural History in Chicago (FMNH Lots: 43992, 58510). The right-lateral side of the head was dissected to expose the muscle subdivisions of the adductor mandibulae complex and the ligaments and bones of the upper and the lower jaws. Digital photos of the dissections were taken with a Nikon 5000 CoolPix camera to clarify certain aspects of the morphology.

Functional morphology and behavior The musculoskeletal architecture of the upper and lower jaws is described from dissections of fresh specimens, digital photos and illustrations using the anatomical nomenclature of Gregory (1933) and Winterbottom (1974). To examine the bite pattern of S. barracuda, small blocks of gelatin (3 cm  2 cm  1 cm) were placed in the jaws of barracuda specimens (N ¼ 3), and the jaws were slowly closed by hand. Care was taken not to completely section the gelatin blocks to preserve the bite impression and the shape of the tooth marks. Blocks were removed and stained with 30% ethanol and alcian blue to visually highlight the bite marks. To establish whether biting prey into pieces is part of the feeding repertoire of juvenile S. barracuda, capture and processing behaviors were recorded at 1500 frames s1 from a juvenile specimen acquired through the aquarium trade (30.1 cm total length), using a Basler A504 k high-speed digital video camera (Basler Vision Technologies, Exton, PA, USA) to qualitatively describe the kinematics of the ram strike and biting, and provide quantitative estimates for use in mechanical modeling. The fish was trained to feed on live, large goldfish prey held in forceps.

Scaling of jaw muscles and bite mechanics As important components of bite strength, muscle masses of the adductor mandibulae subdivisions A1, A2 and A3 (Fig. 1) that function in closing the jaws were

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Table 1. corner

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Results of bite mechanics for Sphyraena barracuda calculated by MandibLever 3.2 at two jaw positions, jaw tip and jaw

Individual (mass [g])

Jaw position

A2 MA

A3 MA

A2 Force

A3 Force

Dynamic bite force

Static bite force

1 (20)

Tip Corner Tip Corner Tip Corner Tip Corner Tip Corner Tip Corner Tip Corner

0.37 0.56 0.35 0.57 0.37 0.64 0.36 0.58 0.33 0.57 0.35 0.54 0.32 0.54

0.3 0.44 0.27 0.43 0.26 0.45 0.29 0.47 0.26 0.45 0.27 0.43 0.24 0.41

0.10 0.15 0.17 0.27 0.82 1.42 0.97 1.59 1.81 3.10 3.58 5.59 8.47 13.95

0.13 0.20 0.19 0.31 0.84 1.45 1.71 2.79 2.57 4.40 4.50 7.03 8.19 14.99

0.48 0.71 0.71 1.15 3.32 5.72 5.36 8.76 8.75 15.00 16.17 25.24 33.23 57.88

0.61 0.90 0.90 1.45 4.19 7.23 6.77 11.06 11.05 18.95 20.43 31.89 42.09 73.11

2 (41) 3 (400) 4 (700) 5 (1100) 6 (2900) 7 (8200)

Mechanical advantage (MA) of the lever for each muscle, and bite force attributed to each muscle (one side of the head) are listed. Dynamic bite force is the peak estimate of total adductor muscle contraction (bilateral) using assumptions of the Hill equation and the effective mechanical advantage of the muscles through the bite cycle (see text for model parameters). Static bite force is the total bilateral bite force at maximum theoretical force potential of the adductor muscles through the simple lever mechanics of the jaw in its closed position.

weighed to the nearest gram and plotted against body mass to determine their scaling relationships. Digital photographs of the dissected specimen were taken with a Nikon CoolPix 5000. Muscle attachments, muscle lengths, lower jaw dimensions and lever ratios were measured from digitized anatomical landmarks of the jaws using the modified QuickImage software (Walker, 1999) following the protocol of MandibLever 3.2 (Westneat, 2003). These morphometrics along with specimen adductor muscle masses for the A2 and A3 subdivisions were analyzed with the MandibLever 3.2 lower jaw model to generate predictions of mechanical advantage, effective mechanical advantage, A2 and A3 muscle torque, individual bite power, and dynamic and static bite forces in S. barracuda. Model simulations assume a muscular-specific force capacity of 200 kPa, an intrinsic shortening velocity of 10 lengths s–1 for muscle fibers (Westneat, 2003), a jaw opening duration of 20 ms, and opening angle of 201 (measured from video sequences of feeding strikes, Fig. 1). We also ran simulations with a lower muscle contraction speed (Vmax of 5 lengths s1) for large individuals. Two sets of data were taken for each individual that marked different outlever positions of the lower jaw: jaw tip (large single canine), jaw corner (tooth position that corresponds to the overlapping premaxilla and opposes the middle of the toothed palatine bone). Results of MandibLever simulations as the lower jaws are drawn close were plotted for the two tooth positions of the largest individual and then corrected for body size among all individuals to examine morphometric variation in bite simulations.

