Begging response of gull chicks to the red spot on the parental bill
, Sin-Yeon Kim
, Jose Carlos Noguera
Departamento de Ecoloxia e Bioloxía Animal, Ediﬁcio de Ciencias Experimentales, Universidade de Vigo, Vigo, Spain
Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, U.K.
Received 9 October 2012
Initial acceptance 8 November 2012
Final acceptance 6 March 2013
Available online 19 April 2013
MS. number: 12-00781R
In some animals, offspring begging is elicited by parents through behavioural or morphological signals.
The red spot on the lower mandible in adult gulls is one of the best-known examples of a signal trig-
gering chick begging. We examined whether the begging response of chicks (pecking for food and the
chatter call for drawing parental attention) was affected by the spot size within the natural range of
variation on a dummy head. Using a cross-fostering experiment, we examined whether these responses
covary with the size of the genetic or social parent’s spot. We found that the natural variation in size of
this parental signal strongly inﬂuenced intensity of chick begging. Pecking increased when chicks were
stimulated by a larger red spot. Additionally, pecking intensity increased in chicks reared by mothers
with a large red spot, suggesting that this begging component is inﬂuenced by previous experience. In
contrast, chick hatching order affected the number of chatter calls produced in relation to the size of the
red spot on the dummy, suggesting the presence of different begging strategies according to brood hi-
erarchy. The differential call response to a small/large red spot on the dummy was positively correlated
with the original mothers’red spot size and negatively with that of the original fathers. These results
suggest a genetic correlation between biased chick response for a large spot and parental signal in
contrasting patterns for mothers and fathers. Our results suggest that the parental red spot and offspring
begging are traits subject to coevolution.
Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
In species with parental care, conﬂicts of interest are expected
over the amount of parental investment that family members
receive because they are not equally related to one another
(Hamilton 1964;Trivers 1985). Communication between parents
and offspring is one possible outcome to have evolved for the
resolution of these conﬂicts (Godfray 1991). Empirical research has
mainly focused on how offspring traits inﬂuence parental behav-
iour (see Royle et al. 2002). Thus, for example, extravagant behav-
iours performed by offspring to solicit food and care from their
parents are thought to be an outcome of parenteoffspring conﬂict
(Trivers 1974;Kilner & Johnstone 1997;Royle et al. 2002;Kilner &
Hinde 2012). Additionally, other studies have examined how
offspring traits that represent their quality, such as coloration or
chemical stimuli, affect parental provisioning (e.g. Lyon et al. 1994;
Mas et al. 2009). Although often neglected, parental traits may also
inﬂuence offspring behaviour in many different taxa. In the burying
beetle Nicrophorus vespilloides, parental chemical cues act as
stimuli for larval begging (Smiseth et al. 2010). In some bird species,
parental calls also trigger nestling begging (e.g. Madden et al.
The red spot on the lower mandible of adults in large gull spe-
cies is probably the earliest example ever studied of parental sig-
nals inﬂuencing offspring behaviour. In 1947, Niko Tinbergen
studied whether the red patch in both sexes of the herring
gull, Larus argentatus, induces begging behaviour of gull chicks
(Tinbergen 1948) based on previous observations that naïve gull
chicks have a strong tendency to peck red objects (Heinroth &
Heinroth 1928;Goethe 1937). From detailed observations and ex-
periments, he showed that the red spot stimulates hatchlings to
peck at the parents’bills (Tinbergen 1948;Tinbergen & Perdeck
1950; see also ten Cate 2009 for a detailed review of Tinbergen’s
work), and this begging behaviour induces the parent to regurgitate
food (Weidmann 1956;Beer 1966). These studies, as recently
conﬁrmed (see ten Cate et al. 2009), have become a model of an
‘innate releasing mechanism’(i.e. ﬁxed patterns of action released
by an external stimulus) in the analysis of instinctive behaviour.
Nevertheless, nothing is known about whether natural variation in
the red spot affects this mechanism.
The red spot size in adult gulls is highly variable among in-
dividuals; this variability is related to carotenoid deposition
(Blount et al. 2002;Pérez et al. 2008) and mirrors the bearer’s
condition and health (Kristiansen et al. 2006;Pérez et al. 2008,
2010a,b). It is known that parents adjust their chick provisioning
effort according to their partner’s red spot size (Morales et al.
*Correspondence: A. Velando, Departamento de Ecoloxía e Bioloxía Animal,
Ediﬁcio de Ciencias Experimentales, Universidade de Vigo, 36310 Vigo, Spain.
E-mail address: email@example.com (A. Velando).
