Buoyancy and maximal diving depth in penguins : do they control inhaling air volume?
1 National Institute of Polar Research, 1-9-10 Kaga, Itabashi, Tokyo
173-8515, Japan
2 Laboratory of Applied Zoology, Faculty of Agriculture, Hokkaido
University, Kita-9, Nishi-9, Kita-ku, Sapporo 060-8589, Japan
3 Japan Science and Technology Corporation, Domestic Research Fellow,
Hokkaido National Fisheries Research Institute, Katsurakoi 116, Kushiro-shi
085-0820, Japan
4 Laboratoire d'Océanographie Physique, Muséum National
d'Histoire Naturelle, 43 rue Cuvier, 75231 Paris Cédex 05,
France
5 Centre d'Ecologie et Physiologie Energétiques, Centre National de
la Recherche Scientifique, 23 rue Becquerel, 67087 Strasbourg Cédex,
France
* e-mail: ksato{at}nipr.ac.jp
Accepted 12 February 2002
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Summary |
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Key words: king penguin, Aptenodytes patagonicus, Adélie penguin, Pygoscelis adeliae, buoyancy, diving, dive depth, data logger, acceleration, biomechanics
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Introduction |
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For swimming penguins, the periodic alternation of up- and down-strokes of
the flippers induce oscillations of the body. This involves acceleration and
deceleration with each propulsive stroke
(Clark and Bemis, 1979;
Bannasch, 1995
). To investigate
the fine-scale movements of penguins in unrestrained dives under natural
conditions, we developed an acceleration data logger
(Yoda et al., 1999
).
Propulsive beating of the flippers, depth and swim speed were recorded every
second from Adélie and king penguins diving at sea. Using these data,
we first determined some diving characteristics of penguins, especially of
their flipper movements. Secondly, air volume in the body was estimated for
each dive of Adélie and king penguins using a biomechanical model.
Finally, the results are discussed in terms of biomechanical and physiological
constraints on optimal diving strategies.
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Materials and methods |
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Swim speed and depth were measured using a 12-bit resolution
speed/depth/temperature (PDT) data logger (UWE-200PDT for Adélie: 59.2
g, 20 or 23 mm diameter at the thickest part, 120 mm length; KS-400PDT for
king: 81.5 g, 25 or 32 mm diameter at the thickest part, 110 mm length;
sampling interval 1 s; Little Leonardo, Tokyo, Japan). The depth ranges were
0-200 m (resolution 0.05 m, for UWE-200PDT) or 0-400 m (resolution 0.1 m, for
KS-400PDT). Any recorded pressure values exceeding 2 m in depth were
considered to constitute a dive. Maximum depth during a dive was represented
as a dive depth. Swim speed was measured by counting the revolutions of a
propeller (RPS; revs s-1) and converting to speed using depth
versus RPS calibration data collected from the same animals (see
Blackwell et al., 1999;
Yoda et al., 1999
). The
calibration lines were obtained from each logger with coefficients of
determination higher than 0.97 within a speed range of 1.2-2.8 m
s-1 for two king penguins and 0.6-2.2 m s-1 for two
Adélie penguins. RPS values were not converted to speed when they were
lower than the stall RPS (0.3 m s-1) of the instrument, as
determined experimentally.
Field experiments
The studies were carried out on Possession Island (46.4 °S, 51.8
°E, Crozet Archipelago) during part of the breeding season of king penguin
Aptenodytes patagonicu (Miller) (FebruaryMarch, 1996) and on
Ile des Pétrels, Dumont d'Urville station, Adélie Land (66.7
°S, 140.0 °E) during the Adélie penguin Pygoscelis
adeliae (Hombron and Jacquinot) breeding season (December,
1996February, 1997).
The loggers were attached caudally to the back to minimize drag
(Bannasch et al., 1994;
Culik et al., 1994a
), using
plastic cable ties and adhesive at Dumont d'Urville and Tesa tape at Crozet.
