brief communications

Energy saving in flight formation

Pelicans flying in a ‘V’ can glide for extended periods using the other birds’ air streams.

M
any species of large bird fly together electronic heart-rate logger (Polar Electro,
in formation, perhaps because Finland) adapted for large birds5; the unit
flight power demands and energy was attached to the back feathers with
expenditure can be reduced when the birds adhesive tape and the electrodes were
fly at an optimal spacing1–3, or because placed dorsally about 250 mm apart directly
orientation is improved by communication under the skin. Heart rates and wing-beat
within groups4. We have measured heart frequencies recorded during the different
rates as an estimate of energy expenditure types of flight were averaged for each
in imprinted great white pelicans (Pelecanus individual over one to four different bouts
onocrotalus) trained to fly in ‘V’ formation, that lasted for 30 seconds to 2 minutes.
and show that these birds save a significant Pelicans flying over water in diagonal
amount of energy by flying in formation. formation used the typical flight pattern of
This advantage is probably a principal pelicans in formation — a few wing-beats,
reason for the evolution of flight formation followed by a short, 1–2-second glide — in
in large birds that migrate in groups. which 42.2% of the time is spent flapping. Figure 1 Great white pelicans flying in formation over a river
We trained eight great white pelicans to Birds flap in time with the leader, either in (photograph, R. Marzin, Galatée Films).
fly after a moving motor boat and an ultra- unison or in regular succession. Within the
light aeroplane in Djoudj National Park, formation, the number of glides per minute the aerodynamic advantage of flight for-
Senegal (Fig. 1). All flight sessions were was similar for all birds (average, 12.651.6 mation7, thus reducing the energy saving8
filmed with a digital camera to measure glides per minute), but the average wing- — so geese, for example, may make an
wing-beat frequency and to synchronize beat frequency decreased from the leader to energy saving of only 2.4% (ref. 8).
recordings of behaviour and heart rate. The the bird in the fourth position (Fig. 2). In our study, pelicans often had difficul-
average heart rate was recorded by using an When flying alone, 1 m above water or ty staying within the formation, particularly
at higher altitude, pelicans beat their wings when flying at the rear. But even though
more frequently than birds flying in for- these birds were regularly adjusting their
mation (Wilcoxon paired signed-rank test: position, they still achieved a significant
Z42.2, n46 birds, P40.028; and Z42.0, energy saving. This saving may be only
n45, P40.043, respectively), but still partly due to effects of the wakes of other
glided briefly. When in formation, birds birds on the power input that results from
105 had a heart rate that was 11.4–14.5% lower formation flight itself. When flying in
heart rate (b.p.m) wingbeat frequency

90 than in birds flying alone at 1-m or 50-m formation, pelicans appear to beat their
75
(b.p.m.)

altitude (Fig. 2; Z42.0, n45, P40.043; wings less frequently and to glide for longer
Mean

60 1
45 2
3 4 5 Last
and Z42.4, n46, P40.018, respectively). periods. A rough calculation based on our
12
0
When gliding, birds’ heart rates decreased estimates of the proportion of time spent
200 further and they beat their wings only flapping and gliding in formation, and
190 occasionally (Fig. 2; Z41.8, n47, P40.068 assuming that the overall costs of the
Mean

