Marine Biology (1998) 131: 703±718
L. A. Ferry-Graham
Feeding kinematics of hatchling swellsharks, Cephaloscyllium ventriosum
(Scyliorhinidae): the importance of predator size
Received: 17 June 1997 / Accepted: 6 March 1998
Abstract Capture, manipulation, and transport of prey
were quanti®ed from high-speed video of hatchling
swellsharks, Cephaloscyllium ventriosum. Kinematic
variables were contrasted with those of 1 yr-old swell-
sharks. Hatchling prey-captures were ram-dominated,
while 1 yr-old prey-capture events had a detectable
suction component. Timing di€erences between kine-
matic patterns of the age groups were not detected.
Signi®cant di€erences in displacement maxima of kine-
matic variables between the two age groups during
feeding were detected, but were consistent with the ex-
pectations of isometry; they doubled in accordance with
a doubling in shark length. A scaling analysis con®rmed
that swellsharks grow isometrically. A simple model of
the head during prey capture con®rmed that buccal ex-
pansion scaled isometrically between age groups. Thus,
this study suggests that hatchlings generally perform the
suite of movements necessary for suction generation
within the buccal cavity during feeding. A suction
component to the strike, however, was generally not
detected by the ``ram:suction index''. It appears that
although it is probably generated within the buccal
cavity, suction has little e€ect on the prey item and
makes a minimal contribution to prey capture. Suction
may be ine€ective due to the highly active nature of the
hatchlings. During a strike, a hatchling's forward loco-
motion may be sucient to overwhelm any suction
produced by the expanding buccal cavity; thus, the
swimming shark e€ectively ``scoops'' the prey up in its
open mouth (i.e. ram feeding) before the prey can be
entrained in the ¯ow of water entering the mouth (i.e.
suction feeding). It is also likely that the hatchling sharks
are suciently small to render any suction generated
ine€ective. Even though the sharks scale isometrically,
Communicated by M.F. Strathmann, Friday Harbor
L.A. Ferry Graham
Department of Ecology and Evolutionary Biology,
University of California, Irvine,
California 92697-2525, USA
Ó Springer-Verlag 1998
the sheer size of the 1 yr-old sharks allows a greater
amount of force to be generated, that will ultimately
draw the prey to the open mouth. Thus, there are ab-
solute consequences of size for feeding behaviors.
Introduction
The importance of predatory experience to the devel-
opment of feeding behaviors has been investigated for
many teleost ®shes (e.g. Atlantic salmon, Salmo salar,
Coughlin 1991; largemouth bass, Micropterus salmoides,
Colgan et al. 1986; anchovy, Engraulis mordax, Hunter
1972). These studies have demonstrated that predatory
experience may be a primary determinant of prey-cap-
ture mode (Coughlin 1991, 1994) and feeding success
(Hunter 1972; Colgan et al. 1986; Coughlin 1991;
Wanzenbock 1992). The majority of these studies,
however, have addressed changes in behavior over major
ontogenetic transitions, mainly the morphological tran-
sition from larva to juvenile (for an exception see Cook
1996). Thus, it is dicult to discount alternative hy-
potheses that may explain changes in feeding behavior,
such as a change in maneuverability with size (see
Blaxter and Staines 1971), or a change in mouth size or
structure with age (see Liem 1990).
Swellsharks, Cephaloscyllium ventriosum (Carcharhi-
niformes: Scyliorhindae), were chosen as subjects to in-
vestigate hypotheses related to predatory experience and
its e€ect on prey capture and transport behaviors be-
cause, like all sharks, they do not have a larval stage of
development. Thus, their development does not include
an extreme morphological transition after the onset of
exogenous feeding that could potentially confound be-
havioral observations. In nature, eggs are laid and then
abandoned by the female shark. Long tendrils attach the
drifting egg cases to benthic vegetation and sessile or-
ganisms (Castro 1983; Compagno 1984). After hatching,
the yolk reserves are depleted (Edwards 1920; Ferry-
Graham personal observations) and acquisition of en-
ergy is paramount for survival. Frazzetta and Prange
704
(1987) hypothesized that, in general, due to a lack of
experience, young sharks should use suction to capture
prey items. The alternative, ram feeding, whereby the
predator overtakes and engulfs the prey item in its open
mouth, should require more stealth, and presumably
more skill or predatory experience. Feeding by hatchling
or newborn sharks of any species has not previously
been described.
In this paper, I describe the kinematic pattern of
capture, manipulation, and transport of prey by hatch-
ling Cephaloscyllium ventriosum. I also examine the hy-
pothesis that predatory experience is of major
importance by contrasting the kinematic patterns of
hatchlings with the previously studied kinematics of
1 yr-old, predatorily experienced C. ventriosum. Di€er-
ences detected between age groups, however, does not
necessarily prove that there is an e€ect of predatory
experience. I therefore tested for the potential con-
founding e€ect of changing predator morphology by
using a scaling analysis of morphometric data across a
wide size range of C. ventriosum; the null hypothesis is
that the species grows isometrically, and there are no
morphological changes between the hatchling and 1 yr-
old life-history stage. If behavioral changes between age
groups do not scale in a manner consistent with the
pattern of growth, e€ects of predatory experience can be
inferred.
To understand the functional consequence of poten-
tial kinematic and morphologic di€erences between age
groups of sharks, I constructed a simple model of the
relaxed and fully expanded buccal cavity for both
hatchling and 1 yr-old Cephaloscyllium ventriosum. The
model allows investigation of the potential e€ects of
both changes in displacement maxima and changes in
morphology. The model is not dynamic, and is meant
only to serve as a tool for visualizing any e€ects of be-
havior or morphology on the buccal cavity. Isometric
growth, used as the null hypothesis (H0) in the scaling
analysis, predicts that volume changes rapidly, scaling as
the cubed function of length. Buccal volume must be
proportionately much greater in 1 yr-olds than in
hatchling sharks. Since such a di€erence could have an
impact on the total suction produced, the model was
also used to estimate change in buccal volume during
prey capture. Thus, the questions examined are: (1) Are
there di€erences in feeding behaviors between hatchling
and 1 yr-old C. ventriosum? (2) Can they be explained
by growth alone? (3) Is growth alone enough to cause
performance consequences? (4) Or are there indications
of an e€ect of predatory experience on feeding behav-
iors?
Materials and methods
Kinematics
Cephaloscyllium ventriosum is an ideal species for study because
adults are oviparous and eggs are easily collected and reared in the
laboratory. Hatching in the laboratory is generally successful, with
minimum e€ort in terms of egg maintenance. For the kinematic
study, egg cases of C. ventriosum were obtained from aquaria or
collected o€ the coast of Santa Barbara, California, USA. They
were tagged and housed together in a 400-liter recirculating tank in
the laboratory and maintained at 18 °C ‹ 2 C°. At hatching,
sharks were sexed and measured (see following paragraphs), and
then placed into 80-liter tanks, maintained at 18 °C ‹ 0.5 C°, for
®lming. Food was o€ered to the hatchling sharks daily or every
other day until the ®rst prey capture occurred.
The prey o€ered, thawed shrimp (Caridea) and smelt (Ather-
inidae), were chosen to facilitate comparison with previous work
(see Ferry-Graham 1997) and to re¯ect the natural prey these
sharks might encounter (see Compagno 1984). Prey pieces were cut
into cubes with sides approximately one-half of the width of the
individual shark's mouth. Prey items were o€ered by placing the
piece of meat on the base of the tank by means of forceps, which
were then removed as quickly as possible. The shark, initially sta-
tionary or swimming, was videotaped as it approached and cap-
tured (the ®rst bite that contacted the prey, also referred to as the
strike), manipulated (additional bites), and transported (taking the
prey fully into the esophagus) the prey. Each food-o€ering event
was videotaped at 250 ®elds s)1 with a NAC HSV-500 high-speed
video camera (described in detail by Ferry-Graham 1997). Two
video cameras were used to simultaneously record a lateral and
ventral view of the feeding sharks. Individual sharks were allowed
to return to their pre-feeding behavior prior to introduction of
another prey item. Four individuals (average total length
(TL) ˆ 15.8 cm; range ˆ 15.5 to 16.3 cm) were successfully vid-
eo-taped. Four feeding sequences were obtained from each indi-
vidual in which the head and jaws were clearly visible and the shark
remained nearly perpendicular to the cameras.
Analysis of video sequences followed the protocol described by
Ferry-Graham (1997). Landmarks (Fig. 1) were digitized on the
video images at 0.024 s intervals starting at ``time zero'' (t0), 0.072 s
prior to the onset of rapid mouth opening. The digitized frame rate
was increased to 0.012 s intervals just prior to maximal mouth
opening, or maximum gape angle, and throughout prey transport.
At the onset of prey transport, or rapid mouth re-opening, t0 was
again determined so that the duration of the two events could be
compared. The coordinate data obtained from the digitized frames
were used to calculate cephalic displacements or kinematic vari-
ables. The rostral margin of the orbit was used as a reference to
determine relative movement of two other points on the head (see
Fig. 1a: lateral view). By subtracting the resting orbit-to-buccal
expansion point distance, absolute displacements (cm) of the hyoid
and buccal region were determined for each time interval (see Ta-
ble 1). Head thickness or depth, and head width were measured at
the ®rst gill arch and at the pectoral ®n insertion (Fig. 1a). Jaw
width was also determined for reference. Head angle (degrees) was
measured as a positive or negative angle relative to the midline of
the body, and gape angle was the angle created between the upper
and lower jaws (Fig. 1b). How these points on the shark head
correspond to actual cartilaginous elements can be seen in Fig. 2.
Strike variables were also determined for prey capture and
transport events if possible. Instantaneous predator velocity
(cm s)1) was calculated for the ®rst three digitized frames of both
the capture and transport phases of the feeding event and an av-
erage value at each t0 is presented. The forward distance moved was
calculated from the ventral view of the pectoral ®n insertion-point.
Predator±prey distance (cm) during capture was determined by
measuring from the anterior tip of a shark's lower jaw to the
leading edge of the prey item. When possible, the ram:suction index
(RSI; Norton and Brainerd 1993) was used to determine propor-
tionally how much ram or suction behavior contributed to a prey
capture event. For this;
ÿ
ÿ
RSI ˆ Dpredator ÿ Dprey : Dpredator ‡ Dprey ;