On removal of the loggers, the cable ties and tape were also removed from the
birds. The remaining adhesive would fall off with the feathers at molt. Five
king penguins were equipped with both PDT and D2G loggers, of which two sets
were recovered with reliable data (see
Ropert-Coudert et al., 2000
for detailed information). Seven Adélie penguins were equipped with D2G
loggers, and other three birds were equipped with both PDT and D2G loggers.
Adélie penguins were caught following their return from foraging trips,
and the loggers were retrieved (see Yoda
et al., 1999
, for detailed information).
Biomechanical model
The data obtained from free-ranging penguins were analyzed using a
biomechanical model, which was modified from a model used for flying birds
(Azuma, 1997). Three forces act
on an ascending, gliding penguin when flipper beating has ceased
(Fig. 1). At ascent angle
, changes in speed U along the swimming path are determined by
the difference between the drag FD and the component of
the buoyancy FB parallel to the path of swimming
(FBsin
) (Fig.
1). Changes in ascent angle
are determined by the
difference between the downward lift FL and the component
of the buoyancy FB perpendicular to the path of swimming
(FBcos
) (Fig.
1). These relationships are described by the following equations.
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Results are presented as means ± S.D. Correlations between variables were tested using the Spearman rank correlation coefficient. Results were considered significant at P<0.05.
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Results |
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According to the acceleration data, flipper movements were substantial during the early descent in every dive made by the penguins (Fig. 2). However, birds stopped beating their flippers during the final stages of the ascent (Fig. 2). Although there was apparently some active propulsion in the late ascent of some dives, which could be attributed to pursuit of prey, all penguins exhibited cessation of flipper beating during the ascent (N=664 dives, 10 Adélies; N=425 dives, 2 kings). The depth at which this occurred differed between dives and individuals. Fig. 2A illustrates the V-shaped dives of an Adélie penguin, which stopped beating its flippers at a depth of 50 m after having descended to approximately 120m. Fig. 2B shows a second Adélie penguin that stopped beating its flippers at around 30 m depth, i.e. close to the bottom of its trapezoid-shaped dives. The mean depth at which Adélie penguins stopped beating their flippers corresponded to an average of 52±20 % of the dive depth (10 birds, 664 dives, mean dive depth=72.9±70.5 m). Fig. 2C shows dives of a king penguin. King penguins stopped beating their flippers at an average of 29±9 % of dive depth (2 birds, 425 dives, mean dive depth=136.8±145.1 m). Fig. 3 shows the relationships between dive depth and the depth of flipper beat cessation. The ten Adélie penguins tended to cease their flipper beating closer to the dive bottom than did the two king penguins (Fig. 3A). The depths of flipper beat cessation expressed as a percentage of dive depth were significantly, but weakly, related to dive depth in both Adélie (Spearman r=0.08, P<0.05) and king penguins (Spearman r=-0.46, P<0.0001) (Fig. 3B).
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The propulsive swim speeds of king and Adélie penguins were about 2 m s-1 during dives. For all deep dives (i.e. over 50 m depth; N=181 dives) of the king penguin, a marked increase in speed, up to approx. 2.9 m s-1 in the most extreme case, occurred after flipper beating stopped (Fig. 2C). This increase in speed occurred for both king penguins (2 birds, 317 dives). In case of another king penguin, where acceleration data were not obtained because the memory of D2G logger was full, the depths at which the bird ceased flipper beating were determined from the increase in swim speed. When Adélie penguins stopped beating their flippers their speed also sometimes increased (26 times in 1454 dives), but less markedly than for king penguins. In the most extreme case, swim speed increased from 1.8 to 2.3 m s-1.
