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First published online October 5, 2006
Journal of Experimental Biology 209, 3974-3983 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02482
Regulation of stroke pattern and swim speed across a range of current velocities: diving by common eiders wintering in polynyas in the Canadian Arctic
1 Centre for Wildlife Ecology / Behavioural Ecology Research Group,
Department of Biological Sciences, Simon Fraser University, Burnaby, British
Columbia, V5A 1S6, Canada
2 National Wildlife Research Centre, Canadian Wildlife Service, 1125 Colonel
by Drive, Raven Road, Carleton University, Ottawa, Ontario, K1A 0H3,
Canada
* Author for correspondence (e-mail: jpheath{at}sfu.ca)
Accepted 9 August 2006
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Summary |
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Key words: current, diving, swimming, wing stroke, glide, biomechanics, locomotion, drag, foot propulsion, underwater video
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Introduction |
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;
Lovvorn et al., 2004). Drag
also increases nonlinearly with speed
(Lovvorn, 2001), and recent
work using accelerometers on diving animals has shown that swim speed is often
maintained within a narrow range that likely minimizes energetic costs of drag
(Watanuki et al., 2003;
Lovvorn et al., 2004).
Propulsion by wings, flippers or feet during diving includes power and
recovery phases of muscle contraction, and limb orientation and instantaneous
velocity and drag can vary widely throughout stroke cycles. Additionally, as
depth increases during descent, less surge during the upstroke is required to
counter buoyancy, and downstrokes can provide primary thrust to maintain speed
of descent (Watanuki et al.,
2003; Lovvorn et al.,
2004). Different stroke patterns and intermittent gliding can
therefore be important in regulating swim speed and minimizing the energetic
costs of diving (Williams et al.,
2000; Watanuki et al.,
2003).
Costs of locomotion and the importance of swim speed and travel time to
foraging patches have received considerable attention in relation to diving
depth. However, there is almost no information concerning how currents affect
the behaviour and energetics of free ranging divers, and how animals regulate
their locomotion across a range of current speeds. Given the substantially
increased effects of drag with speed and expectation that animals should
travel at an average speed that reduces expensive drag costs [(see
Lovvorn et al., 1999;
Pennycuick, 1997) for flight],
strong current velocities could have a considerable influence on locomotion
and time and energy budgets of diving animals.
As drag increases with increasing speed, managing energy costs of diving
entails maintenance of a steady instantaneous velocity during locomotion, in
addition to regulation of average swim speed. This is because strong
drag-induced deceleration during the recovery phase requires strong
acceleration during the power phase to maintain average velocity
(Lovvorn et al., 1999;
Lovvorn and Liggins, 2002).
Maintaining a steady instantaneous velocity could be difficult when diving in
currents. Wing propelled divers can produce thrust during both the upstroke
and down stroke. Greater drag on the wings during the active part of the
upstroke will substantially influence the animals' ability to maintain
constant velocity for a given work per stroke and stroke duration
(Lovvorn and Liggins, 2002;
Lovvorn et al., 2004). In foot
propulsion, little or negative thrust occurs during the recovery phase, and
maintaining average descent speed requires increased instantaneous velocity
during the power phase, which substantially increases drag
(Lovvorn, 2001;
Lovvorn and Liggins, 2002).
Preliminary observations indicate free ranging eiders use both wing and foot
propulsion ubiquitously throughout descent. Co-ordination between wing and
foot propulsion could be particularly important in overcoming deceleration and
maintaining a steadier speed through stroke cycles.
Energetically efficient diving strategies must also incorporate efficient
muscle contraction rates, which are expected to involve constant work per
stroke (Lovvorn et al., 1999;
Kovacs and Meyers, 2000).
Therefore, efficient regulation of average swim speed can require the
maintenance of a constant contraction rate, stroke duration, and work per
stroke, all while altering stroke frequency and/or gliding between strokes.
This has been observed over increasing depths for both birds and mammals
(Williams et al., 2000;
Watanuki et al., 2003;
Lovvorn et al., 2004;
Watanuki et al., 2005).
Regulation of swim speed through altering stroke frequency and/or gliding
could be particularly important under increasing currents, as an increase in
swim speed relative to the fluid would be required just to maintain position
in the water column. Given strong non-linear increases in drag with speed,
maximizing energetic economy across increasing currents likely entails
regulating swim speed within a narrow range that reduces drag costs. Recent
work indicates that there is not a distinct breakpoint of increasing drag with
increasing speed (Lovvorn et al.,
2001); however, birds appear to regulate speed to avoid rapidly
increasing drag at higher speeds (Lovvorn
et al., 2004). Accelerometer data also indicate that efficiency of
muscle contraction is an important component determining efficient work
against drag (Lovvorn et al.,
2004; Watanuki et al.,
2005). Regardless of the mechanism, as currents increase, a diver
could regulate effective swim speed (relative to the water) by maintaining
stroke duration, work per stroke and stroke frequency. This would incur a
reduced vertical descent speed, and therefore an increased number of wing
strokes and time required to reach benthic foraging patches. Despite these
particular details, the component of dive costs due to drag is expected to
increase steeply and non-linearly with current velocity.
