Behavioral
Ecology
The official journal of the
ISBE
International Society for Behavioral Ecology
Behavioral Ecology (2015), 26(4), 1131–1137. doi:10.1093/beheco/arv056
Original Article
Green plants in nests reduce offspring
recruitment rates in the spotless starling
Vicente Polo,a Juan G. Rubalcaba,a and José P. Veigab
aUniversidad Rey Juan Carlos, ESCET, Departamento de Biología, Geología, Física y Química Inorgánica,
Área de Biodiversidad y Conservación, Tulipan s/n, 28933 Móstoles, Madrid, Spain and bMuseo
Nacional de Ciencias Naturales, CSIC, Departamento de Ecología Evolutiva, José Gutierrez Abascal,
2, 28006, Madrid, Spain
Received 8 October 2014; revised 1 April 2015; accepted 3 April 2015; Advance Access publication 1 May 2015.
Although several hypotheses have been proposed to explain the function of fresh green plants in nests of many avian species, the consequences of this behavior on fitness remain poorly understood. In accordance with the nest protection and drug hypotheses, adding
greenery to nests should be naturally selected to facilitate positive fitness effects on offspring. Alternatively, the courtship hypothesis
postulates that green plants function as a sexually selected signal of male attractiveness that might promote female competition for
preferred males. We conducted a long-term study by experimentally increasing the amount of green plants in nests of a wild population
of spotless starlings (Sturnus unicolor). We experimentally decoupled the natural carrying behavior of males in half of the population
and explored the consequences of this manipulation on offspring condition and their rate of local recruitment. Treatment did not affect
the number of fledglings, but it did affect body mass and tarsus in a sexually antagonistic way: a positive effect on female tarsus length
and negative on male body mass. The addition of greenery reduced the probability of local recruitment of both males and females. Our
results suggest that the addition of green plants induces maternal response with complex short- and long-term consequences on the
offspring body condition and recruitment success.
Key words: courtship display, green plants carrying, male ornaments, natural selection, recruitment rate, sexual selection,
Sturnus unicolor.
INTRODUCTION
Nonmorphologic traits specific to males may act in sexually
selected signaling processes during courtship (e.g., Borgia and Gore
1986; Moreno et al. 1994; Duffy and Ball 2002; Polo et al. 2004;
Veiga et al. 2006; Polo et al. 2010). For example, many avian species adorn their nests with a variety of materials, which can act
as an extended phenotype that indicates quality (see Dubiec et al.
2013 for a review). Green plants are one of the materials commonly used by bird species such as storks, ibises, raptors, and herons (Wimberger 1984; Rodgers et al. 1988; Baxter 1996; Smits
et al. 2010; Dubiec et al. 2013). The function of these green plants
carrying behavior has long puzzled biologists (Clark 1991; Hansell
2000) and some hypotheses have been proposed to explain the
functional and evolutionary significance of the trait (Wimberger
1984; Clark and Mason 1985; Rodgers et al. 1988; Clark 1991;
Roulin et al. 1997; Lambrechts and Dos Santos 2000). Some studies support the idea that green plants in nests have positive effects
on nestling health because they reduce the load of ectoparasites
in the nest (i.e., The Nest Protection Hypothesis), or because they
Address correspondence to V. Polo. E-mail: [email protected].
© The Author 2015. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved. For
permissions, please e-mail: [email protected]
directly improve nestling growth and immune response (i.e., The
Drug Hypothesis) (e.g., Wimberger 1984; Clark 1991; Mennerat
et al. 2009; Tomas et al. 2012). Furthermore, evidence in some bird
species suggests that the transport of green plants to nests has an
important function in sexual signaling and courtship (e.g., Feare
1984; Fauth et al. 1991; Brouwer and Komdeur 2004; Tomas et al.
2013).
In the Sturnidae family, the addition of plants to nests is an
ancient behavior that exists across many phylogenetic groups
(Veiga JP, Polo V, Rubalcaba JG, unpublished data). Males of the
European (Sturnus vulgaris) and spotless starling (Sturnus unicolor),
2 related hole-nesting species, carry fresh aromatic herbs, small
branches, and flowers into their nests during nest building and
before the onset of egg-laying (Fauth et al. 1991; Gwinner 1997;
Veiga et al. 2006). However, evidence regarding the function of this
carrying behavior is scarce and controversial in these species. Some
studies on the European starling suggest that greenery has a sanitary effect on nestling growth and body condition (Gwinner et al.
