Regulation of stroke and glide in a foot-propelled avian diver
1 Graduate School of Fisheries Sciences, Hokkaido University, Minato-cho
3-1-1, Hakodate, Hokkaido, 041-8611, Japan
2 NERC Centre for Ecology and Hydrology, Banchory, Aberdeenshire AB31 4BW,
UK
3 National Institute of Polar Research, Itabashi-ku, Tokyo,173-8515,
Japan
* Author for correspondence (e-mail: ywata{at}fish.hokudai.ac.jp)
Accepted 12 April 2005
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Summary |
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Key words: buoyancy, foot-stroke, dive, shag, Phalacrocorax aristotelis, data-logger, biomechanics
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Introduction |
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With the exception of penguins that swim by producing lift during both
upstrokes and downstrokes (Bannasch,
1995), diving seabirds generate forward thrust mainly by the
contraction of major muscles in order to make a propulsive downstroke with
their wings or push their webbed feet backwards (hereafter referred to as the
power stroke; Alexander, 1992
;
Rayner, 1995; Riback et al.,
2004
). Birds decelerate (hereafter glide) either during the
upstroke of the wings or during the forward movement of the feet. By
alternating the power stroke and the glide, seabirds have been shown to swim
within a range of speeds (Lovvorn,
2001
). However, most previous studies have been carried out using
birds swimming horizontally in shallow experimental tanks, where they
experience constant and high buoyancy. To understand fully the regulation of
power stroke and glide, it is essential to collect data on birds diving
vertically to depths over which they will experience large changes in
buoyancy. The recent development of micro data-loggers has enabled wing
propulsion of small seabirds to be measured in the wild using high frequency
sampling of acceleration of the body
(Watanuki et al., 2003
). To
date, however, similar measurements have not been made for foot-propelled
divers.
Shags and cormorants (Phalacrocoracidae) are foot-propelled divers.
Typically they descend directly (descent phase) to a given depth (from 10 m to
>100 m), where they remain foraging (bottom phase) before ascending
directly (ascent phase) to the surface
(Croxall et al., 1991;
Watanuki et al., 1996
;
Grémillet et al., 1998
).
To maximize feeding time, bottom-feeders should minimize transit time, and
hence descend and ascend vertically
(Houston and Carbone, 1992
;
Hansen and Ricklefs, 2004
).
Although shags and cormorants are less buoyant than many other diving birds,
in general, they are positively buoyant over the range of depths used for
foraging (Wilson et al.,
1992a
; Husler, 1992; Riback et
al., 2004
). Shags and cormorants make forward thrusts by pushing
both of their webbed feet backwards simultaneously, i.e. a power stroke
(Schmid et al., 1995
). Hence,
they are expected to make a forward thrust only during a power stroke.
To further understand how power stroke and glide are regulated to achieve efficient diving in foot-propelled divers, we deployed bird-borne miniaturised data-loggers on free-ranging European shags Phalacrocorax aristotelis (hereafter referred to as shags). The loggers enabled us to determine the body angle and the characteristics of foot strokes by recording heave (ventral-to-dorsal) and surge (tail-to-head) accelerations of the bird's body at 64 Hz. We used these data to test three hypotheses: (1) shags descend vertically; (2) shags use a range of swim speeds during descent; and (3) during dive descent shags decrease the frequency of the power stroke by increasing the duration of the glide. We also describe the body angle and the stroke pattern during the bottom and ascent phases.
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Materials and methods |
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A data-logger (16 mm in diameter, 60 mm long, mass in air 16 g; M190-D2GT, Little Leonardo Ltd, Tokyo, Japan) was attached in the middle of the lower back of each bird (Fig. 1). To keep the longitudinal axis of the logger parallel to the bird's head-to-tail axis, loggers were attached using two plastic cable ties and waterproof adhesive tape to a piece of plastic netting (3 cmx5 cm) glued among the feathers with a fast-setting glue (Loctite 401). The attachment process took less than 10 min, after which birds were released; 12 returned directly to the nest, two initially went onto the sea to wash and preen but were still back on the nest within 10 min. The nests of birds with loggers were checked each morning and evening and attendance of the pair and the brood size recorded on each visit. Birds were recaptured within 3 days of logger deployment and the devices removed.