where D distance traveled by either the predator or the prey from
the onset of mouth opening to the time at which the prey item ®rst
enters the mouth. Dpredator was measured from a reference point on
the background grid to the tip of the lower jaw. This avoided any
confounding e€ect of upper-jaw protrusion. Dprey was measured

HDgill1
FO HDfin
a
UJ
LJ Lateral
H VB
HWgill1
HWfin
JW
Ventral
b HA
GA Lateral
c
Lateral
Fig. 1 Cephaloscyllium ventriosum. Traces from NAC video-camera
image of shark biting a prey item. a Simultaneous lateral and ventral
views; relevant distances calculated between digitized points (black
dots) are two head-depth measurements (HDgill1 and HD®n), front of
orbit (FO) to hyoid element (H), and FO to ventral surface of buccal
region at the center of expansion (VB); note that hyoid is depressed in
this image, and the resting FO to H distance would be subtracted to
determine absolute hyoid displacement; lower jaw tip (LJ), and upper
jaw tip (UJ) are also labeled; ventral view shows the two head-width
(HW) measurements, and the jaw-width (JW) measurement. b Head
angle (HA), with a plane parallel to tank base (dashed line), and gape
angle (GA). c Polygon used to estimate functional buccal volume
(dotted lines indicate thicknesses measured by transecting the heads of
preserved individuals); points used for digitizing have been removed
from Graph c for clarity (Modi®ed after Ferry-Graham 1997)
from the same reference point to the edge of the prey nearest the
shark's mouth. RSI can take on values between 1 (a purely ram
strike) and )1 (a purely suction strike). Values between 1 and )1
re¯ect a combination of behaviors.
Cephalic displacement maxima and timing variables (times of
maxima and minima) for hatchling sharks were contrasted with a
previous study of feeding by 1 yr-old Cephaloscyllium ventriosum
(N ˆ 5; average TL ˆ 30.0 cm; range ˆ 23.6±37.0 cm). Princi-
pal-components analysis (PCA) was used on the entire data set to
reduce the many cephalic variables to three independent linear
combinations of variables that could be used in a multivariate
analysis of covariance (MANCOVA; see Table 2). The MANC-
OVA is limited to three variables by the level of within-cell
replication. The correlation matrix was used to determine princi-
pal-component (PC) scores so that variable groupings would not be
a€ected by the units of measure (i.e. cm, degrees). The MANCOVA
was used to compare the ®xed factors of feeding phase (capture vs
transport) and age (hatchling vs one-year old sharks). The covar-
iate of head length was also included in the analyses to account for
the size di€erence between age groups that necessarily exists. A full
705
Neurocranium
Orbit
1 cm
Neurocranium
Rostral Orbit
cartilages
Hyomandibula Hyoid
Palatoquadrate Ceratohyal elements
(upper jaw)
Mandible
(lower jaw)
Fig. 2 Cephaloscyllium ventriosum. Camera lucida drawings of dorsal
and lateral views of skull and related morphological elements from
cleared and stained hatchlings (N ˆ 3). Specimens did not remain
intact through clearing and staining process, so x-radiographs of a
similarly sized individual were used to determine intact position of jaw
cartilages
model that contained all interaction terms was used to test for
signi®cant interaction among the factors and covariate (Super-
ANOVA statistical software package). When interactions were not
detected, the results of the model without the interaction terms was
used. Cochran's tests (Winer 1971) veri®ed that variances were
homogeneous within these variables at the smallest level tested; the
age ´ phase ´ head length interaction. It was assumed that these
analyses were robust to deviations from normality (Underwood
1981).
Prey manipulation was not included in the phase factor of the
above analysis because manipulation bites did not always occur.
Instead, a repeated measures ANCOVA (Systat statistical soft-
ware) was used to detect trends between subsequent bites on the
prey item. Bites 1 ( ˆ capture) and 2 ( ˆ manipulation) were in-
cluded in the repeated measures analyses, since second bites oc-
curred with enough frequency for suitable replication (N ˆ 14
feeding events with ³2 bites). Only ®ve feeding events from both
age groups combined contained 3 bites, and a single event from a
1 yr-old individual had a total of 4 bites. Bite number was treated
as a ``within'' factor in the analysis, while the ``among'' factor of
age and the covariate, head length, were also included in the re-
peated measures ANCOVA model. Prior to performing the
ANCOVAs, PCA was again used to reduce the multiple-bite da-
taset to a few non-correlated variables (see Table 3). This separate
PCA was required because the dataset available for this portion of
the global analysis was small and the previous analyses would
have been reduced to a trivial amount of data had a single, uni®ed
PCA been attempted. Signi®cance levels for these ANCOVAs
were corrected using a Bonferroni correction for conducting sep-
arate tests of the same null hypothesis on multiple dependent
variables.
706
Morphometrics and scaling
A morphometric scaling analysis was used to investigate potential
changes in the head and jaws with size, and potentially to remove
shape as a confounding factor in other analyses. Preserved indi-
viduals (N ˆ 12) were placed on a marked reference grid and
imaged by a SVHS video camera mounted on a tripod. Dorsal,
lateral and ventral views were obtained. Still images of live indi-
viduals (N ˆ 2; not used in the kinematic analysis) were obtained
with the two-camera system described in the previous subsection.
Individuals ranged in size from 14.7 to 77.8 cm TL. A truss net-
work (sensu Bookstein et al. 1985) was created to determine 13
pertinent distances on the head and body (Fig. 3). The resulting
morphometric variables included many of the measurements in the
kinematic analysis as well as additional lengths on the head and
body of the shark for determining general growth relationships (see
Table 4).
Regressions (Systat statistical software) were used to contrast
each morphometric variable (dependent variable) against TL (in-
dependent variable). All data were log-transformed. The slopes and
®t (r2) of the resulting regressions were determined. Student's t-tests
determined if the observed slopes were signi®cantly di€erent from
1, since linear morphologic features should grow at the same rate as
TL if isometric growth is occurring. A Bonferroni correction was
used to determine the signi®cance of individual tests. In addition to
a severe reduction in power caused by the Bonferroni correction,
this analysis su€ered, as might be expected, from collinearity
among the multiple dependent variables. To rectify this, a multi-
variate analysis that is similar in logic to the two PCAs described
earlier was also performed on the entire dataset. Bookstein et al.
(1985) described a PCA method whereby the covariance matrix is
used to estimate component loading-scores. The raw variables must
be in the same units (e.g. cm), and must be log-transformed to
approximately standardize them to their respective means. If all
variables load positively and equally on the ®rst principal compo-
nent, then isometry can be assumed. The primary strength of this
analysis was that it was not dependent upon acceptance of a null
hypothesis to show isometry, as were the regression analyses.
