How do cormorants counter buoyancy during submerged swimming?
1 Faculty of Biology, Technion Israel Institute of Technology,
Israel
2 Faculty of Aerospace Engineering, Technion Israel Institute of
Technology, Haifa 32000, Israel
* Author for correspondence (e-mail: zarad{at}tx.technion.ac.il)
Accepted 23 March 2004
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Summary |
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Key words: buoyancy, diving, kinematics, underwater, cormorant, Phalacrocorax
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Introduction |
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Buoyancy has especially severe implications for diving birds because the
primary anatomic adaptations of birds are for flying. Low body density and
large air volumes (in the respiratory tract and in the plumage) aid birds in
reducing flight costs, resulting in increased buoyancy and thus increased
diving cost (Lovvorn and Jones,
1994; Wilson et al.,
1992
). It has been estimated that, during vertical dives (dives to
the bottom and back), ducks invest up to 95% of the mechanical work generated
by the feet against buoyancy (Stephenson
et al., 1989
). In birds that dive in search and pursuit of prey
(horizontal divers), buoyancy acts at a perpendicular direction to the
swimming direction and hence acts as a de-stabilizing force. Wilson et al.
(1992
) and Lovvorn and Jones
(1991
) showed that horizontal
diving birds are relatively less buoyant than surface swimming or vertical
diving birds, probably due to reduced plumage air volume. Another relatively
simple way to reduce the effect of buoyancy without increasing flying cost is
to dive to depths where ambient pressure compresses the air volumes of the
body (Hustler, 1992
;
Lovvorn et al., 1999
;
Wilson et al., 1992
). Both of
the above mechanisms seem to apply to some cormorant species, as cormorants
have a reduced plumage layer that presumably contains less air
(Lovvorn and Jones, 1991
;
Wilson et al., 1992
), and
telemetry and diet studies of free-ranging cormorants have shown that foraging
focuses on benthic prey (Gremillet and
Wilson, 1999
; Kato et al.,
2000
; Wanless et al.,
1992
). However, cormorants are opportunistic hunters, attracted to
areas of high prey density, and demonstrate high variability of dive sites and
dive depths (Boldreghini et al.,
1997
; Gremillet et al.,
1998
). Cormorants are especially interesting in the sense that
they seem to master both flying and submerged swimming. Although higher than
that of surface-feeding birds, the specific weights of cormorants, measured in
carcasses (Wilson et al.,
1992
) and in forcibly submerged live birds
(Lovvorn and Jones, 1991
), are
still considerably low (
0.8x103 kg
m3). This means that unless the actual specific weight of
voluntary diving cormorants is much higher, shallow-diving cormorants are
still required to invest considerable work against buoyancy.
Cormorants swim underwater by synchronized feet propulsion, with the wings
tightly folded close to the body (Schmid
et al., 1995). The shape of the body is streamlined, with no
specific control surfaces. This reduces the drag on the body but renders
control of destabilizing forces more difficult than for shapes with fins
and/or other control surfaces. Previous studies considered feet propulsion to
be drag-based, as the thrust is generated by kicking the feet backwards, in
the opposite direction to the moving body
(Baudinette and Gill, 1985
).
However, recent reports (Johansson and Lindhe Norberg,
2000
,
2001
;
Johansson and Norberg, 2003
)
have shown that the trajectory and the angle of attack (AoA) of the feet in
cormorants, grebes and perhaps other foot-propelled birds are consistent with
hydrodynamic lift-based propulsion, at least for the later parts of the
stroke. This is because the feet move backwards at about the same speed as the
swimming speed of the body and hence have an almost zero horizontal speed
compared with still water, while there is a large vertical speed component to
the feet trajectory. Thus, hydrodynamic lift may be the major
thrust-contributing force in foot propulsion. In the case of the cormorant,
the trajectory of the feet during the stroke also suggests a significant
vertical force component that can be used to oppose the positive buoyancy.
The question remains: how do cormorants manage to efficiently divide their power output between forward thrust and the maintenance of vertical stability during shallow, straight, horizontal dives?
Here, we study the underwater swimming kinematics of the great cormorant
(Phalacrocorax carbo sinensis), emphasizing the balance of forces in
the vertical direction. The buoyancy of the cormorant, as in other birds, is
relatively high for a submerged swimmer (=
0.8 kg
m3), suggesting the use of specific mechanisms to remain
submerged during underwater horizontal swimming. Specifically, we tested the
contribution of hydrodynamic lift of the body and the tail as well as feet
propulsion to offset effects of buoyancy during horizontal submerged
swimming.