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Data-logger
The loggers had a 16 MB EEPROM memory and recorded depth with a pressure
sensor (±1 m accuracy, FPBS-82A, Fujikura, Tokyo, Japan) every second,
and acceleration along the perpendicular axes with a capacitive accelerometer
(ADXL202E, Analog device, Norwood, MA, USA) at 64 Hz for approximately 24
h.
To calibrate the recorded acceleration values, gravity accelerations (9.8 m
s2) were recorded by each logger set at angles of 90°,
0° and 90°, respectively, to the horizon at room temperature.
Temperature effects of between 720° are <4% and do not require
corrections (Watanuki et al.,
2003). To measure the attachment angles of each logger along the
bird's body axis (
, Fig.
1), we arbitrarily selected ten samples of 4 s duration of surge
acceleration when the bird was on the surface between dives and the body axis
should have been horizontal (see appendix in
Watanuki et al., 2003
). The
average over 4 s was within 96102% of the overall average for each
bird, indicating that the attachment angle was stable during the deployment.
The estimated attachment angle (
) varied between 7° and
9° (Table 1).
|
Body angle, swim speed and stroke
For ten of the shags data-loggers were used to record surge and heave by
aligning the vertical axis of the logger parallel to the bird's
ventral-to-dorsal axis (Table
1). The remaining four birds were used to check for evidence of
sway (rightleft) acceleration by aligning the vertical axis of the
data-loggers parallel to the bird's leftright axis
(Yoda et al., 2001). There was
no evidence of any significant change in sway acceleration during descent or
ascent, indicating that birds did not produce accelerations around the yaw or
roll axes. Total acceleration recorded by the loggers could therefore be
separated into that due to gravity and that due to body movement. The high
frequency component (YH, Fig.
2C) of total surge acceleration (YG, thin line in
Fig. 2A) is caused by the foot
stroke while the low frequency component (YL, thick line in
Fig. 2B) is the gravity
component along the surge axis of the data-logger. Hence YL can be converted
to the angle of the data-logger relative to the horizon (
). YL was
obtained by removing the high frequency component with a filter.
|
|
Swim speed (V in m s1) was estimated as
V=R/sin for each second, where R was
vertical depth change rate (m s1) and
was body
angle. Thus, we could not estimate instantaneous swim speed but rather the
average value over a 1 s interval. Swim speed was not estimated during the
bottom phase because of the small depth change rate and shallow body angle.
Swim speeds previously estimated for a variety of seabird species indicate
that individuals typically cruise at between 1.5 and 2.0 m
s1 and rarely exceed 2.5 m s1 (e.g.
Schmid et al., 1995
;
Wilson et al., 1996
;
Ropert-Coudert et al., 2000
).
Thus, in our analyses we assumed that swim speeds greater than 2.5 m
s1 (N=113 records, 3% of cases excluding those in
the bottom phase) were due to errors in calculating body angle, and such
records were excluded from the dataset.
Heave and surge of the bird's body were given by correcting the logger
attachment angle () as follows:
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In cormorant species the power stroke is generated by sweeping the webbed
feet backwards and upward to make drag- and lift-based forward thrust
(Johansson and Norberg, 2003).
In great cormorants Phalacrocorax carbo swimming horizontally in
shallow water, the body is accelerated downward and forward during the power
stroke of the feet and decelerated during the glide or recovery phase
(Riback et al., 2004
). For
shags we also found that when the body accelerated downwards, it
simultaneously accelerated forwards (Fig.
3A,B). Hence, we classified power stroke and glide as,
respectively, negative and positive heave acceleration of the body
(Fig. 3). Peaks were apparent
in surge, which could be empirically defined if there were more than 0.16 m
s2 changes at 1/64 s intervals (see
Watanuki et al., 2003
)
(Fig. 3A,B). The number of
peaks of surge per second, counted by a Macro program on Igor (Tanaka et al.,
1999) was defined as the frequency of thrust.