The model simulation analysis was conducted for the passive ascent periods of two king penguins and two Adélie penguins, from which a reliable swim speed was recorded. An example of the simulation results for a king penguin is shown in Fig. 4A. The simulated speed under the condition of Va0=0.21 initial air volume at 52.9m depth (6.3 atm; 1 atm=1.013x105Pa), when the bird stopped flipper beating, accords well with the measured speed (Fig. 4A). The initial air volume Va0 is the equivalent of 1.21 at the surface (1 atm). It indicates that the king penguin could ascend passively if 1.21 (1 atm) of air was retained in the body. Indeed, the simulated speed fits well with the measured speed in every dive, except for the final part of the ascent. Here, the simulated speed becomes much higher than the measured speed. The measured decompression ratio (Pt/Pt-1; the ambient pressure at time t divided by the pressure 1 s before) never went lower than 0.8 in any dive of either species. But simulated decompressions are rapid near the surface because of the increase in simulated swim speed (Fig. 4). Calculated lift coefficients CL were nearly constant throughout the passive ascent periods in both species, except for the final parts (Fig. 4). Fig. 4B is one example of the model simulations for an Adélie penguin. An appropriate value of the initial air volume is the equivalent of 0.91 at the sea surface (1 atm) for the dive in question (Fig. 4B), with the model simulation indicating that the bird could ascend passively if 0.91 (1 atm) of air was kept in the body.
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The air volumes kept by penguins were estimated for each dive (N=74 dives, 2 king penguins; N=40 dives, 2 Adélie penguins). Their estimated air volumes range from 0.43 to 1.71 1 for king penguins and from 0.38 to 0.911 for Adélie penguins, respectively. There are significant positive relationships (P<0.05) between dive depth and the estimated air volume for each bird (Fig. 5, Table 1).
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Discussion |
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A passive ascent has been observed in shallow-diving birds such as the
great cormorant Phalacrocorax c. carbo, canvasback Aythya
valisineria, lesser scaup Aythya affinis and ruddy duck
Oxyura jamaicensis (Ross,
1976; Tome and Wrubleski,
1988
; Stephenson et al.,
1989
; Lovvorn,
1994
). Lovvorn et al.
(1999
) assumed in their model
that guillemots Uria lomvia would stop upward swimming to minimize
total cost. Wilson and Wilson
(1995
) suspected that African
penguins Spheniscus demersus may partly surface passively because of
the increase in their measured swim speed. However, there has been no direct
measurement of flipper movement in deep-diving penguins under natural
conditions. The present study is a first report of extended periods of gliding
in ascending penguins.
Slowdown near the surface
The propulsive swim speed was approximately 2 m s-1 during
dives, independent of dive depth and species. This is consistent with the
speed of king penguins measured using another type of data logger
(Kooyman et al., 1992), and
accords well with the optimal speed for minimum cost of transport found in
each species (1.8-2.2 m s-1 for king,
Culik et al., 1996
; 1.7-2.3 m
s-1 for Adélie, Culik and
Wilson, 1991
). When ascending, both penguins stopped beating their
flippers and swim speed sometimes increased beyond the optimal speed.
Biomechanical calculations, together with data obtained from free-ranging
penguins, yield important insights into the movements of these birds during
the passive ascent periods. The model simulations indicate that the passive
ascent of penguins can be attributed to increased buoyancy from the expanding
air volume in the body. From Fig.
4A, the simulated speed matches the measured speed up to 27 s,
after which it becomes much higher than the measured speed. Similar results
were obtained from all other simulations in both species. The discrepancy
suggests that the penguins actually decelerated speed by some means, possibly
correlated to an increase in the profile drag of the flippers or parasite drag
of the body. Fig. 4 indicates
that the calculated lift coefficients suddenly increase during the final part
of ascent, suggesting that penguins might increase the attack angle of their
flippers, and thus increase the profile drag coefficient
(Vogel, 1994). Except for the
final part, lift coefficients were nearly constant throughout the ascent
(Fig. 4), supporting the
assumption that the drag coefficient (including profile drag) remains constant
during most of the passive ascent. Penguins could also increase the parasite
drag of the body. As has been observed for an emperor penguin Aptenodytes
forsteri coming to the surface, the feet can be turned down into the
normal standing posture to act as a brake
(Kooyman et al., 1971
).
