Maneuverability by the sea lion Zalophus californianus: turning performance of an unstable body design
1 Department of Biology, West Chester University, West Chester, PA 19383,
USA
2 Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA
95039-9647, USA
3 Department of Biology and Institute of Marine Sciences, University of
California, Santa Cruz, CA 95064, USA
* Author for correspondence (e-mail: ffish{at}wcupa.edu)
Accepted 13 November 2002
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Summary |
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Key words: maneuverability, stability, turning, swimming, California sea lion, Zalophus californianus
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Introduction |
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The morphology of an animal dictates its movements and limits its locomotor
performance (Webb, 1984;
Weihs, 1989
,
1993
,
2002
;
Taylor, 1989
). Regardless of
locomotor mode (e.g. walking, swimming, flying), various morphologies that
foster maneuverability have evolved within animal lineages, while others have
enhanced stability. The wing geometry of flying vertebrates determines flight
maneuverability (Norberg,
2002
). Minimum turning radius performed by fish is affected by
body and fin morphology (Webb,
1976
,
1983
,
2002
;
Blake et al., 1995
;
Webb et al., 1996
). Boxfishes
(Ostracion) use combinations of fins in conjunction with their rigid
body design for powered and trimming control of stability
(Gordon et al., 2000
;
Webb, 2002
). Differences in
the morphology of cetaceans are associated with turning performance and
habits. Rapid-swimming pelagic dolphins (i.e. Lagenorhynchus) with
compact bodies and restricted mobility of the flippers demonstrate high
turning rates (up to 453 degrees s-1) but have a greater
length-specific minimum turning radius compared with slow-swimming cetaceans
with more flexible bodies and mobile flippers
(Fish, 2002
). Cetaceans with
more flexible body designs sacrifice speed for maneuverability to function in
complex environments (i.e. pack ice, flooded forests or rivers).
Analysis was performed by Fish
(2002) that indicated that
certain morphological characteristics were associated with stability
performance in cetaceans. These characteristics were based on an arrow model
(Harris, 1936
;
Wegener, 1991
;
Fish, 2002
). Stability was
dependent on the location and design of control surface relative to the center
of gravity and on rigidity of the body. In that maneuverability represents a
controlled instability, the possession of morphological characters that
deviate from a design that maintains stability is expected to enhance turning
performance.
As opposed to cetaceans, which have specialized to a fully aquatic
lifestyle, all pinnipeds (sea lions, seals, walrus) possess a morphology that
permits various degrees of movement in both terrestrial and aquatic
environments (Fish, 1993,
1996
). The amphibious habits
of pinnipeds require use of the paired appendages for locomotion
(Howell, 1930
;
Ray, 1963
;
English, 1976
;
Gordon, 1981
;
Fish et al., 1988
). The
divergent body designs and modes of propulsion of pinnipeds suggest
differences in turning performance in water compared with cetaceans.
California sea lions (Zalophus californianu) have relatively large
flippers and highly flexible bodies (Ray,
1963
; Aleyev,
1977
). These sea lions are highly agile in water and have been
considered to swim with a high degree of maneuverability
(Godfrey, 1985
).
We quantitatively examined turning performance of Zalophus californianus using videography. As data are not available for other species of sea lion or fur seals, we compared data on turning performance of Zalophus californianus with similar data collected from cetaceans to assess how differences in morphology influence aquatic maneuverability.
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Materials and methods |
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The sea lions were maintained in an outdoor facility consisting of three interconnecting, saltwater pools (568 000 liter volume) with concrete decking for use as haul-out areas. Animals were tested in a 9.1 m diameter pool with a depth of 2.4 m. The sea lions were maintained on a diet of herring and capelin and were exercised daily and weighed weekly to ensure optimal body condition.
The sea lions were trained using classical and operant conditioning and positive reinforcement techniques to swim rapidly to a target that was affixed to the end of a pole. Each sea lion was directed by a trainer to swim from the concrete deck to a position on the opposite side of the pool indicated by a second trainer striking the target on the water surface. As the sea lion was arriving at the target position, the trainer on the deck recalled the animal with a second target strike. In this manner, the sea lions executed rapid 180° turns. Animals were given 5-min rests between five consecutive turns. White zinc oxide dots were placed on the dorsum and flanks of the animals at a position approximating CG.
