Why do macaroni penguins choose shallow body angles that result in longer descent and ascent durations?
t Charrassin2
1 National Institute of Polar Research, 1-9-10 Kaga, Itabashi, Tokyo
173-8515, Japan
2 Département Milieux et Peuplements Aquatiques, Muséum
National d'Histoire Naturelle, 43 rue Cuvier, 75231 Paris Cedex 05,
France
3 Centre d'Ecologie et de Physiologie Energétiques, Centre National
de la Recherche Scientifique, 23 rue Becquerel, F-67087 Strasbourg,
France
* Author for correspondence at present address: International Coastal Research Center, Ocean Research Institute, University of Tokyo, 2-106-1 Akahama, Otsuchi, Iwate 028-1102, Japan (e-mail: katsu{at}wakame.ori.u-tokyo.ac.jp)
Accepted 27 August 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: dive, acceleration, data logger, stroke, buoyancy, gliding, horizontal transit, penguin, Eudyptes chrysolophus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Physiological factors, such as the potential risk of decompression
sickness, may prevent air-breathing divers from using vertical transit
(Sato et al., 2002). If this
idea is true, then penguins would be expected to adopt shallow body angles to
prolong their ascent durations after having spent relatively long periods at
deep depths. A second explanation may be linked to the concept of optimal
foraging behaviour. It has been proposed that predators remain longer at
depths that have a higher prey density
(Mori, 1998
). If the diver
encounters a good prey patch, it can prolong the time spent at the bottom and
then adopt a steep body angle during its ascent, because it must return
quickly to the surface to breathe. If this hypothesis is true, we would expect
a positive relationship between the bottom-phase duration and body angle
during the ascent.
The use of miniaturized acceleration data loggers allows for fine-scale
monitoring of movements during diving
(Sato et al., 2003).
Low-frequency components of surging acceleration along the long axis of the
body provide information on body angles during dives. Stroke frequency can be
detected from high-frequency components of acceleration data. In the present
study, small acceleration data loggers (depth, 2-D acceleration and
temperature) were attached to macaroni penguins (Eudyptes
chrysolophus). Here, we examine body angles during descent and ascent in
relation to the bottom-phase duration of dives. Our aim was to test the
hypothesis that mid-size penguins adjust their body angles during the transit
phases in relation to their feeding success at the bottom phase of dives. We
discuss our findings in terms of behavioural strategies based on physiological
and environmental conditions during diving.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
All instrumented birds returned from their foraging trips, with trip
durations ranging from 12 to 15 days (mean ± S.D. =
13.6±1.1 days). The trip durations recorded in this study were slightly
longer than the mean of 11.0 days reported for females studied at Bird Island
(Williams and Croxall, 1991)
and Crozet (Stahl et al.,
1985
). Upon their return, birds were recaptured at their nest and
all loggers were retrieved. Body mass, bill length and bill depth were
measured, and the sex of the instrumented birds was confirmed based on bill
length and depth (Williams,
1995
). All equipped birds appeared to have gained weight (by
0.500.95 kg), and no nest was abandoned through the experiment.
Data loggers
The detailed behaviour of diving penguins was studied using acceleration
data loggers (M190-D2GT; Little Leonardo Ltd, Tokyo, Japan). Each instrument
was 15 mm in diameter and 60 mm in length, with a mass of 16 g in air,
corresponding to <0.5% of the body mass of a bird. The cross-sectional area
of the instrument was <1.1% of the maximal cross-sectional area of a bird;
therefore, we estimated the drag impact on swimming behaviour to be minimal
(Wilson et al., 1986). The
data logger was attached to the lower medial portion of the back using
waterproof Tesa tape (Wilson and Wilson,
1989
) and plastic cable ties.
The loggers recorded depth every second (±1 m accuracy and 0.05 m resolution), 2-D acceleration at 16 or 32 Hz via an accelerometer sensor (model ADXL202E; Analog Device, Inc., Norwood, MA, USA) and sea temperature at 30-s intervals. The measuring range of the accelerometer was ±29.4 m s-2 with a resolution of 0.0196 m s-2. The logger recorded tail-to-head (surge) and ventral-to-dorsal (heave) accelerations. The loggers were programmed to start recording one or two days (four birds each) after departure in order to record data during the middle period of the foraging trip.
