Content uploaded by Michel Gauthier-Clerc
Author content
All content in this area was uploaded by Michel Gauthier-Clerc on Nov 22, 2018
Content may be subject to copyright.
The adaptive significance of cre
`ches in the king penguin
CE
´LINE LE BOHEC*, MICHEL GAUTHIER-CLERC†&YVONLEMAHO*
*Centre d’E
´cologie et Physiologie E
´nerge
´tiques-CNRS
yStation Biologique de la Tour du Valat
(Received 14 January 2004; initial acceptance 6 March 2004;
final acceptance 10 November 2004; published online ---; MS. number: 7963R)
Cre
`ching behaviour in penguins is defined as the rearing of chicks by their own parents in large flocks
called ‘cre
`ches’. Although several hypotheses have been proposed to account for the behaviour, the factors
inducing chicks to aggregate remain relatively poorly understood, in particular for colonial seabirds. We
studied cre
`ching behaviour in the king penguin, Aptenodytes patagonicus, by looking at the dynamics of
cre
`che formation and possible costs and benefits associated with this strategy. Cre
`ches increased in size but
declined in number throughout the austral winter. They were located preferentially in the central parts of
the colony. Lone chicks suffered the most aggression from unrelated adults, whereas chicks in a cre
`che
suffered the least. Chicks attacked by unrelated adults preferentially joined a cre
`che. Adult aggression
appeared to be a major factor inducing cre
`ching behaviour. Chicks at the periphery of a cre
`che were more
vigilant while sleeping, as measured by eye openings. Cre
`ches seemed to occasion intense competition
among chicks for access to the centre. Chicks in poor condition were attacked and pushed to the periphery
of the cre
`che, where they were preyed on by giant petrels. During harsh weather conditions, chicks
amalgamated into larger cre
`ches, tolerated lower interindividual distances and turned their backs to the
wind and rain. Our results accord with the idea that cre
`ching behaviour in king penguins is a strategy that
protects chicks from adult aggression, predation and severe weather.
Ó2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Cre
`ching behaviour is a rearing strategy observed in several
colonial species (Gorman & Milne 1972). Coloniality, the
aggregation of conspecific individuals on breeding territo-
ries distinct from foraging sites (Kharitonov & Siegel-
Causey 1988), appears to supply many benefits such as
optimal breeding habitat selection (Danchin & Wagner
1997) and reduction of predation (Wittenberger & Hunt
1985; Siegel-Causey & Kharitonov 1991). However, there
are several obvious disadvantages of colonial breeding, such
as having to forage away from the colony, needing a parent–
offspring recognition system and having to protect young
against conspecific adult aggression (Wittenberger & Hunt
1985; Kharitonov & Siegel-Causey 1988). Cre
`ching appears
to be a partial substitute for continuous parental protection
and care, permitting both parents to leave their young
temporarily and go to foraging areas (Evans 1984; Besnard
2001). Several adaptive advantages have been proposed for
cre
`ching behaviour, including reduced predation (Pettingill
1960; Davis 1982; Tourenq et al. 1995), increased thermo-
regulation efficiency (Pettingill 1960; Yeates 1975; Davis
1982; Evans 1984; Carter & Hobson 1988; Tourenq et al.
1995) and improved social tolerance (Bildstein 1993). Some
authors have suggested that intraspecific aggression could
be the main proximate cause of cre
`che formation (Seddon &
van Heezik 1993; Tourenq et al. 1995; Besnard 2001).
However, there is little agreement on why chicks form
cre
`ches, mainly because the behaviour is so variable
between species.
The term ‘cre
`che’ was first used to describe cases of chick
amalgamation in the emperor penguin, Aptenodytes forsteri
(Wilson 1907). Although this concept of cre
`che applies
specifically to birds (Brown & Root 1971; Gorman & Milne
1972), a few authors have used it to describe offspring
gatherings in mammals such as Mexican free-tailed bats,
Tadarida brasiliensis mexicana (McCracken 1984), harbour
seals, Phoca vitulina richardsi (Slater & Markowitz 1983),
giraffes, Giraffa camelopardalis (Leuthold 1979), Nubian
ibexes, Capra ibex nubiana (Levy & Bernadsky 1991) and
sable antelopes, Hippotragus niger (Thompson 1998). The
king penguin, Aptenodytes patagonicus, is a prime model for
studying cre
`ching behaviour. Its breeding cycle is unusual
for seabirds because it exceeds a year and the chick
fledging period lasts about 11 months (Barrat 1976).
During the austral winter, chicks left alone in the colony
are subject to prolonged starvation (up to 5 months)
Correspondence: Ce
´line Le Bohec, CEPE-CNRS, 23 rue Becquerel, 67087
Strasbourg Cedex 02, France (email: celine.lebohec@c-strasbourg.
fr). Michel Gauthier-Clerc is at the Station Biologique de la Tour du
Valat, Le Sambuc, 13200 Arles, France.
ARTICLE IN PRESS
1
0003–3472/04/$30.00/0 Ó2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
AN IM AL BE HA V IO UR , 2005, --,--–--
doi:10.1016/j.anbehav.2004.11.012
DTD 5
between the infrequent feeding visits by their parents
(Cherel et al. 1987; Descamps et al. 2002). Thus, large
metabolic reserves and cre
`ching behaviour are important
for the chicks’ survival (Barrat 1976; Cherel et al. 1987).
King penguin cre
`ches are aggregations of unrelated chicks,
in which the chicks continue to be fed only by their own
parents. Cre
`ching behaviour in king penguins has been
mentioned by some authors (e.g. Barrat 1976; Descamps
et al. 2002; Le Bohec et al. 2003), but has not been
examined in detail. Our aim in this study was to describe
cre
`ching by king penguin chicks over the annual cycle for
various habitats within a colony. Since king penguins are
very aggressive to conspecifics (Le Maho et al. 1993;
Challet et al. 1994; Co
ˆte
´2000), we tested the effect of
aggression on cre
`ching. Finally, we investigated whether
cre
`ches protect against predation and inclement weather.
METHODS
Study Species
The king penguin is a subantarctic seabird that breeds in
large dense colonies. The pair incubates a single egg
directly on their feet. During incubation and brooding
periods, the birds vigorously defend a small territory
(approximately 0.5–0.8 m
2
) against breeding neighbours
and intruders that approach within pecking distance
(Co
ˆte
´2000). The breeding cycle lasts 14–16 months.
Two peaks of laying occur: a first peak of early breeders
(at the beginning of December) that failed their previous
breeding season and a second peak of breeders (at the end
of January) that bred late because they fledged a chick
during the previous breeding season (Barrat 1976). Chick
rearing can be split into four periods: (1) brooding of
young chicks by their parents; (2) formation of small
prewintering cre
`ches while chicks wait for their parents to
return from feeding trips (Descamps et al. 2002); (3)
formation of large wintering cre
`ches when feeding visits
become infrequent (Descamps et al. 2002) and the
majority of the adults have deserted the colony; (4) at
the end of winter, progressive breaking up of cre
`ches
when adults return to the colony to moult and start
breeding again and the chicks moult before going to sea.
Data Collection
We conducted the study in the breeding colony La
Grande Manchotie
`re (around 16 000 pairs) on Possession
Island, Crozet Archipelago (46250S, 51 450E) during
a complete breeding cycle (2001–2002). For each aspect
of the study we collected data during similar time slots
and under similar weather conditions to minimize bias.