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Materials and methods |
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All animals were trained by rewarding desired behavior with a fish. The animals were trained to perform the following routine: (1) step on an electronic balance, (2) enter the pool used for the experiments through a small window (50x50 cm) connecting the pool with the aviary and (3) dive inside a mesh channel placed on the floor of the pool (see description below). Training lasted two weeks at the most, after which all birds were repeating the desired tasks in response to a vocal or a visual signal from the trainer.
Morphometrics of carcasses
Body mass, density (buoyancy), the position of the center of mass, and
dimensions of the body, tail and feet were measured on carcasses of wild
cormorants shot over fishing ponds as part of a wildlife management program.
Less than two hours elapsed from shooting to freeze-storage of the carcasses.
Measurements were conducted after fully defrosting the birds at room temp
(18°C). Density was measured using the displacement volume technique
(Lovvorn and Jones, 1991
;
Wilson et al., 1992
) with the
following modification. We lowered the carcass (head first) at a 45° angle
and placed it horizontally on the bottom of a flat tank (40x30 cm),
filled with 40 cm of water up to a small outlet tube. The water displaced by
the carcass was collected and weighed to the nearest 1 g. Measurements lasted
3-4 min, during which the carcass was submerged. We made no correction for air
lost from the plumage during that time or for the air volume in the air sacs.
We did, however, seal the throat of the carcass with a cable tie prior to the
measurement to prevent air loss from the trachea during submergence. We chose
to measure the carcass horizontally since we were interested in measuring the
buoyancy of the carcasses at shallow depths. Performing the measurement in a
horizontal position, rather than vertically (see
Lovvorn and Jones, 1991
),
ensured minimal compression of the plumage air and decreased the pressure
gradient over the long axis of the body, which might facilitate air loss from
the plumage. To fit the carcass horizontally in the tank, the neck was folded
backward alongside the body. The position of the center of mass along the long
axis of the body was found by laying the carcass (neck stretched) on a flat
1x0.1 m rod, balanced on a swiveling pole (diameter 7 cm). By sliding
the carcass toward one end of the rod, the position of the point of balance
(distance from the tip of the bill) was found and marked. We assumed that the
center of mass is located on the body midline due to bilateral symmetry. We
made no attempts to measure the exact dorso-ventral position of the center of
mass due to the limitation of the technique.
The cormorant carcasses were positively buoyant. As a result, underwater,
the point where pitch moments are balanced along the longitudinal axis of the
body is determined by the position of the center of mass and the center of
buoyancy (Webb and Weihs,
1994). We termed this point `center of vertical static stability'.
To find the position of the center of vertical static stability of the
carcasses we repeated the procedure in a 30 cm-deep pool where the carcass and
apparatus were completely submerged. The carcass was secured to the apparatus
by three fixed metal cables (same length). The cables pressed the carcass
toward the rod at distances 0 and ±25 cm from the center of rotation.
The apparatus was carefully brushed of air bubbles prior to the underwater
measurements.
The position of the center of mass on the body of the carcasses was allometrically applied to the live trained birds, based on their body length. Similarly, buoyancy of the trained birds was estimated based on their body mass.
The planar area of the left foot of 22 carcasses was measured from
photographs. The feet in the photographs were fixed to an angle of 110°
between digits IV and I (Fig.
1A), similar to the shape of the foot during paddling observed in
our trained birds (110±6°; mean ±
S.E.M.; N=9 birds). We defined the
span of the foot as the maximal projection of the plan of the foot (between
digits I and IV) on the lateral proximal/distal axis of the bird (the
direction perpendicular to the swimming direction). During the stroke, the
foot and the tarsusmetatarsus (TMT) were oriented laterally at an angle of
16±2° (N=9 birds) away from the midline of the body (and
the swimming direction). To account for this change in foot orientation
relative to the motion in the backward and upward directions, the span
measurement was preformed with the left foot rotated at 16° clockwise (see
Fig. 1A). The foot is a thin
surface and, as such, has a significant added mass (the mass of water
accelerated with the foot) only at high AoAs. To calculate the added mass, we
use elongated body theory (Lighthill,
1970), which shows that all elliptic cross-sections from a circle
to a disk with the same diameter will have an added mass approximately equal
to a cylinder of the same diameter. We used a scanned planform photograph of a
left foot of a bird (digit I=4.4 cm; digit IV=10.2 cm) and measured the local
chord of the foot every 6 mm along its span. We then calculated the projected
length of each chord in the cross-flow that results from positioning the foot
at the local AoA. Next, we used each two projected lengths determining a
section (6 mm wide) on the foot as diameters of a circle and calculated the
volume of the section as a truncated cone. Finally, we integrated the volume
of all cones to yield the mass of water moved with the foot. The virtual mass
(M
) is then the sum of the mass of the foot and the
mass of the water moved with it at the specific AoA. The mass of the foot used
as reference was 0.018 kg in air. We used a water density (
) of
103 kg m3 to convert the volume of water to
mass.