Data analyses
Data were analyzed using a custom-written macro program in Igor Pro (Wave
Metrics, Inc., Lake Oswego, OR, USA). We defined dives as bird movements to
depths greater than 1 m. As indicated in
Fig. 1, a dive was divided into
a descent (continuous descent from the initiation of the dive), a bottom phase
(the time between the start and end of the time when birds showed a depth
change of 0 m) and an ascent (continuous ascent to the end of the dive).
|
The accelerometer was able to measure both dynamic acceleration (such as propulsive activities) and static acceleration (such as gravity). Values recorded by loggers were converted into acceleration with linear regression equations. To obtain the calibration equations, values recorded by each logger set at 90° and 90° from the horizon in 4°C waters (corresponding to mean ambient water temperatures) were regressed on the corresponding acceleration (9.8 m s-2 and 9.8 m s-2, respectively). We used high-frequency components of heave and surge accelerations to count stroke cycle frequency. A single stroke cycle included both an upstroke and a downstroke. Mean stroke cycle frequencies (Hz) during descent, bottom phase and ascent were calculated from the total number of stroke cycles divided by the duration of each phase for each dive.
The acceleration sensor along the longitudinal body axis measured the
surging accelerations, which are affected by both the forward movements of the
animal and gravity (Yoda et al.,
2001; Tanaka et al.,
2001
; Sato et al.,
2003
). High-frequency components of the surging accelerations,
which are caused by flipper movements, were filtered out using 1-Hz low-pass
filters (IFDL version 3.1; Wave Matrics, Inc.). Low-frequency components of
the surging acceleration were then used to calculate the body angle of the
animals (for details, see Sato et al.,
2003
). Descending body angles are represented as negative values.
When an animal descends or ascends vertically, its body angle is close to
90° or 90° (`steep' body angle) whereas when an animal swims
horizontally, the body angle is close to 0° (`shallow' body angle). As
described by Watanuki et al.
(2003
) and Sato et al.
(2003
), the loggers were not
exactly parallel to the longitudinal axes of the animals because they were
attached to the lower back of each animal to diminish hydrodynamic drag
(Bannasch et al., 1994). In this position, each logger had an attachment
angle. To measure the attachment angle for each bird, we arbitrarily selected
five samples of 3-s surge acceleration when birds were at the water surface
between dives; their trunks were assumed to be horizontal while at the
surface. The mean surging acceleration during these surface periods was used
to calculate the attachment angle. The estimated attachment angle for each
bird, which ranged from 5.2° to 11.6°, was taken into consideration
when calculating body angles.
Data were analyzed statistically using StatView (version 5.0, SAS, Cary, NC, USA) software. Values are presented as means ± S.D., with significance set at the P<0.05 level. Mean values were calculated for each bird, and correlations were examined individually.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Dives typically had either a V-, U- or W-shaped profile when depth was plotted against time. A typical dive cycle of a macaroni penguin is presented in Fig. 1. Based on acceleration data, the penguin stroked continuously during the descent, stopped stroking during the middle of the ascent and completed the ascent with a prolonged glide (Fig. 1). Small amplitudes and aperiodic fluctuations in acceleration indicated that penguins did not swim during surface intervals (Fig. 1).Porpoising behaviour was observed close to the coast (C.A.B. and K.S., personal observations), but recorded data did not cover the first and last few days of the foraging trip. For each dive, the mean stroke cycle frequency during the descent, bottom phase and ascent was plotted against dive depth (Fig. 2). Each penguin descended with a mean stroke cycle frequency ranging from 2.0 to 2.6 Hz (Fig. 2A; Table 2).Ascending penguins had lower mean stroke cycle frequencies (Fig. 2C; Table 2), and the distribution of the mean stroke cycle frequency during the bottom phase was intermediate between descent and ascent values (Fig. 2B; Table 2). Mean stroke cycle frequencies between the dive phases differed significantly at each dive depth range: <20 m (Scheffé's test: N1=N3=1510, N2=1311, P<0.0001), 2040 m (Scheffé's test: N1=N3=1258, N2=1212, P<0.0001), 4060 m (Scheffé's test: N1=N3=1514, N2=1464, P<0.0001), >60 m (Scheffé's test: N1=N3=1069, N2=1040, P<0.0001).
