The Journal of Experimental Biology 214, 1463-1472 2011. Published by The Company of Biologists Ltddoi:10.1242/jeb.050153
Benefits associated with escalated begging behaviour of black-billed magpie
nestlings overcompensate the associated energetic costs
David Martín-Gálvez1,2,*, Tomás Pérez-Contreras1,2,3, Manuel Soler2,3 and Juan José Soler1,2
1Departamento de Ecología Evolutiva y Funcional, Estación Experimental de Zonas Áridas (CSIC), 04120 Almería, Spain, 2Grupo
de Coevolución, Unidad Asociada al CSIC, Universidad de Granada, 18071 Granada, Spain and 3Departamento de Biología Animal,
Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain
*Author for correspondence (firstname.lastname@example.org)
Several experimental results support the existence of costs associated with exaggerated begging behaviour, which are assumed
by some theoretical models of honest signalling in parent–offspring communication. However, to understand how honest begging
behaviour is evolutionarily maintained in nature, the long-term cost–benefit output associated with exaggerated signals should
also be estimated. As far as we know, the net cost–benefit balance of begging display has not previously been explored. Here, we
used an appetite stimulant, cyproheptadine hydrochloride, to increase the feeling of hunger in some magpie nestlings. Supporting
the use of cyproheptadine to manipulate hunger level and thereby begging behaviour, we found that experimental nestlings
increased the frequency of begging and received more food than their control nestmates. Contrary to the expectation that
physiological costs per se counteract the associated benefits of escalated begging signals, we found that near-fledging
experimental magpies showed a better physical condition than control nestlings. These findings stress the interesting question
of why magpie nestlings do not show to adults an escalated level of hunger if it implies an advantage. We discuss the
responsibility of inclusive fitness costs and indirect genetic effects for the maintenance of honesty in parent–offspring
Key words: begging behaviour, black-billed magpie, costs and benefits of begging, cyproheptadine, food allocation, honest signalling,parent–offspring conflict, Pica pica.
marginal fitness gain experienced by an offspring from receiving
Offspring are genetically different to their parents, and gaining more
the next unit of parental investment [but see Mock et al. (Mock et
parental care than parents are selected to provide is of selective
al., 2011) for a review about other two active-choice alternatives].
advantage (Trivers, 1974). Since this parent–offspring conflict was
According to Godfray’s model, parents would preferentially feed
proposed, several models have tried to explain its resolution in
those offspring showing the most intense signals because they would
general and the evolution of conspicuous and extravagant offspring
signals during solicitation of care in particular (for reviews, see Mock
Three predictions are generated from this hypothesis (see Kilner
and Parker, 1997; Godfray and Johnstone, 2000; Budden and Wright,
and Johnstone, 1997; Royle et al., 2002): (1) parental investment
2001; Johnstone and Godfray, 2002). A group of these models
is regulated according to offspring signals; (2) the intensity of
suggests that the conflict can be solved by the existence of costs
the begging signal varies according to offspring need; and (3)
associated with offspring solicitation signals that are constraining
begging signals should be costly to produce. There exists a
their expression. The alluded costs include physiological costs of
substantial experimental and empirical body of results supporting
production of signals and costs related to risk of predation and loss
parent use of offspring begging behaviour to adjust feeding effort
of indirect fitness (e.g. depriving relatives – either nestmates or future
and to allocate food within the brood (e.g. Smith et al., 1988;
unborn siblings – of food) (Godfray and Johnstone, 2000). In this
Ottosson et al., 1997; Kilner and Johnstone, 1997; Burford et al.,
situation, dishonest begging behaviour would not be compensated
1998) (but see Clark and Lee, 1998). However, although
by the extra benefits gained (i.e. more food). Parents, thus, would
considerable evidence also exists about the relationship between
be able to use these honest signals actively to properly adjust their
begging intensity and levels of food deprivation and offspring
effort as well as the food allocation among siblings (active-choice
condition (Redondo and Castro, 1992b; Price et al., 1996;
Mock et al., 2011), or passively by feeding the
Iacovides and Evans, 1998; Sacchi et al., 2002), it is still not clear
offspring that emerges victorious from scramble competition
how food deprivation (i.e. hunger) and offspring condition are
(Rodríguez-Gironés et al., 2001a; Parker et al., 2002) or negotiation
related to offspring need as defined by Godfray (Godfray, 1991)
(Roulin, 2002) among siblings. Between the active-choice models,
[see Mock et al. (Mock et al., 2011) for a further disscussion about
the most widely recognized is that developed by Godfray (Godfray,
this issue]. With regard to costs associated with offspring begging
1991; Godfray, 1995a; Godfray, 1995b), which assumes that
behaviour, its existence is not widely supported and sometimes
begging signals could be reflecting offspring need, defined as the
is controversial (reviewed in Kilner and Johnstone, 1997; Budden
and Wright, 2001; Wright and Leonard, 2002; Moreno-Rueda,
1967). Cyproheptadine is broadly used in humans, including
children, as a safe and effective appetite stimulant (Chinuck et al.,
Perhaps the clearest support for the costs of escalated begging
2007; Couluris et al., 2008; Mahachoklertwattana et al., 2009). It
behaviour comes from several articles showing that predation risk
is also often used in other animals, mainly in cats (see e.g. Plumb,
can constrain begging expression (especially offspring vocalizations)
1999), and its property as appetite stimulant has also been manifested
(e.g. Redondo and Castro, 1992a; Haskell, 1994; Haskell, 2002;
in two bird species, domestic fowl (Gallus domesticus
) (Injidi and
Leech and Leonard, 1997; Briskie et al., 1999; Dearborn, 1999) and
Forbes, 1987; Muralidharan et al., 1998) (but see Rao and
from four articles giving support to the existence of physiological
Varadarajulu, 1979) and domestic pigeons (Columba livia
costs associated with begging signals (Kilner, 2001; Rodríguez-
(Gunturkun et al., 1989). The use of this methodology allows
Gironés et al., 2001b; Moreno-Rueda, 2010; Noguera et al., 2010).
nestlings to be raised in their natural nests being fed by their parents.