Variables from the kinematic analysis were subsequently se-
lected (post-hoc) to determine if movements by the sharks con-
formed to the predictions of isometry. Since a doubling in length
(TL) occurred between the two age groups used in the kinematic
analysis, values for a displacement variable for 1 yr-old sharks
could be tested using Student's t-tests against double the value for
the variable for hatchling sharks; the prediction being that the
values should have doubled over the age groups studied. Power
analysis was performed on all non-signi®cant tests using the sta-
Fig. 3 Cephaloscyllium ven-
triosum. Trace of still image
used to create truss network
of measurements for mor-
phometric analysis. Lateral
and ventral views were ob-
tained separately. Continuous
straight lines indicate dis-
tances calculated for each
individual; dashed lines indi-
cate endpoints used to mea-
sure head length and total
length. Paired distances
(those measured on both
right and left side of each
individual) were averaged
and mean was used in anal-
yses
tistical software package G-Power (Macintosh Verson 2.1.1;
A. Buchner, F. Faul, E. Erdfelder, University of Trier, Germany).
For all power analyses, the power to detect an e€ect size of 20%
was estimated.
Modeling the buccal cavity, and potential hydrodynamic e€ects
To determine the change in buccal volume, this was estimated for a
relaxed (pre-feeding) condition and multiple fully expanded con-
ditions (at the time of peak hyoid depression, peak buccal expan-
sion, and peak gape if they did not occur simultaneously) in each
individual used in the kinematic analysis. Coordinate data were
used to estimate the maximum functional buccal volume, rather
than an absolute estimate obtained by ®lling the buccal cavity with
a molding agent. Maximum functional buccal volume, veri®ed by
viewing video footage, is considerably smaller than the absolute
maximum volume that can be measured through direct manipula-
tion of dead specimens. Kinematic coordinates for the following
variables were used: the tip of the upper jaw (UJ), tip of the lower
jaw (LJ), hyoid (H), ventral buccal surface at the point of maxi-
mum depression of the region during the kinematic analysis (VB),
and the pectoral ®n insertion-point combined with the point im-
mediately dorsal to the pectoral ®n insertion (HD®n on Fig. 1). To
convert external coordinate data to internal coordinate data, three
additional preserved individuals of sizes approximately represent-
ing hatchling and 1 yr-old sharks (18.3 to 27.1 cm) were transected,
and the thickness of the dorsal and ventral musculoskeletal ele-
ments at the hyoid, the ventral buccal expansion region, the pec-
toral ®n insertion, and the dorsal surface over the pectoral ®n
insertion were determined (see Fig. 1c). This thickness, expressed as
a percentage of total head depth, was consistent among the three
sharks measured. This value was used to adjust the Y coordinates
of the appropriate kinematic variables in order to recreate the in-
ternal shape of the buccal cavity in lateral view. The internal shape
of the cavity was modeled by plotting the sets of coordinates on a
standard Cartesian coordinate grid to form a polygon (Fig. 1c).
The polygon was subsequently divided into triangular sections for
the determination of surface areas which were then combined to
estimate a two-dimensional (lateral or X, Y view) buccal-surface
area. This surface area was multiplied by mouth diameter to esti-
mate buccal volume. This had the e€ect of modeling the mouth
opening as a rectangle. This estimate provided values '20%
greater than if a circle had been used to approximate the area of the
open mouth and the buccal volume calculated as a cylinder; how-
ever, it is presumed that the former is more accurate, because the
shape of the mouth, open or closed, is not circular.
Lateral
Ventral

Changes in buccal volume were used to approximate a ``¯ow
index'' for water drawn into the newly expanded buccal region.
This provides an estimate independent from the actual movement
of the shark or the prey item (which is a€ected by its own density
and surface area, and the position of the shark as it moves for-
ward). Thus, it is free of the problems associated with RSI values.
The ¯ow index (cm s)1) was calculated by ®rst estimating an ``ex-
pansion index'', or the change in buccal volume divided by the
surface area of the open mouth. The change in volume was deter-
mined as the maximum volume (cm3) estimated by the model minus
the starting ( ˆ minimum) volume. Surface area of the mouth was
determined as the jaw width multiplied by the peak gape (cm2). The
expansion index (cm) divided by the time taken for expansion(s)
estimated the ¯ow index. Index estimates for the two age groups
were compared using a Student's t-test.
Results
Kinematics of prey capture
As might be expected, hatchling sharks rarely missed the
non-elusive prey items provided in this experiment. Prey
capture by hatchling Cephaloscyllium ventriosum con-
sisted of a ram-dominated strike (Fig. 4), whereby the
prey item was often actually pushed away by the lower
jaw of the shark as it swam forward. Hatchling sharks
generally swam slowly around the tank prior to feeding,
and a fairly constant velocity of 3 cm s)1 was main-
tained throughout the feeding event (Table 1). The av-
erage predator±prey distance at the onset of the strike
was only 0.19 cm (Table 1), yet the distance moved by
the predator from the onset until the time the prey
707
entered the mouth, or Dpredator, was 0.63 cm (Table 1).
This means that the prey items were pushed an average
of 0.44 cm and that RSI values were often >1 (Table 1).
Thus, the ram:suction index is generally not appropriate
for analyzing the mode of prey capture used by hatch-
ling sharks. For 1 yr-olds, capture of similarly scaled
prey was also ram-dominated, but a suction component
was evident from the ram:suction index; RSI values fell
between )0.58 and 0.86 (Table 1). Extremely limited
RSI data suggested that hatchling sharks probably could
produce suction during prey capture, as four strikes
from three di€erent individuals were recorded with RSI
values from 0.09 to 0.85. Presumably, during these
strikes the hatchlings' locomotory behavior did not
overwhelm the generation of suction by the expanding
buccal region. These particular events were not neces-
sarily the last feeding events recorded (i.e. Strike 4) for a
Fig. 4 Cephaloscyllium ventriosum. Composite of two-camera video
images of successful strike by hatchling swellshark. Time (min:s:ms) is
indicated in upper left corner of each image; background grid contains
2 cm squares. Frames A±D Prey capture: mouth opening (beginning
in Frame A), maximum gape angle (reached in Frame B), and hyoid
depression (evident by Frame C); note that prey item moves forward
with the shark, as indicated by diminishing distance between arrows
identifying trailing edge of prey item (leading edge is entering shark's
mouth) and a reference point. Bite is complete in Frame D, and prey
item is held in the teeth. In Frame E Transport initiation: mouth is
opening again and prey will be taken into the mouth (F). Frames G±H
Mouth closure: closing in Frame G and fully closed by Frame H.
(Note that forceps used to present prey item are not actually holding
prey item in the frames shown)
708