The null scaling hypothesis was that jaw muscle masses would scale isometrically with body mass, and that bite force would scale isometrically to the square of length (the 0.67 power of body mass), due to muscle force being proportional to muscle cross-sectional area. Adductor muscle mass, muscle torque, and predicted total dynamic bite force for each of the two lower jaw positions were analyzed with a least-squares regression against body mass to examine how jaw morphology, jaw biomechanics, and bite strength change with growth in S. barracuda.

Fig. 1. Illustration of musculoskeletal anatomy of the head and jaws of Sphyraena barracuda. Musculature includes the three subdivisions of the adductor mandibulae complex: A1, A2 and A3. Bone abbreviations: Art, articular; Dent, dentary; Iop, interopercular; Max, maxilla; Op, opercular; Pal, palatine; Pre, preopercular; Premax, premaxilla; Qd, quadrate; Soc, supraoccipital crest.

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Results Jaw anatomy and feeding behavior The signature morphology of S. barracuda jaws is the spear-like under-bite of the mandible that projects beyond the upper jaws into a conical cartilaginous point. One to two large, recurved fang-like canines protrude from this symphysis that connects the two bilateral elements and fits neatly in a recess between the anterior-most canines of the upper jaws (Figs. 1 and 2). The mandible is composed of two bones: (1) an elongate tapering blade-like dentary and (2) a roughly triangular articular. On the dentary, a series of flat triangular teeth are aligned in palisade fashion in sockets extending posteriorly nearly to the coronoid process of the

Fig. 2. (A) Dissection of S. barracuda jaw anatomy showing lines of actions of adductor mandibulae muscle subdivisions that control biting (a1, a2, a3). (B) Skeletal elements of the lower jaw and suspensorium revealing lever mechanics and the robust toothed palatine bone against which the rear of the lower jaw bites in a scissor-like action. Note the architectural similarity to man-made bone shears (inset) where two long opposing blades slide past each other and generate cutting forces at the intersection. Arrows (tip, mid, corner) indicate outlever positions on the lower jaw that result in increasing mechanical advantage towards the corner of the jaw that opposes the palatine bone. The jaw morphology thus mimics scissor mechanics where cutting forces are greatest near the hinge or jaw joint. Arrow a2 demonstrates the effective mechanical advantage (a) of the A2 muscle on the closing inlever. The enlarged palatoquadrate cartilage that likely absorbs impact and bite forces during the strike is shown and its relative position within the palatine bone is indicated.

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articular bone (Figs. 1 and 2B). The articular bone has a deeper lateral profile and constitutes the posterior third of the mandible. It provides the insertion sites for the A2 and A3 muscle subdivisions and has a stalwart dorsally oriented saddle at its posterior end that forms the fulcrum of the jaw joint with the quadrate (Figs. 1 and 2B). The biting elements of the upper jaws are made up of the maxilla, premaxilla and palatine. The maxilla and premaxilla are tightly fitted along their lengths by strong connective tissue and function as a single anteriorly swinging unit. There is no protrusion of the premaxilla as the jaws are opened; however, the tip is mobile and lined with two bilateral pairs of large canine teeth. Opening the jaws pivots the maxilla at the palatomaxillary joint and, in turn, dorsally rotates the ascending rami of the premaxilla resulting in the recurved teeth pointing forward at an increased angle (Fig. 2A). In the closed position, the elongate maxilla/ premaxilla bones extend posteriorly to a position just below the eye. The lateral posterior extending process of the premaxilla is serrated with many small canine teeth (Fig. 2A). From the quadrate, the ectopterygoid bone arches anteriorly suturing into a hollow cavity at the posterior end of a robust palatine bone (Fig. 2A). The palatine has a deep lateral profile and is buttressed with thick bone at the anterior end. Ventrally, it has six to eight large canines seated in sockets that medially oppose the rear dentary teeth of the lower jaw. Anteriorly, it has a large palato-maxillary hinge joint that attaches via ligaments to the anterior condyle of the maxilla and medially to the cartilaginous symphysis of the premaxilla bones. Invested within the hollow cavity at the posterior end of the bone is an enlarged cone-shaped palatoquadrate cartilage (Fig. 2B). The jaw closing muscles of barracuda, the adductor mandibulae complex, is composed of three distinct subdivisions: A1, A2 and A3 (Fig. 1). The A2 and A3 subdivisions are the primary bite force muscles, are roughly equal in size, and have highly effective mechanical advantages at the jaw corners resulting in maximal adductor muscle force transmitted into bite force which will be discussed below (Table 1). Architecturally, A2 and A3 are predominantly fusiform muscles while A1 appears to have both parallel fibers and some pennate fiber bundles (Fig. 1). The A2 is the most ventral subdivision originating on the anterior face of the preopercle, crossing the suspensorium at a shallow angle, and inserting along the dorso-posterior edge of the coronoid process of the articular bone of the mandible. A3 originates high up on the sphenotic and hyomandibular bones and approaches the lower jaw at a much steeper angle crossing just beneath the eye and medial to the A2 to insert via a long tendon onto the Meckelian fossa at the junction of the articular and