Predation costs of begging signals are based on the possibility that
Thus, and conversely to traditional methodologies based on food
predators could more easily detect nests that contain nestlings that
deprivation to increase begging signals, this experimental approach
beg loudly. However, in broods with more than one nestling,
allows us to estimate variables related to the net balance between
predation costs would be shared by the entire brood because, once
benefit and costs (e.g. fledging performance) associated with the
a nest is located, all nestlings will probably be eaten. For this reason,
predation costs would hardly explain individual differences in
The aims of this experimental study were to test three different
intensity of begging signals among nestlings within a brood and,
methodological and theoretical predictions: (1) cyproheptadine, by
thus, this cost would not prevent an escalation of dishonest nestling
increasing the level of hunger of nestling, also increases the intensity
behaviour [see Rodríguez-Gironés et al. (Rodríguez-Gironés et al.,
of begging signals (frequency and/or intensity of begging); (2) the
2001b) for further discussion]. Regarding the physiological cost of
enhanced beggars receive more food from the parents than their control
escalated begging, the first two articles from the four referred to
nestmates; and (3) if physiological costs associated to signals are at
above have shown the existence of negative effects on nestling
least partially responsible for maintenance of honesty in signalling,
growth in canaries (Serinus canaria
) (Kilner, 2001) and black-billed
the energetic net balance of an exaggerated begging behaviour should
magpies (Pica pica
) (Rodríguez-Gironés et al., 2001b); the third
be negative for enhanced beggars. We addressed these predictions
article gives support to the immunological cost of exaggerated
by using four different methodological approximations. First, we
begging signals in the house sparrow (Passer domesticus
video-recorded the behaviour of magpie nestlings and adults in their
Rueda, 2010); and the fourth provides evidence about the oxidative
nests in order to determine whether nestlings treated with
cost of begging in yellow-legged gulls (Larus michahellis
cyproheptadine beg more (frequency and/or intensity) and whether
et al. 2010). In the first three studies, experimental nestlings were
they are preferentially fed over their control nestmates. Second, in
forced to beg for food at a higher rate than control nestlings (different
laboratory conditions, we estimated the effect of experimental
costs) and both groups received the same amount of food (same
treatment and food deprivation time on the begging behaviour of
benefits) (Kilner, 2001; Rodríguez-Gironés et al., 2001b; Moreno-
nestlings. Third, in natural conditions, we quantified the amount of
Rueda, 2010). The fourth study showed an increased begging display
food received and change in body mass (used as an index of begging
of nestlings experimentally supplemented with vitamin E, possibly
effort) for control and experimental nestlings for a period of 2.5h.
because of the reduced oxidative cost of begging (Noguera et al.,
Finally, we estimated the effect of our experimental treatment on
2010). Nonetheless, these experimental approaches do not allow the
variables related to nestling probability of recruitment, such as T-cell
estimation of net cost–benefit output of the exaggeration of begging
immune response (e.g. Møller and Saino, 2004; Cichon and Dubiec,
behaviour, nor do they allow us to determine whether exaggerated
2005; Moreno et al., 2005), body size (lengths of tarsi, wings and
begging behaviour is cost-effective in the sense of garnering more
tails) and body mass (e.g. Magrath, 1991; Gebhart-Henrich and
energy than the signal’s transmission expends. Parents, following
Richner, 1998; Schwagmeyer and Mock, 2008).
the exaggerated signal of ‘selfish’ offspring could evenovercompensate energetic costs associated with the production of
MATERIALS AND METHODS
the signal. Thus, it is possible that, even assuming extra costs, a
Study area and species
certain level of exaggeration could still be advantageous for
Fieldwork was performed in two close localities of southern Spain
offspring. Theoretical studies modelling the evolution of honest
during the springs of 2002–2003 and 2008: in the Hoya de Guadix
begging behaviours refer to the net balance between benefits and
(37°14ЈN, 3°11ЈW) and in Iznalloz (37°25ЈN, 3°33ЈW), respectively.
costs, rather than merely the costs of signals, as the keystone that
The Hoya de Guadix is a high-altitude plateau (~1000m above sea
predicts honesty in parent–offspring communication (e.g. Godfray
level) with cereal crops (especially barley, Hordeum vulgare
and Johnstone, 2000). Therefore, the experimental increase in
alternate with more or less dispersed plots of almond groves
offspring solicitation signals in natural conditions and the estimation
) or holm-oak trees (Quercus rotundifolia
of the net physiological cost–benefit balance of this manipulation
are preferentially used by magpies to build their nests (for details,
are important for the understanding of the evolution of honest
see Soler, 1990). Iznalloz has an undulated landscape mainly
consisting of small patches of holm-oak forest coexisting with
In the present study, we performed such an experiment in black-
plantations of olive trees (Olea europea
). In this population, magpies
billed magpies, one of the two bird species in which the cost of
prefer to build their nests mainly in holm-oak trees and secondarily
exaggerated begging behaviour on nestling growth has been reported
(Rodríguez-Gironés et al., 2001b). Briefly, we increased the hunger
The black-billed magpie (Pica pica
Linnaeus 1758) is a territorial,
level in some nestlings within broods by the administration of an
sedentary and relatively long-lived passerine bird with a well-studied
appetite stimulant, cyproheptadine hydrochloride, which affected
biology (reviewed in Birkhead, 1991). It occurs throughout large
begging behaviour (see Results). This pharmaceutical is a type 2
parts of the Holarctic region where, in some places, it becomes
serotonin receptor antagonist, which directly acts on the hunger
abundant. Magpies lay a single clutch between March and May with
centre at the hypothalamus (Stone et al., 1961; Chakrabarty et al.,
five to seven eggs (range3–10). The female starts to incubate before
clutch completion (usually once the fourth egg is laid); this results
(0.32mgml–1) (Injidi and Forbes, 1987). After the first dose (at first
in broods that hatch asynchronously where some of the smallest
weighing, 2–4days old), we revisited nests every 2days to recolor
nestlings may starve soon after hatching (Birkhead, 1991).