Table 1 Cephaloscyllium ventriosum. Means (‹SE) of cephalic sharks (Superscript percentages timing of events expressed as %
displacement variables and strike variables quanti®ed for prey cycle time; D distance traveled; RSI ram:suction index; t0 time zero)
capture and transport for hatchling (N = 4) and 1 yr-old (N = 5)

Variable Capture Transport

Hatchlings 1 yr-olds Hatchlings 1 yr-olds

Max. hyoid depression (cm) 0.49 1.06 0.50 1.28

(0.09) (0.14) (0.58) (0.13)
Max. buccal expansion (cm) 0.42 1.10 0.52 1.54
(0.08) (0.11) (0.10) (0.17)
Max. gape angle (°) 88.96 80.03 97.66 75.90
(4.73) (7.89) (4.27) (1.85)
Time to max. hyoid depression (s) 0.2175% 0.3187% 0.0635% 0.0426%
(0.01) (0.03) (0.01) (0.01)
Time to max. gape angle (s) 0.2175% 0.3187% 0.0528% 0.0320%
(0.01) (0.04) (0.01) (0.01)
Time to max. buccal expansion (s) 0.2383% 0.3597% 0.1161% 0.0743%
(0.03) (0.04) (0.02) (0.01)
Time to min. gape angle (s)a 0.28100% 0.36100% 0.18100% 0.16100%
(0.01) (0.04) (0.03) (0.01)
Initial predator velocity (cm.s)1) at t0 3.16 1.73 3.90 7.60
(0.07) (0.47) (0.50) (1.42)
Predator±prey distance (cm) at t0 0.19 1.15 ± ±
(0.11) (0.21)
Dpredator 0.63 0.80 ± ±
(0.17) (0.25)
RSI 2.417 0.18 ± ±
(0.93) (0.13)
Total number of manipulation bites 1.69 1.20 ± ±
(0.28) (0.56)
Holding time of prey in jaws (s) 0.29 0.30 ± ±
(0.04) (0.02)
a
equals cycle time, as this event always occurred last in the preceding series of events listed

given individual, and additional regression analysis and
repeated measures ANOVA (data not given here) failed
to ®nd a signi®cant trend among subsequent strikes that
might indicate learning. The greatest evidence for suc-
tion-producing ability in hatchlings, however, was ob-
tained from the kinematic pro®les.
In hatchling sharks during prey capture, mouth
opening (increased gape angle) appeared to precede only
slightly the start of hyoid depression (Fig. 5a). Head
angle was highly variable within and among strikes and
among individuals; however, it generally reached a
maximum near maximum gape angle. Maximum hyoid
depression appeared to occur coincident with maximum
gape, which was followed by maximum buccal expan-
sion. Increases in head depth and width were small, but
present. A trend can be seen in Fig. 5a that suggests a
wave of expansion passing posteriorly along the head,
and generally indicating the production of suction.
In 1 yr-old sharks, the pattern of kinematic events
during prey capture showed only a few di€erences from
those of hatchlings (Table 1). 1 yr-olds were generally
stationary prior to feeding and thus had a slower in-
stantaneous predator velocity at t0 during capture. 1 yr-
olds tended to lunge forward to capture the prey item, as
evidenced by the increased velocity still present at t0
during prey transport. Mouth opening was initiated
more than a centimeter from the prey item, and Dpredator
was 0.80 cm. A more noticeable increase in head depth
at both the ®rst gill arch and the pectoral ®n insertion
occurred. Hyoid depression and buccal expansion re-
mained constant until gape angle reached a minimum (at
this point the prey item was held in the teeth). Head
width appeared to increase slowly and by small incre-
ments throughout the strike. In general, most of the
displacement events occurred with a larger magnitude in
1 yr-old sharks than in hatchlings.
For statistical comparison of the kinematic patterns
between age groups, the PCA grouped the kinematic
variables into three factors (Table 2). All the variables
loaded greater than 90% on their respective principal
components. The ®rst PC described 55% of the variance
in the dataset and contained all the timing variables. The
second described 26% of the variance and contained
maximum hyoid depression and maximum buccal ex-
pansion. Maximum gape loaded alone on the third
principal component and described 14% of the variance.
The MANCOVA model detected signi®cant age e€ects
within the principal components (F ˆ 9.69 df ˆ 3, 60;
p < 0.0001), despite the presence of equally signi®cant
e€ects of the covariate head length (F ˆ 10.89 df ˆ 3,
60; p < 0.0001). Investigation of the univariate ANC-
OVAs on each principal component indicated signi®cant
di€erences between hatchlings and 1 yr-olds in the
amount of maximum hyoid depression and maximum
buccal expansion (Table 2: PC 2). This separation of age
groups is presented graphically in Fig. 6. The maximum
hyoid depression and buccal expansion produced by
1 yr-olds, however, was not signi®cantly di€erent from
 709

a b
120 120
Gape angle (°)

100 100
80 80
60 60
40 40
20 20
0 0
10 10
Head angle (°)

0 0
-10 -10
-20 -20
-30 -30
1.5
Hyoid (cm)

1.0 1.0
0.5 0.5
0 0
1.5
Head depth Buccal exp.

1.0 1.0
(cm)

0.5 0.5
0 0
-0.5
2.5 2.5
2.0 2.0
(cm)

1.5 1.5
1.0 1.0
0 0
4.5
3.5
4.0
Head widths (cm)