2000; Gwinner and Berger 2005). However, other studies in the
same species and in the spotless starling suggest that green plants
carried by males to nests are mainly related to mate attraction
(Fauth et al. 1991; Brouwer and Komdeur 2004; Veiga et al. 2006).
Behavioral Ecology
1132
In the spotless starling, green nest material conveys important behavioral and physiological effects on female owners. First,
the experimental addition of plants to nests increased the rate of
female-to-female aggressive encounters and their level of circulating testosterone (Polo et al. 2010). Second, females examined the
greenery carried by males and immediately removed all of this
material from their nests (Veiga and Polo 2012). Therefore, the
presence of green plants in the nests may be involved in a sexual
conflict. That is, while greenery might be used by males to attract
females, females on the other hand might be inclined to remove
greenery to prevent female–female competition and thus loss
of fitness. This female removal behavior supports the idea that
green plants mainly function as sources of mate attraction and
mostly serve to convey information on male quality (Feare 1984;
Fauth et al. 1991; Brouwer and Komdeur 2004; Polo and Veiga
2006; Polo et al. 2010; Veiga and Polo 2012). Thus, the greenery
itself and their volatile compounds possibly never enter into direct
contact with the nestlings, which will appear 2 or 3 weeks later.
Therefore, the possible sanitary function of nest green material is
not well supported for the spotless starling.
Avian females may adjust their offspring sex ratio in response to
individual differences in male sexual traits or displays (e.g., Ellegren
et al. 1996; Sheldon et al. 1999). Additionally, females may enhance
their levels of circulating androgens as a consequence of the
increase in intrasexual competition generated by the presence of
more attractive males (Wingfield et al. 1990; Ketterson et al. 2005;
Goymann et al. 2007). Our work with starlings has shown that the
male plant-carrying behavior is one such male trait that can illicit
female responses such as adjustment of offspring sex ratio (Polo
et al. 2004), the level of circulating testosterone of females during
laying (Polo et al. 2010), and their contribution to the decoration
of nests by using big foreign feathers during the incubation period
(Polo and Veiga 2006). These results suggest a complex functional
relationship between endocrinology and behavior and support the
idea that male plant-carrying behavior is a sexually selected display
with different consequences for males and females. In this respect,
the implication on fitness is of great relevance.
In this study, we present the first experimental evidence that
the provisioning of green plants to nests by male spotless starlings
influences their rate of offspring local recruitment (using the offspring rate of local recruitment as a measure of fitness). We used
this species because of their high philopatry (see Veiga and Polo
2002) which allows to discern the future recruitment of fledglings
in natal or in surrounding colonies. Here, we increased the amount
of aromatic fresh green plants in nests and examined the effects
on number and condition of male and female fledglings and their
future recruitment success. An increase of fitness return would
be expected if greenery played a primarily sanitary function that
benefits both sexes, but the greenery-fitness relationship would be
unclear (or there would be a negative relationship) if the main function of the male plant-carrying behavior plays a different role on
sexual selection for males and females.
MATERIALS AND METHODS
Study area and species
The spotless starling is a medium-sized, facultatively polygynous,
and relatively long lived passerine (Cramp et al. 1983; Feare and
Craig 1999; Moreno et al. 1999; Veiga et al. 2002; Veiga and
Polo 2002). Females commonly lay 2 clutches per season; the first
by mid-April and the second near the end of May. During both
reproductive periods, male spotless starlings, like those of the
related European starling, carry herbaceous fresh plants, leaves
of trees, and flowers into their nests during 7–10 days before the
beginning of laying (Gwinner 1997; Veiga et al. 2006). Males use
this material during courtship (Brouwer and Komdeur 2004; Veiga
et al. 2006).
The experimental study was conducted over 4 years (2002, 2004,
2005, and 2006) in a colony of spotless starlings in Manzanares el
Real (40° 45′ N; 3° 50′ W Madrid province, central Spain). The
breeding habitat is a pasture at 1000 m a.s.l. with scattered trees
(ashes, Fraxinus angustifolia, oaks, Quercus pyrenaica, and Holm oaks,
Quercus rotundifolia) with 54 nest-boxes, spaced 30–60 m from one
another, which have been established since 1997. Most nest-boxes
remained occupied during the entire breeding season. Most breeders were banded with an aluminum ring and an individual combination of plastic color rings to allow future identification.
Experimental procedures
We experimentally manipulated the amount of greenery in a total
of 27 nest-boxes during 2002, 2004, 2005, and 2006. The same
amount of nest-boxes was used as controls during each year.