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Experimental setup
Birds entered the pool (8x5 m; 1 m deep) one at a time. The pool was
divided into two sections, connected through a straight 7 m-long metal mesh
channel, with a rectangular 0.5x0.5 m profile, placed on the floor of
the pool. The mesh of the channel was a 0.02x0.05 m grid. A door at the
entrance to the channel allowed timing of the dives through the channel. The
opening of the door provided the auditory and visual signal for the birds to
enter the channel and swim along it until exiting from the other side and
receiving a fish as a reward. A 2 m-long section of the channel, starting 3.5
m away from the entrance, was used as the test section. The position of the
test section along the channel was chosen to allow sufficient distance for the
birds to develop straight and uniform swimming prior to the measurement of
swimming parameters. The testing section was equipped with a mirror
(2x0.7 m) angled at 45° above the channel. The birds were filmed
swimming in the test section using a CCTV video camera (VK-C77E; Hitachi),
inside an underwater housing, connected to a S-VHS video (HR-S7600AM; JVC).
The camera was positioned 0.5 m above the bottom, 2 m away from the middle of
the testing section, and covered the testing section and the mirror, allowing
both lateral and dorsal (through the mirror) views of the swimming bird using
a single camera. The channel was positioned along the floor at the center of
the pool, at least 1 m away from the nearest wall. We calculated the ground
effect (Hoerner, 1975b) on the
cormorants and found it to be negligible beyond a distance of one body
thickness (maximum distance between dorsal and ventral sides of the body) from
the floor at a Reynolds number of >106, and hence used only
swims that were >10 cm distant from the floor. The upper 0.5 m height
limitation of the channel ensured that the birds were swimming away from the
surface at a distance of more than four times the body thickness. Hence,
formation of surface waves by the swimming bird and the resulting added drag
were considered negligible. This was also confirmed by observation of the
absence of surface deformations.
Kinematics
Video sequences were converted to separate digital fields (50 fields
s1) using a video editing system (Edit 6; Autodesk Inc., San
Rafael, CA, USA). The data derived from each field were thus separated by a
time interval of 0.02 s from the previous and next fields. The position of
specific points on the birds in each field was measured using Scion Image
(Scion Corp., Frederick, MD, USA). The points measured
(Fig. 1B,C) were: the tip of
the bill from the side (point 1 in Fig.
1) and from above (point 9), the base of the foot (joint between
the tarsusmetatarsus and digits) from the side (point 4), the tip of digit IV
from the side (point 5) and from above (point 12), and the base and the tip of
the tail from the side (points 6, 7) and from above (points 13, 14). Two
additional points at the center of the body from the lateral and dorsal view
(points 3, 11) were marked by gluing (SuperWiz, Loctite glue) small round
distinguishable tags (1.5 cm in diameter) onto the center of the wing facing
the camera and on the back of the bird along the longitudinal midline of the
body. From the glued tags and the base of the tail, four additional points
were calculated trigonometrically by applying their position from the
morphometric data, measured on the carcasses, relative to the digitized points
(3, 6 and 11, 13). These points were the center of mass (points 8, 15) and the
point of connection between the body and neck (base of neck; points 2, 10). We
also digitized the point of maximum curvature of the dorsal and ventral sides
of the body in the lateral view. We used these points (15, 16 in
Fig. 1) and the point at the
base of the tail (6) to measure the mean sloping angle of the aft (rear end)
of the body. We used a Cartesian 3-D-axis system throughout the work to
describe the position of the points, where X is the horizontal
direction of swimming, Y is the vertical direction (height of the
channel, up/down) and Z is the lateral direction (width of the
channel, left/right).
Only complete paddling sequences with no significant side motions were analyzed. The sequences taken included one complete paddling cycle that followed at least three earlier cycles of horizontal straight swimming and was followed by at least another cycle of horizontal straight swimming. The points from the upper view were used to isolate straight swimming sequences where no neck turns to one side were evident (tip of bill compared with mid body point). The position of the point (11) marked on the back, relative to the frame of the channel, was used to measure the distance of the bird from the camera for scale and parallax elimination. A total of five swimming sequences for each of the nine birds was analyzed. Several sequences had an average slight vertical deviation during the cycle, i.e. the birds were swimming with a small angle to the water surface (<6°). To account for this, the mean straight path of the bird was calculated for each sequence as a straight line connecting the starting and ending position of the bird's marked point (3), and all calculations of tilting angles and positions are presented relative to this mean swimming direction. A similar procedure was applied for the upper view using point 11.