3.0
3.5
2.5 3.0
2.0 2.5

1.5 2.0
0 0
0 0.05 0.10 0.15 0.20 0.25 0.30 0 0.05 0.10 0.15 0.20 0.25 0.30 0.35
Time (s) Time (s)

the values predicted if movements were isometric (i.e. the
maximum displacements doubled). The power of these
two tests was '89% and >60%, respectively. Thus, the
degree of head expansion linearly appears to scale with
length isometrically between the two size classes.
Within the capture cycle, however, many events oc-
curred relatively later for 1 yr-olds (see values, expressed
as % cycle time, Table 1). It took longer both in
absolute time and % cycle time for 1 yr-olds to reach
maximum hyoid depression, which was reached simul-
taneously with maximum gape angle for both ages.
Maximum buccal expansion occurred about 35 ms later
than these two events for both ages, making the relative
time for prey capture for 1 yr-olds slightly longer. The
ANCOVA, however, did not detect signi®cant di€eren-
ces in the timing between the two age groups. This was
true if the MANCOVA on PC scores was used or if
separate univariate ANCOVAs were performed on the
timing variables.
Fig. 5 Cephaloscyllium ventriosum. Selected variables quantifying
cephalic displacement during prey capture by hatchling (a) and 1 yr-
old (b). a Single representative hatchling (16.0 cm female); b repre-
sentative 1 yr-old individual (23.6 cm female; after Ferry-Graham
1997) capturing prey items of similar size relative to diameter of
mouth. Values are means for four strikes; sampling rate has been
reduced to 24 ms (0.024 s) between images. Plots of head depth show
depth measured at ®rst gill (j), and depth measured at point of
pectoral ®n insertion (d); plots of head width show jaw width (j),
width of head at the ®rst gill (d), and width at pectoral ®n insertion
(m) (error bars are ‹1 SE) (Note that Y-axes in head-width plot are
slightly di€erent in order to increase resolution)
Kinematics of prey manipulation
The general patterns described for prey capture were
often repeated in subsequent bites (manipulation bites)
on the prey item (Fig. 7). Repeated measures ANCOVA
indicated that maximum hyoid depression and buccal
expansion increased during manipulation bites on the
710
Table 2 Cephaloscyllium ventriosum. Results of univariate AN-
COVAs following MANCOVA analysis in which age, phase, and
covariate head length were signi®cant ( p < 0.0001) on ®rst three
principal components (PC ). The three PCs cumulatively described
95% of variance in dataset. Beneath each PC are listed variables
Principal component Age e€ect
F p
PC 1: timing variables 0.71 0.400
time to max. gape angle (s)
time to max. hyoid depression (s)
time to max. buccal expansion (s)
time to min. gape angle (s)
PC 2: head expansion variables 29.97 0.0001
max. hyoid depression (cm)
max. buccal expansion (cm)
PC 3: max. gape angle (°) 1.88 0.168
prey item (Table 3: PC 2), although this result was non-
signi®cant after Bonferroni correction. A trend of in-
creasing head expansion with head length for capture
bites was absent for manipulation bites (Fig. 8), as in-
dicated by the signi®cant interaction between the main
e€ect and the covariate. The trend between bites is
consistent with the ®ndings of the previous MANCOVA
analysis of head expansion (see Table 2). The manipu-
lation event was slower than the capture event (Table 3:
PC 1), although a signi®cant interaction was also de-
tected with the covariate. Fig. 8 illustrates that timing of
prey-manipulation bites was related to head length while
the timing of events during the capture bite was not, the
latter ®nding being consistent with the previous
MANCOVA analysis of timing e€ects (see Table 2).
Generally, 1 yr-olds made fewer prey-manipulation
bites than hatchlings (Table 1). An e€ect of age was
detected in the timing of kinematic events between bites
(Table 3: PC 1), which is graphically presented in Fig. 8.
This should not be confused with the highly non-signi-
®cant age e€ect presented in Table 2 for the MANC-
OVA analysis. The repeated measures analysis suggests
that the manipulation event occurs much more slowly
than the capture event in 1 yr-olds, while the manipu-
lation event occurs only slightly more slowly than the
capture event in hatchlings (Fig. 8; Table 3).
Kinematics of prey transport
Following manipulation, the prey item was held in the
teeth with the jaws at a minimum gape angle for '0.3 s
by both hatchlings and 1 yr-olds (Table 1). Re-opening
of the mouth after this phase signi®ed the initiation of
prey transport. Sharks were generally not actively
swimming during transport, but at the initiation of
transport were often still moving forward due to the
momentum of the strike.
Prey transport in hatchlings was a suction-dominated
event, as it had to be to move into the esophagus an item
which it comprises. All variables loaded ³90% on their respective
PCs. No signi®cant interactions were detected by full MANCOVA
model. For all e€ects shown, F-ratio was calculated over error term
(df = 1, 62: six replicates were excluded because of a missing val-
ue); F-ratios and p values are given
Phase e€ect Head length e€ect
F p F p
112.64 0.0001 3.939 0.059
0.488 0.487 8.41 0.005
1.57 0.211 12.72 0.0007
already held in the teeth. Head expansion began with
maximum gape angle increasing only slightly to allow
passage of the prey item into the oral cavity (Fig. 9a).
Maximum hyoid depression was small, as the hyoid
stayed partially depressed throughout manipulation and
into transport. The buccal cavity expanded initially and
then appeared to increase slowly throughout transport.
Head depth increased throughout the transport cycle
and appeared to reach a maximum during mouth closure
(decreased gape angle).
The MANCOVA model detected signi®cant phase
e€ects (F ˆ 39.267 df ˆ 3, 60; p < 0.0001) and inv-
estigation of the univariate analyses revealed that
changes in the timing of the events described above were
responsible (Table 2: PC 1 and Fig. 6). Prey transport
was signi®cantly shorter in duration than prey capture
(Tables 1 and 2). For all strikes combined, the mouth
opened more quickly during transport than during prey
capture (Table 1; also note steeper slope on Fig. 9a,
gape-angle plot), which was followed rapidly by hyoid
depression and then mouth closure.
For 1 yr-olds, prey transport was also more rapid
than prey capture ± even more rapid than the hatchling
transport event. In Table 1, the time to maximum hyoid
depression occurs about 50 ms earlier than maximum
buccal expansion for hatchlings, but only 30 ms earlier
for 1 yr-olds. Maximum hyoid depression occurs by 35%
of the transport cycle time in hatchlings, but by 26% of
the cycle time for 1 yr-olds. Maximum buccal expansion
occurs by 61% of the transport cycle time in hatchlings,
but by only 43% of the cycle in 1 yr-olds. A signi®cant
interaction, however, was not detected by MANCOVA.
Morphometrics and scaling
A majority of the morphometric variables had slopes
nearly equal to one, and Fig. 10 shows several variables
particularly relevant to feeding and the good ®t of the
individual regressions to the data, despite the small
 711

slower 3.5 a
120
3.0

Gape angle
100
80
Principal component 1

2.5

(°)
One-year 60
2.0 olds 40
1.5 20
0
1.0 Hatchlings 100

Head angle
0.5 90
80

(°)
0 70
-0.5 60
50
faster

-1.0 1.0

Buccal exp. Hyoid

(cm)
-1.5 0.5
-2.5 -2.0 -1.5 -1.0 -0.5 0 0.5 1.0 1.5 2.0 0
less more -0.5
expansion expansion 1.0
Principal component 2

(cm)
0.5
0
-0.5
expansion

2.0
1.5 b 120
more

Gape angle
100
Principal component 2

1.0 One-year
olds 80
0.5

(°)
60
0 40
20
-0.5 0
-1.0 100
Head angle

Hatchlings 90
expansion

-1.5 80
(°)

70
-2.0 60
less

-2.5 50
1.0
-2.5 -2.0 -1.5 -1.0 -0.5 0 0.5 1.0 1.5 2.0 2.5 3.0
Buccal exp. Hyoid
(cm)

0.5
smaller larger
0
gape gape -0.5
Principal component 3
1.0
(cm)

0.5
larger

3.0 0
gape

2.5 -0.5
0 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55
2.0 Time (s)
Principal component 3

