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First published online March 17, 2006
Journal of Experimental Biology 209, 1231-1244 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02135
Kinematics of foraging dives and lunge-feeding in fin whales
1 Department of Zoology, University of British Columbia, 6270 University
Boulevard, Vancouver, British Columbia, V6T 1Z4, Canada
2 Scripps Institution of Oceanography, University of California, San Diego,
La Jolla, CA 92093-0205, USA
3 Cascadia Research Collective, Olympia, WA 98501, USA
4 Whale Acoustics, Bellvue, CO 80512, USA
* Author for correspondence (e-mail: jergold{at}zoology.ubc.ca)
Accepted 31 January 2006
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Summary |
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Key words: fin whale, Balaenoptera physalus, diving, lunge-feeding, swimming, kinematics
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Kooyman and Ponganis,
1998). Conflicting metabolic demands of locomotor activity with a
limited oxygen supply must therefore be balanced in order to maximize foraging
efforts at depth (Castellini et al.,
1985; Hochachka,
1986; Davis et al.,
2004). Limits to diving capacity, defined by the ability to
aerobically dive deeper and longer, are determined by the magnitude of oxygen
stores within the body and the rate at which that oxygen supply is consumed
(Scholander, 1940;
Snyder, 1983;
Kooyman, 1989). As body size
increases, oxygen stores increase while mass-specific metabolic rates decrease
(Klieber, 1932), suggesting that larger animals should be able to dive longer
(Butler and Jones, 1982). In
general, marine mammals have indeed been shown to dive longer and deeper with
increasing size, although this allometric relationship appears to be effected
by ecological, behavioral and physiological differences among species (Shreer
and Kovacs, 1997; Noren and Williams,
2000; Halsey et al.,
2006). Ultimately, oxygen stores must be used wisely during a dive
through the implementation of strategies to reduce the cost of locomotion.
Cetaceans and phocid seals use lift to generate thrust by the periodic
oscillation of a crescent-shaped hydrofoil
(Fish et al., 1988;
Fish, 1993b;
Fish, 1998;
Fish and Rohr, 1999). The
number of strokes taken during a dive directly increases the energetic cost of
foraging (Davis et al., 1985;
Fish et al., 1988;
Williams et al., 2004). To
reduce this cost and enhance diving capacity, locomotor activity is decreased
by taking advantage of changes in buoyancy associated with lunge collapse at
depth and employing gliding or stroke-and-glide gaits
(Skrovan et al., 1999;
Williams et al., 2000;
Williams, 2001). Differences
in body composition among different marine mammals permit the use of gliding
gaits at different stages of a dive. Phocid seals
(Sato et al., 2003),
bottlenose dolphins (Skrovan et al.,
1999) and blue whales
(Williams et al., 2000) glide
during descent and actively stroke to the surface, whereas more positively
buoyant right whales (Nowacek et al.,
2001) and sperm whales (Miller
et al., 2004) actively stroke to depth and glide more during
ascent. Drag forces resist forward motion of the body throughout a dive and
pose a considerable energetic cost, but the fusiform body shape characteristic
of all accomplished swimmers reduces drag by minimizing the development of
pressure gradients along the body and delaying separation of a turbulent
boundary layer (Vogel, 1994;
Fish, 1993a;
Fish and Rohr, 1999).
The fin whale, Balaenoptera physalus (Linnaeus 1758), is a fast,
streamlined swimmer and one of the largest animals on earth
(Bose and Lien, 1989;
Bose et al., 1990). Mysticete
cetaceans of the crown group Balaenopteridae (sensu
Rice, 1998), namely blue and
fin whales, exhibit significantly shorter dive durations than would be
predicted from their extreme body size
(Croll et al., 2001). The
rorquals are most notably distinguished from other baleen whales by their
lunge-feeding behavior, an extraordinary biomechanical process in which large
amounts of water and prey are engulfed and filtered
(Brodie, 1993;
Pivorunas, 1979;
Werth, 2000). This mode of
intermittent filter feeding requires that the whale uses inertia of the body
to stretch its buccal cavity around a volume of prey-laden water
(Orton and Brodie, 1987). Blue
whale diving behavior combined with oceanographic data show that feeding
efforts are primarily directed towards subsurface aggregations of euphausiid
crustaceans associated with steep submarine canyon topography
(Croll et al., 1998;
Fiedler et al., 1998;
Croll et al., 2005). Fin whale
tracks are also closely linked to aggregations of krill and capelin situated
against similar topographic features
(Simard et al., 2002). Dive
profiles of blue and fin whales reveal longer recovery time at the surface
following foraging dives in comparison with non-foraging dives, suggesting
that lunge-feeding is energetically costly and consequently limits maximum
dive duration (Acevedo-Gutierrez et al.,
2002).