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journal homepage: www.elsevier.com/locate/anbehav
0003-3472/$38.00 Ó2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 85 (2013) 1359e136 6
2009). Therefore, this signal may play a role in communication
between all family members by providing a network environment
for signallers and receivers (Horn & Leonard 2005). It is necessary
to determine whether the natural variability of this coloured
signal also inﬂuences chick begging, and hence parenteoffspring
conﬂict, to conﬁrm a unique case of a signal that plays a simul-
taneous role in different conﬂicts among family members over
The evolution of parental traits and the evolution of offspring
begging are not independent from each other (Cheverud & Moore
1994) because both simultaneously inﬂuence the social environ-
ment in which both phenotypes are expressed (i.e. indirect genetic
effects, Wolf et al. 1998). Therefore, genetic covariationbetween the
parental and offspring traits may be expected. Additionally,
offspring begging signals can be manipulated by mothers (e.g. by
adding hormones to the egg) to match parental conditions that
offspring will encounter (e.g. Hinde et al. 2009,2010), thereby
producing covariation between parental trait and offspring
begging. Both indirect genetic and maternal effects may produce
coadaptation of traits expressed by parents and offspring (Moore
et al. 1997;Wolf et al. 1998;Kölliker et al. 2005). In gulls, parents
respond to offspring demand (Morales et al. 2009); thus coadap-
tation of the parental red spot and offspring begging may occur if
the red spot inﬂuences offspring solicitation within the range over
which parents are sensitive.
In the present study, we explored whether the frequency of the
begging display is inﬂuenced by the size (within the natural range
of variation) of the parent’s red spot in chicks of the yellow-legged
gull, Larus michahellis. This study species nests on the ground,
where parents and the semialtricial young communicate inten-
sively during the nestling period. Chicks display a series of begging
calls and behaviours, which presumably have different functions in
parenteoffspring communication (Impekoven 1971;Noguera et al.
2010;Kim et al. 2011). First, chicks produce ‘chatter calls’from a
distance to attract the parents’attention, for example immediately
after the parents return to the territory (Impekoven 1971;Beer
1979). The chatter call, which is characterized by rapidly repeated
sound elements with a wide frequency range, is a costly signal that
probably induces oxidative stress (Noguera et al. 2010). Fathers,
more than mothers, feed their offspring in response to chatter calls
(J. C. Noguera, S.-Y. Kim & A. Velando, unpublished data). Parents
approach chicks with their head down, then the chicks, in a
hunched posture, peck at the red spot on the parent’s bill
(Impekoven 1971). Pecking seems to stimulate parental provi-
sioning, since the number of pecks and feeding rates of both par-
ents are highly correlated (Morales et al. 2009; J. C. Noguera, S.-Y.
Kim & A. Velando, unpublished data). We ﬁrst examined the ef-
fect of the size of the red spot on these complex begging compo-
nents by performing two sequential begging tests with small and
large spots and 1-day-old chicks, an age at which the red spot is
especially important for triggering offspring behaviour (Tinbergen
& Perdeck 1950). We predicted more intense begging when
chicks were stimulated with a larger red spot.
In our study, chicks were reared in foster nests, thus disrupting
the natural covariance between begging response to parental signal
and parental traits. Thus, we also studied the relationship between
the red spot size of the original and foster parents and the chicks’
response to red spots of different sizes. During the ﬁrst few days of
life, gull chicks are intensively brooded by their parents. If experi-
ence with foster parents during the ﬁrst day of life inﬂuences the
chicks’begging response to red spot size, a relationship between
chick response and spot size of foster parents is predicted (see
Hailman 1967;ten Cate et al. 2009). In contrast, a relationship
between begging response to red spot size and the spot size of the
original parents is predicted if there is either a genetic correlation
between chick begging biases and parental signals (e.g. by conﬂict
and coadaptation; Smiseth et al. 2008;Kilner & Hinde 2012;
Kölliker et al. 2012) or prehatching maternal inﬂuences on begging
behaviours (e.g. coadaptation by maternal effects, Hinde et al. 2009,
General Field Procedures
This study was carried out from April to June 2011 at a large
colony of yellow-legged gulls in the Parque Nacional das Illas
Atlánticas, Sálvora Island, Galicia, Spain (42
Yellow-legged gulls are socially monogamous colonial breeders
that defend a small breeding territory (Alonso-Alvarez & Velando
2001). Clutches typically contain three eggs (modal clutch size)
and eggs are laid at intervals of 1e3 days (Kim et al. 2011). In large
gull species, the ﬁrst two chicks hatch with little difference in time
but third chicks hatch later and have a disadvantage in competition
with their broodmates (Kim & Monaghan 2006). During egg laying,
we selected 21 nests with a clutch of two or three eggs. We
captured 26 adults from these nests with nest traps (R60 special
tilting cage; www.moudry.cz). A nest trap was placed over each
nest for less than 20 min, avoiding the midday hours to reduce heat
stress, and a maximum of three attempts per nest were made on
nonconsecutive days. Thus, in 16 nests we captured only one adult
per nest, and in the rest (ﬁve nests) we captured both incubating
parents. No nest was abandoned by birds in the days following
capture attempts. Birds were weighed (10 g) and head length, bill
depth, wing length and tarsus length were measured (0.05 mm).