Cre
`che formation and dynamics
A cre
`che has been defined as two or more chicks in close
association (Evans 1984; Carter & Hobson 1988), where
individuals are less than two chick wing lengths apart (i.e.
less than 60 cm in king penguins). From February 2001 to
February 2002, we determined cre
`che numbers and sizes
(chicks per cre
`che) in two designated parts of the colony
(Fig. 1): Zone A (beach and river, 0.6 ha) and Zone B (side
of the valley, 0.8 ha). The high frequency of observations
conducted in Zone A (twice a week until May then once
a week when cre
`che sizes varied less) allowed us to follow
in detail the progressive formation of cre
`ches during the
annual cycle. To investigate whether chicks gather prefer-
entially in particular areas, we divided Zone B into 60
squares (each of about 10 !10 m) which we observed
once a week until May and then twice a month. We
defined four categories of habitat in Zone B: Central zone:
nonfloodable central areas; Floodable zone: areas poten-
tially floodable at the bottom of the slope; Peripheral
zone: peripheral areas at the top of the slope; Rocky zone:
rocky faced areas. The average number of chicks per cre
`che
per square and the average number of cre
`ches per square
were determined for each category. We made these
observations for the three cre
`ching phases of the annual
cycle: prewintering (February to May), wintering (June to
October) and postwintering (November to February).
Intraspecific aggressiveness
To record aggressive behaviours, we used the focal
animal and continuous sampling method (Altmann
1974; Martin & Bateson 1993). We quantified agonistic
interactions (number of bill strokes, hits and misses)
between an individual selected randomly in the colony
and conspecifics during 10-min observation periods. A
total of 720 focal observations were conducted in Zone A
from February to November 2001.
Adult–adult aggressive interactions. From 3 to 13 February,
we counted the acts of aggression on neighbours by adults
at different breeding stages: incubating (NZ40), brood-
ing a 1-week-old chick (NZ40) and brooding a 3-week-
old chick (NZ40). We estimated chick size by the chick’s
height relative to that of its parent to define the following
two categories: (1) approximate height of 10%, 1-week-old
grey chick (with no down, hence dependent on its parent)
and (2) approximate height of 30%, 3-week-old brown
chick (covered by down).
Adult–chick aggressive interactions. From about 20 days,
when they can thermoregulate (Barre
´1984), chicks are left
alone between feeding visits. At this age chicks either
remain alone or approach other adults or chicks. From 15
February to 10 March 2001, we recorded the number of
pecks that chicks received from breeding adults and other
chicks (guarded by an adult and/or in a cre
`che; NZ120).
Chicks guarded by parents were used as a control situation
(NZ120). We used the method of all occurrence behav-
iour sampling (Altmann 1974) to record lone chicks
starting to move, (2) duration and number of pecks
received from adults during the movement, and (3) the
chicks’ destination.
Chick–chick aggressive interactions. Agonistic interactions
between chicks in good and poor condition were observed
at the beginning of cre
`che formation (March) and at the
end of the wintering cre
`ches (September). Chicks in good
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
2
DTD 5
condition were the tallest and heaviest individuals in the
cre
`che: 70–80% (March, NZ20) or 90% (September,
NZ20) of an adult’s height, with an invisible breastbone
and protruding abdomen. Chicks in poor condition were
the smallest and thinnest individuals in the cre
`che: 30–
50% (March, NZ20) or 60% (September, NZ20) of an
adult’s height, with a prominent breastbone and abdomen
not protruding. We also took focal samples of chicks fed
by an adult and chicks in a cre
`che from March to
November to compare their aggressiveness (N Z260).
Body mass of chicks and position in the cre
`che
We defined the cre
`che periphery as that part formed by
the first two rows of chicks on the outside of the group.
Chicks on the periphery (NZ25) and in the centre
(NZ25) of cre
`ches in Zone A were caught by hand and
weighed with an electronic balance (G10g) monthly from
March to October to establish a correlation between chick
position in the cre
`che and body condition.
Vigilance and sleep
We collected vigilance and sleep data using the focal
animal and continuous sampling technique (Altmann
1974; Martin & Bateson 1993). Observations lasted
2 min. Using a 40!telescope, a tape recorder and
a stopwatch, we recorded the frequency of eye openings,
the duration of consecutive eye openings and intervals
between eye openings for randomly selected individuals
(Gauthier-Clerc et al. 1998, 2000). These data were
collected for birds on the periphery (NZ30) and in the
centre (NZ30) of cre
`ches adopting the typical sleep
posture, i.e. standing up, head lying on back, with the
visible eye closed and bill tucked underneath a flipper
(Challet et al. 1994; Dewasmes et al. 1989). This part of
the study was conducted in Zone A in May (beginning of
wintering cre
`ches), at the end of June (middle of wintering
cre
`ches) and at the end of August (end of wintering
cre
`ches).
Predation
We recorded instances of predation (NZ157) according
to the method of all occurrence behaviour sampling
(Altmann 1974). In all zones we recorded the type of
predator (giant petrels Macronectes halli and M. giganteus,
brown skua, Catharacta lonnbergi, kelp gull, Larus domi-
nicanus, or lesser sheathbill, Chionis minor), chick size
(small, medium or tall, depending on its height relative to
the adult), chick body condition (see above), and pre-
dation outcome: success or failure.
Weather conditions
We investigated cre
`ching in relation to weather in
Zone C (beach and river, 0.3 ha, Fig. 1): (1) winter,
Cold)Wind)Rain (NZ8 days, %5C, wind R28 knots,
La Baie
du Marin
Zone B
Zone A
Technical
area
Zone C
road
Camp River
30 m
Scale
01020
Central zone
Floodable zone
Peripheral zone
Rocky zone
Figure 1. Schematic map of the breeding colony La Baie du Marin showing the various study areas. Dashes: boundary of the breeding colony
La Grande Manchotie
`re. Zone A (beach and river, blue outline), for study of cre
`che formation dynamics during the annual cycle; Zone B (side
of the valley, red outline), for study of the habitat; Zone C (beach and river, green outline), for study of the effect of weather conditions.
ARTICLE IN PRESS
LE BOHEC ET AL.: CRE
`CHING IN KING PENGUINS 3
DTD 5
with rain); (2) winter, Cold)Wind)No rain (NZ12 days,
%5C, wind R28 knots, without rain); (3) winter,
Cold)No wind)No rain (NZ10 days, %5C, no wind,
no rain); and (4) summer, Warm)No wind)No rain (NZ8
days, R10C, wind 0–6 knots, without rain). Variables
recorded were number and size of cre
`ches, interindividual
distance (NZ100) estimated in units of chick flipper
length, and position of chicks in good condition
(NZ20) and poor condition (NZ20) within the cre
`che.
Data Analysis
Results are reported as means GSE. We assume that our
random samplings did not include significant replication
because there were more than 20 000 king penguin chicks
in the colony, and the same bird was unlikely to be
observed more than once. When the data were normally
distributed and homoscedasticity of data was confirmed,
we compared samples using one-way or two-way ANOVAs
followed by a parametric post hoc test adjusted by
Tukey (parametric tests, Scherrer 1984). When application
conditions for ANOVA were not satisfied (even after
transformation), we used nonparametric tests (Sheirer–
Ray–Hare test (two-way analysis of variance by ranks) or
Kruskal–Wallis test (one-way analysis of variance by
ranks), Siegel & Castellan 1988) to compare more than
two samples. These tests were followed by a nonparametric
post hoc test adjusted by Dunn (samples of different size).
To compare means of two independent groups and to
analyse frequencies we used the Mann–Whitney Utest
and the chi-square test, respectively. For correlations
between variables we used Spearman rank and Kendall
rank partial correlation coefficients. For the statistical
analyses we used SYSTAT 9.0 and Sigmastat 2.0 (SPSS
Inc., Chicago, IL, U.S.A.). All tests were two tailed with
significance level set at aZ0.05.