|
|
Time allocation during dives
Dive duration was positively correlated with dive depth
(Fig. 3), and this relationship
was significant for each bird (Table
3). Descent and ascent durations were significantly correlated
with the depths at the beginning and at the end of the bottom phase,
respectively (Fig. 4;
Table 4). However, descent and
ascent durations at a given depth showed a large range of variation
(Fig. 4). For example, the time
necessary to reach the surface from a 60-m depth ranged from 27.5 s to 90 s
(Fig. 4B). As shown in
Fig. 5 (bird MK1), descent and
ascent durations recorded during the different dives were significantly
affected by mean body angle during each dive, with descent durations
decreasing with steeper descent body angles at each depth range: <20 m
(Spearman R=0.437, N=470, P<0.0001), 2040
m (Spearman R=0.820, N=478, P<0.0001),
4060 m(Spearman R=0.893, N=255,
P<0.0001), >60 m (Spearman R=0.767, N=79,
P<0.0001). Similarly, ascent durations decreased with steeper
ascent body angles in each depth range deeper than 20 m: <20 m (Spearman
R=0.002, N=544, P=0.958), 2040 m
(Spearman R=0.763, N=475, P<0.0001),
4060 m (Spearman R=0.891, N=194,
P<0.0001), >60 m(Spearman R=0.912,
N=69, P<0.0001). This tendency was significant for all
birds except bird MK3, for which only a small number of dives were recorded.
The significance of body angle and duration of the eight birds at each depth
range is summarized in Table
5.
|
|
|
|
|
|
Body angles during descent and ascent
Mean body angles during descent and ascent were not vertical
(Table 6). Mean descent angles
ranged from 23.7° to 42.6° among birds. Mean ascent
angles ranged from 24.4° to 32.1°, and the maximum angles were
shallower than 70° in most dives (Table
6). The large S.D. indicates that, for a given bird,
body angles were highly variable among dives. Body angles were significantly
correlated with time spent at the bottom, and significant regression lines for
ascent and subsequent descent were obtained for each depth range
(Table 7). Significant
regression lines were obtained for all birds except birds MK3 and MK4, for
which only a small number of dives were recorded. A typical example of this
relationship is shown in Fig.
6, with data from bird MK1. When birds spent long periods at the
bottom, they adopted steep body angles during ascent and subsequent descent.
By contrast, they maintained shallow body angles after they had short or no
bottom phases.
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Therefore, if we consider that long bottom-phase durations indicate
foraging success, as compared with short bottom-phase periods, two main
hypotheses could help explain the steep body angle that is related to more
time spent at the bottom. First, steeper ascent angles presumably occur when
birds have depleted their oxygen stores and must return to the surface more
quickly to breathe (Wilson and Wilson,
1995). Second, when a dive is successful, as suggested by a long
bottom-phase duration, and, if we assume that penguins will try to relocate
the same prey patch, steep ascent and subsequent descent angles will increase
the probability of encountering the patch in the following dive because the
horizontal component of the dive will be minimized
(Wilson and Wilson, 1995
).
However, even when they ascended at a steeper angle after a long bottom-phase
duration, the ascent angles in macaroni penguins were not vertical
(Table 6).
Several factors may explain the oblique body angles. First, it is possible
that penguins ascended obliquely to prolong their ascent time and thereby
avoid decompression sickness (Sato et al.,
2002). However, there are no data to support this idea, as yet.
Although we expected penguins to delay their ascent after they stayed longer
at deep depths, they actually ascended relatively quickly after spending long
periods in the bottom phase (W-shaped dives) and prolonged their ascent
duration in dives with a short or no bottom phase (V-shaped dives).