Birds were sexed (17 females and nine males) by a discriminant
function including these morphometric variables (Bosch 1996),
known to be 100% consistent with sex determined by copulatory
behaviour (Alonso-Alvarez & Velando 2003). We photographed the
whole bill of each bird (Nikon Coolpix 5200) against a white
standard together with a red standard and a millimetre scale in a
dark box with controlled light, keeping a constant distance (15 cm)
from the lens to the bill (see Pérez et al. 2008). The sharply deﬁned
red spot area visible in photographs (in mm
) was measured by the
same person (J.C.N.) with image analysis software (Adobe Photo-
shop CS3). The measures of six randomly selected photographs in
triplicate indicated that this method was highly repeatable
To tease apart genetic or maternal and early environmental ef-
fects on begging behaviours, we swapped all clutches close to
hatching, when at least one egg showed a crack in the shell (ex-
pected to hatch 3 days later). The whole clutches were inter-
changed between two or three nests of similar clutch size and
stage. To identify hatching order, we marked the tip of the chick’s
bill through the egg hole made by the fully developed chick and
hatchlings using leg ﬂags made with coloured Velcro. On the day of
hatching, chicks were weighed (1 g) and, to identify the sex of the
chicks, we collected a droplet of blood from the brachial vein of
each chick using a sterile needle and a capillary tube. Chick sex was
identiﬁed from blood cell DNA by detecting two CHD genes
(CHD1W and CHD1Z; Fridolfsson & Ellegren 1999). The study was
done with permission of the Parque Nacional das Illas Atlánticas
(permit number 161/2011) and Xunta de Galicia (permit number
57/2011), and all the ﬁeld procedures that we performed complied
with the current laws of Spain.
We tested for frequency of begging behaviours in all hatchlings
that survived until 1 day old (N¼41 chicks from 18 broods). In
A. Velando et al. / Animal Behaviour 85 (2013) 1359e13661360
three nests all eggs failed to hatch; in the rest, ﬁve eggs failed to
hatch and two chicks died before the begging test. During the ﬁrst
few hours after hatching, chicks mainly remain with the eyes
closed, and they are not fed by parents (Tinbergen & Perdeck 1950);
for this reason we performed the begging test with 1-day-old
chicks (i.e. 1 day after hatching). In gull chicks, begging behaviours
can be elicited by the presentation of a dummy that simulates the
head of an adult (Tinbergen & Perdeck 1950;Tinbergen 1953;
Rubolini et al. 2006). We tested for intensity of begging compo-
nents using the standard protocol from Tinbergen & Perdeck (1950)
with minor modiﬁcations (see also Noguera et al. 2010;Kim et al.
A begging test was performed for each chick individually (in the
absence of sibling competition) in a hide placed outside the dense
gull colony to avoid disturbance tothe chick’s performance by adult
gulls’alarm calls. A lateral side of the hide remained open to adjust
the light conditions inside the hide close to external levels. We
transported 1-day-old chicks from their nests to the hide in cloth
bags. We ﬁrst placed each chick on the ground and coveredit with a
cloth until it stayed calm and quiet. The chick received a playback of
three mew calls (a parental call to attract their chicks; Tinbergen
1953), which were previously recorded at the same colony, to
simulate a natural feeding event. Immediately afterwards we
removed the cloth and presented a dummy, mimicking an adult
gull’s head. The dummy was made of white plaster and the bill was
painted yellow; a removable red spot (see below) made of sticky
paper was placed on the lower mandible. The intensity of the red
colour of these adhesive spots (CIELAB colour space measured by a
MINOLTA CM-2600d spectrophotometer, a* ¼49 and b* ¼36) was
within the natural range of red spots in breeding gulls (see Morales
et al. 2009). The visual stimulation was performed by nodding the
dummy head close to the chick 30 times in 1 min. To standardize
the visual stimulation across all study chicks, a researcher nodded
the dummy head while listening to 30 mechanical sounds, recorded
in an mp3 player, through an earphone. Another researcher
recorded the begging behaviours of chicks after removing the cloth
(note that in Noguera et al. 2010;Kim et al. 2011, but not in the
present study, begging behaviour was also recorded during the
playback of mew calls). To study the effect of red spot size on chick
behaviour, we used interchangeable red spots of two different sizes.
