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Ethology
Is Territory Defence related to Plumage Ornaments in the King
Penguin Aptenodytes patagonicus?
Vanessa M. Viera* , Paul M. Nolanà, Steeve D. Côté*, Pierre Jouventin§ & René Groscolas *
à
§
Département de Biologie and Centre d’Études Nordiques, Université Laval, Sainte-Foy, QC, Canada
Département d’Ecologie Physiologie et Ethologie, IPHC, CNRS, Strasbourg Cedex, France
Department of Biology, The Citadel, Charleston, SC, USA
Equipe d’Ecologie Comportementale, Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier Cedex, France
Correspondence
Vanessa Viera, Département de Biologie,
Université Laval, Sainte-Foy, QC, Canada G1K
7P4. E-mail: [email protected]
Received: August 8, 2007
Initial acceptance: September 11, 2007
Final acceptance: September 11, 2007
(S. A. Foster)
doi: 10.1111/j.1439-0310.2007.01454.x
Abstract
Colourful ornaments in monogamous birds may be directed at potential
mates or other conspecifics to signal individual condition, reproductive
status or fighting ability, especially in monogamous and territorial species. We investigated whether the size of the orange auricular patch
may be an indicator of aggressiveness in the king penguin Aptenodytes
patagonicus, a monogamous and territorial seabird. The relationship
between auricular patch size and defence behaviour was explored relative to territory location (centre vs. periphery of the colony), period of
reproduction (early vs. late), state of reproduction (incubation vs. brooding) and sex. The proportion of time spent in territorial defence and the
rate of aggressive behaviours were positively correlated with auricular
patch size, mainly because central birds were more aggressive than
peripheral birds and also had larger patch sizes. The period of reproduction, state of reproduction and sex did not interact with patch size to
affect aggressiveness. Our results suggest that the size of the auricular
patch in king penguins may be a reliable signal allowing individuals to
evaluate the quality of mates or competitors in terms of aggressiveness.
Whether aggressiveness is directly linked to patch size or indirectly
through body condition, however, remains to be determined. In any
event, birds with larger patches seem to gain central territories in the
colony, thereby increasing their reproductive success. Finally, our study
adds to the growing evidence that the evolution of sexually monomorphic ornaments may stem from mutual sexual selection.
Introduction
Sexual selection is thought to explain the evolution
of ornamental traits and preference for mates displaying such traits (Andersson 1994). However, the
evolution and function of ornamentation in both
sexes, especially in monogamous species, are still
puzzling (Wachtmeister 2001). Two main hypotheses
have been proposed to explain the widespread
occurrence of mutual ornamentation: such traits are
a by-product of genetic constraints on sex-limited
146
trait expression (Lande 1980), or sexual selection
acts on females as well as on males (Amundsen
2000). Selective forces driving ornamentation in
both sexes include mate choice and intrasexual competition for mates (mutual sexual selection), social
competition over resources other than mates (social
selection), and selection for sexual mimicry. These
three mechanisms, however, are not mutually exclusive (review in Amundsen & Pärn 2006; Kraaijeveld
et al. 2007). Ornamentation might serve as a signal
of phenotypic quality or individual identity to
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
Defence and Patch Size in King Penguins
V. M. Viera et al.
conspecifics (Zahavi 1975; Kodric-Brown & Brown
1984; Tibbetts & Curtis 2007) and models still debate
whether those signals are condition dependent or
not (Dale et al. 2001; Tibbetts & Curtis 2007).
Carotenoid and melanin pigmentation (either the
colour intensity or the extent of the coloured area)
correlate with aspects of individual quality, such
as immunocompetence, fighting ability, parental
quality, general health, breeding performance or
even offspring quality (Hill 1991; Hill & McGraw
2006a,b). Furthermore, conspicuous patches of
colour mediate aggressive interactions in many vertebrates, including birds (Pryke et al. 2001, 2002;
Quesada & Senar 2007), lizards (Lopez et al. 2004;
Huyghe et al. 2005; Whiting et al. 2006) and fish
(Horth 2003). Models suggest that the evolution of
ornaments in socially monogamous and sexually
monochromatic species could be driven by mutual
mate choice or by intrasexual signalling within both
sexes (Johnstone et al. 1996; Kokko & Johnstone
2002). Many monogamous species are territorial and
what appears to be signalling between the pair
members may in reality be directed at other conspecifics as signals of status or fighting ability (Enquist
& Leimar 1983; Andersson 1994). It has been suggested that the biological function of the strikingly
coloured feathers and bill spots of penguins is related
to mate acquisition (Massaro et al. 2003; Jouventin
et al. 2007, 2005). A pioneering experiment manipulating plumage of three penguin species (Aptenodytes
patagonicus, Eudyptes chrysocome and E. chrysolophus)
found that the removal of yellow feathers from the
head resulted in males having difficulty acquiring a
mate, although it was unclear if those males fared
poorly in mate choice or in male–male competition
(Jouventin 1982).