Penguins might also reduce speed by exhaling the air to decrease buoyancy, as
can be seen in a photograph of a surfacing Adélie penguin
(Kooyman, 1975
).
Oblique ascent angle
Ascent angles were not vertical and became shallower the closer the bird
was to the surface (Fig. 4).
According to equation 2, ascent angle is affected by buoyancy and downward
lift. Penguins can control the ascent angle via the lift coefficient
mediated by the attack angle of their flippers. If penguins kept the ascent
angle steep and did not brake near the surface, then buoyancy would take them
rapidly to the surface without flipper stroke effort. For example, the king
penguin in Fig. 4A could reduce
the 38 s ascent duration by 13 s by ascending vertically. Therefore, the
oblique ascent angle and braking near the surface seem to be energetically
expensive and do not accord with optimal diving theory predicting that animals
maximize the proportion of time spent at the foraging depth
(Kramer, 1988;
Ydenberg and Clark, 1989
). Why
then might the birds delay a prompt return to the surface?
Wilson et al. (1996)
hypothesized that an oblique ascent angle allows the birds to search both the
vertical and horizontal components of the water column. Results showing that
ascent angles during feeding dives were greater than during non-feeding dives
in Adélie penguins support the searching hypothesis
(Ropert-Coudert et al.,
2001b
). However, the ascent angles became shallower nearer to the
surface (Ropert-Coudert et al.,
2001b
), where the probability of prey acquisition should be low
because ingestion events (detected as abrupt decreases in oesophageal
temperature) were mostly observed at depths greater than than 40 m
(Ropert-Coudert et al.,
2001a
). Hence, it seems unlikely that searching for prey can
explain the oblique ascent angle.
There may be physiological reasons why the penguins delay their ascent
time. Seals are known to exhale air before diving, and the free-swimming
Weddell seal Leptonychotes weddellii protects itself from nitrogen
narcosis and decompression sickness by limiting blood nitrogen uptake through
alveolar collapse (Falke et al.,
1985), but how deep-diving birds avoid the bends is not clear
(Kooyman and Ponganis, 1997
).
The bird's lung may not collapse during a dive; blood nitrogen tensions in
Adélie penguins during simulated dives to 68m rose to levels that were
borderline for decompression sickness
(Kooyman et al., 1973
),
leading the authors to suggest that shallow-diving penguins such as
Adélies and gentoos Pygoscelis papua avoid the risk of
elevated partial pressure of dissolved nitrogen by making short, shallow
dives. Ponganis et al. (1999
)
suggested that king penguins have adapted to deep diving by reducing their
respiratory air volume compared to that in shallow-diving penguins. Indeed,
the measured air volume (69 ml kg-1;
Ponganis et al., 1999
),
including respiratory and plumage air, of restrained king penguins during
simulated dives of up to 136m was much smaller than in shallow-diving
Adélie penguins of similar body size (165 ml kg-1;
Kooyman et al., 1973
).
Similarly we found that the maximum mass-specific total air volume (125 ml
kg-1; calculated from Fig.
5A) of king penguins was smaller than that of Adélie
penguins (200 ml kg-1; calculated from
Fig. 5B). It is still unclear
how these birds avoid the risk of decompression sickness, because free-ranging
king penguins frequently repeat dives that are deeper and longer than the
simulated dives of 136m depth. As indicated by Kooyman et al.
(1973
), use of short and
shallow dives only may not completely avoid the hazards of inert gas
absorption in Adélie penguins. It is known that symptoms characteristic
of decompression sickness can occur in man even after repetitive breath-hold
dives of short duration to shallow (15-20 m) depths
(Paulev, 1965
).
Thus, there still seems to be a potential risk of decompression sickness in
free-ranging Adélie and king penguins.
