ANIMAL BEHAVIOUR, 2006, 71, 457–462
doi:10.1016/j.anbehav.2005.07.007
Alloparental feeding in the king penguin
NICOLAS LECOMTE *†‡, G REGOI RE K UN TZ *, N IC OLAS LAM BERT †, JEAN- PAUL GENDNER†,
YV E S H A NDR I CH †, Y VON LE M AH O† & CHARLES-ANDRÉ BOST §
*Université du Québec à Rimouski, Rimouski, Québec, Canada
yCentre d’Écologie et de Physiologie Énergétiques, Centre National de la Recherche Scientifique, Strasbourg, France
zDépartement de Biologie and Centre d’Études Nordiques, Université Laval, Québec, Canada
xCentre d’Études Biologiques de Chizé, Centre National de la Recherche Scientifique, Beauvoir/Niort, France
(Received 25 May 2004; initial acceptance 7 July 2004;
final acceptance 28 June 2005; published online 17 January 2006; MS. number: A9898R)
We investigated allofeeding (feeding of offspring by adults other than their own parents) in the king penguin, Aptenodytes patagonicus, a long-lived pelagic bird that faces severe food shortages during its reproduction and in
which parents leave their fasting chick in dense crèches. A 1-year monitoring of 103 breeding pairs and 70 chicks
was carried out in a colony in the Crozet Archipelago. We examined whether allofeeding was common enough to
alter survival costs or benefits for both the allofed chicks and the allofeeders. Twenty-two per cent of marked
adults allofed more than 65% of all the chicks without repeatedly feeding the same chick. Allofeeding in king penguins benefited allofed chicks by increasing their survival, yet little or no fitness cost was detected among allofeeders. We identified proximal factors affecting allofeeding: (1) the breeding conditions of the population
were not unusual; (2) allofeeding occurred mostly when parental provisioning was low; (3) alloparents did not
respond to increased begging by regurgitating more meals; (4) allofeeders were mostly failed breeders, although
successful breeders occasionally allofed; (5) when the colony was no longer organized into breeder territories, allofeeders preferentially fed chicks that had been reared by close neighbours at the time of brooding.
Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Alloparental feeding occurs when one or several individuals provide temporary feeding to alien young. Allofeeding can also include full adoption of young when a ’foster
parent(s)’ provides exclusive care of another’s offspring in
the absence of one or both original parents (Riedman
1982). Allofeeding raises intriguing evolutionary questions, because it can be viewed as an altruistic and reproductively costly behaviour (Wilson 1975). Allofed
offspring survival is promoted at the expense of the allofeeders, but the energetic or fitness costs are not experienced by the allofed offspring (Brown 1987). In this
case, an ‘intergenerational conflict’ might appear, where
offspring are selected to gain from alloparental feeding,
but alloparents are selected not to provide such allofeeding (Pierotti & Murphy 1987).
Most of the 150 bird species that allofeed are seabird
species that show several specific life-history traits and
environmental constraints that promote allofeeding
(Riedman 1982; Brown 1987; Heinsohn et al. 1990;
Correspondence: N. Lecomte, Département de Biologie, Université
Laval, Ste Foy G1K7P4, Québec, Canada (email: nicolas.lecomte@
bio.ulaval.ca).
0003–3472/05/$30.00/0
Arnold & Owen 1999). For example, seabird chicks are
semiprecocial or altricial at hatching. They require prolonged periods of biparental care because of slow growth
rates, and they endure long periods of parental absenteeism because of distant and unpredictable food resources.