Sample dives and analyses
Data from nine of the 14 birds could be used to measure acceleration. Data
from six individuals (three males and three females) carrying data-loggers
attached so as to record the heave-axis gave surge and heave acceleration
directly since the loggers were almost vertical (>75°;
Table 1) to the body axis of
the birds. For the other three individuals (including two for which sway
rather than heave was measured), we could only estimate uncorrected surge
acceleration since the attachment angle () (see
Fig. 1) was <2° and the
heave or sway axis of the loggers was not vertical to the body axis
(Table 1). From these nine
birds, we sampled 100 dives between 7 and 43 m deep that showed a clearly
defined bottom phase and no rapid changes of body angle or acceleration during
descent and ascent.
We ran separate statistical analyses on the descent, ascent and bottom
phases. For the descent and ascent phases, we carried out separate Restricted
Maximum Likelihood (REML; Patterson and
Thompson, 1971) analyses on body angle, frequency of thrust and
swim speed, with the exception of frequency of thrust during ascent, since
negligible thrust takes place during this phase and so no analyses were
necessary (see Results). For each analysis, we included individual as a random
effect, and instantaneous (i.e. current) depth (referred to in the results as
`depth') as a covariate. Previous studies have shown that diving seabirds may
change body angle and swim speed according to the bottom or maximum depth to
which an individual dives (Wilson et al.,
1996
; Sato et al.,
2002
; Watanuki et al.,
2003
). We therefore also included mean bottom depth as a covariate
in the analyses. An interaction term between current depth and mean bottom
depth was also included. For the bottom phase, we carried out analyses on body
angle and frequency of thrust only. Since instantaneous depth and mean bottom
depth are almost identical during the bottom phase, only the former was
included in the analyses. In addition, there were consistent differences in
bottom depth between individuals, resulting in the REML analyses not producing
robust results. Therefore, we pooled data for all individuals and used linear
regression analyses with ANOVA. In total, three analyses were carried out on
the descent phase, two on the ascent phase and two on the bottom phase.
To analyze the stroke pattern during descent further, we sampled 17 `deep
dives' (>40 m) from three birds for which surge and heave were measured. We
sampled heave and surge acceleration over 1 s intervals at depths of 1 m, 2 m,
5 m, 10 m, and at 5 m intervals thereafter to 35 m. In each 1 s sample, there
were between one and three strokes from which we selected one at random. The
duration of the power stroke and glide, and maximum positive heave and surge
acceleration were measured on the print out of the data. The sum of the
duration of the power stroke (the period when the heave was negative) and the
duration of the glide (the period when the heave was positive) was defined as
the stroke cycle (Fig. 3A,B),
and the reciprocal of the stroke cycle as the frequency of the power stroke.
Effects of current depth on the frequency of power stroke, power stroke
duration, glide duration, maximum heave acceleration and maximum surge
acceleration were examined using five separate REML analyses, each with
individual as a random effect and current depth as a covariate. In all REML
analyses, significance of variables and interaction terms was determined by
comparing Wald statistics with percentiles of 2 distributions
(Elston et al., 2001
).
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Results |
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For the subset of 100 dives from the nine birds where surge and body angle were measured, the distribution of depth change rate showed a trimodal pattern with gaps between 0.6 to 0.3 m s1 and +0.3 to 1.0 m s1. Accordingly the descent and ascent phases were defined as depth change rates below 0.6 m s1 and above 1 m s1, respectively. Birds were classified as being in the bottom phase of the dive if they had a narrow range of depth change rates between 0.3 m s1 and +0.3 m s1. 113 (1.4%) of records could not be classified into these categories and were therefore excluded from subsequent analyses.
|
At the start of the descent, body angle was almost vertical (80°) but became significantly shallower (70 to 60°) by the time a bird reached a depth of 510 m depth (Fig. 4A, Table 2). There was a significant effect of mean bottom depth on body angle during descent, with body angle remaining closer to vertical on deeper dives. There was a significant interaction between depth and mean bottom depth such that for a given depth, body angle was steeper on deeper dives (Fig. 4A,Table 2). The frequency of thrust decreased with increasing depth and increased with mean bottom depth (Fig. 4B, Table 2). The interaction between depth and mean bottom depth was significant with the frequency of thrust decreasing less rapidly on deeper dives (Fig. 4B, Table 2). Swim speed did not vary with depth but was significantly higher for dives with greater mean bottom depth (Fig. 4C, Table 2). The interaction between depth and mean bottom depth was not significant.
|
There was a highly significant decrease in the frequency of the power stroke with depth (Fig. 5A, Table 2) due to a fivefold increase in glide duration and a 1.2-fold increase in power stroke duration (Fig. 5B, Table 2). Maximum heave acceleration recorded during a power stroke declined significantly with depth, but there was no effect of depth on maximum forward surge during a power stroke (Fig. 5C,Table 2).
|
Behavior during the bottom phase of the dive
There was no evidence of a cyclic surge during the bottom phase
(Fig. 3C), indicating that
shags did not swim horizontally using a cyclic power stroke. Mean body angle
of individuals during the bottom phase of the dive was negative and varied
between 10 and 69° (overall mean for all individuals
35°) for 100 dives. We found a positive and significant effect of
depth on body angle such that body angle increased from
42±20° at 2025 m depth to 33±14° at
4045 m depth (Table 2).
Depth did not affect the frequency of thrusts.
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Discussion |
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We also assumed that the angle of dives was the same as the body angle.
Great cormorants swimming horizontally in shallow (<1 m) water have a
negative tilt (angle of body axis against swimming direction) of
615°, which gives negative lift, presumably to compensate high
buoyancy (Riback et al.,
2004). When the shags have a body angle of 70° during
descent, the maximum error of estimated speed is 15% allowing 15° of tilt.
In our study we did not measure tilt directly but as shags descended almost
vertically they might not require tilt to compensate buoyancy. Clearly it
would be advantageous to collect information on body angle and tilt for shags
but until such data are available we believe that the assumption that the
angle of dive is equivalent to the body angle is reasonable.
Regulation of stroke
Buoyancy in cormorant species of similar mass to European shags has
previously been estimated to be between 2.2 and 8 N at the surface, to have
decreased markedly by 2040 m, and to remain positive down to depths of
at least 100 m (Lovvorn et al., 1991b;
Wilson et al., 1992a;
Riback et al., 2004
). In our
study, in which shags did not dive deeper than 40 m, birds ascended passively
from this depth, indicating that they had positive buoyancy down to at least
40 m.
During descent shags maintained an approximately constant swim speed and
apparently responded to decreasing buoyancy by reducing the frequency of
thrust by decreasing the rate of power strokes (Figs
4A,
5A). A decrease in the
frequency of forward thrusts during descent has also been described in
Brünnich's guillemots Uria lomvia, a wing-propelled diving
seabird (Watanuki et al.,
2003).
Shags did not alter the maximum forward thrust acceleration in a power
stroke during descent (Fig.
5C). They decreased the maximum heave acceleration, but the
decrease was small (<5%). Therefore, a decrease in the frequency of forward
thrusts, rather than a change in strength, was the main mechanism used to
adjust average forward thrust. This decrease in the frequency of stroke was
not achieved by varying the duration of the power stroke, which showed only a
slight (1.2-fold) increase with depth; rather, shags adjusted the duration of
the glide (fivefold variation; Fig.
5B). Our findings therefore support the general idea that seabirds
keep within a range of high physiological efficiency of contracting muscle
(Goldspink, 1977;
Pennycuick, 1996
;
Lovvorn et al., 1999
;
Lovvorn, 2001
). However, in
zebra finch Taenopygia guttata flying in a wind tunnel, contractile
velocity in the pectoralis muscle changes with flight speed
(Tobalske et al., 1999
). The
regulation of strokes in air and water therefore needs to be compared using
consistent technique.
The pattern of regulation used by a foot-propelled species such as the
European shag, apparently differs markedly from that of wing-propelled divers
such as penguins and auks. Magellanic penguins Spheniscus
magellanicus, generate forward thrust on both the downstroke and the
upstroke (Bannasch, 1995), and
decrease the amplitude and the frequency of the wing stroke while they are
descending (Wilson and Liebsch,
2003
). Brünnich's guillemots have a higher frequency of
forward thrust during descent to 20 m due to forward thrust being produced on
the downstroke and the upstroke, but forward thrust occurs only on the
downstroke at deeper depths (Watanuki et
al., 2003
).
|
Body angle and swim speed
Shags descended and ascended almost vertically and hence minimized transit
time between the surface and foraging depth. However, below 5 m on the
descent, body angle became significantly less vertical (60 to
70°; Fig. 4). The
reason for this change is obscure. One possibility is that birds make
horizontal movements as they descend in response to shoals of fish near the
bottom. This potential benefit in terms of increased prey capture presumably
offsets the cost of increased transit time (for example a 3 s increase in
descent time at a body angle of 70° and 1.6 m s1
swim speed over a depth range of 1040 m). Hustler
(1992) hypothesized that
diving birds keep the body angle vertical in order to stay down, particularly
in shallower water where buoyancy is greater because the birds have to direct
force downward. In our study shags had a significantly shallower body angle
when they foraged in deeper water, also supporting this hypothesis.
During ascent, body angle became less vertical (8060°) above 5
m. An oblique ascent angle in penguins has been suggested to allow birds to
search both the vertical and horizontal components of the water column
(Wilson et al, 1996) or move
horizontally by using increased buoyancy near the surface
(Sato et al., 2004
). However,
shags are generally believed to feed almost exclusively during the bottom part
of the dive rather than during the ascent. Sato et al.
(2002
) suggested that slowing
down near the surface could be one way of potentially avoiding decompression
sickness in King penguins Aptenodytes patagonicus diving deeper than
100 m. However, in shags ascending from depths of less than 40 m the decrease
in body angle was small and ascent swim speed was still high near the surface
(Fig. 4B), so this explanation
is unlikely in this case.
Shags descended at an approximately constant swim speed (1.21.8 m
s1). To minimize the energy lost to the water through
friction, seabirds are suggested to keep within a range of speeds that
minimize the drag coefficient (Lovvorn et
al., 1999). During descent Brünnich's guillemots keep within
a range of swim speeds (1.21.8 m s1) that are
estimated to minimize the drag coefficient (1.21.5 m
s1; Lovvoren et al., 1999;
Watanuki et al., 2003
). In
contrast, in Brandt's cormorant P. penicillatus there is no clear
evidence, based on the drag coefficient vs Reynolds number curve
(fig. 8 in Lovvron et al., 2001), to support the idea that this species
selects the maximum speed that avoids a rapid non-linear increase in drag.
Thus the reason why shags keep within a narrow range of swim speeds while they
descend is uncertain.
Effects of bottom depth
During the breeding season shags on the Isle of May feed predominantly on
sandlance Ammodytes marinus, which they catch on or just above the
seabed (Wanless et al.,
1991a,b
).
In the present study we found that, on average, shags maintained a body angle
of 35° during the bottom phase of the dive and rarely showed active
horizontal swimming. This suggests that the birds may move relatively slowly
over the seabed and concentrate their foraging effort in one place with the
body pointing down towards the sand. Therefore, they are most likely to
determine their foraging site and depth prior to each dive, and have the
potential to regulate swim speed, body angle and stroke pattern depending on
the depth finally attained as well as the depth changes during descent.
Because of air compression, buoyant resistance decreases dramatically with
depth. Based on biomechanical modeling, it is suggested that seabirds can
decrease mean mechanical power output when they make deeper dives
(Hansen and Ricklefs, 2004).
Assuming that shags do not change the pre-dive air volume according to the
bottom depth, our data support this idea. Shags decreased the mean frequency
of power stroke throughout the descent phase as they made dives with deeper
bottom depth (Fig. 6). Maximum
heave acceleration of the body by power stroke did not vary greatly with depth
and actually decreased slightly with depth
(Fig. 5). Thus mean mechanical
power output per unit time should decrease as the birds make dives with deeper
bottom depth.
In conclusion, we have shown that foot-propelled diving European shags descend almost vertically. They decrease the frequency of the power stroke with increasing depth, possibly in response to decreasing buoyancy. This regulation is achieved mainly by changes in glide duration. Birds appear to maintain the duration and maximum strength of the power stroke and thus optimize muscle contraction efficiency.
List of symbols
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Acknowledgments |
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Footnotes |
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Present address: International Coastal Research Center, Ocean Research
Institute, University of Tokyo, Otsuchi, Iwate, 012-1102, Japan
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