Experimental and control nest-boxes were randomly allocated each
year, and the assignment of a given nest-box was maintained over
consecutive clutches within the same year. We monitored nest construction to estimate the beginning of laying in the colony each
year and, thus, to establish when to start the experimental protocol
(see Polo et al. 2010). For first clutches, we started adding greenery
approximately 10 days before the onset of laying (mean 8.2 days,
range 4–12 days before laying initiation), and for second clutches,
immediately after fledgling of the first brood (mean 6.3 days,
range 3–0 days), mimicking the natural behavior of male starlings.
We ceased greenery addition when the first egg appeared in the
nest-box.
We incorporated daily ca. 10 g of shredded fresh aromatic herbs
of the species added naturally by starlings in this population (mainly
Lavandula stoechas, Santolina rosmarinifolia, Geranium robertianum, and
Lamium purpureum). The amount of plants was similar to the highest amount recorded in nests. Therefore, we simulated the stimulus
within the natural range experienced by starlings in natural conditions, which may prevent complications such as overstimulation
of the immune system (e.g., allergic reactions). Control nest-boxes
were checked daily and the natural greenery added by the male
was not removed. We spent the same daily time in the inspection
and the manipulation of the control and experimental nests to prevent differential stress that could affect prelaying females during the
period of greenery addition (see also Mennerat et al. 2009 for a
similar procedure). Spotless starling females generally removed the
green nesting material, both the plants added by the researchers
and those carried by males. Therefore, we suspect that the experimental protocol did not affect the behavior of the males themselves. The number of polygynous and monogamous males and the
number of secondary females were balanced among control and
experimental nests (mean rate of polygyny: 1.21 vs. 1.23 females
per male in control vs. experimental nests; total number of secondary females: 17 vs. 18 females in control vs. experimental nests). We
considered the primary female the one that started breeding earlier
among the nests controlled by the same polygynous male.
Breeders were captured by means of custom-made traps fitted
into the nest-boxes. Most males were captured in March, during
the beginning of their breeding activity associated with the acquisition and defense of nest-boxes against other males. Females were
Polo et al. • Nest green plants and recruitment rate
1133
captured during feeding when nestlings were 5 days old to minimize the probability of nest abandonment by human disturbance.
Nestlings were sexed, using molecular markers from blood taken
from chicks at 5 days old (see Griffiths et al. 1998), and marked
with a numbered aluminum ring for individual identification.
When nestlings were 16 days old, they were weighed (to the
nearest 0.1 g) and measured (tarsus–metatarsus length, to the nearest 0.01 mm). We recaptured ca. 5–10% of all fledged chicks (418
vs. 414 fledglings in control vs. experimental treatments; Table 1)
as breeders in the future years in the natal colony and in 2 surrounding areas 1 and 2 km apart from the natal colony. These
surrounding areas were also provided with nest-boxes (50 and 150
nest-boxes, respectively). Both colonies were monitored until the
breeding season of 2014, but no experimental or control individuals were recruited beyond the spring of 2010. In total, 75 new
breeders (25 males and 50 females) were recruited out of the 832
fledglings (Table 1). Fifty-four of them bred for the first time in the
natal colony and 21 (6 males and 15 females) bred in the 2 surrounding areas. Most females that were recruited were 1 year old,
while it took 2 or more years to recruit males. All of the recruited
birds, in the natal or in the surrounding colonies, were used in the
analyses. We did not consider 15 juvenile birds that were captured
in the boxes but were not observed as breeders until the present
day. Results did not differ when those individuals were included in
the analyses (effect of treatment on the offspring rate of recruitment was also significant with 75 recruits + 15 non breeding juveniles: χ2 = 4.83, P = 0.020).
The primary sex ratio was male-biased in the experimental nests
in all the years of the experiment: 2002 (results published in Polo
et al. 2004), 2004, 2005, and 2006 (0.50 ± 0.026 vs. 0.43 ± 0.026
mean sex ratio ± SE in control vs. experimental nests; data corrected for common mothers; F1, 225.7 = 4.77, P = 0.03). The effect
of greenery on increasing the proportion of males is consistent and
confirms the previous results found by Polo et al. (2004).