We selected the extreme sizes in the natural range in our popula-
tion (Morales et al. 2009): the ‘small’red spot corresponded to the
minimum area (78 mm
) and the ‘large’red spot to the maximum
). Each chick received two consecutive begging trials with
the two sizes of the red spot on the lower mandible of the dummy
head. The second trial was carried out once the chick was calm and
quiet under a cloth cover, usually 5 min after the ﬁrst trial. The
order of presentation of large and small spots in begging trials was
sequentially altered to control for the effect of the presentation
order. We recorded the number of distinct pecks at the red spot and
the number of chatter calls made by chicks during the dummy
presentation (Tinbergen & Perdeck 1950;Impekoven 1971;
Noguera et al. 2010). All chicks were returned to their foster nests
after the begging test, usually within 30 min after having been
collected. All leg ﬂags were removed at the end of the study. Each
chick was protected from wind and strong sunlight by keeping it
inside a cloth bag and under thick vegetation while away from the
nest (Kim & Monaghan 2005;Kim et al. 2011).
We ﬁrst examined whether begging intensity of chicks changed
according to the red spot size on the dummy. We analysed begging
behaviours (number of pecks and chatter calls) of gull chicks using
generalized linear mixed-effect models (GLMMs) with a Poisson
error distribution and a log link, including individual (nested in
nest identity) as subject random term and nest identity and the
interaction between nest identity and hatching order as random
slope to account for the nonindependence of chicks from the same
broods (Littell et al. 2006). Red spot size treatment and presenta-
tion order were included as ﬁxed effects in the models. Sex,
hatching order, brood size, hatching date, body mass at hatching
and all two-way interactions were also included in the models.
Nonsigniﬁcant interactions and main terms (at the alpha 0.05
level), except presentation order, were dropped sequentially to
simplify the model. The ﬁnal models were conﬁrmed using a for-
ward procedure (at the alpha 0.05 level).
In a subset of nests, we also had information on the red spot size
of the original and foster parents (original mother, N¼15 nests;
foster mother, N¼15; original father, N¼8; foster father, N¼9).
Thus, to investigate the relationship between parental red spot area
and begging response to different sizes of red spot on the dummy
head, we included the red spot area (in mm
) of the foster and
original parents and their interactions with the dummy’s red spot
size treatment in the ﬁnal models (see above). These interactions
tested whether the effect of the dummy’s red spot size on chick
begging behaviour depended on the area of the parental (original
or foster) red spot. We did not analyse three-way interactions
(e.g. hatching order*dummy’s red spot*parent’s red spot) to
avoid model overparameterization. Red spot size did not differ
between the sexes (mean SE; females: 192.45 6.27 mm
males: 192.28 10.14 mm
¼0.14, P¼0.99; see also Morales
et al. 2009;Pérez et al. 2010a,b). Variance in red spot area was
not explained by the cross-foster group (mixed model, group
random effect: F
¼0.66 P¼0.73) or its interaction with sex
¼0.21, P¼0.97), indicating that red spots of foster parents did
not resemble those of the original parents (r
Laying date did not inﬂuence red spot area (linear model:
¼1.7 3, P¼0.20). The relationship between differential
begging response to different spot size treatment and parental red
spot size was analysed separately for male and female parents
because we only captured both parents in ﬁve cases. The variance of
Pearson residuals indicated that models were not overdispersed
(see Littell et al. 2006). All tests were two tailed and the alpha
level was set at 0.05. Descriptive statistics are expressed as
Effects of Red Spot Size on Begging Intensity
Pecks and chatter calls were not correlated in either large or
small red spot trials (large red spot trial: r
¼0.12, P¼0.45; small
red spot trial: r
The number of pecks was affected by the presentation order
(Table 1): the dummy head received 26% more pecks at the ﬁrst
than at the second presentation. The size of the red spot strongly
affected the number of pecks to the dummy (Table 1): the large
red spot elicited 36% more pecks than the small spot (Fig. 1). Brood
size also inﬂuenced the number of pecks: chicks from larger
broods pecked more frequently (Tabl e 1). Hatching order, hatch-
ing date, hatching body mass, sex and any of the two-way in-
teractions did not affect the number of pecks signiﬁcantly
(P>0.25 in all cases).
For chatter calls, there was a signiﬁcant interaction between
hatching order and red spot size on the dummy (Table 1). Thus, ﬁrst
chicks produced signiﬁcantly more chatter calls when exposed to a
large red spot than to a small spot, but the opposite pattern
occurred in second chicks (Fig. 2); in third chicks, no difference in
A. Velando et al. / Animal Behaviour 85 (2013) 1359e1366 1361
chatter calls according to red spot size treatment was found (Fig. 2).
Other factors and interactions did not signiﬁcantly inﬂuence chat-
ter calls (P>0.13 in all cases).