King penguins, Aptenodytes patagonicus, show all those
life-history traits that may be favourable to alloparental
feeding. As pelagic predators (Bost et al. 1997; Charrassin
& Bost 2001), they leave their colony for long periods, and
return periodically with food for the chick. Their breeding
cycle takes over 14 months (Stonehouse 1960; Barrat
1976; Weimerskirch et al. 1992; Olsson 1996). The large
size of the species (Stonehouse 1960), combined with
a short window of food abundance during the austral
summer (El Sayed 1988), make completing chick rearing
impossible before the onset of winter, but only until the
next summer. Breeders do not build a nest, but brood their
egg and single chick on their feet for 53 days during the
austral summer (Barrat 1976). Before the onset of winter,
breeding territories no longer exist and chicks aggregate
in dense groups called crèches (Stonehouse 1960; Davis
1982; Evans 1984; Tourenq et al. 1995). During the winter,
feeding of their single chicks by parents is reduced and
may not even occur from the beginning of autumn until
457
Ó 2005 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
458
ANIMAL BEHAVIOUR, 71, 2
the next spring (Stonehouse 1960; Barrat 1976; Cherel &
Le Maho 1985; Cherel et al. 1987; Jouventin & Lagarde
1995). In king penguins, chick prewinter mass, crèching
behaviour and the age of the chick are the key variables
that explain winter survival (Stonehouse 1960; Barrat
1976).
We studied alloparental feeding in a king penguin
colony by observing feeding exchanges between adults
and chicks during one breeding cycle. We assessed
whether allofeeding was common enough to alter survival costs or benefits for both the allofed chicks and the
allofeeders. We verified whether the same alloparent fed
repeatedly the same chick. We then explored in king
penguins five hypotheses of behavioural mechanisms
commonly associated with allofeeding in colonial seabirds species: (1) occasional and unusual breeding conditions (such as changes in the breeding habitat or
breeding success of a colony: Roberts & Hatch 1994),
(2) young solicitation towards alloparents (Birkhead &
Nettleship 1984; Mock 1984; Pierotti & Murphy 1987;
Hebert 1988; Morris et al. 1991; Brown 1998), (3) suboptimal parental care (Pierotti & Murphy 1987; Hebert
1988; Morris et al. 1991), (4) breeding failure (Riedman
1982; Birkhead & Nettleship 1984; Jouventin et al.
1995) and (5) spatial proximity of breeding adults in colonies (Roulin 2002).
METHODS
This study was undertaken at Possession Island (Crozet
Archipelago, 46 250 S, 51 450 E), which has a subantarctic
climate (mean annual temperature and precipitation: 5 C,
2800 mm). Winter conditions prevail from April to November, when marine resources are at their minimum
(Hart 1942; Foxton 1956).
We carried out an all-occurrence sampling of feeding
events on one subcolony (N ¼ 200 breeding pairs) in a central part of the ‘La Grande Manchotière’ colony
(N ¼ 30 000 breeding pairs), from the beginning of incubation (December 1998) to the departure of the juveniles
(February 2000). We also recorded the rate of crèching
chick calls (average number of calls per minute) each
time they encountered an adult (parent or alloparent) during the winter. Clear topographic features (slope and
rocks) defined the limits of our subcolony and prevented
mixing with the populations of other subcolonies.
We marked 74 breeding adults with no identified
partner and 103 breeding pairs with a unique dye-mark
code of Nyanzol-D (dark colouring) on their white underbellies. We also implanted a miniaturized transponder
(TIRIS, Texas Instruments, Dallas, Texas, U.S.A.; Gendner
et al. 1992; Le Maho et al. 1993; E. F. Prentice & D. L.
Park, unpublished data, available at NWFSC, 2725 Montlake Blvd., Seattle, WA 98112-2097, U.S.A.) subcutaneously
in the tail fold of each animal. We defined ‘young
chicks’ as those with a parent, ‘crèching chicks’ as those
with brown down in close association with other crèching
chicks, and ‘juveniles’ as those with growing subadult
feathers and no longer in the crèches. Breeding failure
(offspring abandonment or mortality) may occur at the
egg stage, early chick age or crèching stage. Successful
breeding was established by the departure of the juveniles
to the sea. Chick mortality was determined either by seeing giant petrels (Macronectes sp.) kill starving chicks or
by finding carcasses at a distance from the colony. Early
marking of the young chicks was essential to associate
a single chick with its biological parents. Among the 103
breeding pairs, 95 chicks were marked under the skin
with a transponder and externally with an individual tag
on their back (made by Floy Tag Inc., Seattle, Washington,
U.S.A.) when they were 5–10 days old. During handling,
each chick was replaced by a dummy egg to avoid parent
abandonment. At the beginning of the crèching period
(April), we banded and weighed the remaining 70 marked
chicks. We removed bands from all marked juveniles just
before their departure to the sea (from the end of the following December to the beginning of February). Daily observations were carried out with a spotting scope (20 60)
and binoculars (10 50) in three blinds situated more
than 7 m from the subcolony. Three pairs of antennae at
the subcolony entrance detected all departures and arrivals of the transponded individuals (Descamps et al.
2002). A video system provided additional data (infrared
video camera connected to a videotape recorder), especially
at night.
Between foraging trips, adults regurgitated their stomach contents to one or more chicks in the colony while
partly joining bills with them. Feeding transfers were
considered to be alloparental when an adult provided
food to a nonoffspring chick. To estimate the amount of
food delivered to the chick, we established a semiquantitative scale of three meal sizes that were distinguishable at
a distance: F (large meal), f (small meal), L (liquid similar
to a thick mucus). To avoid disturbance in the subcolony
under study, F and f masses were calibrated in another
subcolony by weighing 30 chicks before and after feeding.
These observations suggested the following mean SE
mass for each meal size: F: 80 2.5 g (N ¼ 51); f:
80 1.8 g (N ¼ 59); L: 25 1.2 g (N ¼ 43).
We calculated the proximity of neighbouring breeders
to each other using daily photographs of the subcolony
and monitoring with the Animal Movement 2.04b extension (Hooge & Eichenlaub 1997) for ArcView 3.2c (ESRI
2000). We established a proximity index, where 1 corresponds to the nearest neighbour of a breeding pair and
15 means a neighbour 15 breeders away from the pair
(maximum value obtained from the limited size of the
subcolony under study).
All statistical analyses were performed using SAS software (SAS Institute 1998). For all data, normality was
checked with the Kolgomorov–Smirnov test (Lilliefors option). When necessary, independent variables were logtransformed to improve normality and homoscedasticity.
The alpha level of all tests was 0.05. For multiple analyses
on similar hypotheses, we used the Bonferroni correction.
We used a multiple logistic regression model (Trexler &
Travis 1993; Legendre & Legendre 2000) to test the null
hypothesis that chick survival (binary variable) during
winter did not differ by chick age (days), chick prewinter
mass (g), number of winter parental and alloparental
food events for each food meal class received by each
LECOMTE ET AL.: KING PENGUIN ALLOFEEDING
chick (F, f and L) and all possible interactions. All independent variables were standardized, and multicollinearity between each of those variables was nonsignificant. We used
a multimodel inference procedure derived from the AIC
procedure to select our model (Akaike 1973; Hurvich &
Tsai 1991; Burnham & Anderson 1998; a ¼ 0.05; PROC
LOGISTIC). If the 95% confidence intervals of the weighted average (b) for the estimates of one independent variable among all the selected models did not include 0,
then this variable was considered to have an effect on
the dependent variable.
Ethical Note
Our study was undertaken under the approval of the
Ethical Committee of the French Polar Institute (IPEV)
and of the Scientific Committee of IPEV, following the
SCAR (Scientific Committee for Antarctic Research) code
of conduct. The species under study is listed in Appendix
III to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). The
minimum number of birds needed for our study was
a function of survival rate of the chicks, which was
previously estimated by two pilot studies (N. Lambert &
C. A. Bost, unpublished data).
RESULTS
In our subcolony, 25% of the adults (Table 1) performed
alloparental feedings. The mean SE number of allofeeding events per alloparent was 22.1 9.5 during winter
(N ¼ 583). At least 91.43% of chicks were fed by their parents (64 of 70), although 65.71% of all the chicks (46 of
70) were also allofed. Each alloparent that failed to breed
returned to the subcolony, on average, four times (1,
N ¼ 46) and allofed different chicks each time.
Only 23 chicks survived to the onset of the fledgling
period from the 70 chicks that were banded at the
beginning of winter. A one-tailed t test indicated that
chicks that survived were heavier at the beginning of winter (X SE ¼ 7:41 1:13 kg, N ¼ 24) than were nonsurvivors (6.70 1.28 kg, N ¼ 44; PROC TTEST: t64 ¼ 2.35,
P ¼ 0.02). Chicks that survived were also allofed more
than were nonsurvivors (X SE number of allofeeding
events: survivors: 10.12 1.1, N ¼ 23; nonsurvivors:
Table 1. Percentage of marked alloparental feeders classified by
breeding status in the king penguin subcolony under study (sample
sizes in parentheses)
Breeding status
Successful breeders
Breeders failed at egg stage
Breeders failed at early
chick stage
Breeders failed at crèching
Total
Percentage of Percentage of all
alloparental adult feeders of
feeders
the subcolony
18.64 (13)
48.31 (34)
17.80 (12)
52.47 (147)
25.21 (70)
11.32 (32)
15.25 (11)
(70)
11.00 (31)
(280)
4.28 0.8, N ¼ 47; PROC TTEST: t68 ¼ 2.78, P ¼ 0.01;
significant after Bonferroni correction at 0.05/2 ¼ 0.025).
The multimodel inference procedure showed that chick
age, chick prewinter mass, parental L and alloparental L
had no effect on chick survival (95% CI of their b included
0). However, we found a positive effect on chick survival
of parental f (b ¼ 87.41; 95% CI: 85.27–89.03), parental F
(b ¼ 83.72; 95% CI: 83.11–86.02), alloparental f (b ¼ 3.89;
95% CI: 3.15–4.37), and alloparental F (b ¼ 3.27; 95% CI:
2.92–3.72). Seven crèching chicks that lost meals because
one or both of the parents allocated food to foreign young
survived until the fledgling period. This was also the case
for seven crèching chicks that never received alloparental
meals. In both cases, all chicks returned to their natal colony after 2 years.
All observed allofeeders returned to the colony the year
after and 2 years after allofeeding (their transponders were
detected by the TIRIS antenna). We found no significant
correlations between the number or the rate of crèching
chicks calls and the number of alloparental meal classes
given to the chick immediately after the calls (PROC CORR:
number of calls: r ¼ 0.07, N ¼ 125, P ¼ 0.89, R2 ¼ 0.005;
rate of calls: r ¼ 0.04, N ¼ 125, P ¼ 0.61, R2 ¼ 0.001) and
one foraging trip after the calls (PROC CORR: number of
calls: r ¼ 0.01, N ¼ 17, P ¼ 0.81, R2 ¼ 0.0001; rate of calls:
r ¼ 0.08, N ¼ 17, P ¼ 0.24, R2 ¼ 0.009).
In our subcolony, the number and the types of alloparental meals varied from April to November (Fig. 1b). However, 81.98% of allofeeding events (478 of 583) occurred
between May and September (Fig. 1b). This coincided
with a decrease in parental feeding (Fig. 1a).
Mean SE breeding success in the subcolony was
24.21 4.5% (N ¼ 95), which was not significantly different from the mean breeding success previously observed in
king penguin colonies on Possession Island (Weimerskirch
et al. 1992; X SE ¼ 30:6 4:2%; c21 ¼ 0.05, P ¼ 0.82).
Only adults performed allofeeding. An average SE of
81.4 2.43% (N ¼ 57) of allofeeders were failed breeders
(Table 1). Parents that had lost their chick during winter
did more allofeeding after the death of their chick than before (PROC UNIVARIATE for paired t tests: t12 ¼ 3.21,
P ¼ 0.03; X SE number of allofeeding events: before
death: 9.10 1.00; after death: 12.90 2.10). We observed
four events of allofeeding (0.68% of the total number of
allofeeding events, N ¼ 583) by two adults that had just
completed their moult, and thus were no longer raising
a chick.
The index of proximity between the breeding territory
of allofed chicks and of adults that became their allofeeders was negatively correlated with the number of
allofeeding meals received by those chicks during crèching
(PROC CORR: rS ¼ 0.90, N ¼ 17, P ¼ 0.001). About 90%
of alloparents for each chick were present within six
breeding places, even though breeding territories and
crèches were in different locations.
DISCUSSION
Our study provides information on a poorly documented
stage of the king penguin’s life cycle and is the first
459
ANIMAL BEHAVIOUR, 71, 2
(a) Parental feeding events
Percentage of feeding events
12
256 251
188
8
155
6
4
281
L
F
f
246
10
14
98
88
88
70
2
70
33
0
Percentage of
feeding events
(b) Allofeeding events
14
12
10
8
6
4
2
0
Number of dead
chicks
460
14
12
10
8
6
4
2
0
133
106
119
66
39
54
46
20
(c) Crèching chick mortality
Jan Feb Mar Apr May Jun
Jul Aug Sep Oct Nov Dec Jan
Months
Figure 1. Relative importance of allofeeding events during the king penguin breeding cycle with regard to parental rearing, level of marine
resources and crèching chick mortality in the king penguin subcolony under study. (a) Relative importance (%) of each meal class
(N ¼ 1968; sample sizes over bars) given by parents. Feeding classes are: f (feeding 80 g); F (feeding > 80 g); L (liquid feeding). (b) Relative
importance (%) of meal class (N ¼ 583; sample sizes over bars) given by alloparents. We adjusted the scale of the ordinate axis in (b) to be
proportional to (a) by considering that winter allofeeding (F, f and L) represented 26.9% of the total amount of winter chick feeding. (c) Chick
mortality (N ¼ 41) during the crèching period.
extensive investigation of alloparental feeding in this
species. We found that allofeeding among king penguins
is common during the breeding cycle and that many
allofeeders, especially failed breeders, may donate meals
repeatedly, thereby enhancing allofed chick survival.
Allofeeding in the king penguin does not correspond to
adoption of the allofed chick, because allofeeders do not
feed the same chick several times. Allofeeding might be
considered a cost for the offspring that lost parental meals;
however, all the chicks in this situation survived for at
least 2 years after crèching. The alloparental cost of
feeding foreign chicks (several grams) is minimal relative
to the nutritional costs for an adult king penguin (several
kilograms; Green & Gales 1990). Therefore, allofeeders
might contribute to foreign chick survival without deleterious effects to themselves. All observed allofeeders returned to the colony the following year and after 2
years. Moreover, to our knowledge there is no published
evidence of reduced survival or reduced future fecundity
of alloparents (Emlen et al. 1991). Alloparental and parental meal classes, except the liquid food class, enhanced
winter survival of chicks, yet any direct benefits to alloparents are difficult to demonstrate, especially for failed
breeders.
What mechanistic factors might influence alloparental
feeding in the king penguin? Roberts & Hatch (1994) argued that unusual breeding conditions might influence allofeeding behaviour. Breeders in our king penguin
subcolony, however, did not face abnormal breeding conditions; breeding success was close to the mean breeding
success of the colony. In addition, two pilot studies confirmed the occurrence of allofeeding behaviour elsewhere
in the colony (N. Lambert & C. A. Bost, unpublished data)
and Stonehouse (1960) briefly described potential alloparental brooding in king penguin colonies on South Georgia
Island (54 170 S, 36 300 W). Other observations of alloparental behaviour were also made in other king penguin colonies in the Crozet Islands and also in the Kerguelen
LECOMTE ET AL.: KING PENGUIN ALLOFEEDING
Archipelago (49 200 S, 70 200 E; Dobson & Jouventin 2003;
N. Lecomte & C. A. Bost, unpublished data).
In our study, the number and the rate of chick calls did
not appear to influence the amount of allofeeding a chick
received. Adults did not respond to increased begging by
regurgitating more meals to the chick. It is well established
that competitive siblings signal hunger to their parents by
using begging behaviour (e.g. Leonard & Horn 2001).
However, there are only two studies, with contrasting results, on begging behaviour in the absence of sibling competition, as in the case of the king penguin chicks.
Granadeiro et al. (2000) concluded that begging rate had
no effect on the provisioning rate in Cory’s shearwater,
Calonectis diomedea. Quillfeldt (2002) found a positive relation between the number of begging events and provisioning rates in Wilson’s storm petrels, Oceanites
oceanicus. Quillfeldt argued that the use of begging rates
by Granadeiro et al. (2000) instead of the total number
of begging calls by the chicks led to a difference between
the two studies. However, in our study, these two parameters were used and we found no link between chick solicitation and alloparental response.
In many seabird species, a period of low parental rate of
provisioning might be a factor allowing the expression of
alloparental care (Pierotti & Murphy 1987). In our study,
allofeeding occurred mostly during winter when parental
absenteeism is high and food provisioning is low. During
that period, crèching chicks and allofeeders are accessible
to each other. However, before that, when the chicks were
kept on the feet of their parents, no alloparent could gain
access to neighbouring chicks because of the protection
and the territorial behaviour of their parents.
We confirmed that allofeeders were mostly failed
breeders, which is consistent with Stonehouse’s (1960)
earlier observations, although successful breeders were
occasionally involved in allofeeding events. However,
having a living chick to care for seemed to reduce the
likelihood of allofeeding. Adults performed more allofeeding events after the death of their crèching chick
than they did before their breeding failure. The pronounced occurrence of allofeeding at the beginning of
winter might be explained by the high number of
allofeeders that had just failed reproduction. Four adults
that had started a new breeding cycle were also seen
allofeeding. This observation suggests that the breeding
status of allofeeders in king penguins is more variable
than expected according to studies involving other
species (Riedman 1982).
Finally, allofeeding in the king penguin seemed to be
affected by the spatial proximity of breeding adults in
colonies. Allofeeders preferentially fed crèching chicks
that were reared by close neighbours at the time of
brooding. Hence, the closer that a breeding neighbour
was, the greater the chance that a chick would be allofed
by this adult at the crèching stage. It is remarkable that the
colony was no longer divided into breeding territories at
the time of crèching. This observation suggests that
allofeeders may recognize the chicks that they feed by
a mechanism that has not been described. Further studies
of chick recognition by adults during brooding are needed
to explore this hypothesis.
Acknowledgments
This study was a part of a long-term research project on
penguin ecophysiology (ECOPHY Program). The Institut
Polaire Français Paul-Émile Victor (IPEV) and the Terres
Australes et Antarctiques Françaises (TAAF) provided
financial and logistical support. We thank Yohann Mainguy,
Guillaume Froget, Cyprien Bourrihlon, Pierre-Emmanuel
Chaillon, Colin Gilly and Gilles Rudelles as well as all the
members of the 36th Mission at Crozet Islands for
contributing to the data collection and monitoring. We
are truly indebted to Alain Caron for help during data
analysis and to Jean-Pierre Ouellet, Stéphanie Boucher,
Corentin Chaillon and Michel Gauthier-Clerc for their
support and advice. We thank F. Stephen Dobson, Geoffrey Hill, France Dufresnes, Bruno Vincent, Jean Ferron,
Bernard Thierry, Vanessa Viera, François Fournier, Steeve
Côté, Gilles Gauthier and one anonymous referee for
comments on an early draft of this article. We thank Anna
M. Calvert, Derek Mueller and K. Burner for proofreading.
Finally, we are grateful for funding provided by Université
du Québec à Rimouski (UQAR; Alain Potvin Grant).
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