For analysis, the body length of the birds was divided into three subunits (Fig. 1C): neck (N), body (B) and tail (T). N was defined between the points of the tip of the bill and the base of the neck, thus including the head and neck (between points 1 and 2). B was defined between the base of the neck and the base of the tail, including the folded wings (between points 2 and 6). T was defined from the base to the tip of the tail (between points 6 and 7). Using the digitized points, we measured for each field the following:
In the kinematic analysis of the dorsal view, it was not possible to follow the base of the foot (point 4 in Fig. 1) during paddling, as it passed beneath the body and tail. For the analysis of foot motion in the XZ plane during the stroke, we used an additional set of video sequences, obtained separately, showing ventral views of the swimming birds during paddling. To obtain these sequences, a mirror was placed on the bottom of the channel at a 20° angle. The video camera was tilted at 50° below the horizon towards the mirror. The horizontal distance of the camera from the center of the mirror was 89 cm. The upper corners of the mirror protruded 16 cm into the channel, and the feet and ventral side of the birds were filmed at 2040 cm above the bottom. To minimize error from parallax, due to the proximity of the camera, we measured a scale calibration factor for each of the junction points of a 5x6 cm grid placed horizontally in the channel and elevated by 5 cm between measurements. We thus calibrated a volume in the center of the mirror (55x30 cm and 20 cm high) and assigned the correct value to each digitized point based on its coordinates.
Model of hydrodynamic resistance to buoyancy
To test the hypothesis that lift from the body and tail, as well as part of
the propulsive force, can be used to counter buoyancy, we used a mathematical
model based on quasi-steady fluid dynamics. The compatibility and contribution
of the hydrodynamic forces to vertical stability was tested by estimating the
magnitude and direction of forces and comparing the resultant vertical force
with buoyancy.
The lift generated by a tilted body can be calculated using the equation:
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For the lift force generated by the tail, the model (equation 1) is similar
but we used values of CL/
(0.035; from
fig. 13 in chapter 18 of Hoerner,
1975b
) relevant to delta wing theory and A as the
planform area of the tail [tail length=0.178±0.006 m; span at the
trailing edge= 0.086±0.004 m, values are the means ±
S.E.M. from the video sequences of nine
birds; aspect ratio (AR) is the ratio of span2/wing area,
AR=1]. We used the geometric area of a trapezoid with bases of 0.086
m and 0.02 m and a height of 0.0138 m as the planform area of the feathers of
the tail (A=0.00731 m2). The tail is trailing after the
body and, as a result, the flow it encounters is affected by the streamlining
of the aft of the body (Evans et al.,
2002
; Maybury et al.,
2001
; Maybury and Rayner,
2001
). To calculate the actual AoA of the tail, we measured the
slope between points 17 and 6 (Fig.
1C) on the dorsal side and 16 and 6 on the ventral side of the
posterior tip of the body. We used the average of the two slope angles as an
estimate of the direction of flow encountered by the tail and calculated the
AoA as the difference between this average direction and the tilting angle of
the tail. While this estimate may not be an accurate description of the actual
flow over the tail, it is probably closer to reality than neglecting the
effect of the body altogether.
The propulsive forces generated by the feet are mainly the result of
hydrodynamic lift, hydrodynamic drag and inertia (acceleration reaction). When
the foot motion has a vertical component, lift generated by the feet can be
directed forward. The generated lift results in added drag (induced drag), and
the generated drag and (generally) the inertia are directed in the opposite
direction to the moving feet, mainly downward. Assuming that the feet may be
considered as lifting surfaces (Johansson
and Norberg, 2003), we used coefficients from the literature for
lift (
CL/
=0.06; figs 3, 14 in chapter 17 in
Hoerner, 1975b
), induced drag
(Cdi=0.09CL2; figs 3, 4 in
chapter 7 in Hoerner, 1975a
)
and drag at zero lift (Cd0=0.007; fig. 2 in chapter 6 in
Hoerner, 1975a
) for a thin (4%
thickness to span ratio) profiled, low aspect ratio (AR=4) wing to
estimate the magnitude and direction of the force.
Lift of the feet is calculated as explained above for the body (equation
1), with the exception that the characteristic area used (A) is the
area of the foot. Drag is calculated as:
D=D0+Di, where
D0 is the drag of the foot aligned with the direction of
motion and Di is the induced drag due to lift when the
foot is tilted at an AoA=. The expansion of this expression is:
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![]() | (3) |
All forces were calculated for the left foot of the birds. The total force was then doubled to account for the contribution of the right foot.
Data analysis
All the swim sequences analyzed contained exactly one complete paddling
cycle. However, cycle duration and the relative portion of the power and
recovery phases of the cycles differed among individuals. To calculate the
average tilt angles and excursions during a paddling cycle, we normalized the
data for the average paddling cycle for all the birds. Each paddling cycle
included three distinct phases, based on the motion of the feet relative to
the body: (1) stroke, when the feet moved backwards, in the opposite direction
to the moving body, and the digits were stretched; (2) glide, when the feet
were stretched backwards with no movement relative to the body; and (3)
recovery, when the feet and legs moved forward in the direction of the moving
body and the digits were curled. The mean duration of each of the phases was
calculated from all the birds, and all sequences were normalized by dividing
the duration of each phase in the cycle by the mean duration of that phase.