Ethical Note
Observations were made 10–100 m from outside the
colony. At short distances, we observed the birds from
behind a low wall or from a blind. This type of observation
did not cause any disturbance nor did it expose birds to
predators. During monthly weighings we minimized
disturbance by moving slowly towards the cre
`ches and
releasing captured chicks close to the cre
`che from where
they came. We verified that the cre
`ches reformed imme-
diately after the capture. No predation was observed
during that time. Observed and weighed birds were
selected randomly in the colony and were not marked.
The study received the consent of the Ethics Committee of
the Institut Polaire Franc¸ais – Paul-Emile Victor.
RESULTS
Number and Size of Cre
`ches
The first chicks abandoned temporarily were seen
during the week 9–15 February. The number of such
chicks increased progressively until the end of June (to
about 6500 chicks in Zone A). At the same time, the
number of cre
`ches with up to 20 chicks increased until 6
April, when it reached a maximum (357 in Zone A; Fig. 2).
The number of cre
`ches was highly correlated with the
number of chicks left unattended by their parents (Spear-
man rank correlation: r
S
Z0.90, NZ17, P!0.005).
Cre
`che size was negatively related to the number of
cre
`ches (Kendall rank partial correlation coefficient:
r
DE
Z0.25, NZ60, P!0.005) and size increased pro-
gressively from February to September (Fig. 2). The
number of cre
`ches started to decrease at the beginning
of April. This decrease resulted from the grouping of
several small cre
`ches (less than 50 chicks) into larger ones.
The minimum number of cre
`ches (8) and the maximum
size (about 500 chicks) were observed between 13 August
and 24 October. At the end of October, cre
`ches split up
and became more numerous but smaller in size.
Location in the colony and period of the year had
a significant effect on the number of chicks in cre
`ches per
square (two-way ANOVA: zone: F
3,141
Z15.66, P!0.005;
period: F
2,142
Z22.11, P!0.005; interaction:
F
6,133
Z3.51, PZ0.001; Fig. 3a) and the number of cre
`ches
per square (two-way ANOVA: zone: F
3,141
Z16.77,
P!0.005; period: F
2,142
Z81.75, P!0.005; interaction:
F
6,133
Z4.73, P!0.005; Fig. 3b). During the prewintering
and wintering periods, the number of chicks in cre
`ches and
the number of cre
`ches were significantly higher in the
central zone than in the other three locations (Tukey tests:
P!0.005). There were no significant differences between
the four locations during the postwintering period (Tukey
tests: NS). These were significantly more prewintering than
wintering and postwintering cre
`ches in the floodable and
peripheral zones (Tukey tests: P!0.05) and more post-
wintering than wintering cre
`ches in the floodable and
rocky zones (Tukey tests: P!0.05).
Intraspecific Aggression
The level of adult aggression was on average very high
whatever their reproductive status (23 G2 agonistic in-
teractions per 10 min, NZ120). Adult aggressive behav-
iour varied significantly with reproductive status (ANOVA:
F
2,117
Z3.59, PZ0.031) and was highest for adults
brooding a 3-week-old chick (30 G3 interactions,
NZ40; Tukey tests: P!0.05). However, there was no
significant difference between adults incubating and
adults brooding a 1-week-old chick (19 G2 and 20 G2
interactions, respectively, NZ40 for both cases, Tukey
test: NS).
Aggression towards a chick by adults and by other chicks
(guarded by an adult and/or in a cre
`che) differed in the four
scenarios (Kruskal–Wallis tests: from adults: H
3
Z139.26,
NZ240, P!0.001; from chicks: H
3
Z91.76, NZ240,
P!0.001; Fig. 4). A chick with one of its parents
experienced the fewest pecks in both cases (0.14 G0.06
and 0.21 G0.07, respectively; Dunn tests: P!0.05).
Attacks by adults on a lone chick (20.98 G2.99) were
about four times higher than aggression towards a chick
with an unrelated adult (4.90 G1.30; Dunn test: P!0.05)
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
4
DTD 5
or towards a chick in a cre
`che (3.23 G0.54; Dunn test:
P!0.05). Conversely, other chicks pecked a lone chick
less (1.30 G0.72) than a chick with an unrelated adult
(3.25 G1.43; Dunn test: P!0.05) or a chick in a cre
`che
(3.63 G0.46; Dunn test: P!0.05).
Lone unguarded chicks mainly moved away in response
to adult aggression (72%). During the displacement
(which lasted on average 33 G5 s), a chick received on
average 1 peck/s. Chicks usually moved to cre
`ches and
stayed in them (61%).
Interindividual Relations within the Cre
`che
Within a cre
`che, chicks in good condition were signif-
icantly more aggressive than chicks in poor condition at
the beginning of cre
`che formation in March and at the
end of winter in September (Mann–Whitney Utests:
March: UZ342, N
1
ZN
2
Z20, P!0.005; September:
UZ328, N
1
ZN
2
Z20, P!0.005; Fig. 5). Chicks in poor
condition received significantly more pecks than chicks in
good condition, in March and in September (March:
UZ73, N
1
ZN
2
Z20, PZ0.001; September:
UZ66.50, N
1
ZN
2
Z20, P!0.005). Chicks in cre
`ches
became significantly less aggressive between March and
September (Fig. 5).
The presence of a feeder adult and period of the year had
a significant effect on the agonistic interactions between
chicks (two-way Sheirer–Ray–Hare tests: effect on the
number of pecks given: adult present: F
1,258
Z119.71,
P!0.005; period: F
4,255
Z15.234, P!0.005; interaction:
F
4,250
Z19.70, P!0.005; effect on the number of pecks
received: adult present: F
1,258
Z52.19, P!0.005; period:
F
4,255
Z17.782, P!0.005; interaction: F
4,250
Z13.76,
PZ0.005). A chick fed by an adult was more aggressive
than a lone chick in a cre
`che (Dunn tests: P!0.05; Fig. 6)
except in November (Dunn test: P!0.05). Lone chicks in
cre
`ches were least aggressive from May to August.
Predation
Chick body mass was significantly different according
to position within the cre
`che and month (two-way
ANOVA: position: F
1,389
Z51.13, P!0.005; month:
F
7,383
Z30.40, P!0.005; interaction: F
7,375
Z4,82,
P!0.005; Fig. 7). Throughout the wintering period,
chicks situated on the periphery of cre
`ches weighed less
than chicks in a central position.
The time spent with an eye open in a typical sleep
posture corresponds to both the vigilance level and the
time spent awake. Position within the cre
`che and month
had a significant effect on the proportion of time spent
with one eye open (two-way Sheirer–Ray–Hare test: posi-
tion: F
1,177
Z368.48, P!0.001; month: F
2,176
Z9.51,
P!0.001; interaction: F
1,177
Z11.33, PZ0.001), the
frequency of eye openings (two-way Sheirer–Ray–Hare test:
position: F
1,177
Z368.48, P!0.001; month: F
2,176
Z9.51, P!0.001; interaction: F
1,177
Z11.33, PZ
0.001) and the duration of eye closure (two-way Sheirer–
Ray–Hare test: position: F
1,177
Z372.68, P!0.001;
month: F
2,176
Z9.52, P!0.001; interaction: F
1,177
Z11.95, P!0.001). The proportion of time spent with
one eye open and frequency of eye openings were signif-
icantly higher among peripheral chicks than central chicks
whatever the month (Dunn tests: P!0.05; Table 1). The
duration of eye closure was significantly higher among
central chicks than peripheral chicks whatever the month
(Dunn tests: P!0.05). Time spent with one eye open and
frequency of eye openings increased from May to August in
the periphery, but were minimal in June in the central
position. The duration of eye closure decreased from May
0Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
20022001
100
200
Number of crèches
0
750
600
450
300
150
Crèche size
300
400
Figure 2. Change in number (histogram) and size (curve) of cre
`ches in Zone A. Cre
`che sizes (number of chicks per cre
`che) are reported as
means CSE.