Lunge-feeding is facilitated by a host of remarkable morphological and
biomechanical adaptations, most of which have been described post
mortem. The throat wall is lined with a series of longitudinal throat
grooves that consist of tough ridges connected by furrows of delicate elastic
tissue (Brodie, 1977;
Orton and Brodie, 1987;
deBakker et al., 1997). The
ventral groove blubber is reversibly extensible up to several times its
resting length to accommodate an expanding buccal cavity during engulfment
feeding (Orton and Brodie,
1987). From the forces required to stretch this tissue, Orton and
Brodie predicted that a swimming speed of 3.0 m s–1 would
generate enough hydrodynamic force to completely inflate the buccal cavity
(Orton and Brodie, 1987).
Opening of the mouth causes a lateral expansion and outward rotation of the
mandibles, effectively increasing surface area of the mouth to oncoming flow
(Lambersten et al., 1995). Excellent underwater video footage of lunging dwarf
minke whales has confirmed this phenomenon of mandible rotation in
situ (Arnold et al.,
2005). An elastic, weakly muscularized tongue is thought to
initiate distension of the ventral pouch and increase the capacity of the
mouth through invagination into a hollow sac
(Lambertsen, 1983). A
well-developed coronoid process of the mandible is mechanically linked to the
frontal bone by a fibrous frontomandibular stay that is closely associated
with the temporalis muscle (Lambersten et al., 1995). This tendon may act to
limit hyperdepression of the lower jaw, provide elastic recoil to reverse the
direction of jaw movement, and enhance mechanical power output of the
temporalis when acting to elevate the lower jaw (Lambersten et al., 1995).
Once the jaws have closed around the volume of prey-laden seawater, a novel
articulation between the mandibles and maxillary suborbital plate may provide
a hydrodynamic seal of the buccal cavity, thereby maintaining a fusiform body
shape in spite of possessing a highly expandable mouth
(Lambertsen and Hintz, 2004).
The forces to deflate the ventral pouch are suggested to come from the dynamic
pressure from oncoming flow, elastic energy stored within the stretched
tissues and active muscle shortening beneath the blubber
(Orton and Brodie, 1987).
Video footage at the sea surface of lunge-feeding rorquals has provided
evidence of a rebounding wave within the ventral pouch that is thought to
enhance filtration (Kot,
2005).
Our knowledge of the lunge-feeding process in situ is limited to
aerial or ship observations near the sea surface. Humpback whales
lunge-feeding at the sea surface exhibit three kinematic modes that are
distinguished by the orientation of the body with respect to the water surface
(Jurasz and Jurasz, 1979). Two
of these modes were termed `lateral lunge feeding' and `inverted lunge
feeding', which involved rotations about the whale's longitudinal axis (roll)
of approximately 90° and 180°, respectively
(Jurasz and Jurasz, 1979).
Lateral lunge-feeding was also observed for blue and fin whales
surface-feeding on euphausiids or schooling fish
(Andrews, 1909;
Tomilin, 1957;
Watkins and Schevill, 1979;
Gaskin, 1982; Corkeron, 1999).
However, Watkins and Schevill reported that fin whales primarily lunged with
their ventral sides down (Watkins and
Schevill, 1979). Underwater observations of lunge-feeding include
humpbacks executing lateral lunges while bottom feeding on sand lance at 30 m
depth (Hain et al., 1995) and
Crittercam video of a blue whale performing inverted lunges on pelagic krill
aggregations (J.C., personal communication). Fin whales have also been
observed to feed in shallow waters on sand lance
(Bigelow and Schroeder, 1953;
Overholtz and Nicolas, 1979)
and herring (Nottestad et al.,
2002), but the types of feeding modes used were not reported.
Overall, lunge-feeding behavior appears to be modal as well as highly variable
across species, but the detailed mechanics of the process remain elusive.