1.5
1.0 Fig. 7 Cephaloscyllium ventriosum. Samples of individual strikes used
to estimate average strike of hatchling shown in Fig. 5a. a Third, and
0.5 b fourth prey-capture events. Manipulation bites that occurred
0 following each strike are included as a second peak in each variable.
-0.5 Capture Manipulation bites did not occur in every strike, thus mean kinematic
-1.0 plots such as in Fig. 5a are not provided. Notice, in particular,
di€erences in path of head angle between strikes
-1.5
smaller

Transport
gape

-2.0
-2.5
-1.5 -1.0 -0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5
faster slower
Principal component 1
Fig. 6 Cephaloscyllium ventriosum. Principal-components plots. Clus-
ters are outlined according to separations among data detected in
analyses (s, h hatchlings; d, j 1 yr-olds; s, d prey capture; h, j
prey transport)
sample sizes. After Bonferroni correction, Student's
t-tests indicated that only the slopes of head width (at
the pectoral ®n insertion) and jaw width against total
length deviated signi®cantly from the expected slope of
1.0 (Table 4). The Bonferroni correction, however,
makes detection of signi®cant di€erences dicult, and
caution is warranted in assuming that overall isometric
growth has been demonstrated from this analysis alone.
The Bookstein-method PCA performed using the co-
variance matrix provides further evidence that this spe-
cies grows isometrically over the size range studied. All
the variables loaded positively and similarly on the ®rst
PC (Table 4), and that PC alone explained 91% of the
variance in the dataset.
Buccal-cavity model and hydrodynamics
Despite potential morphological changes with growth,
the simple, schematic models of the expanded buccal
cavities of hatchling and 1 yr-old sharks were similar
(Fig. 11). In models for both ages, the relaxed buccal
cavity in lateral view was roughly rectangular in shape.
At the time of maximum buccal volume, the buccal
space became more like a triangle, with its base at the
712

Table 3 Cephaloscyllium ventriosum. Results of separate repeated-
measures ANCOVAs on ®rst three principal components (PC)
associated with prey manipulation. In this analysis, initial prey
capture bite is contrasted with ®rst manipulation bite. This is a
separate analysis from that in Table 2 because of limited sample
size (N = 6 hatchlings; N = 8 one-year-olds), although the vari-
ables still grouped identically (see Fig. 8). The three PCs cumula-
tively described 93% of variance in dataset. All variables loaded
³79% on their respective PCs; F-ratios and p values are given. For
all e€ects shown, F-ratio was calculated over error term (df = 1,
11) (* p-values £0.017 are considered signi®cant at 0.05 probability
level according to Bonferroni correction; Superscripts a, b sig-
ni®cant interactions detected by full ANCOVA model and included
in model: a head length ´ bite interaction: F = 12.18; p = 0.010; b
head length ´ bite interaction: F = 6.75; p = 0.021)

Principal component Bite e€ect Age e€ect Head length e€ect

F p F p F p

PC 1: timing variablesa 9.39 0.011* 7.54 0.016* 0.67 0.432

time to max. gape angle (s)
time to max. hyoid depression (s)
time to max. buccal expansion (s)
time to min. gape angle (s)
PC 2: head expansion variablesb 6.50 0.032 1.51 0.251 0.17 0.689
max. hyoid depression (cm)
max. buccal expansion (cm)
PC 3: max. gape angle (°) 0.03 0.867 1.97 0.187 5.25 0.040

mouth. Generating this shape are the positions of the item (a reduced head angle) while gape angle is at a
selected cephalic components that move in concert to maximum; across all individuals, this head depression
allow food to be taken into the mouth. In the hatchling often occurred slightly after maximum gape angle (see
shown in Fig. 11a, the snout is bent towards the prey Table 1). At this time, the hyoid is not only depressed

3.0
slower

2.5
2.0
Principal component 1

s
1.5 bite One-year olds
lat ion)
1.0 nipu
(ma
ond
0.5 Sec
0 re) bites
First (captu
-0.5
faster

-1.0 Hatchlings
-1.5
2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 -2.0 -1.5 -1.0 -0.5 0 0.5 1.0 1.5 2.0 2.5
less more
expansion expansion
Head length (cm) Principal component 2

2.5
expansion

2.0
more

1.5
Principal component 2

s
1.0 ) bite
cap ture
0.5 First (
0 Second (manipulation) bites
-0.5
expansion

-1.0
-1.5
less

-2.0
2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 -2.5 -2.0 -1.5 -1.0 -0.5 0 0.5 1.0 1.5 2.0 2.5
smaller larger
gape gape
Head length (cm) Principal component 3

but quite retracted, while the point of ventral buccal
expansion is only slightly depressed. In the 1 yr-old
model, a reduced head angle at the time of maximum
buccal volume is not evident, although the movement of
the hyoid and ventral buccal region is similar.
The buccal volumes estimated using the shape model
suggest that the buccal cavity in hatchling sharks ex-
panded by 1 cm3 during the change from minimum to
maximum volume (Table 5). The volume change for
1 yr-olds was >7 cm3. This is strikingly similar to the
value predicted for 1 yr-olds by isometry; assuming a
doubling in length, the volume should change from
hatchlings to 1 yr-olds by a doubling raised to the third
power (´23); the resulting prediction of buccal volume is
8 cm3. The maximum buccal volume estimated for 1 yr-
olds was also not signi®cantly di€erent from the iso-
metric expectation (Table 5). The expansion index for
1 yr-olds was not signi®cantly di€erent from that ex-
pected if the indices for hatchlings are doubled in ac-
cordance with the assumption of isometry and a
doubling of length. Across all individuals, the resulting
¯ow index for 1 yr-olds was approximately twice that
for hatchlings, as predicted by a doubling in head size
with no change in the timing of events (Table 5).
Discussion
A large ram component to hatchling prey capture events
was evident in Cephaloscyllium ventriosum; the hatch-
lings were very mobile and tended to push the prey
forward prior to overtaking it. When determining if
there are e€ects of predatory experience the question
remains: did the hatchlings also generate suction during
the strike, as did 1 yr-olds? A suction component to the
strike was measured in a few cases, suggesting that
hatchlings were capable of generating suction. For the
cases in which the RSI could not tell us if suction was
being produced, however, what must be determined is
whether hatchlings sometimes failed to perform the
combination of movements that generate suction, or if
the suction generated in the buccal cavity simply had no
e€ect on the prey item (e.g. it was initiated too far from
the prey item or was overwhelmed by the forward lo-
comotory component). The kinematic data suggest that
suction-producing behaviors were always generated. In
both age groups, a general trend suggests a wave of
expansion moving posteriorly in the head during prey
capture, a pattern consistent with the generation of
suction (Lauder 1985).
b regardless of the behaviors performed. A majority of the
Fig. 8 Cephaloscyllium ventriosum. Principal-components plots from
the principal-components analysis on prey-manipulation variables
(recall that manipulation data required separate analysis as dataset
was quite small). Six feeding events with one or more manipulation
bites occurred in hatchlings (s, h), while eight were recorded for 1 yr-
olds (d, j). Two signi®cant interactions with the covariate were
detected in serial ``repeated measures'' ANCOVAs (s, d prey
capture; h, j prey manipulation)
713
This wave-like pattern is re¯ected primarily in the
times of peak movements, as the time of maximum bu-
ccal expansion (for example) is later than the time of
maximum hyoid depression. Timing has been considered
an important attribute of suction production; the faster
an organism can expand the head posterior to the
mouth, the greater the velocity of suction produced
(Liem 1990). Although the strike duration is longer for
1 yr-old Cephaloscyllium ventriosum, the absolute timing
of kinematic events was not signi®cantly di€erent be-
tween age groups (Table 2). These results are contrary to
the predictions of Hill (1950), whose classic paper sug-
gested that timing should scale isometrically with length.
Richard and Wainwright (1995) began one of the most
comprehensive studies of scaling e€ects in ®shes by
proposing a hypothesis in opposition to Hill (1950) that
stated that timing of kinematic events should not change
if morphological features scale isometrically. Although
the shark data appear to corroborate that hypothesis,
because a small size range of sharks was used the data
should not be interpreted as absolute support of the
hypothesis. Richard and Wainwright actually found that
their data supported neither of the two models, and that
timing variables scaled with an exponent of 0.33 with
increases in length. If the shark data are added to the
Richard and Wainwright data, they fall well within the
range of measurements reported by the researchers,
generally supporting their ®nding. Thus, how the timing
of the expansive wave is changed in 1 yr-olds versus
hatchlings remains unclear, and timing may not be a
useful metric for understanding suction-feeding perfor-
mance in these sharks.
The amplitude of the expansive wave is an equally
important factor to consider when determining if suction
can be generated. The maximum displacements of the
hyoid and the ventral buccal region were signi®cantly
di€erent between the two age groups. Both elements
expand the buccal cavity posterior to the mouth, and
di€ering magnitudes of displacement could lead to dif-
ferences in suction-producing ability (see Lauder 1983;
Liem 1990). Comparison of the mean displacements for
the kinematic variables (see Table 1), however, indicates
that they are what would be expected given isometry;
they nearly double in accordance with length. Thus,
changes in hyoid depression and ventral buccal expan-
sion may be potentially attributable to growth alone.
What must be considered at this point is the nature of
the growth that occurs in this species. If growth is al-
lometric, the changes that occur in single elements with
subsequent changes in total length could lead to shape
di€erences in the head that impact suction production
variables used indicated isometric growth. Of the few
that did not suggest isometry, the component changes in
size with total length were on the order of 10%, and of
questionable biological relevance to sharks of the sizes
studied here. Further, PCA suggests that isometric
growth occurs for all variables considered. Other studies
that have examined the scaling of morphological vari-
714