180 for both heart rate and wing-beat frequen- glide–flap sequence is the sum of the gliding
170
160
cy). Birds flying alone over water had a and flapping components, reveals an actual
150 slightly higher mean wing-beat frequency saving of 1.7–3.4% as a result of wake
Gliding Alone at Alone at In and lower heart rates than birds flying at effects on power input — this value is
50 m 1m formation
higher altitude (Fig. 2); however, the differ- comparable to that estimated for geese8.
Figure 2 Wing-beat frequency and heart rate of pelicans engaged ences were not significant (Z41.1, n46, The main benefit of flight formation, which
in various types of flight (mean51 s.d.). Birds flying over a river P40.249; and Z40.1, n45, P40.893, until now has not been recognized, could be
following a motor boat cruising at a constant speed of 48 km h11 respectively), suggesting that any ground that by flying in a vortex wake, pelicans are
flew at an average altitude of 1 m above the water, initially alone effect6 was not significant. able to glide for a greater proportion of
at a distance from the boat (‘alone at 1 m’), but then joining other Our results provide empirical evidence their total flight time, with the total energy
birds in formation (‘in formation’). Numbering of circles indicates that, compared with solo flight, formation savings of 11.4–14.0% being achieved
the position in the formation, ‘1’ being the leader. In formation flight confers a significant aerodynamic primarily through this strategy.
flights, only birds in or behind the third position were used to advantage which allows birds to reduce Formation flight, by allowing birds to
measure heart rate, to avoid the possible effects of motor-boat their energy expenditure while flying at a reduce their energy expenditure, enables
turbulence on flight pattern. Wing-beat frequency of the lead and similar speed. In birds flying in formation, them to increase their foraging or mig-
second birds was measured in groups flying far from the boat. each wing moves in an upwash field that is ratory range. Oblique and V formations are
Birds flying with an ultralight aeroplane cruising at 55–60 km h11 generated by the wings of the other birds in comparable in terms of energy gain for
at an altitude of about 50 m were not able or willing to fly in the the formation. Modelling has shown that individual birds apart from the leader, and
wake of the aircraft, and generally flew at a distance, using a when birds are flying with optimal spacing, are aerodynamically the most advantageous
flapping flight, at a speed of 45–50 km h11 (‘alone at 50 m’). a maximal reduction in power can be compared with other types of flight in
Pelicans following the plane finished their flight of 3 km with a achieved3 and total transport costs can be flocks9. Pelicans use such flight patterns
glide of 2–3 min (‘gliding’) before landing on the water. Heart substantially reduced2. However, field extensively, not only during migration but
rates averaged 77.6515.2 beats per min (b.p.m.) when resting, observations of V formations indicate that also during group commuting trips
and reached 198.2518.7 and 204.9515.7 b.p.m. when birds often shift from their optimal posi- between colonies and foraging zones10.
paddling in water and when walking, respectively. tioning, perhaps in an attempt to maximize Although pelicans benefit by saving
NATURE | VOL 413 | 18 OCTOBER 2001 | www.nature.com © 2001 Macmillan Magazines Ltd 697
brief communications
energy when flying in formation, this e-mail: [email protected] moved back into cold water (Fig. 1c).
arrangement may also favour communica- †Galatée Films, Le Peuple Migrateur — Jacques The large difference in temperature
tion and coordination within the group — Perrin, 92 Rue Jouffroy d’Abbans, tolerance between adults (20–80 7C) and
for example, by helping birds to stay in 75017 Paris, France embryos (2–20 7C) precludes the possibility
visual contact4,10 and enabling flight-pass 1. Lissaman, P. B. S. & Shollenberg, C. A. Science 168,
of embryonic development inside adult
and velocity information to be conveyed 1003–1005 (1970). worm tubes. Optimal temperatures for
between them6. This may explain why 2. Badgerow, J. P. & Hainsworth, F. R. J. Theor. Biol. 93, development (10–15 7C) are found close to
41–52 (1981).
several other naturally occurring config- 3. Hummel, D. J. Theor. Biol. 104, 321–347 (1983).
the bases of hydrothermal-vent chimneys.
urations of bird flocks are aerodynamically 4. Hamilton, W. J. in Animal Orientation and Navigation (ed. As eggs are negatively buoyant upon
neutral or even disadvantageous relative to Storm, R. M.) 57–71 (Oregon State Univ. Press, Corvallis, 1967). release, some embryos probably develop on
solitary flight8,11. 5. Weimerskirch, H. et al. Proc. R. Soc. Lond. B 267, or near the sea floor, just below the adult
1869–1874 (2000).
Henri Weimerskirch*, Julien Martin*, 6. Hainsworth, F. R. J. Exp. Biol. 135, 431–444 (1988).
habitat. However, it is likely that at least
Yannick Clerquin†, Peggy Alexandre†, 7. Badgerow, J. P. Auk 105, 749–755 (1988). some embryos are dispersed by currents
Sarka Jiraskova† 8. Cutts, C. J. & Speakman, J. R. J. Exp. Biol. 189, 251–261 (1999). and carried to new sites through cold (2 7C)
9. Higdon, J. J. L. & Corrsin, S. Am. Nat. 112, 727–744 (1978).
*Centre d’Etudes Biologiques de Chizé, abyssal sea water, as occurs in other vent
10. O’Malley, J. B. E. & Evans, R. M. Can. J. Zool. 60,
Centre National de la Recherche Scientifique, 1388–1396 (1982). species5,6. Our results show that embryos of
79360 Villiers en Bois, France 11. Gould, L. L. & Heppner, F. Auk 91, 494–506 (1974). A. pompejana survive but do not develop
at this temperature.
It has been suggested that dispersing
larvae of hydrothermal-vent bivalves7 and
Deep-sea ecology we obtained qualitatively similar results polychaetes8 may delay their development
(Fig. 1b), with fewer abnormalities. until they encounter warm water. Our
Developmental arrest in To investigate whether cold-water devel- results provide empirical evidence for such
vent worm embryos opmental arrest is reversible, we maintained
zygotes at 2 7C for 72 h, exposed them to a
reversible developmental arrest in a vent
species; a similar phenomenon has been
10 7C heat pulse for 45 min, and incubated