To investigate the swimming kinematics during foraging dives, we attached high-resolution digital tags to the backs of surfacing fin whales in the Southern California Bight. Accelerometer data were used to analyze both body orientation and fluking behavior, while hydrophone-measured flow noise was used to estimate body speeds throughout the dive cycle. We present the first kinematic analysis of a diving rorqual, including lunge-feeding behavior at depth.
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Materials and methods |
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) included a hydrophone (sampling rate, 1025 Hz), a depth
gauge and a two-axis accelerometer (MXA2500GL/ML; MEMSIC Inc., North Andover,
MA, USA) encapsulated in a cylindrical polyurethane shell with a hemispheric
nose. Data from the depth gauge and accelerometer were digitally recorded at 1
Hz and stored within the tag. The tag was attached to two silicon suction cups
with zip-ties and harnessed with a flotation device
(Fig. 1). Typically, the tag
stayed attached for several hours, fell off during lunges at depth and then
floated to the surface. Upon tag recapture, the data were downloaded for
analysis via infrared transmission.
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Tagging methodology
Fin whales (Balaenoptera physalus; family Balaenopteridae) were
tagged off the Tanner-Cortez banks in the Southern California Bight during a
visual and acoustic marine mammal monitoring operation in the summer of 2003
(Oleson, 2005). A 5.3 m
Rigid-Hulled Inflatable Boat approached whales from behind, and tags were
attached using a 4 m fiberglass pole. We aimed to place the tag so that its
long axis was largely parallel with the long axis of the animal
(Fig. 2). However, as soon as
the whale started to dive, it was apparent that flow forces helped to align
the tag more parallel with the longitudinal axis of the body. When possible,
tagged whales were followed visually or by radio VHF transmission.
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;
Fletcher et al., 1996;
Burgess et al., 1998). We
utilized this approach to estimate the instantaneous speed of whales for a
given level of flow noise recorded by the hydrophone on the tag. To determine
the magnitude of flow noise at different flow velocities, the tag was attached
to a dihedral wing (V-FIN, Type 166; Endeco/YSI Inc., Marion, MA, USA) and
towed at approximately 0, 1.5, 3.0 and 5.0 m s–1 by the R/V
Sproul. The flow noise was analyzed at different frequencies at each
flow velocity by calculating the root-mean-square sound pressure over 1/3
octave bands. The 50 Hz spectrum exhibited both the highest flow noise level
and the most distinct partitioning of this noise level for each flow velocity.
Therefore, we used the 50-Hz 1/3 octave band of the flow noise signal in order
to determine flow speed. A positive relationship between flow speed and flow
noise was obtained through a least-squares curvilinear regression
(Fig. 3;
r2=0.99). This relationship was used to calculate
instantaneous velocity, VS, for a given flow noise level
recorded from the tag deployments. As a corollary, whale speed derived from
the kinematics of the body, VK, was estimated by dividing
the vertical velocity obtained from the depth profile by the sine of the body
pitch angle (see Miller et al.,
2004). The first derivative of speed with respect to time was
determined in order to estimate the instantaneous acceleration of the body
throughout the dive cycle.
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Body orientation: theory
The accelerometer measured both static (gravitational acceleration) and
dynamic acceleration at 1 Hz, which allowed for the analysis of body
orientation and fluking, respectively. Accelerometer signals were low-pass
filtered (cutoff frequency, 0.1 Hz) to remove higher frequency oscillations
for analysis; the low-frequency signal became the data used to determine
orientation while the high-frequency signal was used to analyze fluking
patterns (see Fluking analysis section below). A linear scaling adjustment
performed at acquisition time accounted for the fact that the accelerometer
was being sampled before it completely settled (W. C. Burgess, personal
communication).
Body orientation was represented by two kinematic degrees of freedom: pitch
and roll. The x-axis was defined as the long axis of the tag, which
is parallel to one axis of the accelerometer, while the y-axis was
defined as perpendicular to this axis, which extends radially on the tag.
Acceleration along each axis was measured in gravitational units (range,
±1 g; g=9.8 m s–2).
Changes in acceleration detected by the x-axis were used to estimate
body pitch or tilt:
 | (1) |
is the pitch of the long axis of the animal with respect to
horizontal. Equation 1 describes the revolution of the accelerometer axis
about the arc of a unit circle and its resulting nonlinear response.