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dentary bones. A1 has the most anterior position originating in front of the eye on the infraorbitals and ectopterygoid bone and traversing between the lateral protective lacrimal bone and the medial palatine bone to insert through a short robust tendon onto the anterior condyle of the maxilla. A tendinous sheet extends ventrally from this insertion point connecting along the medial edge of the descending process of the maxilla all the way to the maxillo-mandibular ligament (Fig. 2A). More ventrally positioned fibers of the A1 insert into this sheet at oblique angles indicating pennation. The musculoskeletal design of the lower jaws in barracuda is arranged as a typical third class lever (Fig. 2B). The closing inlevers are defined as the distances between the jaw joint and muscle insertions of the A2 and A3 on the mandible. The opening inlever is the distance between the jaw joint and the interopercular–mandibular ligament. In most studies of fish feeding, the outlever has been classically defined as the distance between the jaw joint and the tip of the jaws. In barracuda, this distance creates a long outlever indicating a fast but relatively weak bite at the tip. However, as noted above, the mandible is lined with sharp triangular teeth along its length. When the distances of these rear teeth are defined as outlevers, the length reduces by approximately half at the corner of the jaws increasing its mechanical advantage (Fig. 2B). Bite patterns of the barracuda jaw mechanism in gelatin molds illustrate the shearing action of these shorter outlevers (Fig. 3). Upon closing the jaws, the rear dentary teeth slice past two dorsal rows of functionally different teeth: (1) laterally, the small serrating teeth of the premaxilla and (2) medially, the large impaling teeth of the palatine. Juvenile barracudas have a fast strike, usually completing jaw opening and closing within 40–50 ms (Fig. 4A). Barracudas employ a ram-feeding mode to capture large prey by slamming into the prey with extremely high body velocity. The strike begins with rapid acceleration towards the prey from an S-start body posture (with the anterior section of the body bending in one direction, and the posterior end of the body bending in the opposite direction), typical of many piscivores (Schriefer and Hale, 2004). Maximum gape occurs in approximately 20–30 ms. During jaw opening, the mandible rotates ventrally 201 and the maxilla and toothed premaxilla swing forward. The jaws are rapidly closed (approximately 20 ms) once the prey makes contact with the mobile maxilla/premaxilla at the back of the jaws. Jaw kinematics after capture show that the mandible and particularly the posterior region of the jaws are instrumental in biting into the prey with a scissor-like mechanism (Fig. 4B). Barracudas process large prey with a series of powerful bites and rapid lateral headshakes. In several instances, post-capture

Fig. 3. Bite impression from the teeth of Sphyraena barracuda in a gelatin mold. The biting pattern demonstrates the position of the palatine and rear dentary teeth when the jaws are closed. The different rows of teeth are offset from one another, inducing a fracture pattern towards one another, facilitating the rapid cutting of the teeth through fish skin and flesh.

biting observed in the juvenile barracuda in this study resulted in severing the prey into pieces. Bite duration during processing cycles is similar to the jaw kinematics of the initial capture (Fig. 4B).