Parental Red Spot Size and Begging
As we had additional information on the size of bill spot of the
original and foster parents for some nests (see Methods), we ran
the ﬁnal models again (Table 1) including parental spot areas and
their interactions with dummy red spot size (see Methods). When
the red spot area of the original parents was included in the ﬁnal
model, it did not inﬂuence the differential chick response to the
dummy red spot size treatment in terms of the number of pecks
(red spot area of original parent*dummy red spot size: P>0.29 in
both cases: mothers and fathers; see Appendix). The red spot area
of the foster mother affected the number of pecks at a large and
small red spot (red spot area of foster mother*dummy red spot size:
¼4.87, P¼0.035; Appendix Table A1). Overall, a large dummy
spot elicited more pecks than a small dummy spot especially in
chicks brooded by a foster mother with a small spot (Fig. 3,
Appendix Table A1).
The begging response of chicks, in terms of chatter calls, to
the red spot size on the dummy head was affected by the red
skcep fo .oN
Figure 1. Number of pecks (least square means SE) of 1-day-old yellow-legged gull
chicks according to red spot size treatment on the dummy head (N¼41 chicks from 18
No. of chatter calls
Figure 2. Number of chatter calls (least square means SE) of 1-day-old yellow-
legged gull chicks according to hatching order (‘a’being ﬁrst to hatch and ‘c’being
last to hatch) and red spot size treatment (closed circles: large spot; open circles: small
spot; N¼41 chicks from 18 broods). Probability of mean difference (L SD test) in
chatter calls according to dummy spot size (i.e. chick preferences) for each chick order
Results of the generalized linear mixed model analyses of begging response to a
dummy head by 1-day-old chicks (N¼41 from 18 broods)
Response variable Source of variation EstimateSE FdfP
Number of pecks
Full model Intercept 1.131.19
Hatching body mass 0.00580.018 0.01 1,35 0.75
Hatching date 0.0660.06 1.16 1,35 0.28
Hatching order (HO)
0.370.37 0.62 2,35 0.54
Chick sex (S)
0.240.45 0.26 1,35 0.61
Brood size (BS) 0.350.20 5.13 1,35 0.029
Order of presentation
0.270.07 15.25 1,35 0.0004
Red spot size (RSS)
0.890.43 4.10 1,35 0.050
HO*RSS [ﬁrst small] 0.300.18 1.60 2,35 0.22
[second small] 0.100.19
S*RSS [female small] 0.0980.14 0.49 1,35 0.49
HO*S [ﬁrst female] 0.280.50 0.80 2,35 0.46
[second female] 0.600.51
BS*RSS [small] 0.190.15 1.62 1,35 0.21
Final model Intercept 1.430.40
Order of presentation
0.240.06 13.55 1,39 0.0007
Red spot size [small]l 0.280.07 18.15 1,39 0.0001
Brood size 0.370.15 6.08 1,39 0.018
Full model Intercept 1.192.93
Hatching body mass 0.0410.044 0.86 1,35 0.36
Hatching date 0.230.16 1.88 1,35 0.18
Hatching order (HO)
0.280.97 0.21 2,35 0.81
Chick sex (S) [female] 0.211.20 0.01 1,35 0.94
Brood size (BS) 0.950.53 2.50 1,35 0.12
Order of presentation
0.340.20 2.97 1,35 0.09
Red spot size (RSS)
1.451.02 0.96 1,35 0.33
HO*RSS [ﬁrst small] 0.160.51 6.02 2,35 0.006
[second small] 1.360.55
S*RSS [female small] 0.380.42 0.78 1,35 0.38
HO*S [ﬁrst female] 0.481.39 0.59 2,35 0.55
[second female] 0.681.40
BS*RSS [small] 0.310.33 0.90 1,35 0.34
Final model Intercept 0.400.53
Hatching order (HO)
0.340.64 0.42 2,37 0.66
Order of presentation
0.300.19 2.38 1,37 0.13
Red spot size (RSS)
0.460.34 0.28 1,37 0.60
HO*RSS [ﬁrst small] 0.370.44 10.91 2,37 0.0002
[second small] 1.440.44
A. Velando et al. / Animal Behaviour 85 (2013) 1359e13661362
spot area of the original mother (red spot area of original
mother*dummy red spot size: F
¼4.81, P¼0.037; Appendix
Table A1, Fig. 4a). Thus, the more intense begging to a large
spot was only evident in chicks from females with a large spot
(Fig. 4a). In contrast, the differential chatter response to different
spot sizes was negatively affected by the spot area of the original
father (red spot area of original father*dummy red spot size:
¼8.71, P¼0.008; Appendix Tab le A1, Fig. 4b). The chicks
whose original father had a smaller red spot showed a higher
begging rate to a larger red spot on the dummy (Fig. 4b). The red
spot area of the foster parents did not affect chatter calls (P>0.11
in all cases; see Appendix).