Therefore, =0° would represent a horizontal body angle and
=±90° would reflect vertical body orientations.
Rotations about the x-axis signify body roll and will be observed
in changes in static acceleration by the y-axis of the accelerometer,
Ay. Body roll estimates are affected by different pitch
orientations such that progressive degrees of tilt significantly decrease the
magnitude of static acceleration measured along the y-axis. Instead
of the accelerometer axis revolving about the arc of a circle, its path
effectively becomes an arc of a projected ellipse of diminished height onto
the plane perpendicular to gravity. The magnitude of reduced height of the
projected ellipse is determined by:
 | (2) |
, about this ellipse is augmented to
become:
 | (3) |
The three terms of Eqn 3, as denoted by brackets, each describe a
particular characteristic of the accelerometer response, which ultimately
combine to give a roll estimate, , for a given output of the dual axis
accelerometer within the tag. Term 1 describes a `tilt factor', where high
levels of pitch drastically increase the sensitivity of the response and
decrease the overall magnitude of the response. Term 2 is related to an
ellipse of decreasing height with increasing values of body pitch, while term
3 is analogous to Eqn 1, the revolution about an arc of a unit circle.
Body orientation: calibration
To experimentally test the validity of Eqn 3, the accelerometer was
calibrated in a custom-made device. The apparatus statically held the tag at
different degrees of tilt. At each level of tilt, as determined by Eqn 1, the
tag was rolled at 5° intervals as measured by a laser pointer and
protractor attached parallel to the long axis of the tag. Data from this
calibration were used to describe the range of in the context of the
orthogonal dependence of Ay on Ax
(Fig. 4). For static
orientations, the maximum value recorded by the accelerometer was 0.9
g, which may be due to the interaction between sampling and
settling rates of the accelerometer (W. C. Burgess, personal communication).
However, standardizing the response with respect to the maximum value is
expected to account for this difference (Eqns 1, 3).
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is limited to 180° if the axis of the
accelerometer begins in the plane parallel to gravity, whereas the range of
is limited to 90° if the axis begins in the plane perpendicular to
gravity. This dependence of Ay on Ax
did not allow for an analysis of roll angle during descent or ascent where
exceeded 65° and high Ax values were
involved. The position of the tag may move during the course of the dive, which would significantly alter kinematic analysis. To address this potentially confounding factor, tag orientation was examined when the whale was at the surface. Before and after each dive, the mean pitch angle was 2.5±2.7° (N=28) from horizontal when the whale was at the surface, suggesting that the tag was largely parallel with the long axis of the whale's body and maintained this orientation throughout the deployment. The orientation of the y-axis of the accelerometer (radial axis of the tag) was also determined before and after a dive. In this way, sliding of the tag was sometimes observed, which discounted the dive from being included in further analysis. With the assumption that the whale did not roll on average while at the surface, the average value of Ay was recorded at the surface. This served as an indication of when the whale was level at depth and also to what extent the body rolled during lunges or maneuvers.
Fluking analysis
Dorsal–ventral oscillations of the flukes were detected as
small-amplitude oscillations by the x-axis of the accelerometer.
These distinct patterns of dynamic acceleration, likely to be a result of
recoil forces manifest throughout the body (see
Fish et al., 2003), were
isolated from the static acceleration profile used to determine body
orientation by low-pass filtering at 0.10 Hz. These patterns were so distinct
and repeatable in form and fashion that we consider this filtering process to
have removed all accelerations due to fluking itself. However, it was not
possible to account for surge, heave or sideslip (see fig. 8 in
Fish, 2004 for definitions)
that may have contributed to the accelerometer signal. Fluking frequencies
were calculated by counting the number of acceleration maxima divided by the
time of a given bout of fluking. Either through recoil forces detected by the
tag in the mid-body region or by actual tilting with the caudal stock,
downstrokes produced positive peaks in the fluking profile while upstrokes
resulted in negative peaks.
Dive profiles
Data from the pressure transducer within the tag recorded changes in depth
over time and provided a context for which to evaluate other kinematic
parameters. Depth profiles were categorized into several phases. Descent was
defined as the time between a depth value of zero and the time when maximum
velocity was recorded, since each whale continued to accelerate until a
preferred depth was attained. Ascent time was defined as the time from the
last velocity minimum (end of last lunge) until the time when depth equaled
zero again. Lunging time, or foraging time, was defined as the time between
descent and ascent. Post-dive time, or recovery time, was the time spent at
the surface after a dive, until another foraging dive was recorded.