Thus, instead of using actual time units, the data are presented on a scale of
01 of an average paddling cycle.
In the XY plane (see below), we used the model developed above to
calculate the magnitude and direction of forces generated by the feet during
the stroke. The webbed area of the foot resembles a triangle. We chose to
describe the motion of this surface in the XY plane using a point
located at two-thirds of the distance between the base of the foot and the tip
of the longest digit (points 4 and 5 in
Fig. 1). This point represents
the center of the hydrodynamic forces on the foot. We calculated the forces
from each swimming stroke sequence using the velocity and trajectory of the
feet (first derivative) and the axial accelerations (second derivative) from
the translation of the foot in time using a piecewise four-points derivative
equation (Hildebrand, 1956).
The foot was assumed to produce propulsive forces as long as it had a positive
(up) vertical component of speed. We then calculated the mean force and its
variation from all the birds (N=9). To present the forces' direction
and magnitude, we also calculated the forces on a foot trajectory that is the
average of the trajectories from all the birds. Although this is not a true
trajectory, we chose to present these data because they averaged individual
variation in swimming speed, paddling frequency, foot trajectory and foot
size, which influences interpretation of the results. We discovered that the
average trajectory of the moving foot was a circular arch and hence used this
fact to calculate the direction and magnitude of speed and circumferential
acceleration of the moving feet, rather than using the more general
interpolation described above. We calculated the center of the circle and the
radius from the points on the perimeter and calculated the tangential speeds
and circumferential acceleration at each point from the change in arch length
traversed with time. Since these inertia and drag forces work on the same axis
as speed, and lift acts at a perpendicular angle, the direction of forces lies
on the radial and tangential axes of a circular motion, presenting a
simplified balance of forces. Not all foot trajectories followed a precise arc
of a circle (although this was quite common); hence, the more general approach
used for calculating individual sequences. At the point of transition between
the recovery and the stroke phases (first field of the stroke phase), the feet
may have some inertia from deceleration, although their speed is 0 m
s1. We did not account for this added force at that stage
since it is a consequence of the recovery phase and it is mainly in the
swimming direction (horizontal) and therefore irrelevant to vertical force
balance.
Statistical analysis was performed using STATISTICA (StatSoft Inc., Tulsa, OK, USA). The data set comprised five analyzed swims for each of the nine birds. To compare among birds, the means of the five runs for each bird were used (N=9). Significance level was set to 95% (P<0.05).
Throughout, error values are presented as ± standard error of the mean (S.E.M.).
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Results |
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Added mass at different AoAs ranged from 0 kg (atAoA=0) to 0.166 kg
(at AoA=90°).
Kinematics of body and tail
The mean swimming speed of all the birds (N=9), calculated as the
distance traveled in one paddling cycle divided by cycle duration, was
1.50±0.03 m s1 or equivalent to 1.98±0.09 bird
lengths s1. The mean paddling frequency was 1.60±0.04
Hz. The birds used burst-and-glide swimming in all the runs. The paddling
cycle consisted of three distinct phases, as described above. The mean period
of a paddling cycle comprised 0.156±0.003 s for the stroke phase (25%),
0.292±0.031 s for the glide phase (47%) and 0.175±0.008 s for
the recovery phase (28%). The mean swimming speed was significantly correlated
with body length (r2=0.77, P<0.02,
N=9).
Birds accelerated during most of the stroke phase but started decelerating toward the end of the phase, continuing to decelerate during the following glide and recovery phases (Fig. 2).
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Tilting of the body, tail and neck units relative to the mean swimming
direction changed distinctively during the different phases of the paddling
cycle (Fig. 3). The body and
tail units maintained a negative angle to the mean swimming direction
throughout the entire paddling cycle (in an average sequence, the ranges of
these angles were 14.5°< B<6.1°
and 18.4°<
T<5.2° for the body
and tail, respectively).
N was mostly negative but reached
0° at the beginning of the glide phase. During the stroke phase, the
changes in
B,
N and
T
were rapid. The tilting angle of the body unit initially increased
(
B decreased since
B<0) and then
decreased. By contrast, tilting of the tail initially decreased and then
increased during the stroke phase. Tilting of the neck unit decreased
throughout the stroke phase until the neck was aligned with the swimming
direction (
N=0). In the following glide phase, the tilting
angle of the body and the tail gradually decreased and remained fairly steady
until the next stroke, except a slight increase in the tilt of the body during
the recovery phase coupled with a slight decrease in the tilt of the tail. In
general, the body was tilted further than the tail during the stroke and less
than the tail during the glide and recovery phases. Tilting angle of the neck
gradually increased from the middle of the glide phase and during the recovery
phase.