The king penguin (Aptenodytes patagonicus) is a territorial seabird in which both sexes are characterized
by bright auricular and breast patches of yellow–
orange feathers (Jouventin 1982), and an orange
beak horn reflecting intensely in the ultraviolet (UV)
wavelengths (Dresp et al. 2005; Jouventin et al.
2005). King penguin feathers lack carotenoids and
contain only a small amount of melanin pigments;
the feathers on their breast and auricular regions
appear to be coloured by an undescribed pterin pigment (McGraw et al. 2004, 2007).
King penguins nest in dense colonies where pairs
vigorously defend a small territory of approx.
0.5 m2 during incubation and brooding (Côté
2000). Aggressive behaviour varies significantly
depending on territory location within the colony
(central birds are more aggressive than peripheral
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
birds) or the state of reproduction (aggressiveness
during incubation is lower than during brooding),
but both sexes are equally aggressive (Côté 2000).
Moreover, breeding birds experience differential
reproductive success depending on the period of
reproduction (early breeders had a threefold higher
success than that of late breeders) and territory
location (central territories have a higher success
than those on the edge; Weimerskirch et al. 1992;
Côté 2000). Territory defence may represent the
degree of parental investment or parental quality of
breeding birds and consequently may play a crucial
role in predicting reproductive success in this
species.
Despite extensive studies on the evolution and
role of colour ornaments, monomorphic seabirds like
penguins are still poorly known in this regard. This
is surprising because seemingly monomorphic species do exhibit strikingly coloured feathers, and their
breeding and behavioural ecology suggest a socially
or sexually selected role for their plumage ornaments. Previous studies have suggested that auricular feathers play a role in mate acquisition in king
penguins (Jouventin 1982; Jouventin et al. 2007),
but were unable to tease apart any separate roles of
mate choice vs. intrasexual aggression to control
access to mates. Therefore, we investigated whether
the size of the orange auricular patch may be an
indicator of aggressiveness in this sexually monochromatic species. We tested the relationship
between auricular patch size and defence behaviour
according to the territory location (centre vs. periphery), period of reproduction (early vs. late), state of
reproduction (incubation vs. brooding) and sex of
breeding pairs.
Methods
King penguins are pelagic seabirds that breed
throughout the subantarctic islands. We studied king
penguins in a subcolony of ca. 16 000 pairs in the
colony ‘La Baie du Marin’, Possession Island, Crozet
Archipelago (4625¢S, 5145¢E). The laying period
extends from Nov. to Mar. and hatching occurs on
average 54 d after the beginning of incubation
(Stonehouse 1960), i.e. starting at the beginning of
Jan. at Crozet. King penguins do not build a nest,
and incubate a single egg on their feet (Stonehouse
1960). Male and female king penguins share incubation and chick-rearing duties. The male performs the
first shift, which typically lasts about 2 wk, whereas
the duration of each remaining incubation shift lasts
5–15 d (Stonehouse 1960).
147
Defence and Patch Size in King Penguins
Data Collection
We collected data during the austral summers of
2004 and 2005. We located pairs on their breeding
territory during pair formation, sprayed them from a
distance with a non-permanent blue dye (PORCIMARK; Kruuse, UK) on their white breast, and
then flipper-banded males and females with a plastic
tag during their first incubation shift. The dye on the
chest lasted 1–15 d depending on the rain, and disappeared completely after going to sea. Flipper
length was also measured at capture. Sex was
known for all birds, because the male always performs the first incubation shift (Stonehouse 1960;
Weimerskirch et al. 1992). The exact day of laying
was known for each pair and birds were surveyed
daily during incubation and brooding to measure
shift durations and to record hatching dates. Early
breeders lay their egg in late Nov.-early Dec. (Weimerskirch et al. 1992). Those that laid after the first
hatching was observed were considered late breeders
(Côté 2000). We defined peripheral territories as
those situated within approx. 2 m of the colony edge
(Côté 2000). Peripheral individuals were therefore
the first birds to interact with predators attempting
to enter the colony (Côté 2000). Approx. 61% of
king penguins on the periphery of the colony were
still incubating in late Feb.-early Mar. Late breeders
were thus much more common on the colony edge
than in the centre. In contrast, only 13% of central
birds were incubating at that time, indicating that
most central territories were occupied by early
breeders.