The red spot on the lower mandible in adult gulls is well
known to trigger chick pecking, a classical example of a signale
response mechanism (Tinbergen & Perdeck 1950;tenCateetal.
2009). In this study we found that the natural variation in size
of this parental signal strongly inﬂuenced the intensity of chick
begging, but its effects differed between two different begging
components. When parents approach, chicks peck at the red spot
to solicit food, and in our study this begging component was
enhanced when chicks were stimulated by a larger red spot. On
the other hand, red spot size treatment inﬂuenced begging calls
but in different ways according to hatching order, supporting the
view that gull chicks have different begging strategies according
to brood hierarchy (Kim et al. 2011). Importantly, in a previous
study it was shown that the red spot size also inﬂuences the
partner’s behaviour: mates of birds with an experimentally
enlarged spot increased their food provisioning to offspring
compared to controls (Morales et al. 2009). Overall these results
suggest that the gulls’red spot represents an unusual signal that
plays a simultaneous role in different intrafamilial conﬂicts over
care (Morales & Velando, in press).
Current evidence suggests that different begging components in
gull chicks may have different functions in parenteoffspring
communication (Noguera et al. 2010;Kim et al. 2011). Chicks call
for their parent’s attention but peck the red spot of the parent’s
mandible to stimulate the parent to feed them (Impekoven 1971;
Beer 1979). Typically, pecking occurs after a parent approaches and
bows its head over only one of the chicks; thus it is a dyadic
communication event between a single parent and a single chick.
Importantly, the parent promotes pecking behaviour by lowering
its head towards the chick; thus parents probably have some con-
trol over this behaviour. A food deprivation experiment showed
that pecking behaviour is a reliable indicator of chick nutritional
status (Noguera et al. 2010). Thus, parents may use pecking fre-
quency to feed chicks according to their need for food. Indeed, it
120 160 200 240
ot area of foster mother
Figure 3. Relationship between the number of pecks of 1-day-old yellow-l egged gull
chicks (N¼33 chicks from 15 broods) according to the dummy’s red spot size treat-
ment (closed circles and solid line: large spot; open circles and dotted line: small
spot) and to the foster mother’s red spot area (mm
). The presented values for
number of pecks are residuals from the model correcting for presentation order and
brood size (Tab le 1 ) plus trait mean (11.7 0.69). Note that individual chick s are
represented by a pair of response s, one to a large spot (closed circle) and the othe r to
a small spot (open circl e).
120 160 200 240
Red spot area of original mother
120 160 200 240
ot area of ori
Figure 4. Relationship between the number of pecks of 1-day-old yellow-legged gull
chicks according to the dummy’s red spot size treatment (closed circles and solid line:
large spot; open circles and dotted line: small spot) and to (a) the original mother’s red
spot area (mm
)(N¼33 chicks from 15 broods), and (b) the original father’s red spot
)(N¼23 chicks from nine broods). The presented values for number of
chatter calls are residuals from the model correcting for presentation order, hatching
order and the interaction between hatching order and red spot size (Table 1) plus trait
mean (1.95 0.50). Note that individual chicks are represented by a pair of responses,
one to a large spot (closed circle) and the other to a small spot (open circle).
A. Velando et al. / Animal Behaviour 85 (2013) 1359e1366 1363
seems that both parents use the pecking behaviour to allocate food
(Morales et al. 2009; J. C. Noguera, S.-Y. Kim & A. Velando, unpub-
An interesting remaining question is the function, if any, of
pecking intensity according to parental signal, that is, red spot
size. Expression of the red spot is costly for adult gulls and re-
ﬂects their current condition and health (Pérez et al. 2008,2010a,
b). Chick begging preference for a larger red spot may be a
strategy to beg to high-quality caregivers (e.g. Velando et al.
2005). Additionally, parents may use the chick’s sensory bias to
obtain information about their need for food. The marginal cost,
that is, the change in cost of the signal according to begging
intensity, may increase only above a certain begging level (i.e.
there may be a convex function). In this situation, by imposing an
overall higher rate of begging above this threshold, parents with
a large red spot may prevent dishonest begging in their chicks
In the present study, intensity of pecks declined in the second
presentation, probably owing to the lack of reward in the ﬁrst
trial, conﬁrming the ‘negative conditioning’(i.e. decline in in-
terest as result of frequent exposure) in gull chicks (see ten Cate
et al. 2009). Pecking increased with brood size, similar to our
previous ﬁnding (Kim et al. 2011), suggesting that increased
sibling competition resulted in escalated food solicitation (e.g.