ARTICLE IN PRESS
LE BOHEC ET AL.: CRE
`CHING IN KING PENGUINS 5
DTD 5
to August in the periphery, but was maximal in June in the
central position.
Out of 157 instances of predation observed on chicks,
giant petrels were the most frequent predators with 95%
of the attacks. Brown skuas, kelp gulls and lesser sheath-
bills committed only 1% of the attacks and were generally
scavengers and detritivores, feeding notably on carcasses
abandoned by giant petrels. The remaining 4% corre-
sponded to attacks by mixed groups of these four preda-
tors. Small chicks were the object of 77% of the attacks
(Table 2). Attacks on chicks in poor condition and/or
already weakened by previous injuries represented 43% of
the instances of predation and generally ended with
predator success (97%). In contrast, attacks on chicks in
12
10
8
6
4
2
0Poor
(N = 20)
Good
(N = 20)
Poor
(N = 20)
Good
(N = 20)
March September
Received from chicks
By chicks
Aggressive behaviour per 10 min
(number of pecks)
Figure 5. Aggressive behaviour between chicks in a cre
`che according
to body condition. Values are means CSE. Mann–Whitney Utests
comparing March and September data: number of pecks received by
chicks in good condition: UZ338, N
1
ZN
2
Z20, P!0.001;
chicks in poor condition: UZ343, N
1
ZN
2
Z20, P!0.001;
number of pecks by chicks in good condition: UZ335,
N
1
ZN
2
Z20, P!0.001; chicks in poor condition: UZ287,
N
1
ZN
2
Z20, PZ0.004.
20
40
Prewintering
(a)
(b)
Wintering
Postwintering
60
80
2
4
6
Central Floodable Peripheral
Area of Zone B
Rocky
8
100
120
140
160
180
Number of chicks in crèches
per square
Number of crèches
per square
Figure 3. (a) Number of chicks in cre
`ches per square and (b) number
of cre
`ches per square by zone in the colony (Central zone:
nonfloodable central area; Floodable zone: areas potentially flood-
able at the bottom of the slope; Peripheral zone: peripheral areas at
the top of the slope; Rocky zone: rocky areas) and period
(prewintering cre
`ches: February to May; wintering cre
`ches: June to
October; postwintering cre
`ches: November to February). Values are
means CSE.
100
10
1
0.1
0.01
Aggressive behaviour per 10 min
log (number of pecks)
Received from adults
Received from chicks
ad
be
c
f
be
With
parent
(N = 120)
With
unrelated
adult
(N = 40)
Alone
(N = 40)
In crèche
(N = 40)
Figure 4. Aggressive behaviour shown by adults and by other chicks
to a chick with one of its parents, a chick with an unrelated adult,
a lone chick and a chick in a cre
`che. Values are means CSE. Values
not assigned the same letter (aggression from adult: a,b,c;
aggression from chicks: d,e,f) are significantly different (post hoc
test adjusted by Dunn: P!0.05).
20
15
10
5
0Mar
(N = 60)
May
(N = 50)
Jun
(N = 50)
Aug
(N = 50)
Nov
(N = 50)
a
c
bb
dd
b
da
e
*
****
Chick alone in crèche
Chick fed by an adult
Aggressive behaviour per 10 min
(number of pecks)
Figure 6. Aggression shown by a chick fed by an adult or by a lone
chick in a cre
`che during the austral winter. Values are means CSE.
Values not assigned the same letter (lone chick: a,b; fed chick: c,d,e)
are significantly different (post hoc test adjusted by Dunn). Compar-
ison of lone and fed chicks: *P!0.05, post hoc test adjusted by Dunn.
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
6
DTD 5
good condition (57% of attacks) succeeded only 24% of
the time.
Weather Conditions
Weather conditions had a significant effect on number
of cre
`ches (ANOVA: F
3,34
Z11.85, P!0.001) and size of
cre
`ches (ANOVA: F
3,34
Z6.33, PZ0.002; Fig. 8). The
number of cre
`ches was significantly lower in Cold)Wind)
Rain and Cold)Wind)No rain conditions than in
Warm)No wind)No rain (Tukey tests: P%0.001). There
were also fewer cre
`ches during Cold)Wind)Rain than in
Cold)No wind)No rain (Tukey test: PZ0.005). Cre
`che
size was markedly higher in Cold)Wind)Rain than in
Warm)No wind)No rain or Cold)No wind)No rain
(Tukey tests: PZ0.009 and PZ0.003, respectively).
Weather conditions had a significant effect on distance
between chicks (ANOVAs: chicks half a flipper apart:
F
3,34
Z12.42, P!0.001; chicks one flipper apart: F
3,34
Z2.94, PZ0.047; chicks two flippers apart: F
3,34
Z8.69,
PZ0.007; chicks three flippers or more apart: F
3,34
Z16.93, P!0.001). Interindividual distance was lower
during the Cold weather conditions (nearly 70% of chicks
up to half a flipper apart) than when it was Warm)No
wind)No rain (25% of chicks; Tukey tests: P!0.005). On
the other hand, cre
`ches were clearly looser when weather
conditions were better (30% of chicks three flippers or
more apart versus 6% during Cold weather conditions,
Tukey tests: P!0.001).
During harsh weather conditions (Cold)Wind)Rain
and Cold)Wind)No rain), the distribution within the
cre
`che of chicks in good and poor condition was not
uniform (ANOVAs: good: F
3,28
Z15.84, P!0.001; poor:
F
3,40
Z50.07, P!0.001). Fewer chicks were in poor
condition in the central position than on the periphery
(4.68 G0.76 versus 15.32 G0.76 chicks; Tukey tests:
P!0.001) and more chicks were in good condition in
the centre (13.37 G0.51 chicks; Tukey test: P!0.001).
Fewer chicks were in good condition on the periphery
(6.63 G0.51 chicks) than in the central position (Tukey
test: P!0.005). In contrast, when it was Cold)No
wind)No rain and Warm)No wind)No rain, chicks had
a uniform distribution within the cre
`che for both body
conditions (10 G0.53 chicks for each category; ANOVAs:
good: F
3,36
Z2.35, PZ0.088; poor: F
3,28
Z0.07,
PZ0.975).
DISCUSSION
Dynamics of Cre
`che Formation
Cre
`che size gradually increased from February to Sep-
tember, whereas the number of cre
`ches dropped from the
beginning of April as a result of small cre
`ches grouping
together into larger ones. The process of gradual amal-
gamation first into numerous small prewintering cre
`ches
can be explained as the consequence of hatching asyn-
chrony, which generates an asynchrony of temporary
chick desertions and the formation of cre
`ches constituted
of chicks of all ages. At the end of the summer, the colony
is deserted by adults, freeing space for chicks to gather into
fewer and larger cre
`ches. White ibis, Eudocimus albus, and
greater flamingo, Phoenicopterus ruber, chicks also gather
first in small then in larger groups and finally into a single
cre
`che (Dinep 1988; Tourenq et al. 1995). Evans (1984)
considered that the temporary desertion of young by
parents is the single most important factor triggering the
onset of cre
`ching, whereas the return of parents to the
Peripheral chicks
Central chicks
10
9
8
7
6
5
4
Body mass (kg)
Mar
(N = 40)
Apr
(N= 50)
May
(N = 50)
Jul
(N = 50)
Aug
(N = 50)
Sep
(N = 50)
Oct
(N = 50)
Jun
(N = 51)
**
*
*
Figure 7. Chick body mass and distribution in cre
`ches (peripheral or
central position) during the austral winter. Values are means GSE.