Between Dec. and Feb., we performed 278 focal
animal samples of 15 min each on 74 marked birds
from different pairs (two to 11 focals ⁄ individual) to
study their aggressive behaviour (Altmann 1974;
Côté 2000). Observations were conducted between
06:30 and 20:30 hours and were carried out from
outside the colony at distances of 10–250 m, using
binoculars and spotting scopes when necessary to
avoid disturbing the birds. We recorded territorial
defence as the following aggressive behaviours: beak
pointing (no vocalization, beak closed, body
stretched out), gaping (pointing but with bill open
and vocalizing, body stretched out), pecking and
flipper blows (Côté 2000). We also noted the number of direct neighbours of the territory, i.e. those
close enough to allow interactions with body contact, for each focal sample (Côté 2000).
We took digital photographs of the heads of all
marked individuals (44 males, 30 females), using a
Canon digital camera (Canon, France, EOS 300D).
148
V. M. Viera et al.
We captured all birds once and held them briefly
inside a nearby field hut, to obtain similar light conditions and standard background. We used a standardized posture: birds in profile, head lightly
extended and bill pointing up at 30 from the horizontal. Photographs were taken from 40 cm away
and using 50 mm as the focal distance (Canon EF-S
18–55 lens ⁄ f5.6). In each photograph, we held a
ruler in the same plane as the plumage badge, to
allow measurement of the patch size. Badge sizes
were measured from digital images on a Macintosh
computer using the public domain NIH Image software (http://rsb.info.nih.gov/nih-image).
Statistical Analyses
We estimated the proportion of time spent in territory defence and the rates of threat displays involving (1) no body contact (beak pointing and gaping)
and (2) body contact (pecking and flipper blows).
The proportion of time spent defending the territory
was arcsine square-root transformed, while the rates
of threat displays and aggressive interactions with
body contact were square-root transformed to satisfy
normality (Sokal & Rohlf 1995). Mixed GLMs
(GLMM) with individual as a random factor were
used to assess the relationships between patch size
and the different measures of aggressive behaviour
(dependent variables). Because the number of neighbours may affect aggressiveness and body size (as
indexed by flipper length) may affect patch size, we
considered them as covariates in the models. Sex,
territory location (central vs. peripheral), period of
reproduction (early vs. late laying), state of reproduction (incubation vs. brooding) and all two-way
interactions with patch size were included in the
mixed models. We also tested the effects of sex, territory location, period of reproduction and state of
reproduction on measures of patch size. Models took
into account the dependence between observations
from the same subject with a compound symmetry
structure (Littel et al. 2006). Given that a dataset
consists of repeated measurements within individuals, the simplest possible correlation structure is to
assume (most likely incorrectly) that any observation
collected from one individual is uncorrelated with
every other observation measured in that individual.
Compound Symmetry assumes non-zero, yet equal
correlations exist for all combinations of observations
defined by the within-subject factors. That is, every
observation collected from an experimental unit is
equally correlated with every other observation from
that unit. All statistical analyses were performed
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
Defence and Patch Size in King Penguins
V. M. Viera et al.
with sas statistical software (version 9.1; SAS Institute, Cary, NC, USA). Mean values are reported 1
SE and the significance level was set at 0.05.
Ethical Note
We captured penguins from a sector of the colony
inhabited by about 1600 pairs, and placed a hood
over the heads of captured birds to keep them calm
during handling, which lasted 5–10 min. To minimize disturbance, we only took a picture of the right
profile of each bird. Removing the birds from the
colony to standardize conditions for pictures and
limit the disturbance of neighbours did not result in
any egg lost and, after releasing birds, no predation
was observed in the colony. When focal observations
were conducted at short distances, we observed the
birds from behind a low wall. Birds were banded at
the onset of the breeding season and tags were
removed before the winter. Capture and tagging procedures were approved by the Ethical Committee of
the Institut Polaire Français – Paul-Emile Victor and
the experiments comply with the current laws of
France.
Time spent in territory defence increased with
patch size (F1,228 = 141.9, p < 0.001, R2=0.34;
Fig. 1). Similarly, the rate of threat displays
(F1,228 = 9.91, p = 0.002) and body contact interactions (F1,228 = 5.88, p = 0.01) increased with patch
size. There was also an interaction between patch
size and territory location (proportion of time spent
in defence: F1,224 = 6.95, p = 0.009; threat displays:
F1,224 = 8.90, p = 0.003; body contacts: F1,224 =
29.14, p < 0.001), indicating that aggressiveness
increased more rapidly with patch size for birds on
central territories than for birds on peripheral territories (Fig. 1). Moreover, aggressiveness was higher for
central birds than for birds occupying the periphery
of the colony (all p’s < 0.02; Table 1). The interactions between patch size and either the period of
reproduction, the state of reproduction or sex did
not affect measures of aggressiveness (all p’s > 0.2).