Video recordings of sea lion turning were made using a Panasonic camcorder
(DV-510) at 60 Hz. The camcorder was held by an observer 2.7 m directly above
the position of the turn. Video records were analyzed frame-by-frame at 30 Hz
with a video recorder (Panasonic AG-7300) and video monitor (Panasonic
CTJ-2042R). Only those records in which the animal's body remained horizontal
to the water surface throughout the turn were used. The sequential positions
of the CG marker were recorded onto transparencies from the video monitor. As
the sea lions rolled 90° during the turn
(Godfrey, 1985), the position
of the lateral zinc oxide dot was followed through its curved trajectory. The
center of rotation of the turn was determined geometrically
(Youm et al., 1978
). This
technique allowed for determination of the trajectory of CG, despite
distortion in observing the actual position of the marker due to refraction
from surface waves. Absolute and length-specific values of turning radius
(r; measured in m and L, respectively) and average velocity
(U; measured in m s-1 and L s-1,
respectively) were measured. Centripetal acceleration (ac)
was measured in m s-2 and multiples of gravitational acceleration
(g; 9.8 m s-2), where ac was
computed according to:
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![]() | (2) |
As maximal performance was being evaluated, the highest values of turning velocity and turning rate and the smallest values of turn radius were reported for each sea lion. In addition, mean values for the extreme 20% of values were calculated. Means were calculated with variation expressed as ±1 S.D.). Comparisons of means were made using t-test (Data Desk, version 3.0). Regression equations and correlation coefficients were computed using KaleidaGraph version 3.0 software.
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Results |
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A total of 88 steered turning sequences was analyzed for the male (N=36) and female (N=52) sea lions. Sea lions approached the target position at a depth of 0.5-1.0 m below the water surface. Before initiating the turn, each sea lion was oriented with its venter facing ventrally, its pectoral flippers adducted (i.e. movement towards the midline of the body) against the lateral flanks of the body, and the pelvic flippers and the digits adducted. At the start of the turn, the head was displaced into the turn and rolled slightly by twisting and flexing of the neck. The pectoral flippers then were abducted (i.e. movement away from the midline of the body) and supinated (i.e. outward rotation) as the body rolled approximately 90°. The head and body were hyperextended, assuming a U-shaped configuration through the middle of the turn. The pelvic flippers were abducted. The digits of the pelvic flippers were also abducted, which spread the interdigital webbing and increased the projected area of the flippers. As the sea lion straightened the body at the end of the turn, the head and body were rolled, restoring the orientation of the body with the venter facing downwards. The pectoral flippers were pronated (i.e. inward rotation) and adducted against the body, increasing streamlining. The digits of the pelvic flippers were adducted, decreasing the area of the interdigital webbing, and the flippers were adducted so that they were oppressed with the plantar surfaces in contact to each another.
The above locomotor sequence was executed in 1.07±0.08 s and 0.90±0.25 s for the male and female sea lions, respectively. The smaller female had faster maximum absolute and length-specific turning velocities of 4.47 m s-1 and 2.61 L s-1, respectively, compared with the maximum velocities of 3.58 m s-1 and 1.89 L s-1 for the male sea lion (Fig. 1). For the fastest 20% of velocities (Table 2), the female sea lion swam statistically faster than the male (t=-6.56, d.f.=15, P<0.05). Turning radius was significantly different (t=-10.02, d.f.=15, P<0.05) between the two sea lions (Fig. 1; Table 2). The minimum length-specific turning radius of the male sea lion was 0.09 L, which was 43.8% smaller than the length-specific turning radius of the female.
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The maximum ac of the female sea lion was 1.84 times higher than that of the male sea lion (Table 2). When expressed as a multiple of g, the maximum value for ac was 5.13! Despite the difference in extreme values of ac between the two sea lions, the difference in body mass resulted in maximum centripetal forces that were not significantly different (t=2.00, d.f.=15, P>0.05) between the two animals.
Plots of ac as a function of turning rate
(Fig. 2) showed significant
correlations for both male (r=0.66, P<0.001,
N=36) and female (r=0.92; P<0.001,
N=52) sea lions. The equations describing the relationship are
ac=0.179+0.004TR for the male and
ac=-0.696+0.008TR for the female sea lions. The
slopes of these relationships were significantly different (t=21.90,
d.f.=84, P<0.001) (Zar,
1984).
|
F was found to increase linearly with v (m
s-1) for both sea lions (Fig.
3). Regressions of the data were found to be significantly
correlated at P<0.001 for r=0.70 for the male and
r=0.81 for the female. The regressions are described for the male and
female sea lion by the equations F=392.71+777.22v and
F=-1741.50+1243.50v, respectively. Comparison of the slopes
showed significant difference (t=11.78, d.f.=84, P<0.001)
for the two lines (Zar,
1984).
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Discussion |
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The control surfaces of sea lions are represented by pectoral and pelvic flippers. The roots of the larger pectoral flippers are located near the center of gravity. This placement of the pectoral flippers is dynamically unstable. The flippers provide little rotational dampening about the yaw and pitch axes (Fig. 4), although they could retard rotational and translational motion in regard to roll and heave, respectively. The smaller pelvic flippers are in the preferred location to develop sufficient torque to act like an aeroplane stabilizer or ship rudder and to resist rotational instabilities (Fig. 4).