Among the Belcher Islands of south-east Hudson Bay, strong tidal currents
pass between islands; in winter, these currents maintain persistent open water
areas called `polynyas'. These polynyas are important winter habitat for a
variety of marine mammals and birds, including common eiders Somateria
mollissima sedentaria, which dive to the sea floor to forage on benthic
invertebrates (Gilchrist and Robertson,
2000). Current speed in these polynyas vary predictably from 0 m
s–1 at slack tide, to in excess of 1.5 m
s–1, providing a naturally occurring flume tank over the
tidal cycle. Preliminary observations showed that common eiders stop foraging
and rest on the ice edge at peak currents, leading us to question how tidal
currents influence their diving and foraging behaviour and affect their
ability to balance energy budgets during the winter in the arctic.
Data obtained from recent advances in animal-borne devices have helped
elucidate diving behaviour of birds and mammals at sea. However, logger
attachment is potentially invasive and may have negative effects on
hydrodynamics of birds (Ropert-Coudert and
Wilson, 2005). Further, both field and captive dive tank studies
have typically been restricted to a small number of individuals, and
individual variation in dive parameters is often high (e.g.
Halsey et al., 2003). In the
present study, the clear arctic water and restricted area of the open water
habitat allowed us to deploy a video camera beneath the ice so that we could
to record complete dives of approximately 100 wintering common eiders as they
descended to forage at a constant depth (11.3 m). Here we describe the diving
behaviour of common eiders in relation to variation in tidal current velocity
ranging from 0–1.0 m s–1. We investigate the prediction
that eiders respond to increasing costs of drag as current speed increases by
maintaining relatively constant swim speed and stroke patterns, at the cost of
increasing travel time to the sea floor. These varying time and energy costs
can have strong influence on foraging patterns over the dive cycle
(Houston and Carbone, 1992;
Thompson et al., 1993;
Boyd, 1997) and could be
particularly important for eiders attempting to balance their energy budgets
in the arctic during winter.
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Video analysis
From digital videos we recorded the durations of descent, frequency and
cumulative number of wing stroke and foot stroke cycles during each descent,
and the timing of wing stroke and foot stroke stages. Departure from the
surface was quantified as the frame in which the bill of the bird broke the
surface of the water. The time at which the bird reached the bottom was
determined by a change in the body axis to a horizontal direction, which was
also accompanied by cessation of wing flaps (only feet and not wings were used
while the birds were foraging at the bottom). The video recorded at 30 frames
per second (f.p.s.), and so maximum accuracy of calculated durations were
1/30th of a second. Wing flaps were counted by recording the point at which
the wings reached a fully closed position within the wing stroke cycle. Foot
strokes were counted when the leg reached full extension following the power
phase.
Quantifying tidal currents
We quantified tidal current velocities using a Nortek Aquadopp 3D current
meter (Vangkronken, Norway) with a directional fin deployed in the middle of
the water column (
5.5 m from the surface) on a mooring line anchored to
both the bottom and the sea ice within several meters of the polynya edge.
This device uses three acoustic beams to measure Doppler velocity to an
accuracy of 1% of measured value ± 0.5 cm s–1 sampled
at 23 Hz and set to average velocity over 10 min intervals throughout the
duration of the study. Synchronizing Aquadopp and video time therefore allowed
us to quantify an average current velocity associated with each eider's
dive.
To evaluate if mid-water current velocity was representative of the water column, we used a Nortek Aquadopp current profiler mounted below the sea ice near the edge of the polynya, within 5 m of where eiders were diving. This instrument allowed quantification of average current velocity within 0.5 m depth categories across the water column, at 10 min intervals (with the exception of current velocities within 0.5 m of the surface and bottom boundaries, which are not accurately quantified by this instrument). As data from this instrument indicated that, across the tidal cycle, there was extremely little variation in current velocity across depth categories (mean coefficient of variation across 24 h on March 05, 2003 was 0.003±0.002 m s–1), only data from the mid-water deployment Aquadopp was used in dive analyses.
Calculation of effective swim velocity
We used vector trigonometry to calculate effective swim speed (m
s–1) relative to the water, based on known vectors of
horizontal current velocity (current) and descent velocity (descent). Ducks
always dived directly into the current and ended upstream of their departing
point. We estimated an average dive angle of 10° given a known depth of
11.3 m and an average difference of about 2 m horizontal distance upstream
from where the birds departed the surface and arrived on the bottom (see
Fig. 1). Therefore, we
calculated swim speed relative to the water (swim) as:
 | (1) |
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Statistics
Regression analysis was used to determine relationships between the
durations of each diving parameter and current velocity. Quadratic regression
was used when it explained more of the variation in diving parameters, which
was expected as the effects of drag are known to increase non-linearly with
speed (Lovvorn et al., 1991).
