Emperor penguins adjust swim speed according to the above-water height of ice holes through which they exit
Katsufumi Sato1,*,
Paul J. Ponganis2,
Yoshiaki Habara3 and
Yasuhiko Naito4
1 International Coastal Research Center, Ocean Research Institute,
University of Tokyo, 2-106-1 Akahama, Otsuchi, Iwate 028-1102,
Japan
2 Center for Marine Biotechnology and Biomedicine, Scripps Institution of
Oceanography, University of California San Diego, La Jolla, CA 92093-0204,
USA
3 Laboratory of Physiology, Department of Biomedical Sciences, Graduate
School of Veterinary Medicine, Hokkaido University, North 18, West 9, Sapporo
060-0818, Japan
4 Biologging Institute, 2-31-10, Rex Yushima 301, Yushima Bunkyo, Tokyo
113-0034, Japan
*
Author for correspondence (e-mail:
katsu{at}wakame.ori.u-tokyo.ac.jp)
Accepted 26 April 2005
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Summary
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Emperor penguins leap from the water onto the sea ice. Their ability to
reach above-water height depends critically on initial vertical speed of their
leaping, assuming that the kinetic energy is converted to gravitational
potential energy. We deliberately changed the above-water heights of ice hole
exits, in order to examine whether penguins adjusted swim speed in accordance
with the above-water height of the ice. Penguins were maintained in a corral
on the fast ice in Antarctica, and voluntarily dived through two artificial
ice holes. Data loggers were deployed on the penguins to monitor under water
behavior. Nine instrumented penguins performed 386 leaps from the holes during
experiments. The maximum swim speeds within 1 s before the exits through the
holes correlated significantly with the above-water height of the holes.
Penguins adopted higher speed to exit through the higher holes than through
the lower holes. Speeds of some failed exits were lower than the theoretical
minimum values to reach a given height. Penguins failed to exit onto the sea
ice in a total of 37 of the trials. There was no preference to use lower holes
after they failed to exit through the higher holes. Rather, swim speed was
increased for subsequent attempts after failed leaps. These data demonstrated
that penguins apparently recognized the above-water height of holes and
adopted speeds greater than the minimal vertical speeds to reach the exit
height. It is likely, especially in the case of higher holes (>40 cm), that
they chose minimum speeds to exit through the holes to avoid excess energy for
swimming before leaping. However, some exceptionally high speeds were recorded
when they directly exited onto the ice from lower depths. In those cases,
birds could increase swim speed without strokes for the final seconds before
exit and they only increased the steepness of their body angles as they
surfaced, which indicates that the speed required for leaps by emperor
penguins were aided by buoyancy, and that penguins can sometimes exit through
the ice holes without any stroking effort before leaping.
Key words: data logger, leap, kinetic energy, gravitational potential energy, buoyancy, Emperor penguins
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Introduction
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The dependence of emperor penguins on diving and foraging in the marine
environment necessitates frequent exits from the ocean onto the sea ice, on
which they breed, rear chicks and rest. Because of the presence of predators
at the ice edge, there is considerable pressure for emperor penguins exit the
sea safely and efficiently. They should leap to exit onto the sea ice. Their
ability to reach above-water height depends critically on the angle and speed
of their leaps. In a video study of Adélie penguins exiting the water,
Yoda and Ropert-Coudert (2004
)
concluded that Adélie penguins adjust their take-off angle according to
the reflected image of the height of ice above the water. However, it is not
known whether penguins also alter their swim speeds proportionately to the
required height of the exit.
We deliberately changed the above-water heights of two ice holes through
which emperor penguins exited. Swim speed, stroke frequency, body angle and
depth were monitored using animal-born recorders. Time of exit and hole choice
of penguins were simultaneously monitored by observers on the ice. We obtained
the first field data to test the hypothesis that penguins adjust swim speed
according to the above-water height of holes. We also described their behavior
after failed exits onto the sea ice and determined whether they change holes
after failed exits and/or whether they increase their swim speed in the
subsequent trials.
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Materials and methods
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Emperor penguins Aptenodytes forsteri Gray were captured near the
ice edge of McMurdo Sound, Antarctica and additionally, in 2003, four penguins
were collected when they passed near our study site. A total of 14 birds in
2003 and 16 birds in 2004 were maintained in a corral at a sea ice camp for 2
months prior to release. The sea ice camp was located on the fast ice of
McMurdo Sound, approximately 8 km and 100 km away from the ice edge in 2003
and 2004, respectively. Two ice holes, 1.2 m in diameter and 8 m apart were
drilled through the 2.3-2.5 m thick ice in the corral. The holes were plugged
by corks during the night to prevent Weddell seals from hauling out on the
ice. When the holes were open, birds voluntarily dove through the two dive
holes to forage beneath the sea ice.