Data analyses
We used linear mixed-effect models to explore the effect of the
addition of green plants to the nests (treatment as a fixed factor) on
the number of fledglings (generalized linear mixed models assuming a Poisson distribution) and on the fledgling body mass and tarsus–metatarsus length (general linear mixed models) of both males
and females (sex as a fixed factor). We consider the mother and the
Table 1
Number of male (M) and female (F) fledglings and postfledgling recruits per treatment (CTR, control and EXP,
experimental) and year
CTR
2002
2004
2005
2006
Total
M
F
M
F
M
F
M
F
M
F
EXP
Fledglings
Recruits
Rate
Fledglings
Recruits
Rate
55
65
30
52
57
55
47
57
189
229
2
11
3
10
7
6
4
5
16
32
0.04
0.17
0.10
0.19
0.12
0.11
0.09
0.09
0.08
0.14
57
69
39
34
58
47
55
55
209
205
0
5
6
4
2
5
1
4
9
18
0.00
0.07
0.15
0.12
0.03
0.11
0.02
0.07
0.04
0.09
Rate represents the total number of recruits per fledged chick.
clutch ID as random factors to avoid pseudoreplication. This structure of random effects allows controlling the nonindependence of
fledglings from the same clutch or from different clutches of the
same mother. Clutch order (i.e., first or second clutches) and year
were included as covariates in the analyses. A Box-Cox transformation was applied to body mass and tarsus–metatarsus length to normalize the residuals of the models. The power parameter for the
Box-Cox was estimated using likelihood-based methods.
The effect of treatment on local recruitment was analyzed by
using a binomial distribution mixed-effects model. We used fledgling body mass, tarsus–metatarsus length and the number of fledglings in the natal nest as fixed effects. Nonsignificant covariates were
removed from the model. Previous studies with the spotless starling
showed that the addition of green plants to the nest increased the
production of males and had sex-specific effects on post-fledgling
dispersal behavior (Polo et al. 2004 and Polo V, Rubalcaba JG, and
Veiga JP, unpublished data). Therefore, the sex of the fledgling was
included as a fixed factor to control for a potential sex-dependent
probability of local recruitment. The structure of random factors
described above was also included in this model. All models were
fitted by using the package “lme4” (generalized mixed-effect models; Bates et al. 2012) in R 3.02.0 software (R Development Core
Team 2012).
RESULTS
Fledgling production
The experimental addition of green plants did not have significant overall effect on fledgling body mass (t = −0.47, P = 0.64)
or tarsus–metatarsus length (t = 1.11, P = 0.27). However, males
from the experimental group had significantly lower body masses
than controls (mean ± SE: 82.2 ± 0.52 g vs. 84.1 ± 0.45; experimental vs. control) although females did not show this reduction (79.5 ± 0.49 vs. 79.3 ± 0.44 g; experimental vs. control;
Interaction treatment × Sex: t = −2.19, P = 0.029; Figure 1a).
Conversely, experimental females had longer tarsus–metatarsus
lengths (30.0 ± 0.06 vs. 29.87 ± 0.05; experimental vs. control)
although tarsus–metatarsus lengths did not differ in males in
relation to treatment (30.4 ± 0.05 vs. 30.4 ± 0.05; experimental
vs. control; Interaction treatment × Sex: t = −2.14, P = 0.032;
Figure 1b). Clutch order was negatively correlated with body
mass (beta = −0.17, t = −10.30, P < 0.001) and tarsus–metatarsus length (beta = −0.01, t = −3.30, P = 0.001).
The treatment did not have any significant effect on the number
of fledglings per breeding attempt (2.50 ± 0.15 vs. 2.58 ± 0.16 fledglings, experimental vs. control; z = −0.9, P = 0.367). Treatments
were unbiased with respect to the hatching date (z = −0.71, P =
0.48).
Post-fledgling recruitment
The probability of local recruitment was significantly lower in the
experimental group (0.065 ± 0.016 vs. 0.118 ± 0.01; experimental vs. control; t = −2.20, P = 0.028; Figure 2 and Table 1). The
probability of recruitment significantly differed between males
and females (0.063 ± 0.012 vs. 0.115 ± 0.015; males vs. females;
t = −2.94, P = 0.003), and it was positively and significantly
related with body mass (t = 2.94; P = 0.02). There was no significant effect of clutch order (t = −2.84, P = 0.41), number of fledglings (t = −0.18; P = 0.85), and tarsus–metatarsus length (t = 0.70,
P = 0.48) on the probability of recruitment.