ables related to feeding in teleosts have found that ju-
venile and adult ®shes basically scale isometrically (see
Richard and Wainwright 1995; Cook 1996).
The simple shape model further illustrated the minor
impact of potential morphological allometries, and
generally suggested not only isometry of form, but also
isometry in function. Shape is a measure of how much
expansion can occur posterior to the mouth and,
therefore, the amount of suction that can be produced.
Maximum buccal volume, as estimated by the shape
model, was not apparently di€erent between age groups
when scaled in accordance with the predictions of

a 120 b 120

100 100
Gape angle (°)

80 80

60 60

40 40

20 20

0 0

10 10
Head angle (°)

0 0

-10 -10

-20 -20

-30 -30

1.5
Hyoid (cm)

1.0 1.0
0.5 0.5
0 0

1.5
Buccal exp. (cm)

1.0 1.0
0.5 0.5
0 0
-0.5
3.0

2.5 2.5
Head depth (cm)

2.0 2.0

1.5 1.5

1.0 1.0
0 0
4.5
3.5

4.0
3.0
Head widths (cm)

3.5
2.5
3.0
2.0
2.5
1.5
0 0
0 0.05 0.10 0.15 0.20 0 0.05 0.10 0.15 0.20
Time (s) Time (s)
 715

2.0 1.2
First gill

1.0 Fin insertion

1.6
log head length (cm)

log head depth (cm)

0.8
1.2

0.6

0.8
0.4

0.4
0.2

0 0
0 0.4 0.8 1.2 1.6 2.0 0 0.4 0.8 1.2 1.6 2.0
log total length (cm) log total length (cm)

2.0 2.0
Front of orbit to hyoid Jaw width

Front of orbit to buccal expansion point Head width at first gill

1.6 1.6

Head width at pectoral fins

log distance (cm)

log width (cm)

1.2 1.2

0.8 0.8

0.4 0.4

0 0
0 0.4 0.8 1.2 1.6 2.0 0 0.4 0.8 1.2 1.6 2.0
log total length (cm) log total length (cm)

isometry. The model also indicated that there were no
deviations from the expectations of isometry in either
the expansion or ¯ow-index estimates. The model can be
criticized, among other simpli®cations, for not including
a component of horizontal expansion at the posterior
margin of the buccal cavity (changes in head width at the
Fig. 10 Cephaloscyllium ventriosum. Scaling plots of selected
variables in morphometric analysis. Values were log-transformed to
determine ®t of linear regression to data. Slope and intercept
information, as well as signi®cance and ®t of regression (r2) are given
in Table 4 [Filled symbols preserved individuals (N ˆ 12); open
symbols live individuals (N ˆ 2): no obvious di€erences in size
between preserved and live individuals were noted]

®n insertion), however, additional analyses indicate that

b the change in head width during expansion across ages
Fig. 9 Cephaloscyllium ventriosum. Cephalic displacement during
prey transport by hatchling (a) and 1 yr-old (b). Individuals are same
as in Fig. 5a, b. Plots standardized to begin at time of mouth
reopening (corresponding to Frame E in Fig. 4). Values are means for
four transport events. For clarity, sampling rate has also been reduced
to 24 ms (0.024 s) in these images. Plots of head depth show depth
measured at ®rst gill (j), and depth measured at point of pectoral ®n
insertion (d); plots of head-width show jaw-width (n), width of head
at the ®rst gill (d), and width at pectoral ®n insertion (m) (error bars
are ‹1 SE). [Note that Y-axes in head-width plot (b) are slightly
di€erent to increase resolution]
does not deviate signi®cantly from that predicted by
isometry.
It should be mentioned that these models di€er from
previous models: (1) The head was not modeled as an
expanding cone (see Muller et al. 1982). Previous models
have used a cone to typify the internal shape of the
buccal cavity during suction production. This cone has
its wider end at the rear of the cavity, indicating that the
mouth opening remains small while the posterior ele-
716

Table 4 Cephaloscyllium ventriosum. Results of univariate re- r2 = adjusted r2; y = y-intercept of model; b slope coecient;
gression analyses of morphometric variables against total length t Student's t value for df = 13; PC shows score for analysis per-
(N = 14) [* p values £0.004 for sequential t-tests (null hypothesis, formed using covariance matrix (note that all are quite similar,
H0: slope = 1) considered signi®cant at 0.05 probability level; indicating isometry)]

Morphometric variable (cm) r2 y b SE t p PC

Head length 0.97 )0.84 1.04 0.046 0.89 0.389 0.221

Eye to lower jaw-tip distance 0.92 )1.56 1.14 0.098 1.45 0.171 0.252
Eye to upper jaw-tip distance 0.88 )1.59 1.15 0.121 1.26 0.231 0.238
Eye to hyoid distance 0.94 )1.19 1.02 0.076 0.26 0.797 0.227
Eye to buccal expansion point distance 0.95 )1.00 0.98 0.067 )0.22 0.826 0.219
Head depth at ®rst gill 0.93 )1.31 1.23 0.093 2.44 0.030 0.270
Head depth at pectoral ®n insertion 0.93 )1.32 1.27 0.102 2.61 0.022 0.279
Snout to base of neurocranium distance 0.91 )0.63 0.83 0.075 )2.29 0.039 0.182
Jaw width 0.97 )1.30 1.24 0.060 3.98 0.002* 0.269
Head width at Meckel's cartilages 0.98 )0.92 1.09 0.040 2.37 0.034 0.237
Head width at ®rst gill 0.98 )0.92 1.11 0.041 2.73 0.017 0.239
Head width at pectoral ®n insertion 0.99 )1.05 1.18 0.041 4.49 0.001* 0.255
Snout to Meckel's cartilage distance 0.96 )1.01 1.09 0.065 1.41 0.180 0.235