Similarly to aggressiveness, patch size was larger
in central birds than that in peripheral birds
Table 1: Aggressiveness (proportion of time spent in defence and
rate of aggressive behaviours) and auricular patch sizes according to
territory location in breeding king penguins (Aptenodytes patagonicus)
from the Crozet Archipelago
Results
The covariates in the models were not significant:
flipper length, an index of body size, was not related
to auricular patch size (GLMM: F24,227 = 0.82,
p = 0.71) or aggressiveness (rate of threat displays,
rate of body contacts and time spent in territory
defence; all p’s > 0.4). Moreover, the number of
neighbours did not affect any measures of aggressiveness (all p’s > 0.3).
Proportion of time spent in
defence (%)
Threat displays (beak pointing
and gaping ⁄ h)
Body contact interactions
(pecking and flipper blows ⁄ h)
Auricular patch size (cm2)
Central birds
(n = 40)
Peripheral birds
(n = 34)
16.6 1.8
13.1 1.9
95.4 1.7
82.4 1.0
21.4 1.0
11.3 0.6
15.1 0.5
13.9 0.5
Fig. 1: Relationship between per cent of time
spent in territory defence and auricular patch
size in breeding king penguins from the Crozet Archipelago. Filled circles are birds on
central territories and empty circles are birds
occupying territories on the edge of the colony. Each data point represents one focal
observation, thus there are multiple data
points per individual.
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
Percentage of time spent in defence (%)
70
60
50
40
30
20
10
0
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Patch size (cm2)
149
Defence and Patch Size in King Penguins
(F1,224 = 18.90, p = 0.001; Table 1), but it did not
differ between early and late breeders (F1,224 = 1.80,
p = 0.18), incubating and brooding birds (F1,224 =
3.39, p = 0.07) or between sexes (F1,224 = 0.63,
p = 0.43).
Discussion
Our study demonstrated that auricular patch size
can convey information on the aggressive behaviour
of both sexes. West-Eberhard (1983) suggested that
bright coloration in both sexes of many bird species
may occur because the two sexes perform aggressive
displays. A few studies on birds have shown that an
ornament may be involved in aggressive displays in
both sexes (Jones & Hunter 1999; Jawor et al. 2004;
Kraaijeveld et al. 2004). Male and female king penguins share territory defence. The risk of injury in
aggressive interactions involving body contacts is
therefore high in both sexes, favouring the evolution
of badges of status (Jones & Hunter 1999). As a
result, both sexes are similarly ornamented in king
penguins and, therefore, we argue that our results
add to the emerging evidence that selection for
social signalling in both sexes could be the product
of mutual sexual selection rather than genetic correlation between the sexes (Jones & Hunter 1993; Kraaijeveld 2003; Griggio et al. 2005; Komdeur et al.
2005). Kraaijeveld et al. (2004) showed that ornamental feathers of monomorphic black swans
(Cygnus atratus) function as a signal of social dominance that is highly correlated with reproductive
success in both sexes. Others have also recently
investigated how ornaments were associated with
reproductive performance in both sexes of different
bird species. Komdeur et al. (2005) found positive
relationships between ornamentation of European
starlings (Sturnus vulgaris) and fitness correlates such
as laying date, clutch size and relative hatching
success, whereas Velando et al. (2001) showed that
ornaments indicated parent and chick quality in Inca
terns (Larosterna inca). To better understand the
evolution of mutual ornamentation in king
penguins, it remains to be tested whether patch size
is related to reproductive success in both sexes.
Patch sizes of birds in the centre of the colony
were larger than those of birds at the edge of the
colony. Reproductive success of penguins varies
according to their territory location mainly because
of higher protection from avian predation in the
centre of the colony than on the edge (Emslie et al.
1995; Côté 2000). For king penguins, it has been
suggested that the first birds to arrive in the colony
150
V. M. Viera et al.
(early breeders) choose the central locations (Côté
2000; Bried & Jouventin 2001). However, our results
indicate that patch size did not vary with the period
of reproduction so that birds with larger patches
seem to move into central territories when they
arrive, even if they are late in the breeding season.