T
emperature is a key factor in controlling reported in larvae of the bathyal echinoid
the distribution of marine organisms them at 2 7C for a further 24 h. Although Linopneustes longispinus9. Although we do
and is particularly important at embryos maintained at 2 7C never under- not know how long the embryos of A. pom-
hydrothermal vents, where steep thermal went cleavage, those exposed to a short heat pejana remain viable at low temperatures,
gradients are present over a scale of cen- pulse resumed development, and cleavage this temperature-sensitive mechanism for
timetres1. The thermophilic worm Alvinella continued even after the embryos were controlling development may result in
pompejana, which is found at the vents of the
East Pacific Rise (2,500-m depth), has an a 20 °C 14 °C 10 °C 2 °C
unusually broad thermotolerance (20–80 7C) 100
* *
as an adult2,3, but we show here that the 80
Survival (%)

temperature range required by the dev-

60
eloping embryo is very different from that
tolerated by adults. Our results indicate that 40
early embryos may disperse through cold 20
abyssal water in a state of developmental 0
arrest, completing their development only
when they encounter water that is warm 100
enough for their growth and survival. 80
Cleavage (%)

We obtained early embryos of A. pom-

60 *
pejana by in vitro fertilization, and reared
*
them at temperatures ranging from 2 7C to 40
20 7C under atmospheric and deep-sea 20
pressures. We monitored mortality (diag-
0
nosed by the breakdown of the plasma 0 24 48 72 24 48 72 24 48 72 24 48 72
membrane or by production of irregular Time after fertilization (h)
cytoplasmic blebs) and zygotic cleavage
during early development. b 100 100 c 100
Embryos kept at 20 7C and one atmos- 80 80 80
Frequency (%)
Survival (%)

Cleavage (%)

phere of pressure all died within 24 h 60 60 60

(Fig. 1a), although many completed the first
cleavage. At 14 7C and 10 7C, 70–90% of 40 40 40
zygotes cleaved, with rates varying as a func- 20 20 20
tion of temperature. At 2 7C, oocytes and 0
0%
0
0% 0%
0
embryos remained intact, without cleaving, 20 °C 10 °C 2 °C 20 °C 10 °C 2 °C U 2 4 8
for 72 h (Fig. 1a) and for at least a further Temperature Developmental stage
8 days, when we stopped the experiment.
As low hydrostatic pressure inhibits cleav- Figure 1 Effects of temperature on early embryos of Alvinella pompejana. a, Percentage of embryos surviving (top) and cleaving (bottom)
age in other deep-sea invertebrates4, some when incubated at one atmosphere of pressure and at temperatures of 2–20 7C. At least 20 embryos were scored per sample, except for
irregular cleavages in our one-atmosphere 2 samples (asterisks), which contained fewer embryos. b, Survival and cleavage at the indicated temperatures after 48 h at a pressure of
incubations were not unexpected. When 250 atmospheres. c, Distribution of cleavage stages in embryos incubated at 2 7C for 24 h (orange bar) and 8 days (blue bar) and in
we repeated the incubation experiments 72-h embryos exposed to a 45-min heat pulse at 10 7C (white bars), then transferred back to 2 7C for a further 24 h. Developmental
at in situ pressures (250 atmospheres), stages are two- to eight-cell stages. U, uncleaved.

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