JPM 5.0.1.2 (SAS Institute, Cary, NC, USA) was used for all statistical
analysis. Values presented in the text are mean ± the standard
deviation (s.d.).
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)], the
lack of bubbles generated by vortex shedding of the wing boundary layer
suggests that this was weak. The benign angle of attack in the direction of
travel suggests that forward momentum in this stage may be primarily through
passive gliding. Further, the head tended to be pointed downwards at the
steepest angle, almost orthogonal to the body axis, during this stage of the
wing stroke cycle (Fig. 2,
frame 5).
The transition phase was considered to have begun once the leading edge of
the wing began to travel downwards (Fig.
2, frame 7). During the transition phase between the upstroke and
downstroke, the trailing edge of the wings were still being raised and the
wings were oriented at a high angle of attack so that the broad side of the
wings were facing the direction of travel
(Fig. 2, frames 7–10).
This indicates there was probably significant drag occurring during this
stage, as suggested by Stettenheim
(Stettenheim, 1959) (see also
Lovvorn et al., 2004);
however, downwards surge to counter buoyancy could also be important in this
stage (Watanuki et al., 2003;
Lovvorn et al., 2004).
Numerous bubbles could be seen shedding off the tips of the secondary wing
feathers in this stage (Fig. 2,
frames 8–9, particularly visible in the bottom two rows). During the
transition phase, the head and neck orientation changed from parallel to its
steepest upwards angle with respect to the body axis
(Fig. 2, frame 10).
During the downstroke, both the leading and trailing edge of the wing were lowered, quickly closing the wings, during which the majority of propulsion appears to have occurred (Fig. 2, frames 11–13). The change in the movement of the trailing edge of the wing from being raised to being lowered is most obvious in the second row of Fig. 2, between frames 10 and 11, as the tips of the primary feathers change from being bent slightly backwards to being bent forwards. Although the steep angle of attack during the transition phase may have entailed considerable drag, this steep angle probably allowed a greater surface area of the wings to contact the water and facilitate propulsion in the downstroke. During the downstroke, the wings were oriented at a low angle of attack, with the broad side of the wings orthogonal to the direction of travel, which presumably reduced drag, increasing forward momentum. Vortex shedding across the tips of the primary feathers also appeared to occur during the final stage of the downstroke, in frames 12 and 13. Additionally, the neck tended to be fully extended parallel with the body axis throughout frames 12 and 13. Overall, neck and body orientation undulated across the wing stroke cycle, which left a distinct saw tooth pattern of bubbles in the water column.
Foot propulsion
Foot strokes were also divided into three categories, thrust, retract and
glide stages. Through the wing stroke cycle, the feet were most often in the
glide phase, which was defined as the legs being fully extended, parallel with
the body and with both feet tucked under the tail. Most often in this stage,
the toes were closed, which could further minimize drag across the webbing.
Foot retraction, or the recovery phase, was defined as the feet being pulled
forwards with the webbing closed (Fig.
2, frame 5–7). Foot retraction was immediately followed by
the power or thrust phase where the leg was quickly pushed backward with the
webbing extended, until the leg was fully extended backward
(Fig. 2, frame 8–10).
Fig. 3 illustrates the stages
of the foot and wing strokes and their timing corresponding with frames in
Fig. 2. This indicates that the
thrust phase of foot strokes corresponded with the transition between the
upstroke and downstroke of the wings, when the angle of attack and drag across
the wings was greatest. Feet were maintained in a gliding position throughout
the remainder of the wing stroke cycle, even though there was adequate time
for another foot stroke.
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Discussion |
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;
Lovvorn et al., 1999;
Lovvorn et al., 2004). For
divers employing drag-based foot propulsion, drag from trailing feet could be
high [(e.g. Pennycuick et al.,
1996) for flight] and deceleration and even negative thrust can
occur during the recovery phase (Lovvorn
et al., 1991). Generally, lift-based wing propulsion is more
efficient than drag-based foot propulsion
(Fish, 1993;
Fish, 1996;
Lovvorn and Liggins, 2002).
For each mode of locomotion separately, increased instantaneous velocity and
therefore increased drag costs during the power phase would be required to
counter deceleration during the recovery phase, in order to maintain a mean
swim speed that keeps work against drag within desirable bounds
(Lovvorn, 2001;
Lovvorn and Liggins, 2002).
Maintaining a more steady velocity through the stroke cycle can therefore
reduce energetic costs of diving (Lovvorn,
2001).