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Deviations from the average straight path are presented in Fig. 4 for the center of mass and other points on the body and in Fig. 5 for the points on the neck. The mid-line of the body followed closely the mean direction of swimming in the horizontal (XZ) plane, with no visible yaw or sideslips. In the vertical (XY) plane, the center of mass descended steeply during the stroke phase, followed by a relatively moderate ascent during the longer glide and recovery phases. The base of the neck (the lowest point on the body when it is tilted at a negative angle) followed the same descent and ascent pattern as the more posterior point of the center of mass. This implies that the observed vertical excursion was not just the outcome of rotation of the body previously described (as the body performs the tilt) but rather that the entire body was descending. The vertical excursions of the base of the neck were only 2 cm on average but were in a clear consistent pattern in all the birds. The tip of the bill revealed a different moving pattern from the points on the body. It was moving in the opposite direction to that of the base of the neck during the stroke and recovery phases (Fig. 5).
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The pattern created by the change in tilting angles of the body during the
paddling cycle was similar in all the birds, but the absolute values of the
tilting angles varied slightly among and within birds. To assess the source of
variation, we tested for correlation between the mean B
during each paddling phase and the mean swimming speed. Indeed, the mean
B of the stroke, glide and recovery phases was weakly, but
significantly, positively correlated with swimming speed (N=45;
stroke r2=0.1, P<0.03; glide
r2=0.37, P<0.001; recovery
r2=0.18, P<0.005), indicating that in general
birds that swam slower tilted their body further (a more negative
B) and vice versa.
In the average paddling cycle, for the range of swimming speeds and AoAs,
the lift generated by the body is in the range of 0.72.9 N. During the
stroke phase, when body tilting is maximal (B<<0), the
lift generated by the body at the instantaneous swimming speed is sufficient
to offset over 60% of the buoyancy. At the end of each cycle, where the speed
is low and the tilting of the body is relatively low, the body lift force
still offsets 30% of the buoyancy. The mean offset of buoyancy (due to body
lift) for the entire paddling cycle was 40%. The lift of the tail adds a down
thrust during the glide and recovery but during the stroke it actually works
in the direction of buoyancy. The total contribution of the tail to countering
buoyancy (down thrust) was 13%.
Feet kinematics
During the stroke, the foot motion (as described by the positions of the
center of hydrodynamic forces of the foot surface) could be divided into two
stages. In the first stage (fields 16), the foot had a lateral (away
from the midline of the body) motion in the XZ plane
(Fig. 6A) and moved upward and
backward. Due to the forward speed of the body, the backward motion of the
foot resulted in only a small horizontal motion relative to still water
(Fig. 6B). By field 4, the feet
ceased to move backwards relative to the water but, in fact, continued moving
backward relative to the body up to field 6
(Fig. 7), at which point the
vertical motion of the foot also ended. In the second stage (fields
68), the foot had only a medial motion (towards the midline of the
body) while following the body in the vertical (Y) and horizontal
(X) directions (Figs
6,
7). This stage was associated
with digit abduction (closure) as the overall planar area of the webbed feet
decreased. The second stage, therefore, contributed little or any to the
thrust of the bird, an assumption that was corroborated by the fact that the
instantaneous speed of the birds decreased after field 6
(Fig. 2). The first stage of
the stroke is thus the power phase of the paddling cycle (the phase when
thrust is applied). During the recovery phase, the feet moved forward,
parallel to the midline of the body, with no visible lateral motions. Since,
during the effective part of the stroke, both feet move laterally in opposite
directions, the lateral forces will cancel each other out, leaving only the
thrust component that is directed in the XY plane. Hence, our
analysis focuses on the XY plane, where pitch moments and vertical
adjustments are more likely to take place.
|
|
The back-sweep motion of the foot followed roughly the contour of the ventral side of the body. Since the body was at maximal tilt during the stroke, the feet were further directed upward during most of the stroke phase (Fig. 7). An analysis of the AoA of the webbed area of the feet compared with the foot trajectory (Fig. 8) shows that the drag and inertia generated by the moving feet are directed mostly downward, in the opposite direction to the moving feet. However, the lift generated by the AoA of the feet would act towards the center of the circle that forms the trajectory arch (Fig. 8). The lift, drag and inertia forces, generated by the moving feet in the XY plane, are directed mainly at a downward angle relative to the swimming direction. The overall propulsive force (resultant vector) is therefore directed below the actual swimming direction, thus actively offsetting buoyancy.