A series of vertical excursions at the bottom of a dive was assumed to
represent a foraging dive. Although we have no direct video evidence to
confirm that these whales were actually feeding, previous studies have shown
that these vertical excursions occur at the precise location of their
preferred prey (Croll et al.,
1998; Croll et al.,
2005). Crittercam deployments on blue whales also confirm the
presence of prey during these types of lunges.
Statistics
All statistical analyses were performed using Minitab (version 13). If a
parameter failed, the Anderson–Darling test for normality, a
Mann–Whitney U-test, was used to test whether two given
kinematic parameters were significantly different from one another. A
P-value less than or equal to 0.05 accepted the hypothesis that the
two parameters were significantly different. Sample sizes among individuals
did not allow for an effect of individuals to be assessed.
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Kinematics during descent and ascent
A representative foraging dive recorded by the tag is presented in
Fig. 6. At the beginning of
descent strong fluking was observed, but stopped or decreased dramatically
(<0.1 g) at a depth of 21±7 m. At the end of
descent, small amplitude oscillations (<0.1 g) were often
observed in the fluking profile, but we attributed these vibrations to an
increasingly turbulent flow regime associated with high speeds (>4 m
s–1). Prolonged gliding was employed during 55±23% of
descent durations but ranged widely from 19 to 95%. Strong fluking was
observed at the end of each descent. Stroke-and-glide gaits were sometimes
observed for many whales on descent (Table
1). By contrast, steady fluking at a frequency of 0.30±0.03
Hz was observed on ascent of every dive recorded. At the end of each ascent,
steady fluking discontinued at a depth of 30±5 m as whales glided to
the surface.
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The relationship between body acceleration and body pitch during descent and ascent is shown in Fig. 8. At depths greater than 21 m on descent, where fluking had typically stopped, the body experienced net positive acceleration at relatively constant pitch angles, which indicated that the body was negatively buoyant and sinking. During ascent, body accelerations were much closer to zero, suggesting that a relatively constant speed was maintained, but gradually decreased as depth decreased. The highest decelerations were recorded at 30 m, the average depth at which gait transition from steady fluking to gliding took place.
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A time series of fluking, body orientation, and translational acceleration
during four consecutive lunges reveals a distinct and consistent kinematic
mode (Fig. 9). Maxima, minima
and zero values of each kinematic variable were superimposed onto depth
profiles to determine the body dynamics that occur during a lunge. Before the
lunge, the whale approaches a prey patch with a slight downward pitch
(<30°). Maximum acceleration of the body typically occurred just
as the first full stroke cycle was completed. At this moment the body begins
to roll. The long axis of the body becomes level, parallel to the sea surface,
as maximum velocity is reached. Opening of the mandibles, which is assumed to
occur at maximum speed, causes a deceleration at the same time that the body
completes a full 90° roll (Fig.
10). Meanwhile, the body begins to tilt upward and roll back as
the final fluke stroke is executed. Maximum pitch is attained as the whale
slows to a minimum speed.
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). Mechanical
principles predict that large body size will decrease agility and
maneuverability (Webb and de Buffrenil,
1990). To circumvent these effects, balaenopterid foraging
behavior incorporates the selection of dense aggregations of small prey
(Weihs and Webb, 1983) and
increased attacking speed during lunges
(Fig. 9;
Table 2). A large body size is
accompanied by a high energetic demand such that B. physalus is
predicted to require one metric ton of krill daily
(Brodie, 1975). Physiological
scaling laws suggest that increasing body size will increase oxygen stores and
decrease mass-specific metabolic rate (Klieber, 1932). Thus, blue and fin
whales appear well-equipped to aerobically dive longer and deeper to exploit
prey patches at depth. However, myoglobin concentration, the primary oxygen
carrier in skeletal muscles, is relatively low for fin whales, indicating that
rorquals have been subject to different selective pressures in terms of
physiological adaptations to enhance dive capacity
(Noren and Williams, 2000).
Also, due to differences in body composition related to oxygen storage,
cetaceans have considerably less oxygen per unit mass available compared with
phocid seals and penguins (Kooyman,
1989).