Comparison of central and peripheral chicks: *P!0.05, post hoc
test adjusted by Tukey.
Table 1. Proportion of time spent with one eye open, frequency of eye openings and duration of eye closure by position in the cre
`che and
month
Periphery Centre
May June August May June August
Sample size
30 30 29 30 30 30
% Time spent with one eye open 14.7G2.9 33.5G4.9 38.6G4.3 0.7G0.3 0.5G0.2 0.8G0.3
Frequency of eye openings (per 2 min) 10.2G1.8 18.8G2.2 26.0G2.4 1.0G0.3 0.6G0.2 0.9G0.3
Duration of eye closure (s) 31.6G7.7 8.3G2.1 3.7G0.5 89.4G7.6 96.4G6.4 92.0G7.1
Values are means GSE.
ARTICLE IN PRESS
LE BOHEC ET AL.: CRE
`CHING IN KING PENGUINS 7
DTD 5
colony stimulates young to leave a cre
`che. Davis (1982)
showed that cre
`ching behaviour is closely associated with
the number of adults present in the colony and suggested
that the cre
`che may serve as an alternative means of
defence against predators when too few adults are present
in the colony to deter predators effectively. This hypoth-
esis does not appear to be valid for king penguins, however,
because, first, they do not cooperate to deter predators and,
second, they are aggressive towards each other during the
breeding period. Cre
`ches are consequently more likely
to be a partial substitute for continuous parental care
(Besnard 2001) and dependent on how much space is
available for their formation.
Habitat Quality
We found that chicks congregated mostly in the central
areas of the colony, as do pelicans and flamingos (Brown
& Root 1971; Tourenq et al. 1995). In other species such as
terns and gulls, cre
`ches are set up on the edge of the
colony (Buckley & Buckley 1976). In king penguins,
central parts of the colony are initially occupied by early
breeders (Co
ˆte
´2000). Individuals that lay first also leave
their chick first once it can thermoregulate efficiently.
Spaces free of adults are then created in those central areas
of the colony, allowing chicks to gather together and form
numerous small prewintering cre
`ches. As the summer
wears on, chicks born later in peripheral and potentially
floodable zones are temporarily abandoned by their
parents and the number of small cre
`ches increases in
these areas.
From June to October, the great majority of adults desert
the colony. The whole area of the colony then becomes
accessible to chicks. However, chick distribution was not
uniform on the space available, and rocky areas, periph-
eral areas at the top of the slope and potentially floodable
areas at the bottom of the slope remained unoccupied.
This suggests that wintering cre
`che locations of king
penguins depend on habitat quality. Central areas are
considered high-quality territories in colonial species
(Kharitonov & Siegel-Causey 1988; Vinuela et al. 1995).
Carter & Hobson (1988) suggested that the location of
cre
`ches of chicks of Brandt’s cormorant, Phalacrocorax
penicillatus, depends on habitat quality. Levy & Bernadsky
(1991) noted that Nubian ibex, Capra ibex nubiana, formed
cre
`ches on shady even terrain.
In our study, cre
`ches broke up progressively in the spring
when adults returned for moulting and courting. As for
prewintering cre
`ches, available space again became a re-
strictive factor because adults occupied most of the colony
area. Chicks were pushed towards peripheral areas of the
colony, probably of lower quality, since they had avoided
these areas before the adults returned. These peripheral
areas are known to be infested by Ixodes uriae ticks, which is
a parasite of the king penguin (Gauthier-Clerc et al. 1999;
Mangin et al. 2003). The parasitic constraint hypothesis
could explain the nonoccupation of peripheral areas by
the chicks when central areas were still available.
Adult Aggression
Breeders were aggressive to alien chicks, especially lone
unguarded chicks. Attacked chicks preferentially joined
cre
`ches where they experienced less aggression and where
the risk of injury was lower compared with pecks and
flipper blows from adults. Other studies have also shown
a high level of aggression between breeders (Le Maho et al.
1993; Challet et al. 1994; Co
ˆte
´2000). Since fights entail
high energetic costs (Ho
¨gstad 1987), the benefits of
defending a territory should therefore be high in terms
of reproductive success (Montgomerie & Weatherhead
1988). Intraspecific aggression in colonial species varies
during the reproductive cycle (Burger & Gochfeld 1990;
Lamey 1993; Challet et al. 1994). The increase in aggres-
sion between adult king penguins from incubation to
brooding may be explained by the higher fitness value of
a chick, as proposed by parental investment theory
(Williams 1966; Trivers 1972; Burger 1981; Siegel-Causey
& Hunt 1981). Adelie penguins, Pygoscelis adeliae (Spurr
1974) and chinstrap penguins, Pygoscelis antarctica
(Vinuela et al. 1995; Amat et al. 1996) similarly defend
chicks more strongly than eggs.
Table 2. Success of predation by giant petrels on chicks according to
chick height (estimated in relation to adult height) and chick
condition (estimated from breastbone and abdomen prominence)
Chick size/condition Attacks (%) Predation success (%)
Small 77
Poor 51 97
Good 49 34
Medium 17
Poor 22 100
Good 78 5
Tall 6
Poor 0 d
Good 100 10
NZ149 predation events.
30
25
20
15
10
5
0
Number of crèches
600
400
200
0
Crèche size
Cold * Wind
* Rain
(N = 8)
Cold * Wind
* No rain
(N = 12)
Cold * No wind
* No rain
(N = 10)
Warm * No wind
* No rain
(N = 8)
Figure 8. Number (histogram) and size (curve) of cre
`ches for four
categories of weather conditions (Zone C, see Methods for
description of categories). Values are means CSE.
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
8
DTD 5
Chicks temporarily abandoned by their parents experi-
enced the highest level of aggression because of the strong
territoriality of incubating and brooding adults. Intraspe-
cific aggression towards such chicks has been frequently
reported in colonial species (Wittenberger & Hunt 1985)
and attack by unrelated adults is generally recognized as
one of the major causes of chick mortality in gulls (Pierotti
1988; Brown & Morris 1995). In our study, aggression by
adults resulted in chicks leaving their natal territory in
72% of cases and joining a cre
`che in 61% of cases. Seddon
& van Heezik (1993), who obtained similar results for the
jackass penguin, Spheniscus demersus (moving towards
a cre
`che: 74%), suggested that intraspecific aggression is
the main proximate cause of cre
`che formation. In March,
up to 10% of adult king penguins guard two or three
chicks and will adopt chicks, at least temporarily. A lone
unguarded chick heads for an unrelated adult in 24% of
movements from the natal territory, tries to take the place
of the legitimate chick and attempts to chase it away by
pecking. Then the parent attacks both chicks without
distinction until its own chick vocalizes. If the parent is
unable to recognize its own chick quickly, the risk of
injuring it is high. The conflict of interest between an
adult and an alien chick may result in a forced adoption
that would then reduce the care for the legitimate chick
and would increase its risk of rejection and injury. This
may explain why a parent defends its territory against
alien chicks.