|
Fig. 9 describes the model's prediction of magnitude and direction of the resultant propulsive force generated by the cormorant (both feet) in the XY plane during the power phase (fields 16). The forces in each field are the averages of all the birds. It serves to show that the overall thrust generated by the feet (drag, inertia and lift) is directed well below the swimming direction (the resultant vector of thrust being directed at 44°). Thus, the thrust generated by the feet in the XY plane serves equally to produce forward motion and to counter buoyancy.
|
Fig. 10 summarizes the net vertical forces produced by the lift of the body and tail and the vertical forces of the foot. The vertical component of the propulsive forces of the feet during the stroke phase exceeds the buoyancy and the positive lift of the tail. This results in the downward motion of the body during the stroke phase and in the up-drift during the glide and recovery phases. For the entire paddling cycle, the vertical component of the propulsive force counters 32% of the buoyancy. Combining the vertical forces of the lift from the body and tail and from the forces of the feet, the vertical force offsets for the entire paddling cycle are about 85% of the positive buoyancy.
|
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Discussion |
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It seems that by simply tilting their body and tail, the cormorants can
roughly halve the effect of buoyancy while swimming horizontally. This implies
an interesting fact: since the buoyancy of birds is mainly the result of
compressible air volume, the reduction in the up-thrust due to body and tail
lift is equivalent to diving at a depth of approximately 10 m. This depth is
well within the diving range of cormorants and is close to the median dive
depth of 6.1 m reported for free-ranging great cormorants by Gremillet et al.
(1999) or to the average dive
depth (10.2 m) according to Ross
(1977
) (cited in
Johansgard, 1993
). Since
tilting of the body affects both the lift of the body and tail and the
vertical component of the propulsive force, it would be interesting to see if
the horizontal swimming of cormorants is optimized for a depth of
10 m,
at which
B can be close to zero during the glide, thus
reducing body drag and hence increasing the distance traveled per paddling
cycle.
It is evident, however, that lift from the body and tail per se is not enough to cancel out buoyancy at 1 m depth. Therefore, the cormorant must invest propulsive energy directly to resist up-thrust.
Cormorants propel themselves through the water by sweeping their feet along
an arch extending from an anterior point along the body's main axis to a
posterior point underneath the tail. The symmetry of the lateral motions of
the feet cancel out the lateral forces (as demonstrated by the fact that the
birds swim with no side-slip), and the net propulsive force is in the
XY plane. Our results are in agreement with Johansson and Norberg
(2003) regarding feet
trajectory and AoA, further indicating that the large vertical component of
the feet trajectory may be increased by the tilting angle of the body and thus
involved in buoyancy offset. Hence, by tilting the body at varying angles to
the swimming direction, the cormorant can shift the direction of the overall
thrust to give priority to resisting buoyancy or to forward motion.
Our estimates of the vertical forces accounted for 85% of the buoyancy of the carcasses. This small discrepancy can be explained by a combination of underestimation of the forces by using lift and drag coefficients obtained for rigid, smooth technical models and of overestimation of the buoyancy of the birds from the measurements on carcasses.
An interesting point regarding cormorant propulsion is that during the
stroke the feet are rotated mainly around the
tarsusmetatarsustarsustibia (TMTTT) joint. The knee and the hip
joints have a much reduced range of motion due to skin and muscle tissue and
due to the large patella (Johansgard,
1993). The TMTTT joint allows almost a 180° rotation of
the TMT around the TT, as evident when the birds are examined by hand or when
wild birds are observed perching on trees. Throughout our experiment, however,
the swimming cormorants seldom rotated the TMT about the TT in an angle
exceeding 90°. The reason for this behavior is unclear and may have an
anatomical explanation. However, the outcome of this limited bending of the
joint to an angle of 90° is that the range of motion during the stroke is
mainly in the vertical direction and, to a much lesser extent, in the
horizontal direction. Bending the joint to its maximum would allow the feet a
further thrust forward that is drag based
(Fig. 7). However, it will also
create a low drag (and optionally lift) component directed upward and even
more so when the bird's body is aligned with the swimming direction. It is
possible that cormorants bend their TMTTT only to 90° to avoid this
vertical component. For lift-based forward thrust, the feet need to move
perpendicular to the direction of the moving body. A 90° rotation of the
TMT about the TT, while the body aligns with the swimming direction, uses only
half of the vertical arch of a circle. Tilting of the body further shifts this
arch to a more vertical trajectory (Fig.
7).