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The attitude of the Zalophus flippers is highly variable because
of the high mobility of the pectoral and pelvic flippers
(English, 1976;
Godfrey, 1985
). Both the sweep
and the dihedral can be changed. Sweep resists yawing, whereas dihedral
combats roll (Breder, 1930
;
Hurt, 1965
). The ability of
the sea lion to adduct the pectoral flippers against the body and adduct the
pelvic flippers can effectively produce a condition where the animal is devoid
of control surfaces and potentially susceptible to all instabilities. The
mobility of the pectoral and pelvic flippers also permits dynamic production
of lift, which can induce torques around CG to promote instabilities. The
location of the pectoral flippers close to CG would not produce large torques
and would be less effective in rapidly inducing turns. The large projected
area of the flippers may help compensate for the reduced torque. However, the
pectoral flippers are used for propulsion
(Howell, 1930
;
Feldkamp, 1987
), and
propulsors arranged around CG are postulated to promote maneuverability
(Webb et al., 1996
).
The body of Z. californianus is highly flexible
(Fig. 5). Bending of the body
and neck is an integral component of turning in conjunction with the flippers
of pinnipeds (Aleyev, 1977;
Godfrey, 1985
). The extremely
pliable neck and body permit a sea lion to bend over backwards, reaching their
pelvic flippers (Riedman,
1990
). This dorsal bending was the preferred bending direction
used by sea lions during turns (Godfrey,
1985
; this study). Dorsal bending of the spine allows the body to
curve smoothly, maintaining a streamlined appearance throughout the turn. As
the turn is unpowered, a streamlined body will minimize drag and limit
deceleration as direction changes.
|
Humbolt penguins (Spheniscus humboldti) and beluga whales
(Delphinapterus leucas) bank during unpowered turns so that the
ventral aspect of the body is directed towards the inside of the turn
(Hui, 1985;
fish, 2002
). Although the
difference in bending direction may be due to vertebral mechanics
(Long et al., 1997
; Gal,
1993a
,b
;
Pabst, 2000
), the use of
banking appears to be common in animals that lack a dorsal keel and use the
pectoral appendages to resist slip. High bank angles provide a greater
projected area facing the axis of the turn.
For the cetaceans, there are multiple control surfaces (e.g. flippers,
flukes, dorsal fin and caudal peduncle) that are arranged in a configuration
promoting a higher degree of stability than in sea lions
(Fish, 2002). The flippers of
most cetaceans have limited mobility. One notable exception is the humpback
whale (Megaptera novaeangliae), which has long, mobile flippers and
is highly acrobatic (Edel and Winn,
1978
; Fish and Battle,
1995
). The humpback whale flippers are for maneuvering associated
with unique prey capture behaviors (Jurasz
and Jurasz, 1979
). However, flexibility in the body of cetaceans
is generally constrained (Bonner,
1989
; Long et al.,
1997
) by comparison to that of otariids.
Maneuvering performance
Turns by Zalophus were executed in a manner as previously
described (Ray, 1963;
Peterson and Bartholomew,
1967
; English,
1976
; Godfrey,
1985
). Horizontal turns were executed by extending the pectoral
flippers, spreading the pelvic flippers and flexing the body.
Similarities have been made between the turning maneuvers of sea lions and
the banking turns displayed by birds and aeroplanes
(Ray, 1963). In the latter
banking turns, the wings generate lift that is resolved into vertical and
horizontal vector components. The vertical component counters the
gravitational force and keeps the aircraft from losing altitude. The
horizontal vector is directed towards the center of rotation and provides the
centripetal force necessary for the turn.
As sea lions swim in an environment with a density similar to the body
composition, these animals can be near neutrally buoyant, negating the
necessity of a vertical component during turns in the horizontal plane. Thus,
the sea lion can bank 90° without changing depth. The horizontally
directed lift from the flippers would produce centripetal force necessary for
the turning maneuver. While the pectoral flippers can be rotated to produce an
angle of attack (i.e. angle between the flipper chord and the incident flow),
bending of the spine would aid in orientation of the flippers for lift
generation. However, there is no direct evidence that the flippers are canted
at an angle of attack to effect a turn. Indeed, the location of the flippers
close to CG reduces the torque to produce the turn. The pectoral flippers are
particularly important in generating lift necessary to roll the body. Other
surfaces used to control the turn are the head and pelvic flippers. The head
leads the turn and determines direction. The pelvic flippers act as
stabilizers to prevent the posterior portion of the body from deviating from
the curved trajectory of the turn
(Godfrey, 1985).