Blue and fin whales typically dive much shorter (<17 min) and shallower
(<200 m) than would be predicted by their large body size (Shreer and
Kovacs, 1997; Croll et al.,
2001). Although fin whales have been reported to dive as deep as
470 m, which is still somewhat shallow for their body size, dive durations
during these excursions were less than 13 min
(Panigada et al., 1999).
Optimality models of dive behavior based on depth profiles of blue and fin
whales suggest that lunge-feeding is energetically costly and thus responsible
for limiting dive capacity
(Acevedo-Gutierrez et al.,
2002). Foraging dives in the Weddell seal are associated with an
increased energetic cost compared with non-foraging dives of the same duration
and such costs can be estimated from the number of strokes taken during a
particular dive (Williams et al.,
2004). Different types of locomotor activity, particularly
involving rapid changes in translational and rotational acceleration, may
significantly increase the energetic costs incurred during a dive
(Weihs, 1981). While the
energetic cost for each stroke does not change with body size among phocid
seals (Williams et al., 2004),
complex maneuvers executed by the largest whales may prove to be much more
energetically expensive.
Here we show that fin whale foraging dives are characterized by a gliding
descent, a series of lunges at depth and an ascent to the surface powered by
steady fluking (Fig. 6). Other
negatively buoyant marine mammals show similar patterns of reduced locomotor
activity during descent (Skrovan et al.,
1999; Sato et al.,
2003), a behavior that is associated with a decrease in oxygen
consumption, which in turn enhances diving capacity (Willliams et al., 2000).
Fin whales were observed to accelerate primarily while gliding at high descent
angles (Fig. 8A), suggesting
that buoyant forces are more effective when vertically directed drag forces
are minimized. When the body is oriented more vertically, pressure drag is
relatively lower because projected area is significantly decreased compared
with when the body is broadside to vertically acting buoyant forces. In this
way, whales accelerated to the highest velocities recorded over the dive cycle
(Fig. 6). Similarly, sperm
whales reached maximum speeds near the end of each descent, but such speeds
were accompanied by fluking (Miller et
al., 2004). Our data suggest that fin whales should be practically
neutrally buoyant or slightly positively buoyant at depths shallower than 30
m, as indicated by the depth at which gait transition occurs during ascent and
descent (Fig. 8;
Table 1). This change in
buoyancy is attributed to gradual lunge collapse with depth in other diving
marine mammals (Skrovan, 1999; Williams et
al., 2000), given that complete lunge collapse is suggested to
occur at a depth of about 100 m
(Scholander, 1940;
Ridgway et al., 1969;
Ridgway and Howard, 1979).
Williams et al. also observed gait transition at similar depths for the blue
whale, Balaenoptera musculus
(Williams et al., 2000).
Negative buoyancy may be counteracted by hydrodynamic lift provided by the
pectoral flippers as they are abducted and extended away from the body
(Fish and Battle, 1995;
Miklosovic et al., 2004).
Accordingly, tethered minke and sei whales were observed to sink while the
flippers were held against the body and pitch toward the surface when they
were extended (Williamson,
1972). Balaenoptera are also reported to be negatively
buoyant and typically sink when killed
(Slijper, 1962;
Brodie, 1977).
In order to utilize oxygen stores wisely at depth, diving animals must not
only reduce locomotor activity but also exhibit an efficient mode of
locomotion. The morphological design of the fin whale is well equipped for
efficient, high-speed swimming (Bose and
Lien, 1989; Bose et al.,
1990). Fin whales are theoretically capable of speeds as high as
13 m s–1 (Bose and Lien,
1989), and maximum speeds of up to 10 m s–1 have
been reported (Gambell, 1985).
Average speeds observed over long-distance tracks, however, are only
0.5–2.0 m s–1
(Notarbartolo-di-Sciara et al.,
2003). In the present study, sustained speeds during ascent
(Table 1) were within the range
predicted to be efficient (2–10 m s–1) but were quite
lower than those predicted to produce maximum propulsive efficiency (6–8
m s–1) by unsteady hydrofoil theory
(Bose and Lien, 1989). Maximum
speeds estimated for fin whales on descent (5.7±0.3 m
s–1; Table 1)
were significantly lower than maximum swim speeds observed in both captive and
wild delphinids (Rohr et al.,
2002). With respect to body size, the speeds observed in this
study by fin whales are very low in comparison with odontocetes.