Fig. 4 shows that measured
decompression was actually kept moderate because birds actively reduced their
rate of change of depth. Therefore, the oblique ascent angle and slowdown near
the surface could be one way to avoid potential decompression sickness; other
hypothetical mechanisms include a reduced cardiac output or a pressure-induced
restriction of pulmonary gas exchange
(Ponganis et al., 1999),
although there is no evidence to conclusively support any of these hypotheses
at present.
Air volume in the body
Whether animals dive on inspiration or expiration is important because
buoyant resistance is determined by the total air volume kept in the body.
However, air volume is difficult to measure in freely diving birds in the
laboratory (Stephenson, 1995),
and no methods have been devised for measuring them in the field
(Lovvorn et al., 1999
).
Stephenson (1994
) first
measured buoyancy in unrestrained shallow-diving lesser scaup Aythya
affinis, using a 1.52m deep tank. However, the same method is impossible
to use for deep-diving birds such as penguins. In the present study we
therefore estimated the total air volume (including respiratory system and
feathers) using data on depth, speed and acceleration, these being the first
data obtained from free-ranging penguins. The air volume of the respiratory
system was calculated to be 0.57 and 0.631 for 4.0 kg and 4.5 kg Adélie
penguins, respectively, and 1.27 and 1.481 for 9.7 kg and 11.5 kg king
penguins, respectively, using the analysis of Lasiewski and Calder
(1971
). The estimated total
air volume for each species was similar to the expected respiratory volumes
for diving birds (Fig. 5),
which suggests that the biomechanical simulations yield good estimates of
respiratory air volume in the birds, although we did not have direct data of
the amount of air present in the feathers.
Ponganis et al. (1999)
calculated the distribution of oxygen stores in king penguins
(Table 2) using their
relatively small air volume of 69 ml O2 kg-1, which was
measured from restrained king penguins during simulated dives of up to 136m.
Kooyman and Ponganis (1998
)
calculated the distribution in Adélie penguins
(Table 2), assuming that they
had a respiratory volume of 165 ml O2 kg-1
(Kooyman et al., 1973
). In the
present study, maximum air volume for each species was larger than in previous
reports. Assuming that our estimated air volumes (125 ml kg-1 for
king; 200 ml kg-1 for Adélie) represent their respiratory
volumes, the total body oxygen and the distribution of oxygen stores are
modified as shown in Table 2.
These are maximum values for the respiratory oxygen stored when the birds
carry the maximum air volume in their respiratory system. As noted by Ponganis
et al. (1999
) and Stephenson
(1995
), the air volume becomes
greater during unrestrained conditions. To improve the accuracy of this
approach, more research is required into several variables, including (1) the
air volume trapped in the feathers; (2) the tidal volume for each species; (3)
the anatomical volume of the respiratory system of penguins; (4) the amount of
air lost from the respiratory system and plumage during dives.
|
Regulation of air volume
The positive relationship between dive depth and estimated air volume
during the late phase of ascending in both species
(Fig. 5) implies that penguins
control their air volume. This could be acheived by alterations in inhaled air
volume and in the volume of air trapped in plumage. Stephenson
(1995) found that the
increasing relative influence of the air in the respiratory system on buoyancy
was due to the loss of 47 % of the air in the plumage layer during a dive (1.5
m depth, 11.9s mean duration). In the present study, air volume was estimated
using data obtained during the latter part of the ascent. The air volume
trapped in the plumage is unknown; however, the positive relationship between
air volume and dive depth suggests that penguins might control their inhaled
air volume according to their intended dive depth.
The air associated with the body makes diving birds buoyant, so many
species must use considerable energy to swim against this buoyancy in order to
remain submerged (Stephenson et al.,
1989; Lovvorn and Jones,
1991a
,b
;
Lovvorn et al., 1991
;
Wilson et al., 1992
;
Stephenson, 1994
). Some flying
birds such as cormorants and ducks have been observed to dive following
expiration (Ross, 1976
;
Butler and Woakes, 1979
;
Tome and Wrubleski, 1988
), so
as to reduce buoyant resistance during dives. However, some penguins have been
observed to dive on inspiration (Kooyman
et al., 1971
) and the present study partly supports this
observation at least for deep dives (Fig.
5). The behavioral difference between flying birds and penguins
could be attributed to differences in dive depth and in plumage air volumes
(Wilson et al., 1992
).
Penguins generally dive much deeper than flying birds, which means that they
spend much of the dive deeper than the critical depth at which air volume is
so compressed that the buoyant force is negligible. Deep-diving penguins were
not affected by buoyancy in the vicinity of the dive bottom, which explains
why deep diving penguins inhale much air at the beginning of the dive. The
lower estimated air volume during shallower dives
(Fig. 5) further supports this
idea. Here, penguins reduce the volume of air so as to avoid buoyant
resistance during shallow dives.
Loggerhead turtles Caretta caretta adjust their residence depth to
the depth of neutral buoyancy, which varies with the air volume in the
respiratory system in order to minimize cost (Minamikawa et al.,
1997,
2000
). In the case of harbor
porpoises Phocoena phocoena, the deeper the dive depth the faster the
initial descent rate, which suggests that porpoises anticipate the depth to
which they will dive before initiating the dive itself
(Otani et al., 1998
). The same
pattern was found in penguins (see Wilson,
1995
, for a review). Importantly, the present study indicates that
penguins control their inhaled air volume according to the intended dive
depth. This means that diving animals may adapt their diving strategy within
their own biomechanical and physiological constraints.
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Acknowledgments |
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References |
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---|
Azuma, A. (1997). Seibutsu no Ugoki no Jiten (in Japanese). Tokyo: Asakura Syoten.266 pp.
Bannasch, R., Wilson, R. P. and Culik, B.
(1994). Hydrodynamic aspects of design and attachment of a
back-mounted device in penguins. J. Exp. Biol.
194, 83-96.
Bannasch, R. (1995). Hydrodynamics of penguins an experimental approach. In The Penguins (ed. P. Dann, I. Norman and P. Reilly), pp. 141-176. Sydney: Surrey Beatty & Sons.
Blackwell, S. B., Haverl, C. A., LeBoeuf, B. J. and Costa, D. P. (1999). A method for calibrating swim-speed recorders. Mar. Mamm. Sci. 15,894 -905.
Butler, P. J. and Woakes, A. J. (1979). Changes in heart rate and respiratory frequency during natural behaviour of ducks, with particular reference to diving. J. Exp. Biol. 79,283 -300.
Clark, B. D. and Bemis, W. (1979). Kinematics of swimming of penguins at the Detroit Zoo. J. Zool., Lond. 188,411 -428.
Culik, B. M. and Wilson, R. P. (1991). Energetics of under-water swimming in Adélie penguins (Pygoscelis adeliae). J. Comp. Physiol. B 161,285 -291.
Culik, B. M., Bannasch, R. and Wilson, R. P. (1994a). External devices on penguins: how important is shape? Mar. Biol. 118,353 -357.
Culik, B. M., Pütz, K., Wilson, R. P., Allers, D., Lage,
J., Bost, C. A. and Le Maho, Y. (1996). Diving energetics in
king penguins (Aptenodytes patagonicus). J. Exp.
Biol. 199,973
-983.
Culik, B. M., Wilson, R. P. and Bannasch, R.
(1994b). Underwater swimming at low energetic cost by Pygoscelid
penguins. J. Exp. Biol.
197, 65-78.
Daniel, T. L. (1984). Unsteady aspect of aquatic locomotion. Amer. Zool. 24,121 -134.
Dehner, E. W. (1946). An analysis of buoyancy in surface-feeding and diving ducks. PhD thesis, Cornell University, Ithaca, NY, USA.
Falke, K., Hill, R. D., Qvist, J., Schneider, R. C., Guppy, M., Liggins, G. C., Hochachka, P. W., Elliott R. E. and Zapol, W. M. (1985). Seal lungs collapse during free diving: evidence from arterial nitrogen tensions. Science 229,556 -558.[Medline]
Kooyman, G. L. (1975). Behaviour and physiology of diving. In The Biology of Penguins (ed. B. Stonehouse), pp. 115-137. London: Macmillan.
Kooyman, G. L. (1989). Diverse Divers. Berlin: Springer-Verlag.200 pp.
Kooyman, G. L. and Ponganis, P. J. (1997). The challenges of diving to depth. Am. Scientist. 85,530 -539.
Kooyman, G. L. and Ponganis, P. J. (1998). The physiological basis of diving to depth: birds and mammals. Annu. Rev. Physiol. 60,19 -32.[Medline]
Kooyman, G. L., Cherel, Y., Le Maho, Y., Croxall, J. P., Thorson, P. H., Ridoux, V. and Kooyman, C. A. (1992). Diving behavior and energetics during foraging cycles in king penguins. Ecol. Monogr. 62,143 -163.
Kooyman, G. L., Drabek, C. M., Elsner, R. and Campbell, W. B. (1971). Diving behavior of the Emperor penguin, Aptenodytes forsteri. Auk 88,775 -795.
Kooyman, G. L., Schroeder, J. P., Greene, D. G. and Smith, V.
A. (1973). Gas exchange in penguins during simulated dives to
30 and 68 m. Am. J. Physiol.
225,1467
-1471.
Kramer, D. L. (1988). The behavioral ecology of air breathing by aquatic animals. Can. J. Zool. 66, 89-94.
Lasiewski, R. C. and Calder, W. A. (1971). A preliminary allometric analysis of respiratory variables in resting birds. Respir. Physiol. 11,152 -166.[Medline]
Lighthill, M. J. (1971). Large-amplitude elongated-body theory of fish locomotion. Proc. R. Soc. Lond. B 179,125 -138.
Lovvorn, J. R. (1994). Biomechanics and foraging profitability: an approach to assessing trophic needs and impacts of diving ducks. Hydrobiologia 279/280,223 -233.
Lovvorn, J. R. and Jones, D. R. (1991a). Effects of body size, body fat, and change in pressure with depth on buoyancy and costs of diving in ducks (Aythya spp.). Can. J. Zool. 69,2879 -2887.
Lovvorn, J. R. and Jones, D. R. (1991b). Body mass, volume, and buoyancy of some aquatic birds, and their relation to locomotor strategies. Can. J. Zool. 69,2888 -2892.
Lovvorn, J. R., Croll, D. A. and Liggins, G. A.
(1999). Mechanical versus physiological determinants of swimming
speeds in diving Brünnich's guillemots. J. Exp.
Biol. 202,1741
-1752.
Lovvorn, J. R., Jones, D. R. and Blake, R. W. (1991). Mechanics of underwater locomotion in diving ducks: drag, buoyancy and acceleration in a size gradient of species. J. Exp. Biol. 159,89 -108.
Minamikawa, S., Naito, Y. and Uchida, I. (1997). Buoyancy control in diving behavior of the loggerhead turtle, Caretta caretta. J. Ethol. 15,109 -118.
Minamikawa, S., Naito, Y., Sato, K., Matsuzawa, Y., Bando, T.
and Sakamoto, W. (2000). Maintenance of neutral buoyancy by
depth selection in the loggerhead turtle Caretta caretta. J. Exp.
Biol. 203,2967
-2975.
Naito, Y., Asaga, T. and Ohyama, Y. (1990). Diving behavior of Adélie penguins determined by time-depth recorder. Condor. 92,582 -586.
Osa, Y. (1994). Study of functional morphology for swimming- and/or flying seabirds. PhD thesis, Tokyo Universiy of Fisheries, Tokyo.
Otani, S., Naito, Y., Kawamura, A., Kawasaki, M. and Kato, A. (1998). Diving behavior and performance of harbor porpoises, Phocoena phocoena, in Funka Bay, Hokkaido, Japan. Mar. Mamm. Sci. 14,209 -220.
Paulev, P. (1965). Decompression sickness following repeated breath-hold dives. J. Appl. Physiol. 20,1028 -1031.[Medline]
Ponganis, P. J., Kooyman, G. L., van Dam, R. and Le Maho, Y.
(1999). Physiological responses of king penguins during simulated
diving to 136 m depth. J. Exp. Biol.
202,2819
-2822.
Ropert-Coudert, Y., Sato, K., Kato, A., Charrassin, J.-B., Bost, C.-A., Le Maho, Y. and Naito, Y. (2000). Preliminary investigations of prey pursuit and capture by king penguins at sea. Polar Biosci. 13,101 -112.
Ropert-Coudert, Y., Kato, A., Baudat, J., Bost, C.-A., Le Maho, Y. and Naito, Y. (2001a). Feeding strategies of free-ranging Adélie penguins Pygoscelis adeliae analysed by multiple data recording. Polar Biol. 24,460 -466.
Ropert-Coudert, Y., Kato, A., Baudat, J., Bost, C.-A., Le Maho, Y. and Naito, Y. (2001b). Time/depth usage of Adélie penguins: an approach based on dive angles. Polar Biol. 24,467 -470.
Ross, R. K. (1976). Notes on the behavior of captive Great Cormorants. Wilson Bull. 88,143 -145.
Stephenson, R., Lovvorn, J. R., Heieis, M. R. A., Jones, D. R. and Blake, R. W. (1989). A hydromechanical estimate of the power requirements of diving and surface swimming in Lesser Scaup (Aythya affinis). J. Exp. Biol. 147,507 -519.
Stephenson, R. (1994). Diving energetics in
Lesser Scaup (Aythyta affinis, Eyton). J. Exp.
Biol. 190,155
-178.
Stephenson, R. (1995). Respiratory and plumage gas volumes in unrestrained diving ducks (Aythya affinis). Respir. Physiol. 100,129 -137.[Medline]
Tome, M. W. and Wrubleski, D. A. (1988). Underwater foraging behavior of Canvasbacks, Lesser Scaups, and Ruddy Ducks. Condor 90,168 -172.
Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow. 2nd edition. Princeton: Princeton University Press. 467pp.
Watanuki, Y., Kato, A., Naito, Y., Robertson, G. and Robinson, S. (1997). Diving and foraging behaviour of Adélie penguins in areas with and without fast sea-ice. Polar Biol. 17,296 -304.
Wilson, R. P. (1995). Foraging ecology. In The Penguins (ed. T. D. Williams), pp.81 -106. Oxford, New York and Tokyo: Oxford University Press.
Wilson, R. P., Hustler, K., Ryan, P. G., Burger, A. E. and Nöldeke, E. C. (1992). Diving birds in cold water: Do archimedes and boyle determine energetic costs? Amer. Nat. 140,179 -200.
Wilson, R. P. and Wilson, M.-P. T. (1995). The foraging behaviour of the African penguin Spheniscus demersus. In The Penguins (ed. P. Dann, I. Norman and P. Reilly), pp. 244-265. Sydney: Surrey Beatty & Sons.
Wilson, R. P., Culik, B. M., Peters, G. and Bannasch, R. (1996). Diving behaviour of gentoo penguins, Pygoscelis papua; factors keeping dive profiles in shape. Mar. Biol. 126,153 -162.
Ydenberg, R. C. and Clark, C. W. (1989). Aerobiosis and anaerobiosis during diving by Western Grebes: an optimal foraging approach. J. theor. Biol. 139,437 -449.
Yoda, K., Sato, K., Niizuma, Y., Kurita, M., Bost, C.-A., Le
Maho, Y. and Naito, Y. (1999). Precise monitoring of
porpoising behaviour of Adélie penguins determined using acceleration
data loggers. J. Exp. Biol.
202,3121
-3126.
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