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This article was published in an Elsevier journal. The attached copy
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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
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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.
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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.
J.R. Grubich et al. / Zoology 111 (2008) 162922
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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.
J.R. Grubich et al. / Zoology 111 (2008) 162924
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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.
J.R. Grubich et al. / Zoology 111 (2008) 1629 25
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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) 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
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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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