The kinematics of the body and flukes during lunges depict an exceptionally
dynamic event. Body acceleration driven by a bout of fluking is immediately
met by a relatively larger deceleration, probably due to the opening of the
mouth. Lowering of the mandibles increases the surface area of the body,
specifically the buccal cavity, perpendicular to flow. The moving buccal
cavity meeting the stationary volume of prey-laden seawater provides the
pressure needed to expand the ventral groove blubber in proportion to the
square of velocity (Orton and Brodie,
1987). A large part of the kinetic energy of the body should be
converted into potential energy stored in the stretched ventral groove
blubber. The Y-shaped fibrocartilage skeleton that lies within the musculature
of the ventral pouch may provide structural rigidity to the region or act as a
tendon to distribute forces involved in the feeding process
(Pivorunas, 1977). Once the
buccal cavity is filled, the `elongated, bloated tadpole' profile of the body
(Orton and Brodie, 1987) must
also increase drag on the body and contribute to the overall deceleration of
the body.
Accelerating a large body is energetically demanding. This appears to be
the reason why lunge-feeding is so costly and thus limits dive time. Since
drag on the body is proportional to the square of its instantaneous velocity,
the thrust and energy needed to overcome drag will be high during a lunge. In
addition, drag should become dramatically larger when the mouth is agape,
dissipating the kinetic energy of the body. Our data support the hypothesis by
Acevedo-Gutierrez et al. that the rapid changes in speed associated with
lunge-feeding at depth are energetically expensive and limit dive capacity in
rorqual whales (Acevedo-Gutierrez et al.,
2002). Quite the opposite seems to be the case for bowhead and
right whales, which appear to swim at relatively constant speeds
(Nowacek et al., 2001) and
continuously filter feed via both hydrodynamic and ram hydraulic
pressures (Werth, 2004;
Lambertsen et al., 2005).
According to mechanical principles, this foraging strategy should be
energetically more efficient than lunge-feeding since the body maintains a
relatively constant speed and thus accelerations of the center of mass will be
minimized. Bowhead whale dive behavior is consistent with this hypothesis;
they exhibit longer dive durations and shorter recovery times between dives
than a larger blue whale diving to the same depth
(Dorsey et al., 1989;
Würsig and Clark, 1993;
Krutzikowsky and Mate, 2000;
Croll et al., 2001).
Steady fluking that occurs during the ascent phase of a dive must also come
at an energetic cost since the whale is negatively buoyant, but this should
not be as costly as lunging given that speed on ascent remained relatively
constant (Fig. 6). Therefore,
it is not surprising to observe rorquals performing deep dives of limited
duration (Panigada et al.,
1999), as long as the number of lunges per dive is low. Body
acceleration observed over the course of ascent decreases steadily
(Fig. 8B), perhaps indicating
fatigue. However, it may also indicate a decrease in motivation associated
with gradually changing buoyant forces near the end of ascent. From these
kinematic data it is unclear whether fin whales were exceeding their aerobic
capacity during foraging dives.
The maximum speeds recorded at jaw opening match the predictions made by
Orton and Brodie for the hydrodynamic forces needed to expand the ventral
groove blubber if feeding was exclusively powered by the locomotor muscles
(Orton and Brodie, 1987).
Also, the slight downward pitch of the body just prior to the lunge may help
to open the mouth by lowering the pressure on the underside of the head
via the Bernoulli effect. Our results show that fin whales fluke
throughout each lunge (Figs 9,
10), even after jaw opening,
supporting the hypothesis that prey-laden water is enveloped by the buccal
cavity (Orton and Brodie,
1987). The timing of jaw opening is critical for successful prey
capture in order to avoid pushing prey away with a bow wave
(Brodie, 1977) and is likely
facilitated by the tactile sensing of prey via vibrissae on the
mandibles (Ogawa and Shida,
1950; Gaskin,
1982). Contraction of the buccal cavity must occur when the whale
is gliding between lunges. If we assume that engulfment is accomplished in the
time elapsed during a fluking bout (16.2±3.9 s;
Table 2) and that a fin whale
engulfs approximately 30 m3 of water and prey during a lunge (see a
previous estimate of 70 m3 for a blue whale)
(Pivorunas, 1979), water must
be filtered at a rate of nearly 1 m3 s–1, since
durations between each consecutive lunge were 44.5±19.1 s. However, we
do not know the extent to which the buccal cavities were filled during each
lunge, as there have been previous accounts of fin and sei whales engulfing
prey without the buccal cavity becoming `enormously expanded'
(Pivorunas, 1979). In
addition, estimates for the volume of engulfed prey and water are entirely
anecdotal.