Behavioral Ecology
1134
(a) 85
n = 189
Fledgling body mass (g)
84
209
83
Females
Males
82
81
80
205
n = 229
79
78
77
CTR
EXP
n = 177
193
Tarsus-metatarsus length (mm)
(b) 30.6
Females
Males
30.4
30.2
183
30.0
n = 229
29.8
29.6
CTR
EXP
Figure 1
Body weight (a) and tarsus–metatarsus length (b) of male and female fledglings in control and experimental treatments (the figure shows parameter estimates
and their standard errors from a mixed-effect model).
Probability of recruitment
0.25
82
0.20
0.15
Control
Experimental
73
112
n = 120
104
104
0.10
110
126
0.05
0.00
2002
2004
2006
2008
Figure 2
Average proportion of post-fledgling recruitments ± SEs in control and experimental treatments each year of the experiment.
Polo et al. • Nest green plants and recruitment rate
DISCUSSION
Fitness consequences of adding herbs treatment
In this study, we provide experimental evidence of a deferred effect
of male behavior (carrying green fresh plants to the nest in days
prior to laying) on fitness return (measured as the success of postfledgling recruitment) in a wild population of birds. Our experiment revealed a negative effect of greenery on the rate of offspring
recruitment that was maintained across years (see Figure 2). This
is a counterintuitive and striking result in the light of the nest protection and drug hypotheses which needs to be explained. The
addition of greenery is a component of male attractiveness in both
starling species (Brouwer and Komdeur 2004; Veiga et al. 2006).
Thus, we have probably decoupled the female perception of the
attractiveness of their mates and increased female–female competition over preferred males (see Polo et al. 2010 for the increase
in female–female competition with the same data of the present
study). Therefore, the negative effect of greenery on the probability of recruitment may be the consequence of those females
unable to withstand higher levels of intrasexual competition.
Although our experimental design was not intended to discard the
presence of a sanitary effect of greenery on nestlings (Wimberger
1984; Clark and Mason 1985; Mennerat et al. 2009), our results
support the hypothesis that green plants may be seen as a signal of
male attractiveness and condition in the context of the courtship
hypothesis (Brouwer and Komdeur 2004; Veiga et al. 2006; Polo
et al. 2010).
The spotless starling, similar to its related species the European
starling, is a hole-nesting bird that routinely reuses the same nest for
years. Earlier studies have proposed that the use of aromatic plants
in hole-nesting species has evolved to prevent high load of parasites
and pathogens of their nestlings (e.g., Wimberger 1984; Clark and
Mason 1985; Clark 1991; Lambrechts and Dos Santos 2000; Petit
et al. 2002; Mennerat et al. 2009). Supporting this hypothesis, green
plants in nests of European starlings have been shown to reduce
bacteria load and to improve fledglings’ immune systems, body
masses, and yearlings’ survival (Gwinner et al. 2000; Gwinner and
Berger 2005). However, experimental studies performed with this
species failed to prove 2 predictions of the nest protection hypothesis: 1) the addition of greenery did not reduce the load of ectoparasites in the nest and 2) the addition of parasites did not increase the
male carrying behavior (Fauth et al. 1991; Brouwer and Komdeur
2004). Nevertheless, they suggested that the fresh plants in the nests
of European starlings mainly served a function in mate attraction
in the context of the courtship hypothesis (Pinxten and Eens 1990;
Fauth et al. 1991; Brouwer and Komdeur 2004; Polo et al. 2010).
This idea is also suggested by the fact that in the spotless starling,
females remove all of this material from their nests during the days
prior to the beginning of laying (Polo et al. 2010; Veiga and Polo
2012), and thus the nestlings are likely never in contact with the
volatile compounds of these plants.
Several reasons may be suggested to explain the detrimental
effect of the fresh herbs treatment on post-fledgling recruitment.
First, greenery is an extended phenotype of males that indicates
quality and attractiveness (e.g., Fauth et al. 1991; Brouwer and
Komdeur 2004). Thus, females of the added green plants group
might increase their level of circulating testosterone to cope with
the increased rate of intrasexual aggressive encounters for the
competition for more attractive males (Polo et al. 2010; see also
Langmore et al. 2002 for the intrasexual competition elevating circulating testosterone in females of Prunella modularis). However, this
1135
female response to greenery has a negative short- and long-term
consequence: experimental females may have devoted less parental care to their nestlings, thus provoking detrimental effects on
body condition and/or in the maturation of the immune system
(see Müller et al. 2005 and proposals in Veiga and Polo 2008), and
finally females reduced their number of future recruits (this study).
These arguments are supported by similar detrimental effects
on body mass of nestlings and on fitness return of spotless starling females with experimentally increased circulating testosterone
(Veiga and Polo 2008): their nestlings paid the cost of the increased
ability of females to acquire and maintain a breeding site and an
attractive male.