Common eiders diving in an arctic polynya used both wings and feet to power
their descent. Diving eiders exclusively timed the power phase of foot
propulsion with the transition between the upstroke and downstroke of the
wings, when drag is high across the steep angle of attack of wings (Figs
2 and
3). This timing could reduce
drag costs if it provided a more steady velocity through both foot and wing
propelled stroke cycles. For example, the use of multiple propulsors by
boxfishes (family Ostraciidae) can allow smooth thrust production and a steady
trajectory during swimming (Hove et al.,
2001; Gordon et al.,
2000). Similarly, river otters (Lutra canadensis)
coordinate hindlimb and tail propulsion to maintain a more constant velocity
during undulatory swimming (Fish,
1994). Integrating synergistic interactions among different
appendages during locomotion will be important for understanding the
energetics of swimming (see Dickinson et
al., 2000). Our observation of co-ordinated timing of foot and
wing stroke patterns suggests an important mechanism by which diving birds
could maintain steady velocity and reduce costs of diving.
Confirming that the alternating timing of wings and feet stroke patterns
provides the most efficient propulsion strategy for eiders would require
measuring instantaneous velocity throughout the stroke cycle (using
accelerometers or spatially referenced video) on birds diving with different
foot–wing stroke patterns, ranging from just wings or feet, to all
temporal combinations. This will be a difficult empirical challenge and
further insight will probably come from modelling (e.g.
Lovvorn et al., 2004). Eiders
kept their feet extended (glide phase) for a large portion of the wing stroke
cycle during which there was adequate time to complete an additional foot
stroke. This could have allowed foot thrust during the transition between the
downstroke and upstroke of the wings. The angle of attack of wings was low
during this stage, so deceleration due to drag may not be adequate to
necessitate an additional foot stroke, particularly if drag during retraction
of feet interferes with gliding. Undulation of the neck and body, as we
observed for eiders, could also be an important consideration in estimating
swimming costs based on dead-drag measurements
(Blake, 1983).
Influence of current velocity
At dive depths up to 11.3 m studied in this analysis, energetic costs to
counter buoyancy during diving are important but decrease with depth
(Wilson et al., 1992;
Lovvorn et al., 2004). Drag
increases at a slower rate than buoyancy decreases with depth, however, drag
can be one of the most important factors influencing the energetics of diving,
particularly as buoyancy decreases
(Lovvorn, 2001;
Lovvorn et al., 2004). Drag is
especially important in relation to increasing swim and current speed, as drag
increases rapidly with increasing speed
(Lovvorn et al., 1991).
Regulation of swim speed within a narrow range that controls drag costs has
been observed over a range of depths for diving Brünnich's guillemots
[1.6±0.2 m s–1 over presumably little current
(Lovvorn et al., 2004)] and
flight speeds of a variety of birds
(Pennycuick, 1997). Our
results indicate that eiders maintained a constant stroke frequency, and that
effective swim speed (relative to the fluid) only slightly increased as
current velocity increased (Figs
5 and
6). Overall, effective swim
speed was therefore regulated at 1.25±0.14 m s–1,
which is particularly impressive given that current velocities ranged from
0.04–0.97 m s–1 during these observations. Although a
distinct breakpoint of increasing drag relative to speed is not obvious from
tow-tank measurements for frozen eiders, the steeply accelerating drag curve
certainly suggest that swim speed is regulated to limit work against rapidly
increasing drag (Lovvorn et al.,
2001; Lovvorn et al.,
2004; Watanuki et al.,
2005; Dial et al.,
1997). The constant stroke frequency we observed may correspond to
an efficient maximum for eiders.
Regulation of swim speed and stroke frequency by necessity resulted in a
decrease in vertical descent speed relative to the bottom, and therefore
increased descent duration and the number of stroke cycles required to descend
to the bottom. While tightly regulated, effective swim speed significantly
increased by approximately 0.18 m s–1 with current velocity.
Overall, this would suggest an important increase in metabolic rate and oxygen
consumption during descent in faster currents
(Hawkins et al., 2000), and
the increase in number of wing strokes probably indicates increasing energetic
costs (Williams et al., 2000;
Williams et al., 2004).
Therefore, while common eiders employ a variety of tactics to reduce energy
costs during diving (timing of foot and wing strokes, regulation of stroke
frequency and swim speed), increasing currents nevertheless increase the time
and energy costs of descent to foraging patches. These costs are expected to
have a strong influence on time allocation over the dive cycles, particularly
on time available to forage at depth
(Houston and Carbone, 1992).
During fast currents, common eiders wintering at Ulutsatuq polynya get out of
the water and rest on the ice edge. Although swim speeds required to descend
in fast currents could be possible, the strong increase in drag and energetic
costs of diving potentially make foraging unprofitable. Consideration of these
factors will be particularly important in developing our understanding of the
energetics of diving by free ranging birds.
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Acknowledgments |
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