ments of the head expand. This prescribed shape was
avoided primarily because the opening of the mouth is
not round, and given the very large mouth it is not
presumed that only the posterior portion of the buccal
region should expand. (2) Muller et al.'s model used
a panding ®sh head is a sink into which water is ¯owing. A
2 cm
b set of behaviors necessary for suction production. At
4 cm
Fig. 11 Cephaloscyllium ventriosum. Models of representative hatch-
ling of 15.6 cm total length (a), and 1 yr-old of 37.0 cm total length
(b). Note scale on each model to facilitate comparison. Images are
scaled so that their sizes relative to one another are accurate. For both
images, coordinate data were used to place the points and an image of
a shark was overlaid to help visualize shape changes and morpho-
logical movement [Grey shading relaxed or pre-feeding condition, a
generally rectangular shape; black shading new position of morpho-
logical elements at peak buccal expansion (see Table 5), a more
triangular or cone-like shape]
complicated mathematical formulations in an attempt to
accurately describe non-steady state ¯ows through the
buccal region. The use of such mathematics still poorly
approximates any dynamic e€ects (Lauder 1983), and
thus were avoided in the present study. The simple
model used here is more similar to the steady-state
model of Weihs (1980), who presumed that the ex-
primary limitation of Weihs' model is his assumption
that the gills remain closed during expansion; an as-
sumption that is probably not realistic for most feeding
®sh (Lauder 1980). This assumption may hold true for
Cephaloscyllium ventriosum, however, as bi-directional
¯ow (where the water taken in during feeding exits the
open mouth rather than the gills) has been documented
(Ferry-Graham 1997).
Returning now to the initial problem of determining
if suction was being produced by the hatchlings, it would
seem that kinematically hatchlings were performing the
some level, however, this suction was ine€ective. There
are at least two potential reasons why this suction pro-
duction generally did not have an e€ect on the prey item
and, therefore, was not detected by the RSI analysis: (1)
Speci®c di€erences in the strike variables quanti®ed.
Hatchlings were more mobile in general, and prior to
and during prey capture they were rarely stationary, as
were 1 yr-old sharks. Although hatchlings began their
strike very close to the prey item, they were potentially
moving quickly enough to preclude any potential
movement of the prey item caused by suction. Thus,
although hatchlings may have produced suction within
the buccal cavity, it had no apparent or detectable e€ect
and the item was subsequently captured by ram feeding.
(2) A suction component to the strike might not have
been detected because of the physics of water and the
manner in which suction feeding is generated. Suction
feeding is the result of drawing into the mouth a volume
of water in which a particle of food is entrained.
Movement of the food particle with the volume of water
is due primarily to the drag force of the water acting on

Table 5 Cephaloscyllium ventriosum. Functional buccal volume,
expansion index and ¯ow-index calculations for hatchling and 1 yr-
old sharks during prey capture. Included are several of functional
parameters relevant to calculation of maximum buccal volume and
Age group Time to max. Max. gape Initial buccal
expansion (s) (cm) vol (cm3)
Hatchlings 0.21 0.90 1.73
(0.01) (0.06) (0.29)
1 yr-olds 0.31 1.68 11.56
(0.04) (0.12) (2.90)
a b
Not signi®cantly di€erent from value expected if value for
hatchlings is multiplied by 8 (assuming a doubling in length, iso-
metry predicts that volume should change by 23); Student's
t = 0.81, df = 3; p = 0.714; power 30%
the prey item. Drag is proportional to surface area, and
thus scales to the second power of velocity. Therefore,
although the ¯ow index doubled as predicted, a doubling
of the velocity of water entering the mouth corresponds
to the generation of a drag force four times as large. It
may simply be that even if all aspects of shark-feeding
scale isometrically, a smaller size entails absolute con-
sequences for prey capture, and suction cannot be used
reliably by smaller sharks.
The idea that hatchlings do not rely on suction to
capture prey contradicts the prediction of Frazzetta and
Prange (1987) and has not previously been considered in
the shark literature. Cook (1996), however, showed that
a juvenile cottid species (Clinocottus analis) possessed a
suction-feeding morphology (small mouth, large buccal
cavity), but still relied primarily on ram-dominated prey
capture. Although kinematic variables were similar be-
tween juveniles and adults during prey capture, the
smallest juveniles did not produce detectable suction,
and only the largest juveniles and adults were found to
produce a strong suction component during prey cap-
ture (Cook 1996).
In summary, the combined ®ndings of the present
study suggest that hatchling Cephaloscyllium ventriosum
feed kinematically in a manner that is quite similar
overall to that of 1 yr-olds. The primary di€erences
detected were in the displacements of cephalic variables
associated with the expansion of the head. These were
potentially attributable to growth alone, and the pattern
of growth does not suggest shape changes leading to a
greater or lesser ability to displace those elements. The
modeling results imply that any di€erences do not spe-
ci®cally preclude successful suction production within
the buccal cavity. The RSI analysis, however, failed to
determine if hatchlings were utilizing the same prey-
capture mode as 1 yr-olds. This failure may be attribu-
tale in part to some di€erences in the behaviors (i.e.
locomotion) of the hatchlings prior to and during a
strike, but is likely also to be due to absolute conse-
quences of size in a dense and viscous environment.
Thus, it would appear that size alone imposes perfor-
mance consequences on suction production.
717
results of Student's t-tests to determine if parameters scale across
age groups as predicted by isometry. All values are overall means
(‹SE) of feedings for each age group (N = 4 hatchlings; N = 5
one-year-olds)
Max. buccal Expansion index Flow index
vol (cm3) (cm) (cm s)1)
2.66 0.59 3.24
(0.44) (0.13) (0.71)
18.96a 1.25b 5.70c
(4.60) (0.15) (1.10)
Not signi®cantly di€erent from value expected given a doubling
of value for hatchlings; t = 0.55, df = 3; p = 0.813; power 59%
c
Not signi®cantly di€erent from value expected given a doubling
of value for hatchlings; t = 0.95, df = 3; p = 0.669; power 53%
Acknowledgements I thank G.V. Lauder, A. Cook, A.C. Gibb,
G.B. Gillis, C.D. Wilga, J. Sisneros, and M.H. Graham for advice,
assistance and thoughtful discussions regarding this work. N. Hol-
land, P. Wainwright and three anonymous reviewers also greatly
improved this manuscript. This work was completed using equip-
ment purchased under NSF Grants IBN 91-19502 and 95-07181 (to
GVL), and through grants from Sigma Xi, the American Museum
of Natural History, the University of California Reserve System/
Mathias Foundation, and the International Women's Fishing As-
sociation (IWFA). Egg cases were obtained from the Cabrillo
Marine Aquarium (San Pedro, California, USA), and S. Anderson
at the University of California, Santa Barbara, USA. Additional
preserved specimens were provided with the assistance of J. Seigel
and Los Angeles County Museum of Natural History, USA.
Sharks used in the kinematics experiments are currently housed at
the Birch Aquarium at the University of California, San Diego,
USA. All experiments were conducted with the approval of the
Animal Care and Use Committee at the University of California,
Irvine, USA, and according to guidelines outlined in ``The Princi-
ples of Laboratory Animal Care'' (NIH Publication No. 86-23,
revised 1985).
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