The cormorant's use of lift for propulsion in the back of the body and the
vertical motions of the propelling appendages slightly resemble the swimming
of marine mammals. However, while cetaceans generate thrust by moving their
tails up and down, the power phase of the cormorant utilizes thrust from
motion in only one direction (up). The symmetrical vertical excursions of the
dolphin swimming (when repeated at equal speeds) cancel out, leaving a mainly
horizontal component of the propulsive force
(Fish, 1993). Our cormorants
seem to use a different tactic, as their asymmetrical paddling in the vertical
direction (only upward) is balanced by their high buoyancy, resulting in the
vertical drift pattern reported herein. This solves the problem of high
buoyancy, on the one hand, and allows the utilization of lift for forward
thrust from vertical motions of the feet, on the other hand.
The cormorant's tail moves separately from the rest of the body and serves
as a control surface, determining the tilting angle of the body throughout the
paddling cycle. During the end of the recovery phase and the following stroke
phase, the tilting angle of the tail changed in anti-phase with the angle of
the body, supporting the notion that it regulates and probably generates the
tilting angle of the body. During the end of the glide, the angle of the body
was kept approximately constant (and so was the steeper angle of the tail),
suggesting that a static pitching moment of the body was countered by the
dynamic pitching moment generated by the tail. This was corroborated by the
position of the center of vertical static stability measured from the
carcasses. This position was always slightly posterior to the center of mass,
meaning that the carcass was not statically stable and hence the body has a
tendency to tilt with the back of the body rising. While swimming, the tail's
posterior position and lift-generating geometry seems to offset and control
these pitching moments on the body, pushing down against the tendency of the
back of the body to tilt during the glide and during the beginning of the
recovery phase. During the stroke, the tail allows and initiates the pitch of
the body, forming the swimming pattern described herein. Only a few water
birds have developed tails to the extent of those of cormorants and anhingas.
The tail feathers of the measured carcasses in the present study constituted
22±0.2% (N=88) of the body length (from the tip of the bill to
the tip of the longest tail feather). They also comprise an area of
18.7±0.2% of the planar area of the body + tail as measured from
carcasses (N=5). The important role we find for the tail in
controlling pitch moments and thus in offsetting buoyancy may explain the
success of these aquatic predators in varying foraging sites, both shallow and
deep. The shape and function of birds' tails during flight has been widely
debated recently (Evans and Thomas,
1992; Hedenstrom,
2002
; Maybury and Rayner,
2001
; Maybury et al.,
2001
). It is generally assumed that the tail helps in maneuvering,
lift generation and drag reduction. Here, the tail seems to serve an
additional function. Unlike flying, during diving the propulsion of the body
is generated at a posterior point to the center of mass (Figs
6,
7) and the propulsive force
generated has a vertical component. This, combined with the fact that,
underwater, the center of vertical static stability is posterior to the center
of mass implies that pitching moments working on the cormorant during
horizontal swimming are substantial.
The neck and head also moved in antiphase with the rest of the body. We
speculate that these motions serve primarily in aligning the head in the
general direction of swimming as the body tilts. The function of such a
behavior can be to reduce drag on the head. These motions may also contribute
to stabilizing pitch moments; however, the laterally compressed shape of the
head and bill suggests that this added role, if it exists, is of minor
significance. Alternative suggestions (unrelated to hydrodynamics) include
visual performance and maintaining balance
(Katzir et al., 2001;
Warrick et al., 2002
).
The tilting of the body during the stroke phase serves to counteract
buoyancy. However, the birds pay an energetic toll for such a behavior. With
an increase in the AoA, the drag of the body increases, resulting in an
increase in the cost of transport. Since the steeper AoAs of the body are
performed during the stroke phase, when swimming speed is high, this is the
phase when the bird's body generates the highest drag. To reduce this added
cost, the cormorants use a burst-and-glide swimming pattern. In the shallow
dives analyzed herein, the average stroke phase lasted only 25% of the
paddling cycle. Burst-and-glide can result in significant energy saving
relative to sustained swimming, when propulsion increases the drag of the body
relative to gliding (Weihs,
1974). This condition seems to apply to the tilting behavior of
the cormorants.
Our trained cormorants were swimming in the experimental setup at speeds
and stroke frequencies similar to those previously reported
(Ancel et al., 2000;
Gremillet et al., 1999
;
Johansgard, 1993
;
Schmid et al., 1995
) and did
not show any difficulty in performing the shallow horizontal dives. Cormorants
in the wild may avoid high buoyancy by diving several meters below the
surface. However, there is a physiological and ecological cost for utilizing
only deeper water. The fact is that free-ranging cormorants in general, and
P. carbo sinensis in particular, often dive in shallow lakes and fish
ponds (Gremillet et al., 1998
,
1999
;
Gremillet and Wilson, 1999
).
The mechanisms detailed herein aid cormorants to cope with the high buoyancy
while foraging in shallow dive sites, increasing the range of diving sites and
depths utilized for efficient foraging.
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Acknowledgments |
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