Such a hypothesis emphasizes the importance of territory location for king penguins because it suggests
that the benefits of being in the centre of the colony
outweigh the costs of being more aggressive. Bried &
Jouventin (2001) also showed in a study conducted
in the same penguin colony that central birds have a
higher reproductive success than that of peripheral
birds. As a consequence, it seems reasonable that the
relationship between aggressiveness and patch size is
related to territory location as birds in good condition are likely to gain access to central territories
because of their aggressive behaviour. Ornamentation thus predicted status, with less ornamented king
penguins less capable of obtaining high quality central territories. The higher aggressiveness of birds on
central territories towards territorial neighbours and
intruders, compared to peripheral birds (Table 1;
Côté 2000), supports this idea. Finally, our new finding on the size of ornaments in relation with the
location of breeders in the colony is the missing link
to understand the relationship between the size of
patches (this study), the acquisition of mate (Jouventin et al. 2007) and the breeding success (Bried
& Jouventin 2001).
In many bird species, breeding success declines
seasonally (Moreno 1998) and often early breeders
are more ornamented than late breeders (Møller
1994; Daunt et al. 2003). Following the general pattern of other birds, early breeders have higher reproductive success than that of late breeders in king
penguins (Weimerskirch et al. 1992). However, this
species is unique among penguins in that a successful reproductive cycle requires an average of 14 mo
(Stonehouse 1960). Such a long breeding cycle
means that individuals cannot breed early 2 yr in a
row if they have fledged a chick 1 yr. In other
words, king penguins can alternate early and late
breeding years independently of their condition
(Weimerskirch et al. 1992). This may help explain
why we did not find any relationship between auricular patch size and the timing of breeding, or
between brooding and incubating birds.
Mate acquisition mediated by the size of a phenotypic trait, such as bill or body size, can also be
explained by a positive relation between age and the
trait, especially in long-lived species where the
expression of a trait often increases with age (Kokko
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
Defence and Patch Size in King Penguins
V. M. Viera et al.
1997). Therefore, an alternative explanation for the
relationship we observed between aggressive behaviour and ornament expression could be that patch
size is related to age. However, Nicolaus et al. (2007)
tested this hypothesis for king penguins at the same
study site and found no difference in mean patch
size for birds of 2 to >7 yr of age.
Individuals best able to assess the quality of potential mates or competitors using colour signals should
be favoured by natural selection, which should lead
to the display of condition-dependent traits such as
colourful plumage patches. Along these lines, Nolan
et al. (2006) showed that hue of the breast plumage
patch of king penguins reflected their innate, genetically based immune response. Jouventin (1982) and
Jouventin et al. (2007) found evidence of sexual
function of patch size and our study demonstrated
that patch size may a reliable cue of aggressiveness
and indicates an individual’s ability to gain and ⁄ or
defend a territory. The next step is to determine
whether aggressiveness is linked to patch size
directly or if body condition determines aggressiveness and patch size independently.
In conclusion, our results suggest that auricular
ornaments signal aggressiveness in both sexes in
king penguins and could be influenced by mutual
sexual or social selection. Current evidence indicates
that ornaments expressed in both sexes function as
‘badges-of-status’ in a variety of taxa, including
birds (Jones 1990; Swaddle & Witter 1995; Jones &
Hunter 1999; Ferns & Hinsley 2004; Jawor et al.
2004; Kraaijeveld et al. 2004; see Kraaijeveld et al.
2007 for a review). Patch size provides reliable
information on aggressive behaviour in king penguins, and perhaps also on individual quality (Kristiansen et al. 2006; Velando et al. 2006; Tibbetts &
Curtis 2007). Therefore, the debate remains as to
whether patch size exerts its effect on pairing speed
(described in Jouventin et al. 2007) by influencing
mate choice or intrasexual competition for access to
mates. Given the central role of aggressiveness in
success at competition, our data seem most consistent with an influence on intrasexual competition.
Acknowledgements
This study was approved and supported by the Institut Polaire Français Paul-Emile Victor (IPEV) and the
Natural Sciences and Engineering Research Council
of Canada (NSERC). Logistic support was provided
by the Terres Australes et Antarctiques Françaises.
We are truly indebted to J. Arnould and S. Geiger
for help in the field and to G. Daigle for help with
Ethology 114 (2008) 146–153 ª 2008 The Authors
Journal compilation ª 2008 Blackwell Verlag, Berlin
statistical analyses. Two anonymous referees and
K. Kraaijeveld provided constructive comments on a
previous version of the manuscript. V.M.V. was
supported by scholarships from the Fondation de
l’Université Laval and NSERC.
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