Second, shallow angles during ascent and subsequent descent might help the
penguins to scan the water column horizontally to locate a new patch of prey.
This hypothesis was first proposed by Wilson et al.
(1996) and Peters et al.
(1998
), who suggested that
scanning the water during the ascent and descent phases is probably essential
for optimal exploration of the water column, with the horizontal scanning of
the habitat being favoured by shallow angles. However, it is hard to believe
that such scanning could be the main reason for the shallow body angles. Body
angles of macaroni penguins became shallower as they approached the surface
(Fig. 1).Adélie and king
penguins also ascended similarly
(Ropert-Coudert et al., 2001
;
Sato et al., 2002
). As
indicated by Wilson and Wilson
(1995
) and Ropert-Coudert et
al. (2001
), shallower body
angles result in a longer time spent per metre depth. It is improbable that
penguins would spend more time searching near the surface, where the
probability of prey acquisition should be lower.
Third, a shallow body angle can contribute towards increased horizontal
distances travelled during the descent and ascent. Indeed, female macaroni
penguins travelled long distances during incubation, averaging 376 km at Bird
Island (Barlow and Croxall,
2002), but our study shows that they did not swim actively while
at the surface between dives (Fig.
1). Shallow and short dives are generally considered to be
travelling dives, while deep and long dives are considered foraging dives
(Wilson, 1995
). Here, we
propose that all dives (including deep foraging ones) contribute to horizontal
transit, because very shallow body angles were observed during the last part
of the ascent in the case of deep foraging dives
(Fig. 1). The shallow body
angle would contribute to horizontal transit at any depth
(Fig. 7) and therefore would
permit penguins to move into a more profitable area for the following dive,
assuming that they do not alter their directions (compass heading) during the
descent and ascent. Particularly in the case of the ascent, macaroni penguins
stopped beating their flippers after the first part of the ascent
(Fig. 1), as has also been
observed in Adélie and king penguins
(Sato et al., 2002
), and they
were able to reach the surface using buoyancy, without any stroking effort.
Body angle can be controlled using outstretched wings
(Sato et al., 2002
; see fig. 1
in Takahashi et al., 2004
), so
penguins can optimize their ascent angle to move horizontally. Decreasing the
ascent angle makes sense because buoyancy increases with ascent. If penguins
decreased their body angles during the ascent, the effect of buoyancy parallel
to the longitudinal axis of a penguin was sufficient against the drag. Thus,
penguins can adopt shallower body angles to move longer horizontal distance
using the increasing buoyancy.
|
It has been observed that terrestrial animals make the decision to remain
in a prey patch or to leave according to the prey richness of the patch. For
example, pipistrelle bats (Pipistrellus pipistrellus) spent a greater
proportion of their time foraging in higher-density patches and searched for
less than 1 min when local prey densities were below a threshold value
(Racey and Swift, 1985). In
the case of air-breathing aquatic animals, time-depth recorders have been used
to monitor their behaviour, as it is difficult to observe animals foraging
underwater. As a result, time-based models have been developed, and empirical
data have been used to test predictions derived from the models
(Boyd et al., 1995
;
Carbone et al., 1996
;
Thompson and Fedak, 2001
;
Mori et al., 2002
;
Mori and Boyd, 2004
). Longer
transit times between the surface and the foraging depth are not beneficial in
terms of time efficiency, but a longer transit time does allow birds to move
horizontally. If they fail to locate prey, they can shorten the proportion of
the dive spent at the bottom and ascend, keeping their body angle shallow in
order to move horizontally so that they can reach a more profitable area for
the following dive.
In conclusion, macaroni penguins modify the time spent at the bottom in accordance with the conditions, both physiological and environmental, that occur during the course of the bottom phase of the dive. If penguins encounter prey, they can prolong the bottom duration of the dive and then adopt steep body angles during the ascent, as they have depleted their oxygen stores and must return to the surface quickly to breathe. If they fail to locate prey on one dive, they can shorten the bottom duration and benefit from travelling horizontally for some distance before reaching the surface. Using increasing buoyancy during the ascent, gliding penguins can move horizontally with minimum stroking effort.
