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ZOOLOGYZoology 111 (2008) 1629

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

Justin R. Grubicha,1, Aaron N. Ricea,b,, Mark W. Westneata

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

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 worlds tropical seas,

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 2m 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 (1 2 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

ARTICLE IN PRESS

www.elsevier.de/zool

0944-2006/$- see front matter r 2007 Elsevier GmbH. All rights reserved.

doi:10.1016/j.zool.2007.05.003

Corresponding author. Present address: Department of Neurobiol-

ogy and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca,

NY 14853-2702, USA. Tel.: +1 607254 4373; fax: +1 607254 1303.

E-mail address: [email protected] (A.N. Rice).1Present address: Bureau of Oceans and International Environ-

mental and Scientific Affairs, U.S. Department of State, Washington,

DC 20520, USA.


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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 perpe-trated by considerably smaller fish (o40kg) (Wright,

1948), a fact that underscores the potentially tremen-

dous 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 (o200mm) (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 thanstatic) 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 develop-

ment (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 ofS. barracuda as

his example.

Our study expands on Gregorys 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 inS. barracuda; (2) to examine scaling patterns

in the jaw musculature, lever mechanics, and bite forces

of barracuda ranging from newly settled juveniles toadult body sizes; and (3) to dynamically model the

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 (208200 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 themuscle subdivisions of the adductor mandibulae com-

plex 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) andWinterbottom (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 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 acquiredthrough 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, A2and A3 (Fig. 1) that function in closing the jaws were

ARTICLE IN PRESS

J.R. Grubich et al. / Zoology 111 (2008) 1629 17


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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 thejaws 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 s1 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 (Vmaxof 5lengthss1) 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 inbite 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 predictedtotal 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.

ARTICLE IN PRESS

Fig. 1. Illustration of musculoskeletal anatomy of the head

and jaws ofSphyraena 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.

Table 1. Results of bite mechanics forSphyraena barracudacalculated by MandibLever 3.2 at two jaw positions, jaw tip and jaw

corner

Individual (mass [g]) Jaw position A2 MA A3 MA A2 Force A3 Force Dynamic bite force Static bite force

1 (20) Tip 0.37 0.3 0.10 0.13 0.48 0.61Corner 0.56 0.44 0.15 0.20 0.71 0.90

2 (41) Tip 0.35 0.27 0.17 0.19 0.71 0.90

Corner 0.57 0.43 0.27 0.31 1.15 1.45

3 (400) Tip 0.37 0.26 0.82 0.84 3.32 4.19

Corner 0.64 0.45 1.42 1.45 5.72 7.23

4 (700) Tip 0.36 0.29 0.97 1.71 5.36 6.77

Corner 0.58 0.47 1.59 2.79 8.76 11.06

5 (1100) Tip 0.33 0.26 1.81 2.57 8.75 11.05

Corner 0.57 0.45 3.10 4.40 15.00 18.95

6 (2900) Tip 0.35 0.27 3.58 4.50 16.17 20.43

Corner 0.54 0.43 5.59 7.03 25.24 31.89

7 (8200) Tip 0.32 0.24 8.47 8.19 33.23 42.09

Corner 0.54 0.41 13.95 14.99 57.88 73.11

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.

J.R. Grubich et al. / Zoology 111 (2008) 162918


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Results

Jaw anatomy and feeding behavior

The signature morphology ofS. barracudajaws is thespear-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

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 formsthe 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 palato-

maxillary 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 jointthat 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). Archi-

tecturally, 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 theMeckelian fossa at the junction of the articular and

ARTICLE IN PRESS

Fig. 2. (A) Dissection ofS. barracuda jaw anatomy showing

lines of actions of adductor mandibulae muscle subdivisions

that control biting (a1, a2, a3). (B) Skeletal elements of thelower 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 shownand its relative position within the palatine bone is indicated.



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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 theanterior 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 inter-

opercularmandibular 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 indicat-

ing 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 shorteroutlevers (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 4050 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 2030 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 rapidlateral headshakes. In several instances, post-capture

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 3040 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 Hillequation (Fig. 5A). The raw mechanical advantages

ARTICLE IN PRESS

Fig. 3. Bite impression from the teeth ofSphyraena 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.



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(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 mechanicaladvantage (EMA, Fig. 5B) is always lower than the

mechanical advantage (MA,Table 1). For example, A2

EMA is usually just 6080% 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 ofinsertion of the muscle onto the jaw increases, and

ARTICLE IN PRESS

Fig. 4. (A) Kinematic sequence of a juvenile great barracuda (TL 30.1 cm) exhibiting ram-biting feeding strategy on a live goldfish

prey. Maximum jaw rotation during the strike was estimated as 20 1 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 (4047 ms). (B) Biting sequence of a juvenile great barracuda (TL 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 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 s 1.



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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 highermuscular 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 inFig. 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 thejaw corner ranged from 0.48 to 0.71 N in a 20 g fish to

33.257.9 N in the largest barracuda we analyzed (8.2 kg;

Table 1). For comparison, the static bite force is also

given inTable 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 com-

puted, when accounting for the size range of individuals

ARTICLE IN PRESS

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 forceand speed.



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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 1.0; A3 0.99; A1 0.98) with A2 and A3 beingapproximately 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 builtfor impaling and then quickly slicing their piscine prey.

ARTICLE IN PRESS

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.



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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 morphol-

ogy 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 feedingmode that we describe here asram-biting,that involves a

ram strike followed by biting with a scissor-like cutting

motion of the jaws.

Ram-biting in barracudas

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, seesupplemental movie at Appendix A). If the prey is not

initially severed, a succession of repeated shearing bites,

manipulations, and rapid lateral headshakes immedi-

ately 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

(seeGudger, 1918). Indeed, the high swimming velocity

of barracudas during the strike (i.e., 7.510 body

lengths s1) (Gero, 1952; Walters, 1966) is certainly

contributing a substantial inertial component of loco-

motor 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 gener-

ated at the jaw corner for a similar-sized barracuda

results in approximately 780 N of force that is trans-

mitted 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-likecanines of the premaxilla angularly rotate forward

ARTICLE IN PRESS

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.



11/15

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 subsequentbites (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 asAmia calvaand more advanced

Actinopterygians like salmonids (Gregory, 1933). How-

ever, 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, andSphyraena 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 MandibLeverallude to the important functional roles of the teeth and

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 elusivefish 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

(sensuEvans 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 configura-

tions (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 theore-

tical estimates of jaw mechanics and bite force forS. barracuda. The substantial increase in mechanical

ARTICLE IN PRESS

Fig. 8. Ontogenetic scaling relationships of total dynamic biteforce of the lower jaws ofS. 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.



12/15

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) andbats 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 Bell-

wood, 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 biomecha-

nical 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) mechanicaladvantage 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 animals

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 contactis 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 themodel. 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. 57). 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 fishs 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

ARTICLE IN PRESS



13/15

net energy return is achieved ranges from 40% to 70%

of the predators 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 attackingand 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 OReilly, 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 severalstudies 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 blue-

fish 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 wasfunded by NSF IBN-0235307 to M.W. Westneat.

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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