Lunges occurred in two distinct modes, which were distinguished by the
degree of body roll at the moment of jaw opening (Figs
9,
10). Lateral lunges involved a
90° roll to the same side on each lunge, while regular lunges involved no
significant roll as the body reached maximum velocity. Why
Balaenoptera roll during lunges is not known. Rotating about the
longitudinal axis may orient the jaws in such a way as to capture prey by
anticipating their escape trajectory (F. E. Fish, personal communication).
Lateral lunges may also be a way to pin or drive prey against a barrier, such
as the sea surface or sea floor. Being negatively buoyant, a 90° roll may
help with maneuvers in the plane perpendicular to buoyancy, where they are
weight neutral (B. Ahlborn, personal communication). Both behaviors have been
previously observed among the rorquals
(Andrews, 1909;
Tomilin, 1957;
Jurasz and Jurasz, 1979;
Watkins and Schevill, 1979;
Gaskin, 1982;
Hain et al., 1995; Corkeron,
1999). Gaskin, who reported both lateral and regular lunges for fin whales off
the southwestern coast of Nova Scotia
(Gaskin, 1982), suggested that
regular lunges were generally less effective and mainly directed towards fish
rather than euphuasiids.
Cetacean maneuvers are primarily driven by lift derived from the flukes and
by the asymmetrical orientation and/or movement of the flippers
(Edel and Winn, 1978;
Fish, 2002;
Fish, 2004;
Fish et al., 2006). Our data
show that body rotation, particularly roll, occurs during fluking bouts
associated with lunges (Fig.
9). However, rolling was sometimes observed during glides,
especially in individuals that exhibited regular lunges, suggesting that fin
whales employ both powered and non-powered lift-based mechanisms to maneuver.
Edel and Winn reported flipper movement and twisting of the caudal stock and
fluke during banked turns in the humpback whale
(Edel and Winn, 1978). Fin
whales performing lateral lunges at the sea surface exhibited strong fluking
in coordination with lateral extensions of a pivotal flipper
(Gaskin, 1982). We were not
able to discern flipper movement during lunges, so the extent to which torque
generated by the fluke was enhanced by control surfaces remains undetermined
for fin whales.
Although three-dimensional dive behavior has been described for phocid
seals (Davis et al., 2001;
Davis et al., 2003;
Mitani et al., 2003;
Mitani et al., 2004),
comprehensive data showing maneuvers effected by six kinematic degrees of
freedom have not been presented for any marine mammal. Our analysis was only
able to resolve two kinematic degrees of freedom with respect to body
rotation, so changes in yaw that occurred through the dive cycle were not
unknown. As a result, the roll moments recorded could have been associated
with maneuvering, as has been observed for beaked whales maneuvering to
capture prey (Madsen et al.,
2005). Considering the repeatable and modal nature of the
behaviors observed (Fig. 8), we
suspect that fin whales were spinning about their longitudinal axis, executing
lateral lunges similar to what was qualitatively described for humpback whales
at the sea surface (Jurasz and Jurasz,
1979) and along the sea floor
(Hain et al., 1995). However,
lateral lunge-feeding behavior can involve a curvilinear trajectory
(Gaskin, 1982). During regular
lunges, roll moments were often observed just before maximum velocity, perhaps
indicating a maneuver or banked turn towards a prey patch. These types of
complex maneuvers typically involve temporal coupling of yaw and roll moments
in flying animals (Schilstra and Van
Hateren, 1999; Horisawa et
al., 2003). More tagging efforts are necessary in order to
determine body yaw and thus resolve full three-dimensional dive behavior in
the context of local bathymetry and prey distribution
(Mitani et al., 2003;
Mitani et al., 2004;
Watanabe et al., 2003).
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Acknowledgments |
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K. Phillips WHALES LUNGE FOR LUNCH J. Exp. Biol., April 1, 2006; 209(7): iii - iii. [Full Text] [PDF]
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