Second, our study indicates a sex-dependent effect of the addition of green plants on fledglings’ body condition. That is, the
addition of greenery provoked a detrimental effect on body mass in
male fledglings but increased growth (i.e., tarsus–metatarsus length)
in female fledglings, although both males and females had a lower
probability of being recruited in the green plant addition treatment. These findings on sex-specific short-term effects should be
treated with caution because they result from an exploratory testing
analysis of an experiment designed with a different propose (i.e., to
analyze the long-term effect on recruitment rate). Therefore, further research is required to elucidate the proximate and ultimate
causes of the sex-specific responses to hormones in this species.
Reproductive success and body condition of
nestlings
The experimental addition of green plants in spotless starling nests
had no effect on the number of fledglings or on their body condition (contrary to Gwinner et al. 2000 and Gwinner and Berger
2005). The sex-specific effect found on fledgling size and body mass
could be interpreted in the light of sex-specific proximate responses
to hormones during the early development of chicks and possible asymmetric costs of testosterone to the nestlings (Muriel et al.
2013). In a recent study, we showed that greenery increases circulating testosterone of spotless starling mothers (Polo et al. 2010). The
level of circulating testosterone causes an increase of the aggression
rate between females, a decrease of the parental effort devoted to
their nestlings and an increase in the level of androgens transferred
to the egg yolk (McGlothlin et al. 2007; Sandell 2007; Veiga and
Polo 2008; López-Rull and Gil 2009). Thus, in a first attempt to
explain the antagonistic sex-specific effects of greenery on fledgling condition, we speculate that maternal androgens could play an
important role, not only reducing the rate of feeding, but altering
the level of androgens transferred by the mother to the egg yolk.
Yolk androgens in avian eggs have received much attention in
recent years because of their potential role in nestlings’ phenotype and future survival (e.g., Hegyi et al. 2011; López-Rull et al.
2011; Muriel et al. 2013). In particular, several experiments have
found short-term complex and antagonistic effects of androgens on
the growth of sons and daughters (Saino et al. 2006; Muriel et al.
2013). For example, yolk concentrations of testosterone (T) and
androstenedione (A) increased body mass and tarsus length in sons
but reduced those of daughters in chicks of Hirundo rustica, during
the first days of growth (Saino et al. 2006). However, similarly to
our findings, the addition of testosterone to eggs of zebra fiches,
Taeniopygia guttata, increased the growth of daughters and reduced
that of sons (von Engelhardt et al. 2006). In a recent experimental study in the spotless starling (Muriel et al. 2013), the injection
of T+A to the eggs also had an antagonistic effect on the different sexes by increasing the tarsus length of daughters and reducing
1136
those of sons during the first 7 days of growth. However, this sexspecific effect in spotless starlings disappeared at the end of the
growing period (Muriel et al. 2013). Our study showed an antagonistic effect of the green plants addition on tarsus length and body
mass of sons and daughters that remained until the end of the
growing period (i.e., 16 days after hatching). This lasting sex-specific
effect on chicks suggests a complex long-term influence of mothers
on the phenotype and performance of their offspring in relation
to environmental conditions and paternal quality (Komdeur et al.
1997; Mousseau and Fox 1998; Polo et al. 2004).
In summary, our results show a clear detrimental effect of greenery on the fitness return of mothers (i.e., a decrease in the offspring
probability of recruitment). This supports the idea that the green
plant-carrying behavior plays a major role in courtship, rather than
benefit nestlings as predicted by the sanitary and the drug hypotheses. Our results also show a long-term antagonistic sex-dependent
influence of green plants on the phenotype of nestlings, suggesting
the existence of a complex maternal influence with short- and longterm consequences on their offspring.
Data accessibility
The datasets supporting this article are available in http://dx.doi.
org/10.6084/m9.figshare.956277.
FUNDING
This research has been carried out with the financial support from the Spanish Government, projects: CGL200400126/BOS, CGL2005-05611-C02-01, CGL2008-02843, and
CGL2011-28095.
The field work was carried out under license of the “Consejería de
Medio Ambiente y Desarrollo de la Comunidad de Madrid” and the
“Ayuntamiento de Manzanares el Real.” We are grateful to Marcos Méndez
and Akiko Matsuda for their helpful suggestions on the writing style and
Wolfgang Forstmeier and 2 anonymous referees for improving the present
version of the manuscript.
Handling editor: Wolfgang Forstmeier
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