the tarsi, weigh the nestlings and supply them with the experimentalor control doses. Survivor nestlings received the treatment with
General field procedures
cyproheptadine or water on alternative days and on six occasions,
At the beginning of the breeding season (end of March to early
except those used for video recordings (see below), which received
April), we intensively searched the study areas to find the location
treatment on five occasions, i.e. until they were filmed.
of new nests. Once a new nest was detected, we visited it regularlyto determine the laying date. During the laying period, nests were
checked at least twice per week to determine laying date, clutch
When required for analysis, outcome variables were graphically
size and the occurrence of brood parasitism by the great spotted
checked for normal distribution of their frequencies (density and
cuckoo (Clamator glandarius
), which is common in these areas
normal probability plots) and, if necessary, ln-transformed. Data
(Soler and Soler, 2000). We used magpie nestlings from natural
from video recordings, laboratory and neck-collar trials were
non-parasitized broods (natural broods) and from experimental
analysed mainly with linear mixed models (LMMs) and generalized
parasitized broods, where two magpie and two great spotted cuckoo
linear mixed models (GLMMs) in R version 2.9.2 (R Development
nestlings shared the nest during development (parasitized broods).
Core Team, 2009) using lme4
(R package v.0.999375-31) (Bates
Parasitized broods were also created to study the begging behaviour
and Maechler, 2009), and were fitted by the restricted maximum
of great spotted cuckoos in comparison with that of nestling hosts;
likelihood and Laplace approximations, respectively. For LMMs,
however, we only used data from magpie nestlings from these
we used Markov-chain Monte Carlo (MCMC) simulations
parasitized broods for the present study.
performed by using the pvals.fnc
command of languageR
Magpie nestlings in natural broods were weighed 2–4days after
2008) to compute the highest posterior density (HPD) 95%
hatching (Pesola spring balance, accuracy 0.1g; Pesola Ag, Baar,
confidence intervals (CI) of the model estimates and P
Switzerland) and marked by painting the tarsus with non-toxic
MCMC simulations (P
MCMC). The chain length for MCMC sampling
waterproof pens of different colours (Mitsubishi Pencil, Rubí,
was fixed at 10,000. For GLMMs, we used Wald-Z
Barcelona, Spain). Nestlings were ranked according to their mass
hypothesis testing. All first-order interactions were initially included
and alternately assigned to the experimental and control treatments.
in the model; the non-significant interactions were later removed
Thus, we created pairs of experimental–control chicks of similar
to improve model parsimony (Zuur et al., 2009). To analyse the
mass within broods (nestling dyads). In this way, we could use paired
effect of cyproheptadine on the physical condition of magpie
statistical tests to reduce the within-nest variance due to other
nestlings, we used general linear models (GLMs) with a repeated-
variables such as body size and competitive abilities of nestlings.
measures design. GLMs were performed in Statistica version 8.0
Further, we alternated the order of assignment of the experimental
(StatSoft Ibérica, Lisbon, Portugal). All tests were two-tailed and
and control treatment between consecutive nests; thus, the heaviest
values in text and tables are reported as means ± s.e.m.
nestling was assigned to the experimental treatment in some broodsand to the control treatment in others. Parasitized broods were also
Video recordings in the field
created when nestlings were 2–4days old both in magpie nests that
Between May and July 2008 and when nestlings were 10–12days
were naturally parasitized by great spotted cuckoo (26 broods) and
old, we filmed nestling begging behaviour and food delivery by
in unparasitized magpie nests (18 broods). The magpie nestlings
parents in 16 non-parasitized magpie nests (natural broods). We used
used in each experiment came mainly from the same magpie brood
a wireless microcamera (KPC-S500, black and white CCD camera,
(in 39 of 44 experimental broods); they were randomly selected
eSentia Systems Inc., Baton Rouge, LA, USA), a hard disk device
from those that hatched within the first or second day of hatching
media recorder (EMTEC, Gennevilliers, France) and a 3inch
and had masses similar to those of cuckoo nestlings. However, and
portable monitor. Before filming, nestlings were administered with
because it is difficult to find two cuckoo nestlings of similar mass
their fifth doses (cyproheptadine or water) and weighed. Nestlings
in the same magpie nest, the two cuckoo nestlings came mainly
were individually marked with a unique combination of white points
from two different nests (36 of 44 experimental broods). Similar to
drawn on the crown using correction fluid (Tipp-Ex). These marks
natural broods, nestlings were ranked within species and we
have a similar appearance to excremental remains, which sometimes
alternated the order of assignment of experimental and control
can be found on nestlings. The mean duration of the video recordings
treatment between nests. In this case, we alternated the four possible
was 3:27h (range2:23–4:39h), resulting in a mean of 5.5 adult
combinations: the heaviest nestlings of each species received the
visits per hour (range2.9–9.3visitsh–1).
same treatment or the heaviest nestlings of each species received
We watched the video recordings using TMPGEnc DVD Author
3 software (Pegasys Europe, London, UK), which allows forward
Treatments consisted of oral administration (by a plastic 1ml
and backward frame stepping. During the visits by the adults, we
syringe) of 0.1mg cyproheptadine hydrochloride (Acofarma, Inc.,
noted whether each nestling begged (begging) (i.e. if the nestling
Barcelona, Spain) diluted in 0.25ml mineral water to the
responded to the adult visit by at least opening its mouth towards
experimental nestlings every 2days (i.e. 0.05mgday–1). Control
the adult), received food or defecated (faeces). Magpies have a
nestlings were administered with 0.25ml mineral water. We
throat pouch used to carry food items to the nest, and thus we could
calculated the dose of cyproheptadine based on that recommended
not directly quantify the amount of food received by each nestling
for children (0.4mgkg–1day–1) (Peisker, 2000) and extrapolated to
from video recordings; however, this was estimated using neck
a nestling of 100g. This dose was similar to that previously used
collars (see below). We also ranked: (1) nestling body position in
in chickens (average dose was ca.