Recordings
Multi-sensor data loggers (W1000L-PD2GT: 22 mm diameter, 124 mm length; 80
g in air; Little Leonardo Corp., Tokyo, Japan) were used to record swim speed
at 0.25-s intervals for six deployments in 2003 and 0.125 s intervals for
seven deployments in 2004, depth at 1 s intervals, two-dimensional
accelerations (for detecting flipper movement from heaving acceleration and
body angle from surging acceleration; see
Sato et al., 2004
) at 1/16 or
1/32 s intervals, and ambient temperature at 10 s intervals. The data loggers
were attached to the back of penguins using waterproof Tesa tape
(Wilson and Wilson, 1989
) and
plastic cable ties. Swim speed was recorded as rotations of an external
propeller. It was converted to swimming speed using the calibration method of
Sato et al. (2003
). The data
loggers were deployed on the birds for 26.1-60.9 h. During the deployment,
birds repeatedly entered and exited through the holes with the other
non-instrumented birds.
Behaviors of the instrumented birds were monitored [time (h:m:s) of exit
and hole choice by birds] and recorded. A total of six deployments on four
birds were monitored from November 12 to Dececember 6 in 2003 and seven
deployments on five birds were monitored from November 14 to December 5 in
2004. Body masses were measured using a platform scale at deployment and
retrieval of the recorder. Body mass at deployment, ranging from 22.2 kg to
29.5 kg (Table 1), were used
for analysis. Food intake during the daily dives has been inferred from guano
deposition on the ice (Ponganis et al.,
1997
) and confirmed by animal-born video cameras
(Ponganis et al., 2000
). They
usually gained weight during the daytime and lost weight during the night.
The above-water heights of the two ice holes (between the edge of the ice
and sea surface) were purposefully changed between two holes and among
deployments in 2003 (Table 1).
At the beginning of the second year (from 7th to 10th deployments), the
above-water heights of the holes were purposefully adjusted within 10 cm
difference (Table 1). The
heights were modified with a chainsaw and ice chisel. Positions of higher and
lower holes were occasionally changed between deployments. Underwater
observations of departures and returns to the dive hole were made from a
sub-ice observation chamber (Kooyman,
1968
).
Analyses and graphics were performed with IGOR Pro (version 3.1) and
StatView (version 5.0). The results of statistical tests were assumed to be
significant at P<0.05.
Calculations
Consider a penguin of mass Mb that exits for a leap
with initial vertical velocity V. As the penguin rises to the highest
point in its leaping and lands on the ice on its belly, the vertical velocity
falls to zero, and the associated kinetic energy just under the sea surface is
converted to gravitational potential energy on the ice:
 | (1) |
where g is the gravitational acceleration (=9.807 m
s-2) and h is the above-water height of the hole
(Fig. 1). The initial vertical
velocity to reach the highest point is given by:
 | (2) |
When Yoda and Ropert-Coudert
(2004
) developed a similar
model for Adélie penguin's leaping, they considered the distance
between the center of gravity of a penguin and its feet, because Adélie
penguins land on the ice on their feet. Emperor penguins land prone on their
belly. According to the observation, they could climb on the ice using their
flippers and feet if the center of gravity reached the height of the ice
surface (see the left penguin in Fig.
1). This is the reason that we did not consider the distance
between the center of gravity and its belly. The maximum swim speed within 1 s
before the exit was compared with the theoretical vertical velocity.
Considering the narrow diameter of the hole (1.2 m), body angles of penguins
were close to vertical. However, they could sometimes leap with a non-vertical
body angles (
in Fig.
1), especially when the above-water height of the ice at the hole
was low. The theoretical vertical velocity could be considered to be the
minimal swim speed to reach the above-water height of the ice. Note that the
required speed is independent of the mass of bird in
Eq. 2. This is why data from all
birds were pooled when comparing measured speeds and the above-water heights
of the ice at the holes.

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Fig. 1. Schematic diagram of exit options for the penguins. As shown on the left,
the bird could climb onto the ice if the center of gravity reached the height
of the ice around the hole, or the exit speed was sufficient to project the
bird onto the ice (the right-hand bird).