Jaw mechanics and bite forces The simulated mechanics of muscle contraction and resultant jaw biomechanics of the largest specimen of S. barracuda in the study (Figs. 5 and 6) illustrate the transfer of forces from muscle, through the mandibular lever, to the bite point at the teeth. The MandibLever simulation initially involves rotating the jaw open to a starting angle of 201 (see online supplemental figure at Appendix A), and then simulating the mechanics of jaw closing. Simulating a peak closing speed of 10 muscle lengths s1 generally resulted in a total time to close the jaws of 30–40 ms, similar to kinematic measures of feeding performance. If large barracudas have slower muscles (5 lengths s1), their closing duration would be double that value, around 75 ms. As the A2 and A3 muscles begin to contract from the stretched position, their contractile force is low but increases to its maximum at the closed position, according to the Hill equation (Fig. 5A). The raw mechanical advantages

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Fig. 4. (A) Kinematic sequence of a juvenile great barracuda (TL ¼ 30.1 cm) exhibiting ram-biting feeding strategy on a live goldfish prey. Maximum jaw rotation during the strike was estimated as 201 with QuickImage and was used as the initial jaw opening parameter in MandibLever 3.2. Note gape closing does not begin until the oversized prey impacts the extended premaxilla/maxilla at the back corner of the jaws (40–47 ms). (B) Biting sequence of a juvenile great barracuda (TL ¼ 30.1 cm) processing the prey after capture with successive cutting bites of the jaws likened to shearing actions of scissors. A rapid bite proceeds (bite cycle duration ¼ 41 ms) with the prey held in an orthogonal position at the back of the jaws. Nearly complete gape closure results in the teeth inflicting deep slicing cuts into the prey. Feeding events were filmed at 1500 frames s1.

(MA) of the jaw lever at the jaw tip and at the mouth corner are the static lever ratios of inlever divided by outlever, as if the muscle were pulling at 901 to the inlever (Table 1). However, the effective mechanical advantage (EMA, Fig. 5B) is always lower than the

mechanical advantage (MA, Table 1). For example, A2 EMA is usually just 60–80% of raw MA values due to the angle of insertion of the A2 muscle on the jaw (Westneat, 2003). As the jaw rotates closed, the angle of insertion of the muscle onto the jaw increases, and

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approaches (but never reaches) the theoretical maximum MA at jaw closing (Fig. 5B). Assuming that a prey item is clamped between the jaws, the torque on the lower jaw (the force multiplied by the lever arm) increases rapidly due to the higher muscular forces and the higher EMA as the jaw closes (Fig. 5C). The bite force components produced by each of the A2 and A3 muscles (Fig. 5D) are the resultant of the jaw lever torque at the tip and rear teeth. For the individual barracuda illustrated in Fig. 5, the A2 and A3 forces are remarkably similar (Fig. 5D), but the peak forces reached at jaw closing for the broader sample of fish (Table 1) show that they are not always equal in bite force contribution. Total dynamic bite force at any time during jaw closing is obtained by summing the A2 and A3 bite force contributions at a particular bite location,

and multiplying by two, assuming that the A2 and A3 muscles on the other side of the head are exerting the same effort. Maximal dynamic bite forces (Table 1) are such sums for each specimen at the point of jaw closing. Estimated dynamic bite forces from the tip to the jaw corner ranged from 0.48 to 0.71 N in a 20 g fish to 33.2–57.9 N in the largest barracuda we analyzed (8.2 kg; Table 1). For comparison, the static bite force is also given in Table 1, in which the Hill equation is not used and the muscle is assumed to exert its maximal force per unit area of 200 kPa. Finally, the work (Fig. 5E) and power curve (Fig. 5F) are illustrated for the major jaw muscles of the largest barracuda specimen. Summary plots for the seven barracudas (Fig. 6) illustrate the variability in some of the metrics computed, when accounting for the size range of individuals

Fig. 5. Results of muscle modeling of the A2 ( ) and A3 ( ) muscle subdivisions of a large Sphyraena barracuda (8.2 kg). (A) Contractile force of the muscle increases as it shortens, according to standard Hill equation muscle kinetics. (B) The effective mechanical advantage (EMA) of the muscle subdivisions at tip and rear of the jaw also increases as the jaw closes. (C) Torque, the ability of the muscle to produce a rotational moment on the jaw. (D) Bite force is greatest at the rear of the jaw at closed position. (E) Work done by the jaw muscles during jaw closing. (F) Power output of the muscles is maximal at intermediate values of force and speed.