0.5mgkg–1day–1) (Rao and
the nest with respect to distance to adult location (nest position),
Varadarajulu, 1979; Injidi and Forbes, 1987; Muralidharan et al.,
(2) height of nestling head whilst begging (height), and (3) the order
1998). Drug dilution was also the same as that used for children
in which each nestling begged in relation to nestmates (order). Two
(0.4mgml–1) (Peisker, 2000) and similar to that used in chicken
or more nestlings had the same rank value when differences
between them were not easily discernible. Because both brood sizes
Table 1. Results from the analyses of video-recordings in magpie
vary among nests (as does the number of begging nestlings within
nests to assess the effect of treatment with cyproheptadine on
nests), we standardized ranking values of nest position, height and
begging behaviour and adult food allocation
order by the formula: (rank–1)/(N
–1) (modified from Smith and
Montgomerie, 1991), where N
equals brood size for the variable
nest position, or the number of nestlings that begged during the
adult visit for the variables height and order. Standardized values
therefore vary between 0 and 1, so those values closest to 0
correspond to nestlings relatively close to the adult, the highest
In order to reduce within-nest variance, we analysed the effect
of cyproheptadine treatment within nestling dyads (i.e. paired tests);
further, to homogenize nestling mass within dyads, we only used
those dyads with nestling mass differences <15g (18 nestling dyads
belong to 11 different nests). Differences in mass between nestlings
within dyads were on average 6.37±0.98% of nestling mass.
Thereby, we compared nestlings with similar competitive abilities.
In such a situation, begging behaviour within a nestling dyad is
assumed to reflect individual differences in interest in receiving food,
independently of whether parent or offspring has total control over
food distribution (see Royle et al., 2002). We have no data about
whether parents or offspring control food distribution during video
recordings. However, nestling behaviours associated with sibling
negotiation or sibling competition should also be constrained by
their associated costs [as is suggested by Royle et al. (Royle et al.,
2002) and Johnstone and Roulin (Johnstone and Roulin, 2003)].
Therefore, the net balance of costs and benefits associated with
escalated begging behaviour could be estimated using our
Analyses are generalized mixed linear models (GLMMs) for begging (788
methodology independently of whether parent or offspring has
observations in 229 adult visits) and linear mixed models (LMMs) for order
control over food distribution. The effect of our treatment on begging
(580 observations in 217 adult visits), height (573 observations in 217
and faeces was analysed using binomial GLMMs, and the effect of
adult visits) and nest position (579 observations in 217 adult visits). Nest
the experimental treatment on the nest position, height and order
identity (11 different nests) and nestling dyad* (nested in nest identity, 18
was estimated using LMMs.
Nest identity and nestling dyad (nested
different nestling dyads) were used as two random factors, whereas
in nest identity) were used as random factors, whereas experimental
experimental treatment, time from the last feeding received (time withoutfood) and nestling mass were included as covariates. For GLMMs, we
treatment, standardized time [(x
–mean)/s.d.; in frames,
also included the number of nestmates competing for food (nestmates
1frame0.04s) from the last feeding received (time without food)
begging) as a further covariate. We used Wald z-tests [z-values and
and nestling weight (g) were included as covariates. For GLMMs,
Pr(>͉z͉)] for GLMMs, and for LMMs we estimated the highest posterior
we also included the number of nestmates competing for food in a
density 95% confidence intervals (HPD 95% CI) and P-values (PMCMC)
given adult visit (nestmates begging) as a further covariate. The
from Markov-chain Monte Carlo (MCMC) simulations.
success of nestlings begging for food was analysed using a GLM
*Nestling dyad, one experimental and one control nestling from the same
with the percentage of feedings each nestling received relative to
the number of adult visits in which it begged as a dependent variable,experimental treatment as a within factor, the mass differences within
piece of fabric to avoid any visual stimulation that could cause the
nestling dyad as a covariable and nest identity as a fixed factor.
nestlings to beg. Early in the morning, each nestling was satiatedwith a mixture of commercial nestling food with water and raw cow
Estimations of begging behaviour in the laboratory
heart. After 1h, each nestling was separately stimulated to beg for
During May and June 2003 and late in the evening (between 20:00
food, but was not fed. We encouraged nestlings to beg by gently
and 21:30h), 50 magpie nestlings (8–10days old) from 22
touching the border of the nest, whistling three times (the stimulus
experimental nests (nine natural broods and 13 parasitized broods)
that we previously used to feed the nestlings) and moving our fingers
were moved to our laboratory (~30min by car). We used only one
above their heads for 35s. Nestlings were encouraged to beg every
magpie nestling dyad from the same nest, except for three natural
20min eight times (begging trials), except for three nests where
broods where we used two nestling dyads per nest. When necessary,
nestlings were only stimulated seven (one nest) and five times (two
nestlings from non-experimental nests were placed in the
nests). After each begging trial, we again covered the experimental
experimental nests in place of those removed in order to prevent
nestlings to prevent any further begging efforts by the experimental
adults from abandoning the nests. Once in the laboratory, the
nestlings. During these begging trials, we were blind to the treatment
nestlings were administered with their fourth dose of cyproheptadine
or water and weighed on a portable digital balance (Sartorius
Nestling behaviour during begging trials was video-recorded.
Portable PT600, precision ±0.01g; Data Weighing Systems Inc.,
Afterwards, video recordings were watched to collect information
Elk Grove, IL, USA). Nestlings were kept separately overnight in
on the following variables: begging (nestling responded to the
artificial nests in a soundless room and under a heating lamp (30
stimulus at least by opening its mouth towards our fingers); begging
to 35°C). The artificial nests consisted of metal nest-shaped moulds
calls (nestling emitted a sound when begging); body posture
lined with raw cotton. Each artificial nest was covered with a small
(nestling had its tarsi extended for begging); and begging duration
[time (s) that the nestling spent begging in each trial]. After the
Neck-collar trials were performed in 2002 (18 and 41
begging trials, nestlings were again fed until they were satiated.
experimental nests with data for biomass received and body mass
Differences in begging behaviour between experimental and control
loss, respectively) and 2003 (15 and 29 experimental nests with data
nestlings were tested using binomial GLMMs (response variables:
for biomass received and body mass loss, respectively). Nonetheless,
begging, begging calls and body posture) and LMMs (response
we decided to pool data from these two years because no significant
variable: begging duration) with nestling treatment (cyproheptadine
differences between years appeared with respect to biomass received
or water) and brood type (i.e. natural or parasitized broods) as fixed
per nestling (LMM, year effect: HPD 95% CI of ln-transformed
factors, and time (min) from the beginning of the experiment and
values–0.84 to –0.37mgh–1, P
MCMC0.44) or body mass loss
nestling mass as covariates. Nestling dyad was included in the model
during the experiment (LMM, year effect: HPD 95% CI of ln-
transformed values–0.38 to 0.03gh–1, P
During all trials, faecal sacs were removed and weighed on a
the effect of the experiment did not differ significantly between years
portable digital balance (precision ±0.01g). Although nestlings
for biomass received (LMM, interaction between year and treatment
defecated mostly during the hand-feeding performed after begging
factors: HPD 95% CI–1.10 to 0.54mgh–1, P
MCMC0.46) or body
trials, we used data from all faeces successfully weighed.
mass loss (LMM, interaction between year and treatment factors:HPD 95% CI–0.16 to 0.40 gh–1, P
MCMC0.44). Besides treatment,
year and its interaction, nestling mass (g) before the neck-collar
During May and June 2002 and 2003 and when nestlings were
trial began was also included as a covariate in these analyses.
~10–12days old (i.e. after their fifth dose), we placed neck collars
The food deprivation during begging trials performed in the
on all the chicks in a group of parasitized and natural broods. The
laboratory (see above) reproduces that suffered by nestlings with
ligature wire around the neck was tight enough to hinder the
neck collars in the field (i.e. begging but not getting food, see below).
swallowing of food and loose enough to avoid strangling the chicks
In field conditions, adult magpies removed faecal sacs from the nest;
[see Soler et al. (Soler et al., 1995) for a further description of the
thus, it was not possible to know the mass of faecal sacs produced
neck-collar method in magpies]. Nestlings wore the neck collar for
during the neck-collar trials. By weighing faecal production of
a period of 2 to 2.5h. This period is ~1h shorter than that previously
experimental and control nestlings during the laboratory trials, we
used in magpies (Soler et al., 1995). Although this shorter
were able to test whether any change in body mass of experimental
experimental period may reduce the hypothetical differences
and control nestlings in natural nests with neck collars could be due
between nestlings of different treatments, it may also reduce the
to previous experience (i.e. food processing in the digestive tract),
possibility of some nestlings regurgitating boluses of food. The food
and whether faecal production was related to nestling body mass
that was delivered by parents to each nestling during neck-collar
(see below). We analysed the relationship between the mass of faecal
trials was kept in absolute ethanol until it was analysed in the
sacs produced during laboratory trials and nestling mass by
laboratory. Biomass of food received by each nestling (mg) was
estimating the correlation coefficient; moreover, we tested the
estimated by dry mass of food samples. Food samples were placed
possible effect of experimental treatment on faeces production (see
in an oven at 60°C for a period of 24h (i.e. until a constant mass),
above) by performing a GLM analysis with treatment as a fixed
after which they were weighed (Adam equipment 120/0.0001g;
factor, nestling mass as a covariable and mass of faecal sacs as the
Adam Equipment Co. Ltd, Bletchley, UK). Nestlings were weighed
outcome variable. Sample sizes were, in this case, reduced to 41
at the beginning and end of the neck-collar trial and change in body
nestlings because in nine nestlings some of the faecal sacs leaked
mass was calculated accordingly. Differences in body mass
before they were weighed. Nestling mass was positively correlated
(before–after the experiment) and biomass of food received were
with the mass of the faecal sacs produced during the laboratory trials
standardized by dividing by the duration of the experiment (h).
0.035), whereas the experimental
Because a gain in nestling body mass during neck-collar application
treatment did not explain a significant proportion of the variance in
would mean that the neck collar was not correctly placed, we only
mass of faeces (F
0.81). Similarly, during the video
used data from those nestlings that lost weight during neck-collar
recordings of the magpie nests in natural conditions, we found that
trials. In only 16 of 226 cases did nestlings maintain or gain mass
probability of nestling defecation in a given adult visit was
during neck-collar trials. Moreover, we only used in the analyses
significantly and positively related to nestling mass [binomial
those nests with data from at least one control and one experimental
GLMM, nestling mass effect (estimate ± s.e.m.): 0.026±0.005,
magpie nestling. Differences in body mass were also used as an
|)0.003, 705 observations (i.e. whether a nestling
estimate of begging effort of nestlings (e.g. Kilner, 2001) during
defecated during a visit), 209 adult visits, 18 nestling dyads in
11 nests], whereas experimental treatment did not affect the
Nests in which regurgitated boluses of food were detected in the
probability of nestling defecation (binomial GLMM, treatment effect
nest cup (i.e. they could not be assigned to nestlings) were not
(estimate ± s.e.m.): –0.014±0.202, z
–0.069, Pr(>|z|)0.95, 705
included in the analyses and, similar to body mass loss, we included
observations, 209 adult visits, 18 nestling dyads in 11 nests).
in the analyses only those nests with data from at least one control
Therefore, the inclusion in the models of the nestling masses before
and one experimental magpie nestlings (i.e. excluding zeros).
the neck-collar experiment allowed us to statistically control the
Consequently, sample sizes for biomass received (33 nests; 17
variation in faecal-sac production among nestlings during the neck-
natural broods and 16 parasitized broods) and body mass loss (59
nests; 31 natural broods and 28 parasitized broods) differed. Weused LMMs to explain the effect of the experiment on ln(biomass
Physical condition of magpie nestlings
of food received) (mg) and ln(change in body mass) (g) per hour
During May and June 2002, we estimated the physical condition of
and per nestling. Nest identity was included in the models as a
control and experimental nestlings from natural broods close to
random factor, brood type (i.e. natural or parasitized broods) as a
fledging time (ca.
18days old). We measured nestling mass (spring
second fixed factor and nestling mass (g) before the neck-collar trial
balance, 300g ±1g), lengths of tarsi (with a digital calliper,
±0.01mm), wings and tail (using a ruler, ±0.1cm), and cell-mediated
immune response estimated from values of skin swelling elicited by
Table 2. Results of comparisons between begging behaviour of
injection of the mitogen phytohemagglutinin (PHA) (reference no.
nestlings with an experimentally increased level of hunger and
L8754, Sigma Chemical Co., St Louis, MO, USA) (see Tella et al.,
control nestlings with no treatment during the laboratory trials
2008). Briefly, we injected fledglings subcutaneously in the right
wing web with 0.5mg of PHA dissolved in 0.1ml of physiological
saline solution (Bausch and Lomb). As a control, the left wing web
was injected with 0.1ml of physiological saline solution. Before and
24h after injection, we measured the thickness of each wing web at
the injection site with a pressure-sensitive digital micrometer (model
547-301, ±0.01mm; Mitutoyo, Andover, Hants, UK). The immune
response variable was then estimated as the change in swelling of
the right wing web minus that of the left wing web (Lochmiller et
al., 1993). We repeated measurements of each wing web three times
and used the mean values in our analyses.
For these analyses, we used a repeated-measures analytical
approach to check the possibility that the treatment effects were
influenced by nestling hierarchy in body mass. We only used
natural broods where at least the two heavier nestling dyads had
survived to this age (N
37 nests). In order to obtain the balanced
statistical design needed for repeated-measures analyses, only data
from these two nestling dyads were used. We included the
experimental treatment as the first within factor, and the assigned
rank in the body mass hierarchies of nestling (i.e. first or second
heaviest nestlings within each treatment) as the second within
factor. This design allowed us to determine whether the treatmenteffect was different for different nestling hierarchies (interaction
factor). We used a Sigma-restricted model to code categorical
factors and the type VI [the effective hypothesis method (Hocking,
1996)] to get the sums of squares. Moreover, we performed a
repeated-measures multivariate ANOVA (RM-MANOVA) by
using the same design but including all dependent variables
Analyses are GLMMs for begging (374 observations in 25 groups), begging
calls (332 observations in 25 groups) and body posture (327 observationsin 25 groups); and LMMs for begging duration (327 observations in 25
groups). Nestling treatment and brood type (i.e. natural or mixed broods)were included in the model as fixed factors, and time from the beginning of
Effect of cyproheptadine on begging behaviour and food
the experiment and nestling mass were included as covariates. Nestling
allocation during video recordings in magpie nests
dyad was considered as a random factor. For GLMMs, we used Wald z-
We found a statistically significant association between
tests for hypothesis testing [z and Pr(>͉z͉)]. For LMMs, we estimated the
experimental treatment and probability of begging during adult
visits (begging; Table1). Nonetheless, we did not find a significant
effect of cyproheptadine on further variables related to nestlingbegging intensity (nest position, height and order; Table1). In
MCMC<0.001] but lost more body mass
relation to food allocation by magpie adults, we found that the
[LMM, with ln(body mass lost) as the dependent variable, nestling
proportion of parent visits where nestlings were fed relative to the
mass effect: HPD 95% CI0.003–0.01 gh–1, P
total of visits where they begged was greater for the experimental
the standardized time of the experiment. After controlling for the
nestlings (46.81±2.62%) than for their control nestmates
allometric effects of nestling mass before trials and the possible
(40.47±2.33%; GLM, treatment effect: F
effect of brood type (see Materials and methods), experimental
suggests that experimental nestlings were more efficient when
nestlings received more food [LMM with ln(food received) as the
begging for food than control nestmates.
dependent variable, treatment effect: HPD 95% CI1.82–
MCMC0.0004; Fig.1] but lost more body mass [LMM
Effect of cyproheptadine on begging behaviour during
with ln(body mass lost) as the dependent variable, treatment effect:
HPD 95% CI0.03–0.31gh–1, P
MCMC0.015; Fig.1] than control
Results from the laboratory were similar to those obtained from
video recordings in the field. Nestlings experimentally provided withcyproheptadine begged more frequently than their control nestmates
Effect of cyproheptadine on the physical condition of magpie
(begging, treatment effect; Table2). The probability of emission of
sound (begging calls), body posture during begging and time of
Magpie nestlings experimentally treated with cyproheptadine
begging during a certain trial (begging duration) were not correlated
showed a better physical condition than control nestlings when they
with the experimental treatment (Table2).
were ~18days old (RM-MANOVA, Wilks’ 0.66, F
0.037). Experimental nestlings exhibited a higher immune
response than their control nestmates (experimental vs
Heavier magpie nestlings received more food [LMM, with ln(food
1.12±0.07mm, GLM: F
0.0497), had a
received) as the dependent variable, nestling mass effect, HPD 95%
longer tarsus (48.0±0.4 vs
47.2±0.4mm, GLM: F
Fig.1. Partial effect of treatments with cyproheptadine
(experimental) or water (control) on biomass received
[mgh–1, N33 nests, effect size (i.e. range)73.88mg] and
body mass loss (gh–1, N59 nests, effect size0.25g) during
neck-collar trials in magpie nestlings. Values were calculated
by back-transformation of estimates obtained from linear
mixed models with ln(biomass received) and ln(body massloss) as dependent variables. Values are means ± highest
posterior density (HPD) 95% confidence intervals.
wing (81.9±1.5 vs
79.8±1.4mm, GLM: F
and Forbes, 1987; Muralidharan et al., 1998) and domestic pigeons
tail (24.6±0.9 vs
23.3±1.0mm, GLM: F
0.045) and a
(Gunturkun et al., 1989), where it resulted in a significant increase
higher body mass (138.3±2.7 vs
132.3±2.9g, GLM: F
of food ingestion. Thus, the use of this drug as appetitive stimulant
0.011). Further, the effect of cyproheptadine was similar in the
was well founded and we tested its effects on begging behaviour
first and second nestling hierarchical dyads (interaction between
treatment and rank of nestling dyad: in all cases P
The use of cyproheptadine as appetite stimulant has several
advantages. It is administered orally diluted in water, and thus the
treatment can be easily done in the field and during short nest visits.
In the present study, by using an appetite stimulant (cyproheptadine
Importantly, experimental nestlings can be administered during
hydrochloride), we have for the first time explored the net
development while they are being fed by their parents, who are the
cost–benefit balance of escalated begging behaviour in natural
receptors of the begging signals. This approach makes possible the
conditions, where the extra costs of begging might be compensated
estimation of variables related to the net cost–benefit balance
by the acquisition of extra resources from parents. In accordance
associated with the experimentally escalated begging behaviour. In
with the widely manifested effects of the level of hunger on begging
addition, experimental nestlings may also suffer from other possible
behaviour, we found that experimental nestlings increased the
sources of energetic costs not directly related to the production of
frequency of begging (but not intensity) and received more food
the begging signals and difficult to take into account in food
than their control nestmates. Our main result was that the net benefit
deprivation laboratory experiments. For example, the effect of
of escalated begging behaviour was positive, i.e. experimental
sibling competition (e.g. Johnstone, 1999; Rodríguez-Gironés,
nestlings showed a better physical condition than control nestlings
1999; Royle et al., 2002; Neuenschwander et al., 2003), the possible
close to the age of nest abandonment. This result suggests that the
costs related to the nestling vigilance for parent arrival (Roulin, 2001)
costs associated with exaggerated begging behaviour do not solely
or those costs suggested for behaviours related to sibling negotiation
counteract associated benefits as suggested and/or assumed by
during the absence of parents (Johnstone and Roulin, 2003).
previous studies (e.g. Kilner, 2001; Rodríguez-Gironés et al., 2001b;
Moreover, because cyproheptadine would exclusively affect hunger
Moreno-Rueda, 2010; Noguera et al., 2010). Below we discuss the
level, this experimental approach allow us to disentangle the effects
methodological approach used for manipulating nestling begging
of body condition and nestling hunger level on begging behaviors
behaviour in natural conditions, as well as the resulting experimental
(e.g. Clark, 2002) to address what offspring are really
effects in a scenario of parent–offspring communication and honest
communicating to their parents via
their begging signals (need,
quality or just hunger) (see Mock et al., 2011).
In accordance with previous results of the effects of hunger
The use of cyproheptadine to increase begging behaviour
level on begging behaviour (e.g. Redondo and Castro, 1992b;
Cyproheptadine is a type 2 serotonin receptor antagonist. It is
Price et al., 1996; Iacovides and Evans, 1998; Sacchi et al., 2002),
assumed that cyproheptadine acts directly on the hypothalamus –
we found that nestlings provided with cyproheptadine begged
cats administered with this drug demonstrated an increased neuronal
more frequently than their control nestmates. In addition, we
activity at this site (Chakrabarty et al., 1967) – by modifying the
found that begging signals of experimental nestlings were more
activity of serotonin on the feeding centre (Delitala et al., 1975).
effective in attracting parental feeding than those of their control
Its action as appetite stimulant appears not to be due to a
nestmates. This suggests the existence of a treatment effect on
hypoglycaemic-induced hyperphagia or an increase in endogenous
non-measured variables of begging intensity. The most important
growth hormones (Bergen, 1964; Stiel et al., 1970). Cyproheptadine
described side effect of cyproheptadine is the reduction of
is broadly used in human patients, including children, that suffer
physical activity because of transient drowsiness, which would
from diseases such as cancer, HIV, cystic fibrosis and eating
predict a reduced rather than an increased begging activity. Thus,
disorders (see Chinuck et al., 2007; Couluris et al., 2008;
the detected effects on begging behaviour are not explained by
Mahachoklertwattana et al., 2009), where an increase in body mass
the drug side effects but by the increased feeling of hunger of
is desirable. Cyproheptadine is also used as an antihistaminic because
it blocks H1 histamine receptors (Stone et al., 1961) and, similar to
other antihistaminic substances, cyproheptadine has minimal side
Evidence of short-term benefits and costs of escalated
effects, consisting mainly of transient drowsiness [see Homnick et
al. (Homnick et al., 2004) and references therein]. In birds, the effect
Experimental nestlings received more food than their control
of cyproheptadine has been tested in two species, chicken (Injidi
siblings did during the neck-collar trials. Therefore, based on our
results on the influence of hunger level on begging behaviour and
resulting differences in mass loss during collar trials, this conclusion
the extensive literature concerning this issue (e.g. Smith and
Montgomerie, 1991; Cotton et al., 1996; Kacelnik et al., 1995;Kilner, 1995; Kölliker et al., 1998), relative to the use of begging
Net cost–benefit balance of exaggerated begging behaviour
by parents to determine which chick to feed (e.g. Smith et al.,
during the nestling period
1988; Ottosson et al., 1997; Kilner and Johnstone, 1997; Burford
If the costs associated with escalated begging behaviour surpass the
et al., 1998) (but see Clark and Lee, 1998), the effect of our
extra benefits, as is assumed by some theoretical models (for
experimental treatment on biomass received during neck-collar
reviews, see Mock and Parker, 1997; Godfray and Johnstone, 2000;
trials by each nestling was probably mediated by a change in
Budden and Wright, 2001; Johnstone and Godfray, 2002; Royle et
begging behaviour associated with the experimentally increased
al., 2002), and the direct costs are physiological and/or energetic,
we should find a negative effect of our experiment on nestling
The neck-collar approach may, however, have methodological
phenotypic quality. Contrary to this expectation, experimental
problems that could affect to the interpretation of the results. For
nestlings showed a better physical condition than their control
instance, feeding decisions of parents might depend on detecting
siblings when abandoning the nest. Briefly, we found that after
food in the nestling’s mouth, or adults might remove non-swallowed
controlling for the effect of body-size hierarchy, experimental
food from one nestling and place it in another chick’s mouth.
nestlings showed a higher immune response and larger body mass
However, rather that predicting more food in the gullet of
and tarsus, tail and wing lengths than their control siblings. Because
cyproheptadine-treated nestlings, the above scenario predicts more
these variables are related to the probability of nestling survival (see
equally distributed food among nestlings. We compared
Introduction and above), these results suggest that magpie nestlings
experimental and control nestlings from the same nest, and thus our
could escalate some aspect of their solicitation signals and gain more
result of experimental nestlings receiving more food than their
resources that are plausibly connected to enhanced personal fitness.
control siblings likely does arise from our experimental approach
Therefore, these results gives rise to an interesting evolutionary
(increased level of hunger). In accordance with this interpretation,
question, namely, why has natural selection not shaped magpie
results from video recordings indicate that parents selected
experimental nestlings among nestlings that beg for food. Parents
Apart from non-functional explanations including physiological
should preferentially feed the hungriest nestlings in the nests (i.e.
or phylogenetic constraints, responses to this question could be
those with more exaggerated begging behaviour); thus, because the
related to the existence of costs other than the energetic costs
hunger level of experimental nestlings was increased, a more
associated with the escalation of begging behaviour and suffered
efficient begging behaviour of cyproheptadine-treated nestlings can
during development. One possibility is the existence of costs related
be predicted. Moreover, during neck-collar trials, nestlings cannot
to risk of predation, because predators would more easily detect
be satiated by parents, and nestlings would therefore beg for food
nests with nestlings that beg loudly (e.g. Redondo and Castro, 1992a;
during more feeding visits than in natural conditions (i.e. video
Haskell, 1994; Leech and Leonard, 1997; Briskie et al., 1999;
recordings). This scenario is therefore the most plausible explanation
Dearborn, 1999; Haskell, 2002). However, and as mentioned
of the resulting larger biomass received by experimental nestlings
previously, these costs are mainly suffered by the whole brood, and
different costs for nestlings that beg and do not beg are necessary
Rodríguez-Gironés et al. reported a delayed growth of magpie
for explaining the evolution of begging behaviour as an honest signal
nestling chicks in relation to experimentally increased begging
[see Rodríguez-Gironés et al. (Rodríguez-Gironés et al., 2001b) for
activity (Rodríguez-Gironés et al., 2001b), which is likely to affect
further discussion], and thus this cost would not prevent an escalation
probability of survival of magpie nestlings (Husby and Slagsvold,
of dishonest nestling behaviour. Further, predation cost would only
1992; Ponz Miranda et al., 2007) (M. Molina-Morales and J. G.
constrain those signals whose exaggeration implies an increased nest
Martínez, unpublished data). This suggests that escalated begging
detectability for predators, as is the case for vocalizations, but not
would be a costly behaviour for magpie nestlings. In our case,
for other kinds of signals such as visual ones. Another cost that
experimental nestlings lost more mass than their control nestmates
might prevent escalation of begging behaviour is that related to the
during the two and a half hours that nestlings wore neck collars
loss of indirect fitness (e.g. Briskie et al., 1994; Johnstone, 1998;
(Fig.1). This result cannot be explained by drowsiness, which is
Lotem, 1998). Bergstrom and Lachmann (Bergstrom and Lachmann,
the main side effect of cyproheptadine (see above) and from which
1998) argued that a cost-free signalling equilibrium is possible
the expected influence on mass loss is just the opposite to that
between parent and offspring if parents and/or siblings pay a
detected (i.e. weight gain) (see Stiel et al., 1970). Another possibility
disproportionally extra cost for dishonest signalling and these
is that, because experimental nestlings may have ingested more food
indirect fitness costs for escalated signallers outweigh the direct
before the experiment, they may also have produced more and/or
benefit that they gain. Other non-explored costs associated with
larger faecal sacs during the time that nestlings wore neck collars.
escalated begging behaviour are those related to the costs of rearing
However, this is unlikely for two reasons. First, our analyses were
dishonest offspring. If begging behaviour has a genetic basis (see
statistically controlled by body mass, a variable that is positively
Kölliker et al., 2000; Kölliker and Richner, 2001; Dor and Lotem,
related to the production of faecal sacs of nestlings in the laboratory
2009), nestlings with an escalated begging display would rear
and in video recordings in the field. Second, experimental treatment
offspring with an escalated begging display. This possibility was
did not explain either faecal weight or probability of defecation. An
proposed by Alexander, who stated that a certain allele causing the
alternative explanation would be that because faecal sac production
dishonest trait in an offspring that, because of its selfish behaviour,
often occurs simultaneously with feeding, the greater mass loss of
receives more than the optimum parental inversion could not spread
experimental nestlings might be the direct consequence of being
because the advantage of this allele to the young offspring would
preferentially fed by parents. We have no data to discount this
be counteracted by the disadvantage of producing dishonest
possibility; therefore, although differences in begging effort between
offspring when adult (Alexander, 1974). Although this idea was
experimental and control nestlings is a tentative explanation of the
controversial (e.g. Dawkins, 1976; Blick, 1977), costs of rearing
offspring with inherited begging behaviour should be added as a
Couluris, M., Mayer, J. L. R., Freyer, D. R., Sandler, E., Xu, P. and Krischer, J. P.
further cost in the equation explaining the maintenance of signal
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Hematol. Oncol. 30
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This research was licensed by the Consejería de Medio Ambiente (Dirección
fibrosis. Pediatr. Pulmonol. 38
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(1992). Postfledging behavior and survival in male and
partially funded by the Junta de Andalucía (RNM 340) and a postgraduate
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