Minimum unpowered turn radii for the two sea lions were 0.16 m and 0.28 m,
representing 0.09 L and 0.16 L, respectively. While the
length-specific radii were small, they were not substantially different from
similar values for cetaceans. Minimum radii for unpowered turns by cetaceans
were reported to range from 0.10 L to 0.15 L
(Fish, 2002). The smallest
radius turn was displayed by the river dolphin Inia geoffrensis,
which had an extremely flexible body and mobile flippers
(Fish, 2002
). Fish display
smaller turning radii than the cetaceans. Domenici and Blake
(1997
) reported that the
knifefish Xenomystus nigri, angelfish Pterophylum eimekei
and pike Esox lucius had minimum turning radii of 0.055 L,
0.065 L and 0.09 L, respectively. Four species of coral-reef
fishes demonstrated minimum turn radii of approximately 0-0.06 L
(Gerstner, 1999
). Similarly,
the boxfish Ostracion meleagris was capable of a 0.0005 L
turn (Walker, 2000
). Such
tight turns in fish are due primarily to the use of multiple propulsors to
rotate about the yawing axis without translation.
Webb (1994) cautioned that
comparisons of turning radius between species should be made at mechanically
equivalent speeds. Despite their comparatively ordinary turning performance
with respect to radius, turning ability of Zalophus is shown to be
better than other marine mammals when turning velocity is considered as a
covariant (Fig. 6).
Zalophus generally can turn in smaller radii than cetaceans at the
same swimming speeds.
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Agility is defined as the rapidity in which direction can be changed and is
measured as the rate of turn (Norberg,
1990; Webb, 1994
).
The maximum turning rate of Zalophus was 690 degrees s-1,
and maximum centripetal acceleration was 5.13 g. Even though
these are singular values, sea lions were still able to turn at high rates of
513.8-599.2 degrees s-1 and 2.26-4.02 g for the
means of the maximum 20% of the data. Such performance is superior to turning
rates for cetaceans (Fig. 2).
Most turning maneuvers by cetaceans are performed at <200 degrees
s-1 and <1.5 g, although turns of 453.3 degrees
s-1 and 3.56 g have been measured in fast-swimming
Lagenorhynchus obliquidens (Fish,
2002
). Penguins have a turn rate equivalent to sea lions at 575.8
degrees s-1 (Hui,
1985
). Fish are capable of higher levels of agility compared with
marine mammals. Data from Webb
(1976
,
1983
), Blake et al.
(1995
) and Gerstner
(1999
) indicate that fish
ranging in size from 0.04 m to 0.39 m could turn at rates of 425.6-7300.6
degrees s-1. Such performance is extraordinary when it is
considered that species such as Salmo gairdneri and Micropterus
dolomieu are able to accelerate to 8.2 g and 11.2
g, respectively (Webb,
1983
).
Ecological relationships
The increased levels of maneuverability, which are displayed by
Zalophus, are associated with complexity of habitat. California sea
lions forage in waters near the mainland coast, being found no further than 16
km from the coast (King,
1983). They hunt in structurally complex environments, including
rocky inshore/kelp forest communities, along the continental shelf, around
seamounts and in the mouths of freshwater rivers
(Riedman, 1990
;
Reeves et al., 2002
).
Similarly, the river dolphin Inia, with its flexible neck and trunk
and mobile flippers, has a small minimum turning radius and occupies
complicated environments, including flooded forests and river systems. Faster
swimming, but less maneuverable, dolphins are found in oceanic, open water
systems (Fish, 2002
).
Coral-reef fishes were shown to have high maneuverability with turning radii
of <0.06 L (Gerstner,
1999
; Walker,
2000
). These fish must operate in a habitat that is confining due
to three-dimensional complexity of the corals.
Predatory behavior also necessitates high maneuverability and agility due
to the scaling effects between the predator and its prey
(Howland, 1974;
Domenici, 2001
). The turning
radius of a large aquatic predator will generally be larger than that of
smaller prey because turn radius is directly related to body mass. Although a
large predator can swim at higher absolute speeds, the prey has superior
turning performance for escape.
Zalophus feed on octopus, squid and fish, including herring,
anchovies, hake, whiting and salmon (King,
1983; Riedman,
1990
). These are fast-swimming prey that require high speed and
maneuverability for capture. Feeding is performed alone unless large schools
of prey are present, when the sea lions can feed cooperatively
(Riedman, 1990
). Prey size for
sea lions typically falls within the 10-30 cm range
(Bowen and Siniff, 1999
). Fish
within this size range can turn with a radius that is one order of magnitude
smaller than that of the sea lion and at rates of 0.7-11.1 times the maximum
rate of the sea lion (see above). Although elusive prey would appear to have
an advantage in terms of turning, the sea lion's pliable neck in conjunction
with its maneuverability could contribute to an advantage for the predator. In
the turning gambit envisioned by Howland
(1974
), closure distance (i.e.
straight line distance between predator and prey) is important in the outcome
of predator prey chases. The mobility of the neck along with its ability to
telescope can reduce closure distance and effectively decrease turn radius and
increase turn rate.
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Acknowledgments |
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