A cre
`che might then offer the most advantages to
unguarded chicks in terms of less aggression and more
safety than close proximity to an unrelated adult. Indeed,
our data show that the level of aggression between chicks
in a cre
`che is low. In contrast, when a chick is joined by
a parent, it leaves the centre of a cre
`che and becomes more
aggressive towards other chicks. This behaviour can
manifest itself as pushing away foreign chicks that might
steal meals (Boersma & Davis 1997).
Protection from Predators
The central position within a cre
`che allows a chick to
reduce its vigilance and increase time spent sleeping. One
of the functions of gregarious behaviour is to reduce
predation risk (Pulliam 1973; Powell 1974; Caraco et al.
1980). Individuals in a group can reduce the time spent in
vigilance against predators by taking advantage of vigi-
lance by other group members, without reducing the
probability of detecting the predator or increasing an
individual’s risk of capture by a predator (Elgar & Catterall
1981). A reduction in individual vigilance with an increase
in group size has been reported for numerous birds,
mammals and fish (Lendrem 1984; Martella et al. 1995;
Gauthier-Clerc et al. 1998). This group size effect has been
explained by the ‘many eyes hypothesis’, i.e. a collective
detection that increases with group size (Dimond &
Lazarus 1974). King penguin chicks should thus have
a two-fold advantage of being in large cre
`ches: an in-
creased likelihood of predator detection (detection effect)
allowing an individual to devote less time to vigilance and
hence more time to sleep, and a reduction in risk for any
given individual (dilution effect, Dehn 1990). Larger
cre
`ches suffer less predation, probably because the pro-
portion of chicks at the periphery of the cre
`che declines
quickly as the cre
`che gets larger (Hamilton 1971). This
may be an influential factor in the tendency for cre
`che size
to increase over the wintering cre
`che period.
Sleep and vigilance are mutually exclusive. The trade-off
between these two activities may vary according to an
individual’s position in the group (Elgar 1989). Individuals
at the periphery are more vigilant than those at the centre
because they are at greater predation risk. They are the
ones that will be encountered first by an approaching
ground predator (Hamilton 1971; Jennings & Evans 1980;
Petit & Bildstein 1987). Our results corroborate this
hypothesis. When a predator approached a cre
`che, pe-
ripheral chicks extended themselves up to their full height
and bumped into central chicks which were alerted to
danger and then all the chicks gathered in a denser flock.
We also noticed changes in sleep and vigilance during the
winter. Vigilance of central chicks was slightly lower in the
middle of the winter. June corresponded to the longest
average durations of eye closure, the shortest proportion
of time spent with one eye open, and the lowest frequency
of eye openings. Conversely, sleep decreased and vigilance
increased throughout the wintering period for peripheral
chicks. In particular, chicks undergo a long period of
fasting during the austral winter (the coldest period of the
year, around 5C). One of the adaptations allowing birds
to tolerate the fasting and cold lies in their ability to
reduce energy expenditure. Several authors have suggested
that sleep is important for energy conservation because it
decreases body temperature and thermoregulatory costs
(Stahel et al. 1984; Berger & Philipps 1993; Criscuolo et al.
2001). Chicks in the centre of cre
`ches (in a safe microen-
vironment and probably thermally more stable) can drop
their vigilance in favour of sleep in midwinter unlike
those on the periphery, which are exposed to predation as
well as the cold, and sleep less. Studies on pigeons,
Columbia livia, green-winged teals, Anas crecca, and little
penguins, Eudyptula minor, also reported a decrease in the
time spent sleeping when birds were subjected to cold
(Stahel et al. 1984; Graf et al. 1987; Tamisier & Dehorter
1999). According to Pulliam et al. (1974) both group size
and vigilance behaviour are influenced by ambient tem-
perature.
We found that chicks in poor condition experienced the
most aggression and were pushed towards the periphery
of a cre
`che. These chicks suffered the highest predation by
giant petrels. Southern and northern giant petrels are
considered the main king penguin predators, in particular
for chicks during the winter (Hunter & Brooke 1992; Le
Bohec et al. 2003). Our results show that 77% of attacks
were directed towards the smallest chicks and 43%
towards chicks in poor condition and/or already weak-
ened by previous injuries, among which were 51% of
small chicks. Predation attempts on small chicks and
chicks in poor condition were generally successful (66%
and 97%, respectively), in contrast to attacks on medium-
sized and large chicks in good condition (6% success).
Thus, a better body condition increases the chances of
chick survival, not only from the standpoint of resistance
ARTICLE IN PRESS
LE BOHEC ET AL.: CRE
`CHING IN KING PENGUINS 9
DTD 5
to starvation, but also considering protection from pred-
ators.
Our data reveal an effect of chick body condition on
intraspecific relation in the cre
`che. Chicks in good
condition were more aggressive than chicks in poor
condition. This dominance status seems to give them
access to the protected area of the cre
`che centre. Chicks in
poor condition, and consequently less able to defend
themselves, were pushed to the periphery. This rejection
of chicks in poor condition to the periphery of cre
`ches was
most evident during harsh weather.
Protection from Harsh Weather
During inclement weather (cold and rain and/or wind),
there were fewer cre
`ches, but these were larger and chicks
were closer together. Choosing a thermally favourable
environment is an integral part of a chick’s thermoregula-
tory ability (Whittow 1976). The cre
`che probably works as
a hygrometrical and thermally stable microenvironment
(Pettingill 1960). This environment may allow chicks to
decrease their energy expenditure and therefore to increase
survival probability. Our results corroborate this hypothe-
sis. Indeed, as winter progresses, weather conditions
become less favourable and king penguin chicks amalgam-
ated into bigger but fewer cre
`ches. In the rockhopper
penguin, Eudyptes chrysocome, variations in cre
`che size
were related to fluctuations in air temperature (Pettingill
1960). According to Yeates (1975), harsh weather may
result in cre
`che formation in Eudyptidae and Pygoscelidae
chicks. In contrast, Davis (1982) noted that cre
`ching in the
Ade
´lie penguin did not vary consistently with fluctuations
in climatic variables. Chick rearing in this species occurs
during the summer and lasts only a month. Owing to the
relatively mild conditions during the short period when
cre
`ching occurs, Ade
´lie chicks can probably maintain
a constant body temperature. On the other hand, contact
behaviour may be most pronounced when ambient tem-
perature is lowest and wind speed and relative humidity
are highest. This contact behaviour apparently has a ther-
moregulatory function (Davis 1982; Evans 1984).
The chill factor associated with high wind speed
dramatically increases heat loss, and this effect is further
accentuated by high relative humidity (Davis 1982). Tight
elongated cre
`ches could reduce the individual convection
surfaces to a single collective surface, which would reduce
individual heat loss and thereby energy expenditure
linked to thermogenesis during extreme climatic condi-
tions (Taylor 1962; Evans 1984). This probably implies
that chicks are in competition for access to the most
sheltered areas in the group. This life in compact groups,
as illustrated by the huddles of emperor penguins, could
be essential for survival and reproductive success (Ancel
et al. 1997). At lower temperatures, dark-eyed juncos Junco
hymelis (Caraco 1979), and willow tits, Parus montanus
(Ho
¨gstad 1988), form larger flocks of birds with little
aggression. The drop in aggression observed among king
penguin chicks during winter might be explained by the
need to lower energy expenditure in harsh weather and to
establish group cohesion against predation. This social
tolerance strategy, by reducing the overall intraspecific
aggression within the cre
`che, may therefore have emerged
in response to environmental constraints.