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Fig. 2. Typical profiles for last 20 s before exit through the ice hole in 6th
deployment by bird no. 314. The closed circle indicates the maximum swim speed
before exit. Horizontal bars indicate strokes based on acceleration.
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Results
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The nine instrumented-penguins performed 232 exits from the lower hole and
154 exits from higher hole in 13 deployments
(Table 1; see supplementary
material). They failed to exit onto the ice in 37 of a total of 386 exits
(10%). Comparing the success:failure ratio of higher and lower holes, there
were significant differences in two deployments (first and third) in which the
difference in heights between two holes was the largest
(Table 1, Fisher's exact
probability test). In the other cases, there was no significant difference in
the success:failure ratio between higher and lower holes
(Table 1, Fisher's exact
probability test).
Swim speeds in relation to the above-water heights of holes
Fig. 2 shows typical depth,
acceleration and swim speed profiles before an exit from the ice hole. The
bird adopted a stroke-and-glide method as it approached the hole. Gliding
phases between wing strokes were observed. Swim speed fluctuated around 2 m
s-1 in correspondence with the stroke pattern. The final
acceleration with three strokes enabled the penguin to reach a speed of 2.8 m
s-1 in less than 2 s. The final decrease in speed indicates that
the bird leapt out of the water, because the propeller does not rotate in the
air. The maximum swim speeds within 1 s before exit, which is represented by a
closed circle in Fig. 2, were
used for further analyses.
The maximum swim speeds before exits were significantly correlated with the
above-water heights of the holes (Fig.
3, N=386 exits in 13 deployments by nine birds; Spearman
R=0.421, P<0.0001). Most speeds of successful exits were
above the minimum vertical velocity theoretically needed to reach the height
(solid curve in Fig. 3).
Swimming speeds of failed exits were sometimes lower than the theoretical
minimum values (Fig. 3).

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Fig. 3. Relationship between above-water height and the maximum speed before exit.
Observed data (386 exits in 13 deployments by nine birds are pooled) are
represented by closed circles (successful exit) and crosses (failed exit). The
solid curve is the theoretical line for initial vertical speed to reach the
height, assuming a take-off angle ( ) of 90° (see text for details).
If penguins adopt non-vertical body angles, higher swim speeds were needed to
obtain the necessary vertical speeds for the height, which are represented by
dotted curves for various take-off angles.
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In the first six deployments in 2003, the differences in the above-water
height of holes were larger than 10 cm
(Table 1). The maximum swim
speeds before exits from higher holes were greater than those of lower holes
and there were significant differences in the speeds between holes in four of
the six deployments in 2003 (two-tailed Mann-Whitney U tests;
Fig. 4). In following four
deployments from the 7th to the 10th in 2004, the above-water heights of the
two holes were almost the same level (to within 10 cm;
Table 1). There was no
significant difference in the four deployments (two-tailed Mann-Whitney
U tests; Fig. 4). In
the last three deployments, the differences in the heights between the two
holes were larger than 10 cm (Table
1). In these last deployments, the swim speeds in higher holes
were greater than those of lower holes and there were significant differences
in the speeds between higher and lower holes in one of the three deployments
(two-tailed Mann-Whitney U tests;
Fig. 4).

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Fig. 4. Box plots for the comparison in the maximum speed before exit between lower
(white bars) and higher (gray bars) holes for each deployment. The differences
in the above-water height of holes were less than 10 cm in four deployments
(from 7th to 10th). *P<0.05;
**P<0.01; ***P<0.001; two-tailed
Mann-Whitney U tests; n.s., not significant.
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Behavior after failed leaps
Penguins failed to exit onto the ice, in total, 37 times, and tried the
next exit within 1 min in 27 of those 37 cases. In these second exit attempts,
there was no tendency for them to choose the lower hole after they failed in
the higher hole. In these second attempts, there were 17 failed exits, the
birds selected the lower hole eight times, and the same higher hole nine
times. Ten initial failed leaps occurred at the lower hole. After these
failures, the birds tried the next exits in the higher holes in four cases.
They tried to exit at the same lower hole in the other six cases. There was a
significant difference between swim speeds for the failed exits and the
velocities for subsequent attempts (P<0.05, Wilcoxon signed-rank
test). Penguins adopted significantly higher speeds in the subsequent attempts
after failed exits.
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Discussion
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Data from this study demonstrate that penguins apparently recognize the
above-water height of ice holes and adjusted their swimming speeds before the
exit according to the height required to clear the ice around the hole. There
were no significant differences in speeds when the differences in height were
smaller than 10 cm (from the 7th to the 10th deployments in
Fig. 4). However, they adopted
higher speeds to exit through the higher holes than those through the lower
holes when the height differences were larger than 10 cm
(Fig. 4). There were
significant differences in exits speed through higher and lower holes in five
deployments but there was no significant difference in the other four
deployments, which might be because of the small number of exits in the 4th,
12th and 13th deployments (Table
1).
Pooled data from all 13 deployments indicate that the swim speed increased
significantly as the above-water height increased
(Fig. 3). When the above-water
heights were smaller than 20 cm, most observed swim speeds were much greater
than the minimal theoretical values (the solid curve in
Fig. 3). This might be because
of the shallow body angles of penguins. If penguins adopt shallow body angles
for lower ice heights, they need higher swim speeds to obtain the necessary
vertical speeds for the heights (as indicated by dotted curves in
Fig. 3). It is likely that
penguins chose vertical take-off angles and minimum speeds to exit through the
holes, especially for the higher holes (>40 cm), to avoid using excess
energy for swimming before leaping (Fig.
3).

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Fig. 5. An example of the last 12 s before exit through the ice hole in the 8th
deployment by bird no. 429. The closed circle indicates the maximum swim speed
before exit. Horizontal bars indicate strokes based on acceleration.
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According to observation from a sub-ice observation chamber, the birds
sometimes directly exited onto the sea ice from deep below the surface. Some
exceptionally high speeds (Fig.
3) were recorded in such cases.
Fig. 5 gives one example of the
direct exit from depth. This bird dived for 17 min 25 s, reached a maximum
depth of 53.3 m and directly exited through the higher hole (33 cm in height)
onto the sea ice. According to the theoretical calculation
(Eq. 2), aswimming speed of 2.5 m
s-1 was needed to exit through this hole. However, the bird reached
a maximum speed of 3.0 m s-1 before the leap
(Fig. 5). The bird did not
stroke for the final 7 s before leaping and it only increased the steepness of
its body angle to 58 degrees as it surfaced
(Fig. 5). Sato et al.
(2002
) demonstrated that
surfacing king and Adélie penguins could increase swim speed using
buoyant force without any stroking effort. Van Dam (2002) reported that, in
emperor penguins, the mean stroke frequency during final ascent to exit
(<0.70 Hz) was lower than that during the initial descent (0.92 Hz). The
present study indicates that leaps by emperor penguins were aided by buoyancy
and that they can sometimes exit through the ice hole without any stroking
effort before the leap. It appears that penguins might know that they do not
need to stroke if they reach enough speed in accordance with the above-water
height of the hole.
Several factors may contribute to the range of exit speeds observed in this
study. In some instances, birds were chased by a Weddell seal (observation
from a sub-ice chamber), so escape from predators might be one reason of some
of the high speeds. In addition, the kinetic energy of swimming penguins may
be converted not only to gravitational potential energy but also to the
creation of waves at the surface, and to kinetic energy of some amount of
splash. However, the present study could not deal with these aspects because
of the difficulty in obtaining quantitative information.
The birds may obtain information on the above-water height of each ice hole
before leaps because they repeated dives and commuted frequently between the
water and the ice throughout the deployments. According to our observation,
they sometimes surfaced in the ice hole for a while, looked at their
surroundings, and then made a brief excursion below the surface before exiting
through the hole. Yoda and Ropert-Coudert
(2004
) demonstrated that
Adélie penguin adjusted their take-off angle to move out of the water
onto the ice. This study indicates that emperor penguins also have a capacity
to adjust swim speed before exits according to the above-water height of the
holes, and that they decided to increase swim speed for subsequent trials
after failed exits, instead of selecting the lower holes.
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Acknowledgments
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We thank T. Knower Stockard, J. Heil, J. Meir, K. V. Ponganis and E.
Stockard for assistance in the field, and R. Kawabe and G. L. Kooyman for
comments on the manuscript. This study was supported by a grant from the
Japanese Antarctic Research Expedition, Japanese Society for the Promotion of
Science (15255003) and National Science Foundation grant OPP-0229638.
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Footnotes
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Supplementary material available online at
http://jeb.biologists.org/cgi/content/full/208/13/2549/DC1
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