![]() |
Acknowledgments |
---|
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Akamatsu, T., Wang, D., Wang, K., Wei, Z., Zhao, Q. and Naito, Y. (2002). Diving behaviour of freshwater finless porpoises (Neophocaena phocaenoides) in an oxbow of the Yangtze River, China. ICES J. Mar. Sci. 59,438 -443.[CrossRef]
Bannasch, R. (1994). Hydrodynamic aspects of
design and attachment of a back-mounted device in penguins. J. Exp.
Biol. 194,83
-96.
Barlow, K. E. and Croxall, J. P. (2002). Seasonal and interannual variation in foraging range and habitat of macaroni penguins Eudyptes chrysolophus at South Georgia. Mar. Ecol. Prog. Ser. 232,291 -304.
Boyd, I. L., Reid, K. and Bevan, R. M. (1995). Swimming speed and allocation of time during the dive cycle in Antarctic fur seals. Anim. Behav. 50,769 -784.[CrossRef]
Boyd, I. L., McCafferty, D. J. and Walker, T. R. (1997). Variation in foraging effort by lactating Antarctic fur seals: response to simulated increased foraging costs. Behav. Ecol. Sociobiol. 40,135 -144.[CrossRef]
Carbone, C., De Leeuw, J. J. and Houston, A. I. (1996). Adjustments in the diving time budgets of tufted duck and pochard: is their evidence for a mix of metabolic pathways? Anim. Behav. 51,1257 -1268.[CrossRef]
Croxall, J. P., Briggs, D. R., Kato, A., Naito, Y., Watanuki, Y. and Williams, T. D. (1993). Diving pattern and performance in the macaroni penguin Eudyptes chrysolophus. J. Zool. Lond. 230,31 -47.
Houston, A. I. and Carbone, C. (1992). The optimal allocation of time during the diving cycle.Behav. Ecol. 3,255 -265.
Kooyman, G. L. (1989). Diverse Divers. Berlin: Springer-Verlag.
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. Monog. 62,143 -163.
Le Boeuf, B. J., Costa, D. P., Huntley, A. C. and Feldkamp, S. D. (1988). Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Can. J. Zool. 66,446 -458.
Mori, Y. (1998). The optimal patch use in divers: optimal time budget and the number of dive cycles during bout. J. Theor. Biol. 190,187 -199.[CrossRef]
Mori, Y. and Boyd, I. L. (2004). The behavioral basis for nonlinear functional responses and optimal foraging in Antarctic fur seals. Ecology 85,398 -410.
Mori, Y., Takahashi, A., Mehlum, F. and Watanuki, Y. (2002). An application of optimal diving models to diving behaviour of Brünnich's guillemots. Anim. Behav. 64,739 -745.[CrossRef]
Otani, S., Naito, Y., Kato, A. and Kawamura, A. (2000). Diving behavior and swimming speed of a free-ranging harbor porpoise, Phocoena phocoena. Mar. Mamm. Sci. 16,811 -814.
Peters, G., Wilson, R. P., Scolaro, J. A., Laurenti, S., Upton, J. and Galleli, H. (1998). The diving behaviour of magelanic penguins at Punta Norte, Peninsula Valdés, Argentina. Colon. Waterbirds 21,1 -10.
Racey, P. A. and Swift, S. M. (1985). Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour. J. Anim. Ecol. 54,205 -215.
Ropert-Coudert, Y., Kato, A., Baudat, J., Bost, C.-A., LeMaho, Y. and Naito, Y. (2001). Time/depth usage of Adélie penguins: an approach based on dive angles. Polar Biol. 24,467 -470.[CrossRef]
Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y.,
Charrassin, J. B., Bost, C.-A., Handrich, Y. and Le Maho, Y.
(2002). Buoyancy and maximal diving depth in penguins: do they
control inhaling air volume? J. Exp. Biol.