This study has allowed us to describe the genesis and
functioning of king penguin cre
`ches during the annual
cycle and to stress the preferential occupation of the
high-quality areas of the colony by cre
`ches. Parental
aggression towards unguarded alien chicks appears to be
an important factor leading to chicks joining a cre
`che.
We suggest that cre
`ching behaviour has adaptive advan-
tages such as protection against predation and severe
weather. Food dispersion and lack of protection against
predators and severe weather, induced by the open
environment characteristic of subantarctic islands, may
be selection pressures that promote the development of
this chick-rearing strategy. Further research should look
into the costs associated with this strategy, such as the
increase in risk of disease and parasite transmission by
the close contact between individuals and food theft (i.e.
kleptoparasitism). Finally, to test the hypothesis that
cre
`ches confer important energy savings, as has already
been shown in emperor penguin huddles (Ancel et al.
1997), the energy expenditure of chicks should be
measured.
Acknowledgments
This work was supported by the Institut Polaire Franc¸ais –
Paul-Emile Victor (Programme 137) and by the project
Zones Ateliers of the Programme Environnement Vie
et Socie
´te
´of the CNRS. We are grateful to C. Gilbert,
D. Gre
´millet, A. Lescroe
¨l, C. Salmon, S. Samtmann,
A. Schmidt and C. Villemin for constructive comments
and the anonymous referees for greatly improving the
manuscript. We thank C. Salmon for his help in preparing
software for analysis of the data sets.
References
Altmann, J. 1974. Observational study of behavior: sampling
methods. Behaviour,49, 227–267.
Amat, J. A., Carrascal, L. M. & Moreno, J. 1996. Nest defence by
chinstrap penguins Pygoscelis antarctica in relation to offspring
number and age. Journal of Avian Biology,27, 177–179.
Ancel, A., Visser, H., Handrich, Y., Masman, D. & Le Maho, Y.
1997. Energy saving in huddling penguins. Nature,385, 304–305.
Barrat, A. 1976. Quelques aspects de la biologie et de l’e
´cologie du
manchot royal (Aptenodytes patagonicus) des ı
ˆles Crozet. Commis-
sion Nationale Franc¸aise de Recherche Antarctique,40, 9–51.
Barre
´,H.1984. Metabolic and insulative changes in winter and
summer acclimatized king penguin chicks. Journal of Comparative
Physiology,154, 317–324.
Berger, R. J. & Philipps, N. H. 1993. Sleep and energy conservation.
Neural Information Processing Systems,8, 276–281.
Besnard, A. 2001. Evolution de l’e
´levage des poussins en cre
`che
chez les Laride
´s. Ph.D. thesis, Universite
´de Montpellier.
Bildstein, K. L. 1993. White Ibis: Wetland Wanderer. Washington:
Smithsonian Institute Press.
Boersma, P. D. & Davis, L. S. 1997. Feeding chases and food
allocation in Ade
´lie penguins, Pygoscelis adeliae.Animal Behaviour,
54, 1047–1052.
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
10
DTD 5
Brown, K. M. & Morris, R. D. 1995. Investigator disturbance, chick
movement and aggressive behavior in ring-billed gulls. Wilson
Bulletin,107, 140–152.
Brown, L. H. & Root, A. 1971. The breeding behaviour of the lesser
flamingo Phoeniconaias minor.Ibis,113, 147–172.
Buckley, P. A. & Buckley, F. G. 1976. Late-blooming terns. Natural
History,84, 46–56.
Burger, J. 1981. Aggressive behaviour of black skimmers (Rynchops
niger). Behaviour,76, 207–222.
Burger, J. & Gochfeld, M. 1990. The Black Skimmer: Social Dynamics
of a Colonial Species. New York: Columbia University Press.
Caraco, T. 1979. Time budgeting and group size: a test of theory.
Ecology,60, 618–627.
Caraco, T., Martindale, S. & Pulliam, H. R. 1980. Avian flocking in
the presence of a predator. Nature,285, 400–401.
Carter, H. R. & Hobson, K. A. 1988. Creching behavior of Brandt’s
cormorant chicks. Condor,90, 395–400.
Challet, E., Bost, C.-A., Handrich, Y., Gendner, J.-P. & Le Maho, Y.
1994. Behavioural time budget of breeding king penguins
(Aptenodytes patagonicus). Journal of Zoology,233, 669–681.
Cherel, Y., Stahl, J. C. & Le Maho, Y. 1987. Ecology and physiology
of fasting king penguin chicks. Auk,104, 254–262.
Co
ˆte
´,S.D.2000. Aggressiveness in king penguins in relation to
reproductive status and territory location. Animal Behaviour,59,
813–821.
Criscuolo, F., Gauthier-Clerc, M., Le Maho, Y., Zorn, T. &
Gabrielsen, G. W. 2001. Sleep changes during long-term fasting
of the incubating common eider Somateria mollissima.Ardea,89,
15–22.
Danchin, E. & Wagner, R. H. 1997. The evolution of coloniality: the
emergence of new perspectives. Trends in Evolution and Ecology,
12, 342–347.
Davis, L. S. 1982. Creching behaviour of Ade
´lie penguin chicks
(Pygoscelis adeliae). New Zealand Journal of Zoology,9,
279–286.
Dehn, M. M. 1990. Vigilance for predators: detection and dilution
effects. Behavioral Ecology and Sociobiology,26, 337–342.
Descamps, S., Gauthier-Clerc, M., Gendner, J.-P. & Le Maho, Y.
2002. The annual breeding cycle of unbanded king penguins
Aptenodytes patagonicus on Possession Island (Crozet). Avian
Science,2, 87–98.
Dewasmes, G., Buchet, C., Geloen, A. & Le Maho, Y. 1989. Sleep
changes in emperor penguins during fasting. American Journal of
Physiology,256, R476–R480.
Dimond, S. & Lazarus, J. 1974. The problem of vigilance in animal
life. Brain, Behavior and Evolution,9, 60–79.
Dinep, A. 1988. Social behavior, parental care, and creching:
a chronology of development in white ibis chicks. Colonial
Waterbird Society Newsletter,12, 42.
Elgar, M. A. 1989. Predator vigilance and group size in mammals
and birds: a critical review of the empirical evidence. Biology
Review,64, 13–33.
Elgar, M. A. & Catterall, C. 1981. Flocking and predator surveillance
in house sparrows: test of an hypothesis. Animal Behaviour,29,
868–872.
Evans, R. M. 1984. Some causal and functional correlates of
creching in young white pelicans. Canadian Journal of Zoology,
62, 814–819.
Gauthier-Clerc, M., Tamisier, A. & Ce
´zilly, F. 1998. Sleep-vigilance
trade-off in green-winged teals (Anas crecca crecca). Canadian
Journal of Zoology,76, 2214–2218.
Gauthier-Clerc, M., Jaulhac, B., Frenot, Y., Bachelard, C., Monteil,
H., Le Maho, Y. & Handrich, Y. 1999. Prevalence of Borrelia
burgdorferi (the Lyme disease agent) antibodies in king penguin
Aptenodytes patagonicus in Crozet Archipelago. Polar Biology,22,
141–143.
Gauthier-Clerc, M., Tamisier, A. & Ce
´zilly, F. 2000. Sleep-vigilance
trade-off in gadwall during winter period. Condor,102, 307–313.
Gorman, M. L. & Milne, H. 1972. Creche behaviour in the common
eider Somateria m. mollissima L. Ornis Scandinavica,3, 21–25.
Graf, R., Heller, H. C., Sakaguchi, S. & Krishna, S. 1987. Influence
of spinal and hypothalamic warming on metabolism and sleep in
pigeons. American Journal of Physiology,252, R661–R667.