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Fig. 6. Kinematics and selected muscle modeling parameters averaged over seven S. barracuda specimens. (A) Gape, the distance between upper and lower jaw tips, (B) the force profile of the A3 muscle, (C) the effective mechanical advantage of the A3 muscle, (D) the torque generated by the A3 muscle, (E) the bite force generated by the A3 muscle, (F) total bite force, the bite force generated by the A2 and A3 muscles on both sides of the head, (G) work performed by the A3 muscle, (H) power profile of the A3 muscle. Error bars are standard errors of the mean.

modeled. As gape distance (Fig. 6A) decreases to zero, the raw contractile force of the jaw muscles increases (Fig. 6B, the A3 is shown). The EMA (Fig. 6C) shows remarkably low variability, indicating that the basic lever dimensions and muscle insertion angles are relatively constant across the size range. Average torque (Fig. 6D), A3 bite force (Fig. 6E), total bite force (Fig. 6F) and work (Fig. 6G) all show large error bars due to the importance of muscle mass scaling in these variables. Muscle power (Fig. 6H) shows relatively low variance. Adductor muscle masses scale isometrically with total body mass for each of the three subdivisions (slopes: A2 ¼ 1.0; A3 ¼ 0.99; A1 ¼ 0.98) with A2 and A3 being approximately twice the size of A1 across body size

(Fig. 7A). Muscle torque for A2 and A3 also reveals isometry, with A3 consistently contributing slightly more torque to the bite throughout ontogeny (Fig. 7B). Dynamic bite forces scale with positive allometry (larger barracudas have proportionately larger bite forces than small barracudas) for both the jaw tip and rear tooth positions (i.e. slopes 40.67), but are 1.5 times greater at the corner of the jaws reflecting the increase in MA from a shorter jaw outlever (Fig. 8).

Discussion The jaws and teeth of the great barracuda are built for impaling and then quickly slicing their piscine prey.

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ram strike followed by biting with a scissor-like cutting motion of the jaws.

Ram-biting in barracudas

Fig. 7. (A) Ontogenetic scaling relationships of adductor muscle masses against body size showing isometry for all three subdivisions, A1 ( ), A2 ( ), and A3 ( ). Note that A2 and A3 which both act to adduct the lower jaw during biting are equal in size and considerably larger than A1 which retracts and stabilizes the upper jaw. (B) Log plot of predicted mean muscle torque for A2 and A3 subdivisions against body size indicating isometry during growth and suggesting slightly greater torque is placed on the lower jaw from the A3.

The anatomy of the lower jaw reveals a strong third class lever mechanism that maximizes force from the adductor muscles through an increased mechanical advantage at the rear of the mandible. Dynamic simulations and static modeling of barracuda jaw mechanics predict moderate bite forces that, when transmitted through the razor sharp teeth, can produce tremendous flesh slicing pressures. This force generating capacity in combination with the scissor-like morphology of a serrated lower jaw that slides past a robust toothed palatine bone produces a shearing bite capable of cutting large fish prey into smaller manageable pieces for swallowing. Barracuda bite forces scale with positive allometry, suggesting that larger fish may use the prey slicing technique to a greater degree than small individuals. Barracudas employ a specialized feeding mode that we describe here as ram-biting, that involves a

Great barracudas are exemplary ram-feeding fishes in the sense that they use rapid body acceleration to capture their prey, yet unlike most ram feeders, they complete the strike with a powerful slicing bite. We suggest that this feeding strategy of barracudas is a combination of typical ram-feeding and biting modes and should be referred to as ram-biting behavior. Descriptive jaw kinematics of prey capture reveal that the jaws reach maximum gape, the hyoid is depressed, and the opercles are opened well before reaching the prey to presumably diminish bow wave effects during the attack (Fig. 4A; VanDamme and Aerts, 1997). Minimal compensatory suction is generated only after the tips of the nonprotrusible jaws have overtaken the prey (Fig. 1A; also see Porter and Motta, 2004). Additional quantitative strike kinematics of juvenile barracuda feeding on small prey corroborate our findings for the timing of the expansive phase of the strike (Porter and Motta, 2004). However, what is unique about barracuda feeding is that with prey items that are too large to be swallowed whole, the compressive phase of the strike results in ramming the fish and pinning it in the back of the jaws where a forceful cutting bite is quickly applied (Fig. 4A, see supplemental movie at Appendix A). If the prey is not initially severed, a succession of repeated shearing bites, manipulations, and rapid lateral headshakes immediately ensues until the prey is cut into manageable pieces (Fig. 4B). This feeding strategy of literally ramming into large prey harkens back to the Greek etymology of the genus name Sphyraena, which means hammerfish (see Gudger, 1918). Indeed, the high swimming velocity of barracudas during the strike (i.e., 7.5–10 body lengths s–1) (Gero, 1952; Walters, 1966) is certainly contributing a substantial inertial component of locomotor force in addition to the bite force from the jaw mechanism that facilitates impaling and cutting into the prey. For example, the ballistic force for a 9 kg fish swimming at 12 ms (Walters, 1966) accelerating over a strike duration of 150 ms (Porter and Motta, 2004) results in a force of 720 N. This body momentum taken together with the theoretical dynamic bite force generated at the jaw corner for a similar-sized barracuda results in approximately 780 N of force that is transmitted through the teeth to the prey upon impact. Aspects of the jaw morphology also appear to be modified for impaling prey during the ramming attack. First, the palatine teeth show a rostral inclination at the thickened anterior end, and second, the large fang-like canines of the premaxilla angularly rotate forward

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Fig. 8. Ontogenetic scaling relationships of total dynamic bite force of the lower jaws of S. barracuda for two jaw positions: tip (n) and corner (J) (see inset). Predicted dynamic bite force scales with strong positive allometry (slopes 40.67) across body size for both tooth positions and increases by a factor of 1.5 from the tip to the corner of the jaws where an increase in strength facilitates shearing prey in the scissor-like jaws.

during jaw opening (Figs. 2 and 4; Gudger, 1918). In addition, the presence of the large palatoquadrate cartilage within the palatine bone suggests a shock absorber function to protect the eye orbit from these high impact forces during the strike and subsequent bites (Fig. 2B). The ram-biting jaw mechanism appears to be a key morphological trait of the Sphyraenidae that is present in fossil forms dating back to the Eocene (see references in Gudger, 1918; de Sylva, 1963). Several fish groups have palatine tooth pads with grasping teeth including primitive lineages such as Amia calva and more advanced Actinopterygians like salmonids (Gregory, 1933). However, with the possible exception of the members of the family Paralepididae (Gregory, 1933) – the appropriately named, but unrelated, barracudinas – we are unaware of any other fish groups that possess a posterior jaw architecture similar to the barracuda (Fig. 2). Diet studies and observations of other barracuda species (Sphyraena viridensis, Sphyraena pinguis, and Sphyraena guachancho) indicate that this ram-biting ability and its underlying morphology may be a functional innovation of the family that enables them to be top level predators in marine habitats (Yasuda, 1960; Barreiros et al., 2002). This rare ability among bony fishes is similar to the feeding mode of megacarnivorous sharks (Dean et al., 2005) or the extinct Dunkleosteus (Anderson and Westneat, 2007), which devour oversized prey by gouging and cutting them into pieces. The moderate bite forces predicted by MandibLever allude to the important functional roles of the teeth and

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jaw arrangement in barracuda feeding mechanics. The jaws of the barracuda have four morphologically different tooth types (Fig. 2) (Gudger, 1918). As mentioned earlier, the large anterior fang-like canines at the jaw tips are used for impaling and grasping elusive fish prey upon capture and preventing escape during manipulation. The dagger-shaped palatine and small caniniform premaxillary tooth rows of the upper jaws are laterally spaced apart, and when the jaw closes, the mandibular teeth fill this gape (Fig. 3; Gudger, 1918). This anatomical configuration creates an effective cutting mechanism, and as Gudger (1918) notes, ‘‘Held in such teeth, no fish can escape save by leaving part of itself behind.’’ We predict that the three sets of teeth function locally as a series of blades coming together which serve to section the prey through point cutting (sensu Evans and Sanson, 2003), and that the closing of the jaws provides sufficient force for the teeth to puncture and propagate cracks through the prey item. Computational modeling predicted a maximum static bite force of 73.1 N at the jaw corners for the largest individual in our study (Table 1). This is lower than that of many smaller durophagous fishes, several reptiles, and some mammals of similar and even smaller body sizes that have been measured or modeled (Herrel et al., 2001; Huber et al., 2005). We suggest that the mechanical demands of barracuda teeth to slice through fish flesh do not require substantially high bite forces, as seen in other mechanical methodologies and configurations (e.g., Dunajski, 1980; Sigurgisladottir et al., 1999; Veland and Torrissen, 1999). Generally, barracuda teeth have a cutting edge or piercing tip that is less than 1 mm2. It is notable that, with regard to the sharpness of the canines (area of the tooth tip: 0.54 mm2), a dynamic bite force of 33 N at the large canine at the end of the lower jaw can theoretically produce a puncturing bite pressure of over 61 MPa. The ability of the barracuda to section its prey results from a combination of the biomechanical architecture of the jaws, their force generating capacity (e.g., Westneat, 1994, 2003), and the sharpness and shape of the teeth (Frazzetta, 1988; Osborn, 1996; Korioth et al., 1997; Popowics and Fortelius, 1997; Evans and Sanson, 1998, 2003; Shergold and Fleck, 2004; Freeman and Lemen, 2006). Thus, with its razor sharp teeth, powerful jaws, and fast swimming speed, the barracuda is literally able to bite its prey items in half during the initial attack; few other fishes possess this unique ram-biting feeding ability.

Modeling bite performance in barracudas Computational modeling provides the first theoretical estimates of jaw mechanics and bite force for S. barracuda. The substantial increase in mechanical

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advantage and subsequently bite forces from the jaw tip to the corner illustrates the importance of the bite position at the rear teeth for increasing force generation through lever mechanics (Table 1; Figs. 2, 5, 8). In vivo studies of bite force in dogfish (Squalus acanthias) and bats support our predictions by showing that posterior bite positions along the mandible increase force in a similar fashion (Dumont and Herrel, 2003; Huber and Motta, 2004), as these posterior positions along the oral jaws are closer to the jaw joint, and have a much higher mechanical advantage, than at the anterior jaw tip. Westneat (2004) identified the opening and closing jaw lever ratios of barracuda (i.e., outlever measured to the jaw tip) as being modified for speed in order to capture evasive fish prey. A general principle of fish feeding ecomorphology is that of a mechanical tradeoff between force and velocity in jaw motions that results from morphological variations in the opening and closing lever ratios of the mandible (e.g., Westneat, 1994; Wainwright and Richard, 1995; Wainwright and Bellwood, 2002; Westneat et al., 2005). This tradeoff is present in each lever system (consisting of muscle to mandible to bite-point), in that these systems cannot be both fast and forceful. However, we conclude here that the architecture of the barracuda lower jaw exhibits two mechanisms that allow it to circumvent this biomechanical constraint. First, the subdivision of the adductor mandibulae muscle into two major units that attach to the mandible at different places (Fig. 2A) allows the possession of a high (A2) and a low (A3) mechanical advantage for the mandible (Table 1). This was identified recently (Westneat, 2003) as one of the important biomechanical consequences of jaw muscle subdivision. In addition, the specialization of the teeth into a long row of shearing teeth fronted by long impaling canines allows each muscle-lever system to have a range of closing lever ratios (by varying the bite point) that provide not only quickness at the tip for capture but strength at the corner for cutting (Figs. 2 and 8). Recent models of suction feeding and jaw closure in clariid catfishes have shown that hydrodynamic forces are important features in modeling the speed and force of prey capture (Van Wassenbergh et al., 2005). A similar approach has also been used to model suction feeding in centrachid fishes (Carroll et al., 2004) and to calculate the added water mass and maximum opening speed of large fossil fishes (Anderson and Westneat, 2007). For many fishes with fast jaw opening and closing, accurately modeling speed would require that the added body mass and the effects of the animal’s acceleration reaction be incorporated into the raw force and speed computations currently provided by the MandibLever software. However, the relatively slow shearing bite of the barracuda after prey contact is not likely to be affected by these hydrodynamic

considerations. Furthermore, it should be noted that the maximum bite forces computed for the jaws assume that the jaws have closed upon a prey item and that the muscles are relatively isometric (constant length) removing the necessity of hydrodynamic factors in the model. An important area of future development of the model is to incorporate hydrodynamic effects on jaw motions and allow the user to model the system in multiple ways. The large size, fiber arrangement, and angles of insertion of barracuda jaw adductors ensure that effective muscle forces are transmitted through the lower jaw to puncture and cut the prey during jaw closure (Figs. 1 and 2). Indeed, the dynamic increase in EMA as the gape angle closes results in a 24% increase (on average) in force transmission from the muscles to the jaws as they close on the prey (Fig. 5B and D). Empirical comparisons of gape angle and bite force in a number of different biting species such as bats and clariid catfishes document similar results (Dumont and Herrel, 2003; Van Wassenbergh et al., 2005). The similar sizes of the A2 and A3 muscles throughout ontogeny indicate their functionally complementary roles in generating large torques and bite forces for shearing prey (Figs. 5–7). The biomechanical prediction that maximum bite power is achieved at approximately 2/3 of jaw closure when oversize prey are most likely to be pinned between the jaws further reflects the capacity of S. barracuda to dismember prey (Figs. 5F and 6H). Deciphering the lever mechanics of the A1 subdivision is a crucial next step in modeling fish jaw kinetics. In great barracuda, the A1 shows an unusual rostral migration in front of the eye onto the lateral face of the palatine. Its line of action and broad variable insertion onto the maxilla suggest it not only retracts but provides muscular stabilization for the upper jaws to facilitate point cutting and resist the dorsally directed bite forces from the mandible. Future studies of feeding in barracudas might investigate the muscle activity patterns of the A1 subdivision to determine its functional role. Its isolated position will enable easy electrode implantation and reduce potential crosstalk with the other adductor subdivisions to facilitate electromyography recordings of the timing and intensity of its contractions during ram biting.

Ecomorphology of feeding on large prey Studies of feeding ability in fishes have shown that the diameter of a fish’s mouth is a generally good predictor of the maximum prey size a fish can successfully capture and consume (Yasuda, 1960; Werner, 1974; Wainwright and Richard, 1995). Typically, the optimal prey size (i.e. body depth) for suction feeding fishes where the greatest

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net energy return is achieved ranges from 40% to 70% of the predator’s mouth diameter (Werner, 1974; Kislalioglu and Gibson, 1976a, b; Werner, 1977; Hoyle and Keast, 1987; Wainwright and Richard, 1995). However, great barracudas are renowned for attacking and eating prey much larger than the gape or width of their jaws (Gudger, 1918; de Sylva, 1963; Randall, 1967). Indeed, large adult barracudas (2 m total length) can sever 1 m long amberjack, Seriola dumerili, in half (Grubich, pers. obs.). This extreme biting ability is not restricted to large individuals, as the juvenile barracuda (30 cm) in this study could also decapitate large goldfish. However, we found that bite force scales with positive allometry across the lower jaw (Fig. 8), suggesting that the importance of prey slicing behavior may increase with increasing predator size. This positive allometry of bite force scaling is similar to that seen in sharks (Huber et al., 2006), lizards and turtles (Herrel and O’Reilly, 2006) and finches (van der Meij and Bout, 2004). Thus, while the size of the oral jaw aperture is a morphological constraint for many ram-suction feeding fishes, great barracudas have combined a rapid ram strike for prey capture with a powerful shearing bite for processing that allows them to feed on much larger prey resources. Being able to consume larger prey may provide greater energy returns per feeding bout for barracudas. To our knowledge, the ecomorphology of this extreme feeding mode of ram biting has received little attention in piscivorous bony fishes compared to the several studies of manipulation by benthic invertebrate feeders and herbivorous reef fishes (Bellwood and Choat, 1990; Wainwright and Turingan, 1993; Hernandez and Motta, 1997; Alfaro and Westneat, 1999; Wainwright et al., 2004). Other marine piscivores that may employ this ram-biting behavior include the bluefish (Pomatomus saltatrix), the mackerels (Scomberomorus sp.), and wahoo (Acanthocybium solandri). In fact, juvenile bluefish which have sharp interdigitating canines on the upper and lower jaws shift foraging modes from swallowing prey whole to biting them into pieces when available prey reach lengths approximately a third of their body length (Juanes and Conover, 1994; Scharf et al., 1997). We suggest the scissor-like jaw morphology of great barracudas enhances their feeding performance as apex predators through the ability to quickly dismember large prey and thereby reduce the effects of gape limitation on prey handling.

Acknowledgments We would like to thank Jason Schratwieser of the IGFA and Sherri Hitz of the Pigeon Key Foundation for help in procuring fresh specimens. This research was funded by NSF IBN-0235307 to M.W. Westneat.

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Appendix A. Supplementary materials Supplementary data associated with this article can be found in the online version at doi:10.1016/j.zool.2007. 05.003

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