Leonard et al. 2000;Neuenschwander et al. 2003). In 2-day-old
chicks, pecking rate was affected by sex and chick condition (Kim
et al. 2011), but in our study on 1-day-old chicks, we did not ﬁnd
these effects. Experience during the ﬁrst few days of life could
modulate the chicks’begging strategies. Bias in pecking intensity
to a larger red spot was stronger in those chicks reared for 1 day
by foster mothers with a small red spot. Since red spot is condi-
tion dependent (Pérez et al. 2008;2010a,b), this effect may
be caused by previous experience with poor-quality caregivers.
This result suggests that previous experience of interacting with
the mother for a day after hatching inﬂuences the begging
Chatter calls were also affected by the size of the red spot on the
dummy head, but in different ways according to the hatching order
of the chick. In large gull species, the ﬁrst two chicks hatch with
little difference in time and they are strong competitors for parental
care. In contrast, third chicks have the disadvantage of hatching
later and being smaller than their broodmates (Kim & Monaghan
2006). Previous studies indicated that third chicks made more
chatter calls, mainly as a response to parental mew calls (Kim et al.
2011). Here, we found that the ﬁrst chicks made more chatter calls
when exposed to a larger red spot. In contrast, second chicks made
more chatter calls when exposed to a smaller red spot. This may be
abehavioural strategy to compete with their senior broodmate
(Smith & Montgomerie 1991) or to negotiate with them (Roulin
et al. 2000;Roulin & Dreiss 2012). Further studies should disen-
tangle how these begging strategies are used by chicks to overcome
interference from their siblings in a family communication network
(Horn & Leonard 2005). In this study, the begging strategy of chicks
was tested in the absence of broodmates, but after the chicks had
experienced natural sibling competition for a day in the foster nest.
The results of both begging components suggest that begging in
gull chicks may, to some extent, be a plastic response inﬂuenced by
their early experience.
Chatter bias for red spot size was positively correlated with the
red spot area of the original mothers and negatively with the red
spot area of the original fathers. Negative assortative mating by
spot size may underlie this opposite pattern in males and females.
Current evidence does not support this idea (within-pair red spot
¼0.16, P¼0.61; our unpublished data), but this
possibility should be explored further. Mothers might adjust
offspring begging signals by allocating substances to the egg to
match parental conditions (coadaptation by maternal effects;
Hinde et al. 2009,2010) or to manipulate partner care (Müller et al.
2007). A previous experimental study in yellow-legged gull chicks
showed that an increase in yolk testosterone enhanced chatter calls
to a dummy head but this response was not affected by the red spot
size on the dummy (J. C. Noguera, S.-Y. Kim & A. Velando, unpub-
lished data). Thus, even if other maternal substances (e.g. Rubolini
et al. 2005) affect intensity of chatter calls according to red spot
size, these results may also be explained by a positive genetic cor-
relation with the maternal spot and a negative genetic correlation
with the paternal spot.
Red spot size in yellow legged-gulls is, at least in part, based on
carotenoids, an exogenous resource (Pérez et al. 2008), but its
variation may also have a genetic basis (e.g. Fitze et al. 2003;Evans
& Sheldon 2012) caused, for example, by genetic differences in
carotenoid acquisition, absorption, transport and deposition (Craig
& Foote 2001;Walsh et al. 2012). On the other hand, a cross-
fostering experiment suggested the presence of signiﬁcant ge-
netic variation in the intensity of chatter calls (h
¼0.33; Kim et al.
2011). Fathers but not mothers allocate food according to the in-
tensity of chatter calls (J. C. Noguera, S.-Y. Kim & A. Velando, un-
published data), indicating that the effect of offspring begging on
parental response differs between mothers and fathers (sex-spe-
ciﬁc effect of demand on supply; Parker et al. 2002). As shown by
theoretical models, parental responsiveness to offspring solicita-
tion is expected to inﬂuence the coadaptation and hence the ge-
netic architecture between parental and offspring traits (see details
in Kölliker et al. 2005). Although these results should be taken with
caution owing to the relatively small sample size (especially in
males), they suggest that parental red spot and offspring begging
are traits subject to coadaptation by either a genetic effect or a
maternal effect and antagonistic coevolution among family mem-
bers (Moore et al. 1997;Wolf et al. 1998;Smiseth et al. 2008;Hinde
et al. 2010).