Hamilton, W. J. 1971. Geometry for selfish herd. Journal of
Theoretical Biology,31, 295–311.
Ho
¨gstad, O. 1987. It is expensive to be dominant. Auk,104, 333–
336.
Ho
¨gstad, O. 1988. Social rank and antipredator behaviour of willow
tits Parus montanus in winter flocks. Ibis,130, 45–56.
Hunter, S. & Brooke, M. D. L. 1992. The diet of giant petrels,
Macronectes spp. at Marion Island, Southern Indian Ocean.
Colonial Waterbirds,15, 56–65.
Jennings, T. & Evans, S. M. 1980. Influence of position in the flock
and flock size on vigilance in the starling, Sturnus vulgaris.Animal
Behaviour,28, 634–635.
Kharitonov, S. P. & Siegel-Causey, D. 1988. Colony formation in
seabirds. Current Ornithology,5, 223–272.
Lamey, T. C. 1993. Territorial aggression, timing of egg loss, and
egg-size differences in rockhopper penguins, Eudyptes c. chrys-
ocome, on New Island, Falkland Islands. Oikos,66, 293–297.
Le Bohec, C., Gauthier-Clerc, M., Gendner, J.-P., Chatelain, N. &
Le Maho, Y. 2003. Nocturnal predation of king penguins by giant
petrels on Crozet Islands. Polar Biology,26, 587–590.
Le Maho, Y., Gendner, J.-P., Challet, E., Bost, C.-A., Gilles, J.,
Verdon, C., Plumere
´, C., Robin, J.-P. & Handrich, Y. 1993.
Undisturbed breeding penguins as indicators of changes in marine
resources. Marine Ecology Progress Series,95, 1–6.
Lendrem, D. W. 1984. Sleeping and vigilance in birds. II. An
experimental study of the Barbary dove (Streptopelia risoria).
Animal Behaviour,32, 243–248.
Leuthold, B. M. 1979. Social organization and behaviour of giraffe
in Tsavo East National Park. African Journal of Ecology,17, 19–34.
Levy, N. & Bernadsky, G. 1991. Cre
`che behavior of nubian ibex
Capra ibex nubiana in the Negev Desert Highlands, Israe¨l. Israe¨l
Journal of Zoology,37, 125–137.
McCracken, G. F. 1984. Communal nursing in Mexican free-tailed
bat maternity colonies. Science,223, 1090–1091.
Mangin, S., Gauthier-Clerc, M., Frenot, Y., Gendner, J.-P. & Le
Maho, Y. 2003. Ticks Ixodes uriae and the breeding performance
of a colonial seabird, king penguin Aptenodytes patagonicus.
Journal of Avian Biology,34, 30–34.
Martella, M. B., Renison, D. & Navarro, J. L. 1995. Vigilance in the
greater rhea: effects of vegetation height and group size. Journal of
Field Ornithology,66, 215–220.
Martin, P. & Bateson, P. 1993. Measuring Behaviour: An Introductory
Guide. Cambridge: Cambridge University Press.
Montgomerie, R. D. & Weatherhead, P. J. 1988. Risks and rewards
of nest defence by parent birds. Quarterly Review of Biology,63,
167–187.
Petit, D. R. & Bildstein, K. L. 1987. Effect of group size and location
within the group on the foraging behavior of white ibises. Condor,
89, 602–609.
Pettingill, O. S., Jr. 1960. Cre
`che behavior and individual
recognition in the colony of rockhopper penguins. Wilson Bulletin,
72, 213–221.
Pierotti, R. 1988. Intergenerational conflicts in species of birds with
precocial offspring. Proceedings of the International Ornithological
Congress,19, 1265–1274.
ARTICLE IN PRESS
LE BOHEC ET AL.: CRE
`CHING IN KING PENGUINS 11
DTD 5
Powell, G. V. N. 1974. Experimental analysis of the social value of
flocking by starlings (Sturnus vulgaris) in relation to predation and
foraging. Animal Behaviour,22, 501–505.
Pulliam, H. R. 1973. On the advantages of flocking. Journal of
Theoretical Biology,38, 419–422.
Pulliam, H. R., Anderson, K. A., Misztal, A. & Moore, N. 1974.
Temperature-dependent social behaviour in juncos. Ibis,116,
360–364.
Scherrer, B. 1984. Biostatistique. Que
´bec: Gae¨tan Morin Editeur.
Seddon, P. J. & van Heezik, Y. 1993. Chick cre
`ching and
intraspecific aggression in the jackass penguin. Journal of Field
Ornithology,64, 90–95.
Siegel, S. & Castellan, N. J., Jr. 1988. Nonparametric Statistics for the
Behavioral Sciences. New York: McGraw-Hill.
Siegel-Causey, D. & Hunt, G. L., Jr. 1981. Colonial defence behavior
in double-crested and pelagic cormorants. Auk,98, 522–531.
Siegel-Causey, D. & Kharitonov, S. P. 1991. The evolution of
coloniality. Current Ornithology,7, 285–330.
Slater, L. M. & Markowitz, H. 1983. Spring population trends in
Phoca vitulina richardi in two central California coastal areas.
California Fish and Game,69, 217–226.
Spurr, E. B. 1974. Individual differences in aggressiveness of Ade
´lie
penguins. Animal Behaviour,22, 611–616.
Stahel, C. D., Megirian, D. & Nicol, S. C. 1984. Sleep and
metabolic rate in the little penguin, Eudyptula minor.Journal of
Comparative Physiology,154, 487–494.
Taylor, R. H. 1962. The Ade
´lie penguin Pygoscelis adeliae at Cape
Royds. Ibis,104, 176–204.
Tamisier, A. & Dehorter, O. 1999. Camargue, Canards et Foulques.
Nı
ˆmes: Centre Ornithologique du Gard.
Thompson, K. V. 1998. Spatial integration in infant sable antelope,
Hippotragus niger.Animal Behaviour,56, 1005–1014.
Tourenq, C., Johnson, A. R. & Gallo, A. 1995. Adult aggressiveness
and cre
`ching behavior in the greater flamingo, Phoenicopterus
ruber roseus.Colonial Waterbirds,18, 216–221.
Trivers, R. L. 1972. Parental investment and sexual selection. In:
Sexual Selection and the Descent of Man 1871–1971 (Ed. by
B. Campbell), pp. 136–179. Chicago: Aldine.
Vinuela, J., Amat, J. A. & Ferrer, M. 1995. Nest defence of nesting
chinstrap penguins (Pygoscelis antarctica) against intruders.
Ethology,99, 323–331.
Whittow, G. C. 1976. Regulation of body temperature. In: Avian
Physiology (Ed. by P. D. Sturkie), pp. 146–173. Berlin: Springer-
Verlag.
Williams, G. C. 1966. Natural selection, costs of reproduction and
a refinement of Lack’s principle. American Naturalist,100, 687–
690.
Wilson, E. A. 1907. Aves. British National Antarctic Expedition
1901–1904. Natural History,2, 1–121.
Wittenberger, J. F. & Hunt, G. L., Jr. 1985. The adaptive
significance of coloniality in birds. In: Avian Biology (Ed. by D. S.
Farner, J. R. King & K. C. Parkes), pp. 1–78. New York: Academic
Press.
Yeates, G. W. 1975. Microclimate, climate and breeding success in
Antarctic penguins. In: The Biology of Penguins (Ed. by B.
Stonehouse), pp. 397–409. London: University Park Press.
ARTICLE IN PRESS
ANIMAL BEHAVIOUR, --,-
12
DTD 5