205,1189
-1197.
Sato, K., Mitani, Y., Cameron, M. F., Siniff, D. B. and Naito,
Y. (2003). Factors affecting stroking patterns and body angle
in diving Weddell seals under natural conditions. J. Exp.
Biol. 206,1461
-1470.
Stahl, J. C., Derenne, P., Jouventin, P., Mougin, J. L., Teulieres, L. and Weimerskirch, H. (1985). Le cycle reproducteur des gorfous de l'archipel Crozet: Eudyptes chrysolophus, le Gorfou macaroni et E. chrysocome, le Gorfou sauteur. L'Oiseau R.F.O. 55,27 -43.
Takahashi, A., Sato, K., Naito, Y., Dunn, M. J., Trathan, P. N. and Croxall, J. P. (2004). Penguin-mounted cameras glimpse underwater group behaviour. Proc. R. Soc. Lond. B (Suppl.) 271,S281 -S282.
Tanaka, H., Takagi, Y. and Naito, Y. (2001). Swimming speeds and buoyancy compensation of migrating adult chum salmon Oncorhynchus keta revealed by speed/depth/acceleration data logger. J. Exp. Biol. 204,3895 -3904.[Medline]
Thompson, D. and Fedak, M. A. (2001). How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim. Behav. 61,287 -296.[CrossRef]
Watanuki, Y., Niizuma, Y., Gabrielsen, G. W., Sato, K. and Naito, Y. (2003). Stroke and glide of wing-propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth. Proc. Roy. Soc. Lond. B 270,483 -488.[CrossRef][Medline]
Weimerskirch, H., Zotier, R. and Jouventin, P. (1988). The avifauna of Kerguelen Islands. Emu 89,15 -29.
Williams, T. D. (1995). Macaroni penguin Eudyptes chrysolophus. In The Penguins (ed. T. D. Williams), pp. 211-220. Oxford: Oxford University Press.
Williams, T. D. and Croxall, J. P. (1991). Annual variation in breeding biology of macaroni penguins, Eudyptes chrysolophus, at Bird Island, South Georgia. J. Zool. Lond. 223,189 -202.
Williams, T. D., Kato, A., Croxall, J. P., Naito, Y., Briggs, D. R., Rodwell, S. and Barton, T. R. (1992). Diving pattern and performance in nonbreeding Gentoo penguins (Pygoscelis papua) during winter. Auk 109,223 -234.
Wilson, R. P. (1995). Foraging ecology. In The Penguins (ed. T. D. Williams), pp.81 -106. Oxford: Oxford University Press.
Wilson, R. P. and Wilson, M. P. (1989). A package-attachment technique for penguins. Wildl. Soc. Bull. 17,77 -79.
Wilson, R. P. and Wilson, M. P. (1995). The foraging behaviour of the African penguin Spheniscus demersus. In The Penguins: Ecology and Management (ed. P. Dann, I. Norman and P. Reilly), pp. 244-265. Sidney: Surrey Beatty and Sons.
Wilson, R. P., Grant, W. S. and Duffy, D. C. (1986). Recording devices on free-ranging marine animals: does measurement affect foraging performance? Ecology 67,1091 -1093.
Wilson, R. P., Culik, B. M., Adelung, D., Spairani, H. J. and Coria, N. R. (1991). Depth utilisation by breeding Adelie penguins, Pygoscelis adeliae, at Esperanza Bay, Antarctica. Mar. Biol. 109,181 -189.
Wilson, R. P., Culik, B. M., Peters, B. M. and Bannasch, R. (1996). Diving behaviour of Gentoo penguins, Pygoscelis papua; factors keeping dive profiles in shape. Mar. Biol. 126,153 -162.
Yoda, K., Naito, Y., Sato, K., Takahashi, A., Nishikawa, J.,
Ropert-Coudert, Y., Kurita, M. and Le Maho, Y. (2001). A new
technique for monitoring the behavior of free-ranging Adélie penguins.
J. Exp. Biol. 204,685
-690.
Related articles in JEB: