Commentary
he Auk 126(3):688–693, 2009
he American Ornithologists’ Union, 2009.
Printed in USA.
CAUSES AND BENEFITS OF CHICK AGGREGATIONS IN PENGUINS
DAVID WILSON1
Department of the Environment, Water, Heritage and the Arts, Australian Antarctic Division, 203 Channel Highway,
Kingston, 7050, Tasmania, Australia
Aggregations of penguin chicks have been noted since the
irst scientiic expeditions to penguin breeding colonies in the
Antarctic and sub-Antarctic areas. Various authors have examined these aggregations in individual species and from limited
perspectives. Chick aggregations are the result of a two-stage
process; initially, chicks are abandoned by their parents, at which
time they may choose to aggregate with other chicks. Here, I
examine the causes and beneits of aggregations in all penguin
species that display this phenomenon to identify any unifying evolutionary reasons for their formation. First, I consider the functional requirements of both parents and chicks before successful
chick abandonment can occur and look at the motivations that
may drive a parent or chick to leave the nest. hen I examine the
evidence supporting the theories as to why a chick should join an
aggregation. Finally, in light of this review, I discuss the appropriateness of applying the term “crèching” to penguin chick aggregations and ofer some possible avenues of future research.
Chick aggregations have been reported in a variety of taxa,
including the Anatidae (Eadie et al. 1988), Pelecaniformes (Johnsgard 1993, Velando 2001), Laridae (del Hoyo et al. 1996, Besnard
et al. 2002), and Spheniscidae (present study). Ducks exhibit true
crèching behavior—that is, young from diferent broods or families combine into a single group and subsequently receive care
from parents other than their own (Eadie et al. 1988), which is
signiicantly diferent from aggregations that occur in other species. In gulls, the evolution of chick aggregations has been linked
to habitat instability leading to high levels of terrestrial predation, whereas low levels of aggression against predators may promote chick aggregation (Besnard et al. 2002). Chick aggregations
are poorly understood in the Pelecaniformes; there is no evidence
that aggregations reduce predation risk (Johnsgard 1993, Velando
2001) or reduce adult aggression (Velando 2001), but they may
have thermoregulatory beneits (Carter and Hobson 1988).
Early reports applied the term “crèche” to groups of penguin chicks, assuming that the few adults present were caring for
the aggregated chicks (e.g., Wilson 1907, Levick 1914). Although
1
this idea has subsequently been shown to be inaccurate (Williams 1995, and references therein), the term has persisted. Young
(1994) highlighted that the term has been applied historically to
two separate processes: a chick can crèche when its parent abandons it, and it can be part of a crèche when it is with other chicks.
Here, I use the term “aggregation” to describe a group of chicks
and “post-guard” to deine the life-history stage once a chick has
been abandoned.
Chick aggregations have been reported in 12 species of penguin: Emperor, King, Adélie, Chinstrap, Gentoo, African, Rockhopper, Macaroni, Fiordland, Erect Crested, Royal, and Snares
penguins (scientiic names are given in Table 1; Müller-Schwarze
1984, Seddon and van Heezik 1993a, Williams 1995). In 11 of these
species, parents abandon their chicks, whereas in Rockhopper
Penguins, chicks leave their parents and form aggregations (Pettingill 1960). he most recent penguin phylogeny (Baker et al.
2006) suggests that aggregation is the ancestral trait in the penguin family, being retained in the two most basal lineages (Aptenodytes and Pygoscelis) and in Eudyptes. Chick aggregation seems
to have been lost in the genera Spheniscus, Eudyptula, and Megadyptula but has recently re-evolved in African Penguin, apparently in response to human disturbance (Cooper 1977).
Because penguins evolved in Antarctica (Baker et al. 2006), it
is likely that chick aggregations initially arose as a way of reducing
heat loss during extreme cold. For example, Emperor Penguins,
which endure extreme conditions, are able to breed only because
of the beneits gained by densely aggregating (Ancel et al. 1997).
Penguins eventually expanded northward, to latitudes where reducing heat loss became less important (Table 1), and chick aggregations then evolved secondary functions such as avoidance
of predators and of adult aggression. Once chicks are freed from
thermoregulatory constraints, predator avoidance appears to be
the main driver of aggregation. Penguin species in which chicks
do not aggregate primarily nest in burrows or, if on the surface,
in locations that protect them from aerial predators (Table 1; Seddon and Davis 1989, Stokes and Boersma 1998). he importance of
E-mail: david.wilson@aad.gov.au
he Auk, Vol. 126, Number 3, pages 688−693. ISSN 0004-8038, electronic ISSN 1938-4254. 2009 by he American Ornithologists’ Union. All rights reserved. Please direct
all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.
com/reprintInfo.asp. DOI: 10.1525/auk.2009.9709b
— 688 —
J ULY 2009
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689
TABLE 1. Latitudinal ranges and preferred nesting locations of penguin species (from Williams 1995) and the benefits of aggregating for chicks of those
species (see text for discussion).
Species
Breeding
latitudes
Preferred nest
location
Fiordland Penguin (Eudyptes pachyrhynchus)
Snares Penguin (E. robustus)
Rockhopper Penguin (E. chrysocome)
Macaroni Penguin (E. chrysolophus)
Royal Penguin (E. schlegeli)
Erect Crested Penguin (E. sclateri)
Yellow-eyed Penguin (Megadyptes antipodes)
African Penguin (Spheniscus demersus)
43–47°S
48°S
37–53°S
46–65°S
54°S
47–49°S
45–52°S
24–33°S
Surface
Surface
Surface
Surface
Surface
Surface
Surface
Burrow–surface
Magellanic Penguin (S. magellanicus)
Galapagos Penguin (S. mendiculus)
Humboldt Penguin (S. humboldti)
Little Penguin (Eudyptula minor)
Chinstrap Penguin (Pygoscelis antarcticus)
29–55°S
1°S
5–42°S
32–47°S
54–64°S
Burrow–surface
Burrow–surface
Burrow
Burrow
Surface
Gentoo Penguin (P. papua)
Adélie Penguin (P. adeliae)
46–65°S
54–77°S
Surface
Surface
Emperor Penguin (Aptenodytes forsteri)
66–78°S
Surface
King Penguin (A. patagonicus)
45–55°S
Surface
predation is highlighted by re-evolution of chick aggregations in
the African Penguin. his species is traditionally a burrow-nester,
but guano mining has removed appropriate substrate for burrows
and has forced some birds to nest on the surface (Frost et al. 1976).
here is signiicantly less predation on chicks in burrows than on
those in a nest on the surface (Frost et al. 1976), and predation is
believed to have increased the prevalence of chick aggregations in
this species (Cooper 1977).
PARENTAL CONSIDERATIONS THAT LEAD
TO CHICK A BANDONMENT
Parental condition.—Penguins with a constrained breeding season face two potentially conlicting interests: the need to successfully raise the current breeding season’s chicks to ledging, and the
need to maintain enough energy reserves to survive to the next
breeding season. In this sense, adults make a tradeof between
the short-term beneits of producing chicks in a speciic year and
their potential lifetime reproductive efort (Maynard Smith 1977).
here is a large body of evidence that this is a critical decision for
parents. During the incubation and guard periods, parents rely
on stored energy reserves and may lose considerable body weight
(e.g., Tremblay and Cherel 2003, Clarke et al. 2006, Green et al.
2007). hese reserves need to be regained before the pre-winter
molting period, when birds cannot feed (Adams and Brown 1990).
It has been suggested that parents have a physiological “trigger”
that alerts them when their own reserves are dangerously low (e.g.,
Olsson 1997) and that this may lead to chick abandonment.
his suggests two predictable outcomes: that adults in
poorer condition will abandon their chicks earlier than adults in
Role of chick aggregations
Poorly understood
Poorly understood
Poorly understood
Poorly understood
Poorly understood
Poorly understood
Not known to aggregate
Reduces adult aggression (Seddon and van Heezik 1993a) and
predation for small chicks (Seddon and van Heezik 1991)
Not known to aggregate
Not known to aggregate
Not known to aggregate
Not known to aggregate
Reduces adult aggression (Penteriani et al. 2003) but not
important for thermoregulation (Martín et al. 2006)
Poorly understood
Reduces thermoregulatory requirements, predation, and adult
aggression (Penney 1968, Davis 1982, Lawless et al. 2001)
Presumably to reduce thermoregulatory requirements
(Ancel et al. 1997)
Reduces thermoregulatory requirements, adult aggression,
and predation (Barré 1984, le Bohec et al. 2005)
better condition (Penteriani et al. 2003), whereas parents with
two chicks will abandon them earlier than parents with only one
chick. In both cases, parents should “recognize” that they require
more time to regain energy reserves and feed chicks than birds
that are in better condition or have only one chick. For instance,
Chinstrap Penguin pairs with lower energy reserves breed later
and abandon chicks at an earlier age (Viñuela et al. 1996). Presumably, this allows them to forage longer before the winter. In years
with decreased food availability, Adélie Penguin chicks are abandoned earlier than average, as adults reach their threshold body
condition earlier than in years with high food abundance (Ainley
2002). In both Adélie and Chinstrap penguins, two-chick broods
are abandoned earlier than one-chick broods (Davis 1982, Lishman 1985). he timing of abandonment may also depend on the
age or breeding experience of the individual, in that more experienced individuals may be better foragers; however, Moreno et al.
(1997) found that age at abandonment was not related to diferences in parental quality.
he timing of parental abandonment of chicks should be related to the energetic requirements of the ofspring in addition to
their own requirements. In Southern Rockhopper Penguins (E.
c. chrysocome), Eastern Rockhopper Penguins (E. c. ilholi), and
Adélie Penguins, parents forage for the same length of time and
bring the same weight of food to chicks at both the guard and
post-guard stages (Chappell et al. 1993, Hull et al. 2004, Rey et
al. 2007), despite the much higher energy requirements of older
chicks. here may be physiological limits to chick-provisioning
rates, controlled by the stomach size of the parents. Modeling of
the energetic requirements of Adélie Penguin chicks has shown
that they could not survive to ledging on the food brought back by
690
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one parent alone (Salihoglu et al. 2001). hus, parents must abandon their chicks to ensure that the chicks’ food requirements are
met, even though individual parents may not increase their fooddelivery rates. In Macaroni Penguins (in which only the female
forages during the guard stage), a chick’s peak food requirement
is ~400 g day−1. However, adult females can bring in only ~290 g
day−1 (Green et al. 2007). hus, in this species, both parents must
forage simultaneously to satisfy the food requirements of chicks
during peak demand.
Constraints on chick-abandonment age.—Although a parent
can abandon a breeding attempt at any stage, for chicks to survive
the initial abandonment, two requirements must be met. First, the
parent–chick bond must be suiciently developed for both to recognize each other among hundreds or potentially thousands of individuals. Second, the chick must be able to regulate its own body
temperature, because it may not aggregate with other chicks. In
African Penguins, parent–chick bonds were absent in chicks <16
days old but fully developed by 21 days (Seddon and van Heezik
1993b). Similarly, in Adélie Penguins, the parent–ofspring bond
was complete by day 17 (hompson and Emlen 1968). Interestingly, Davis and McCafrey (1989) presented evidence that Adélie
Penguin chicks can recognize their parents as early as day 12, almost a week earlier than adults can identify their chicks.
Newly hatched chicks rely on a brooding parent for warmth
because they are unable to produce suicient heat to maintain
their body temperature (Taylor 1985). As chicks age, their capacity to produce heat increases, and then their ability to retain it
through better insulation increases until they become thermally
independent (Duchamp et al. 2002) and are able to be successfully abandoned by their parents. In Gentoo and Chinstrap penguins, chicks reach thermal independence after 15 days (Taylor
1985), whereas in King Penguins, a similar state is reached in two
to three weeks (Duchamp et al. 2002). In the pygoscelid penguins,
the earliest age of abandonment and subsequent aggregation is 16
days for Adélie, 20 days for Gentoo, and 23 days for Chinstrap penguins (Ainley 2002). hus, 15–16 days after hatching appears to be
a critical period: chicks abandoned before then have little chance
of survival, but those abandoned when >16 days old are likely to
survive, especially if they can aggregate with other chicks.
CHICKS’ D ECISIONS O NCE A BANDONED
Once abandoned by its parents, a chick can remain by itself or aggregate with other chicks. his decision must be made in light of
any potential beneits gained by aggregating and may be mediated
by a chick’s age or health status at abandonment (e.g., Martín et
al. 2006). Traditionally, four reasons have been profered to explain chick aggregation behavior in penguins, some of which may
act in unison. Various authors have suggested that aggregations
provide increased protection from predation (Pettingill 1960, Davis 1982) or from aggression by unrelated adults (Seddon and van
Heezik 1993a, Penteriani et al. 2003), reduce the energy requirements of individual chicks for thermoregulation (Le Maho 1977,
Davis 1982), or have some social function (Sladen 1958). Each of
these potential beneits is examined in light of our current knowledge of penguin ecology.
Reduced risk of predation.—One of the functions of gregarious behavior is to reduce predation risk to the individual, for
AUK , VOL . 126
two reasons. First, a group is likely to detect a potential predator
sooner and, second, each individual in the group has a smaller
chance of being the one attacked (Hamilton 1971, Pulliam 1973).
Chicks in larger aggregations should be exposed to less successful predation. For most penguin species, skuas (Catharactes spp.), gulls (Larus spp.), and giant-petrels (Macronectes
spp.) are the main terrestrial predators (Young 1994, Stokes and
Boersma 1998, Le Bohec et al. 2005). hese species can subdue
chicks only up to a certain size, so aggregations should be more
prevalent in smaller chicks. In Adélie Penguins, skuas have only
been recorded killing chicks that were ≤30 days old, and especially chicks that were isolated by feeding chases or at the edge
of an aggregation (Davis 1982). Larger aggregations also lost proportionally fewer chicks to skuas than small ones (Davis 1982).
In African Penguins, chicks of all ages aggregated, even though
only the smallest chicks could be taken by natural predators at
the site (Seddon and van Heezik 1991); hence, predator avoidance
is not the only reason for aggregation in this species. In Rockhopper Penguins, only lone chicks were taken by skuas, whereas
individuals in an aggregation were never preyed upon (Pettingill 1960). Similarly, in Chinstrap Penguins, skuas were never
observed attempting to take chicks from within an aggregation,
regardless of the size of that aggregation (Penteriani et al. 2003).
In general, aggregations appear to confer substantial predatoravoidance beneits to chicks.
To avoid adult aggression.—Initially, abandoned chicks remain at their nest but may move for a variety of reasons. Once
a chick leaves the nest, it can be subject to aggression from both
adjacent nest owners and subadult or “loater” individuals (Seddon and van Heezik 1993a, de León et al. 2002), as has been commonly described for many colonial-nesting species (Wittenberger
and Hunt 1985). his adult aggression has been suggested as a
proximate factor underlying the formation of chick aggregations
(Tourenq et al. 1995). To avoid these attacks, chicks choose, or are
forced, to move away from brooding nests—either to the edge of
the colony or to free space within the colony. Because all chicks
are responding to the same stimuli, they may be directed to the
same areas. In this case, chick aggregations could be argued to be
purely a result, but not the intent, of chicks trying to avoid adult
aggression. However, evidence suggests that chicks move toward
aggregations when attacked. In African Penguins, abandoned individual chicks were attacked by unrelated adults at a much higher
rate than either chicks in an aggregation or guarded chicks. hey
also sufered more attacks than guarded chicks of the same age
(Seddon and van Heezik 1993a). When attacked, unguarded chicks
preferentially moved toward other chicks (74% of the time) rather
than toward unrelated adults or clear areas in the colony (Seddon
and van Heezik 1993a). In Chinstrap Penguins, adult aggression
is suggested as the proximate cause of chick aggregations, given
that lone chicks were attacked more and led farther than those
within an aggregation (Penteriani et al. 2003). Importantly, lone
chicks were often pursued until they reached an aggregation, at
which point the aggression ceased (Penteriani et al. 2003). Interestingly, when guard-stage Rockhopper Penguin chicks were attacked by unrelated adults, they preferentially left their parents
to join a chick aggregation (Pettingill 1960), whereas lone Adélie
Penguin chicks that were attacked by adults also joined aggregations (Penney 1968).
J ULY 2009
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More favorable thermal environment.—Huddling in groups
is an important method of saving energy by conserving heat, and
this behavior may be especially important under environmentally harsh conditions (Barré 1984, Ancel et al. 1997). his energy
saving may increase the survival of chicks while they are waiting
for parents to return from foraging trips. If aggregation confers
thermal beneits, both the percentage of chicks within a colony
and contact with aggregations should increase as conditions become more harsh. However, thermoregulatory costs decrease
with chick age (Lawless et al. 2001), so chick aggregations should
be more prevalent among younger chicks. In Adélie Penguins, the
proportion of young chicks aggregating increased as thermoregulatory demand increased. At the same time, older chicks aggregated only in severe weather events (Lawless et al. 2001), when
thermoregulatory costs were presumably high. In King Penguins,
during harsh conditions, chicks formed fewer but larger aggregations, and individuals were more closely packed within each aggregation (Le Bohec et al. 2005). By contrast, in African Penguins,
chick aggregations were formed even in warm weather and even
thermally mature chicks joined them (Seddon and van Heezik
1993a), which suggests that thermoregulation is less important
in this species.
heir gregarious nature.—Sladen (1958:62) has suggested that
chick aggregations are partially a result of the “gregarious nature
of penguins”; however, there is no evidence that this is the case in
penguins or in any other species in which chicks aggregate. Colonial breeding is widespread in avian species (Lack 1968), and its
social beneits include enhanced food inding through information sharing and prospecting for future mates (e.g., Wagner and
Danchin 2003, Wright et al. 2003). Although these may be important factors in coloniality in penguins, chick aggregations do not
appear to confer any extra beneits over coloniality, unless physical contact between chicks is important. hese functions could all
be achieved more easily by single chicks moving through a colony
than by aggregation. here may be a social basis of aggregation if
aggregations comprise related individuals rather than a random
group of chicks; however this has yet to be tested.
A R EVIEW
OF THE
TERM CRÈCHE
hus far, I have purposely avoided using the term “crèche,” because the behavior of penguin chicks is not crèching sensu stricto
and because the use of this term in the literature has been ambiguous and inconsistent. Traditionally, crèche refers to a group of ofspring adopted and raised by unrelated adults, and this deinition
is applicable in some avian systems. For instance, adults of some
Anatidae adopt, raise, and protect unrelated chicks (e.g., Gorman
and Milne 1972, Kehoe 1989, Eadie and Lyon 1998). However, this
is not the case in penguins. Even though penguin chicks aggregate, parents feed only their own ofspring (hompson 1974), and
adults at the edge of chick aggregations defend their own nest site
or chicks from predators, rather than protecting the crèche per se
(Sladen 1958, de León et al. 2002). hus, although the term crèche
is legitimately applied to some species, it is biologically misleading
to describe penguin behavior in this way.
Traditionally, development of penguin chicks has been separated into guard and crèche stages, the latter deined as starting when chicks are independent of the nest (Richdale 1957,
691
Sladen 1958, Ainley 2002). However, Adélie Penguin chicks may
be abandoned some days before they leave the nest site (D. Wilson pers. obs.), and this may occur in other species, but has perhaps been masked by the deinition of “crèched chicks.” hus,
there is the confusing possibility that chicks are neither in the
guard phase (because parents have left) nor in the crèche phase
(because they are still alone on the nest). here is also the confusion that chicks have crèched but are not in a crèche (i.e., they
have left the nest but have not united with other chicks). Young
(1994) has suggested that the stages of chick development be
designated “guard” and “post-guard” to resolve these potential
confusions. hese two phases are easy to diferentiate: chicks
in the guard phase have a parent present, whereas chicks in the
post-guard phase do not. Chicks in the post-guard phase can either be alone or aggregate with other post-guard chicks. hese
terms can be applied to all penguin species, not just those with
chicks that aggregate.
Young’s (1994) deinition of chick stages also avoids the
diiculties faced by other authors as to when a group of chicks
constitutes a crèche. For example, a crèche has been deined as
“a minimum of three chicks in close association, where the distance between individuals was less than half the mean distance
between nests” (Davis 1982:279); as “more than a normal brood of
two chicks gathered together in a group, which were normally unguarded by adults” (Ainley et al. 1983:18); as “two or more chicks in
close proximity . . . where individuals are less than two chick wing
lengths apart” (Le Bohec et al. 2005:528); and as “a cluster of three
or more chicks” (Seddon and van Heezik 1993a:91). his variation
makes comparisons between studies extremely diicult.
As this review has shown, chick aggregations can be luid
in time and are a response to a variety of stimuli. It appears that
aggregation is an ancestral trait in the penguin group and probably arose in Antarctica as, initially, a way of conserving heat
(and therefore energy) in extreme cold. As penguins expanded
northward, aggregations evolved alternate roles as a method of
increased predator avoidance and to avoid adult aggression. he
importance of each beneit on chick aggregation varies between
species and will also vary across breeding sites and will change as
chicks mature.
here are several areas for potential future research, at both
the species and individual levels. Efort should be directed to species for which there is little information on chick aggregations
(Table 1), primarily Eudyptes. his group could be specially interesting, given the observation that Rockhopper Penguin chicks on
the Falkland Islands (Islas Malvinas) left their nests to aggregate
with other chicks “even while parents were brooding them” (Pettingill 1960:217). Species with a large latitudinal range (Table 1)
would be ideal candidates for testing the inluence of temperature
on aggregation formation, and experimental removal of predators
at some colonies could be used to test the importance of predation
pressure on the formation of chick aggregations. Studies should
also focus on the inluences that cause an individual chick to join
an aggregation. It seems counterintuitive that when some chicks
aggregate, others of the same size remain alone even if the beneits of joining an aggregation are small. It may be that aggregating
chicks are more closely related than chicks that remain alone. his
would be a fascinating social beneit of the formation of aggregations through kin selection.
692
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ACKNOWLEDGMENTS
Discussions with L. Emmerson, C. Southwell, M. Weber, P. Seddon, and one anonymous reviewer greatly improved earlier versions of the manuscript.
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Received 2 September 2008, accepted 18 March 2009
Associate Editor: D. C. Dearborn