An important question to solve is whether this signal ﬁrst
evolved in the context of parenteoffspring communication or as a
result of sexual selection. During courtship, when soliciting food,
female gulls imitate chick solicitation by pecking on the male’s red
spot, and males feed the female in exactly the same way as they
feed chicks (Tinbergen 1959;Velando 2004). This may indicate that
females take advantage by exploiting their partner’s neural ma-
chinery (Ryan 1998) to feed chicks. In this species during courtship,
copulations are more likely to be successful when males provide
food to females prior to mounting (Velando 2004). An anecdotal
but illustrative result is that testosterone-implanted males during
chick rearing have been observed to try to copulate with their
chicks after feeding them (C. Alonso-Alvarez, personal communi-
cation; see also Besnard et al. 2002), suggesting that the same
mechanism governs both responses (courtship or parental feeding),
but is modulated by testosterone levels. A phylogenetic study may
shed light on how this signal coevolves in a familial context and
hence whether sensory preferences of offspring may have resulted
in the evolution of an honest sexual signal (Macías Garcia &
In conclusion, we found that two components of chick begging
display are inﬂuenced by the natural variation in red spot size on
the lower mandible of adult yellow-legged gulls. Our results pro-
vide rare evidence for a parental trait inﬂuencing simultaneously
communication between mates (Morales et al. 2009) and between
parents and offspring.
A. Velando et al. / Animal Behaviour 85 (2013) 1359e1366136 4
We thank Sami Merilaita, Angela Turner and three anonymous
referees for their constructive revision and comments on this
article. We thank Andrea Tato for help during molecular sexing
and J. Morales for fruitful discussion. Fieldwork in Sálvora Island
depended on the generous support and friendship of Jose Antonio
Fernandez Bouzas, Vicente Piorno, Marcos Costas and Marta
Caneda, staff of the Parque Nacional. During our stay in the
lighthouse, el torrero Pepe Pertejo kindly provided many facilities.
Finance was provided by the Spanish Ministerio de Ciencia e
Innovación (FEDER/CGL2009-10883-C02-01 and CGL2012-40229-
C02-02). S.-Y.K. is supported by the Isidro Parga Pondal fellowship
(Xunta de Galicia), J.C.N. by Marie Curie Intra European Fellowship
within the 7th European Framework Program (PIEF-GA-2011-21
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Red spot area of the original parents did not affect the
differential chick response in the number of pecks elicited
by large and small red spots on the dummy (red spot area
of original mother*dummy red spot size treatment:
estimate: 0.003 0.003; F
¼1.13, P¼0.30, red spot area of
original mother: estimate: 0.004 0.003; F
¼1.9 6 , P¼0.17;
red spot area of original father*dummy red spot size treatment:
estimate: 0.001 0.004; F
¼0.18, P¼0.68). The number of
pecks was correlated positively with the red spot area of the
original father (estimate: 0.009 0.003; F
Red spot area of the foster parents did not affect chatter calls (red
spot area of foster mother*dummy red spot size treatment:
estimate: 0.033 0.020; F
¼2.68, P¼0.12; red spot area of
foster mother: estimate: 0.001 0.022; F
red spot area of foster father*dummy red spot size treatment:
estimate: 0.016 0.013; F
¼1.63, P¼0.22; red spot area of
foster father: estimate: 0.016 0.013; F
¼1.5 7, P¼0.23).
The table shows the relationships between number of pecks to
dummy red spot and red spot area of the foster mother, number of
chatter calls to dummy red spot and red spot area of the original
mother and number of chatter calls to dummy red spot and red
spot area of the original father.
Results of the ﬁnal models (from Table 1), additionally testing the covariance
between red spot area of parents and chick begging response to a dummy head by
Response variable Source of variation EstimateSE FdfP
Number of pecks
and red spot
area of foster
Order of presentation
0.300.07 17.08 1,30 0.0003
Red spot size (RSS)
1.780.68 6.84 1,30 0.014
Brood size 0.310.18 2.84 1,30 0.10
Red spot area of
foster mother (SFM)
0.00650.0039 3.77 1,30 0.061
RSS SFM 0.00750.0033 4.87 1,30 0.035
Number of chatter
calls and red
spot area of
Hatching order (HO)
0.110.71 0.14 2,28 0.87
Order of presentation
0.360.22 2.59 1,28 0.12
Red spot size (RSS)
2.041.26 3.98 1,28 0.056
HO RSS [ﬁrst small] 0.510.52 7.83 2,28 0.002
[second small] 1.200.53
Red spot area of
foster mother (SFM)
0.00100.0060 0.79 1,28 0.38
RSS SFM 0.0130.006 4.81 1,28 0.037
Number of chatter
calls and red
spot area of
Hatching order (HO)
0.421.15 0.06 2,18 0.94
Order of presentation
0.68 1,18 0.42
Red spot size (RSS)
6.562.42 8.65 1,18 0.009
HO RSS [ﬁrst small] 0.980.84 7.01 2,18 0.006
[second small] 1.060.83
Red spot area of
foster mother (SFF)
0.0140.015 0.01 1,18 0.90
RSS SFF 0.0320.011 8.71 1,18 0.0085
A. Velando et al. / Animal Behaviour 85 (2013) 1359e1366136 6