Behavioral Ecology
doi:10.1093/beheco/arp028
Advance Access publication 17 March 2009
Testosterone increases UV reflectance of
sexually selected crown plumage in male blue
tits
Mark L. Roberts, Erica Ras, and Anne Peters
Department of Migration and Immuno-ecology, Max Planck Institute for Ornithology, Vogelwarte
Radolfzell, 78315 Radolfzell, Germany
A central assumption of models of sexual selection, including the immunocompetence handicap hypothesis, is that the male sex
hormone testosterone (T) is responsible for the expression of male sexual signaling; however, this has been questioned for
colorful avian plumage. In this experiment, we manipulated T in juvenile male blue tits (Cyanistes caeruleus) during the molt and
measured crown ultraviolet (UV) chroma (a sexually selected trait) immediately after molt and in the following spring during the
breeding season, as well as recording preening behavior during spring. We found that males that were implanted with T during
the molt had higher crown UV chroma than control males (C-males) in the subsequent breeding season but not immediately
after molt. We also found that testosterone-treated males preened more than C-males during the spring but not during the
preceding molt. These results suggest not only that T influences plumage coloration during the mate attraction period, possibly
by increasing preening behavior, but also that exogenous T administered during the juvenile molt may have organizational effects
in the subsequent breeding season. Because our study supports the assumption that T enhances the expression of male sexually
selected plumage coloration, the results indicate that T could enforce costliness, and therefore honesty, of male plumage color as
a signal of quality to females. Key words: blue tit, crown UV chroma, molt, preening, sexual signaling, testosterone. [Behav Ecol
20:535–541 (2009)]
estosterone (T) is viewed as central to male reproductive
trade-offs (Hau 2007); indeed, one of the main assumptions of current sexual selection theory, in particular the immunocompetence handicap hypothesis (ICHH) (Folstad and
Karter 1992), is that male sexual signaling is regulated by T
levels. Although there is considerable evidence to suggest that
male sexual display behavior is controlled by T (Ball and
Balthazart 2004), whether T is involved in the expression of
plumage ornaments in male birds is unclear (Owens and
Short 1995). Many avian species are strongly sexually dichromatic with males usually possessing the more flamboyant or
bright plumage, and it is generally thought that females prefer
males with the most colorful or elaborate feathers (Andersson
1994; Siitari et al. 2002; Calkins and Burley 2003; Zampiga
et al. 2004; Hill and McGraw 2006; Bitton et al. 2007). Therefore, to understand what costs males may incur to maintain
the signaling honesty of sexual traits, it is important to determine whether T is involved in the coloration of male sexually selected plumage regions because high T levels may have
negative effects on immunity (e.g., Peters 2000) as well as
incurring metabolic costs (Buchanan et al. 2001).
Castration studies suggest that in many species absolute differences between the sexes in plumage ornamentation do not
depend on T but on genetic factors or other hormones (Owens
and Short 1995; Kimball and Ligon 1999; Kimball 2006). However, such studies do not address whether T plays a role in
regulating individual differences in the expression of male
sexual plumage. For example, experimental evidence exists
T
Address correspondence to M.L. Roberts, who is now at Division of
Biology, Imperial College London, Silwood Park Campus, Buckhurst
Road, Ascot, Berkshire SL5 7PY, UK. E-mail: m.l.roberts@imperial.
ac.uk.
Received 23 May 2008; revised 23 January 2009; accepted 3
February 2009.
The Author 2009. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
that T may regulate the size of the black throat badge of the
male house sparrow (Passer domesticus, Evans et al. 2000;
Buchanan et al. 2001; Gonzalez et al. 2001) or the development of breeding plumage in superb fairy-wrens (Malurus
cyaneus, Peters et al. 2000), although both signals have a genetic component (Owens and Short 1995; Peters 2007). Nevertheless, despite the fact that correlations between plumage
color and circulating T have been described (Duckworth et al.
2004; Peters et al. 2006), little experimental evidence of causality has been found (or indeed sought) between the coloration of avian male sexually selected plumage and T.
In this study, we examined the effects of T on the elaboration
of a sexually selected plumage region in male blue tits (Cyanistes
caeruleus). This species possesses ultraviolet (UV)/blue feathers
of the crown that are strongly sexually dimorphic, with males
showing more UV-shifted feathers than females (Andersson
et al. 1998; Hunt et al. 1998). Crown UV reflectance is important for male reproductive success by affecting paternity
(Delhey et al. 2003; Delhey et al. 2007b), brood sex ratios
(Sheldon et al. 1999; Korsten et al. 2006; Delhey et al.
2007a), and female reproductive investment (Limbourg et al.
2004; Johnsen et al. 2005). During the spring mating season,
crown UV color is associated with circulating levels of T in an
age-dependent manner, matching patterns of male attractiveness, and in yearling males, T is positively related to crown UV
reflectance (Peters et al. 2006). We experimentally tested
whether T is causally responsible for reflectance of the crown
by manipulating T in juvenile male blue tits undergoing their
first annual molt. In blue tits, as in most birds, there is a long
delay between plumage production during the autumn molt
and the start of reproduction in the following spring. Because
UV reflectance of the crown declines seasonally in blue tits
(Örnborg et al. 2002; Delhey et al. 2006), we investigated not
only whether T directly affects newly molted crown plumage
but also whether it has long-term effects during the following
Behavioral Ecology
536
breeding season. We tested whether T could influence investment in plumage maintenance (preening) as a mechanism to
cosmetically or structurally improve crown UV reflectance for
mate attraction during the courtship period (as suggested by
Peters et al. 2006).
METHODS
Study animals and housing
A nest-box breeding population of blue tits was established in
February 2006 in southwest Germany near Lake Constance
(4775#N, 907#E). From 1 April, the boxes were checked every
other day, and after the chicks had hatched, the boxes were
monitored daily. Between 10 and 13 days of age, the chicks
were fitted with a unique metal ring, and a small blood sample
was taken for molecular sex determination. Between 23 and 30
May 2006, 12 nest-boxes with nestlings (11–14 days old) and
parents were taken into captivity. Families were kept separately
in large, outdoor aviaries (300 3 300 3 190 cm) in the grounds
of the Max Planck Institute for Ornithology, Radolfzell, where
the parents continued to raise their chicks independently.
They were provided with a diet consisting of several types of
adult invertebrates, invertebrate larvae, and egg food (a mix
of hard-boiled mashed hens’ eggs, crushed rusk, and soured
milk with added vitamins Mauserpulver [Claus], Vitakalk
[Marianfelde GmbH, Roth, Germany], and Korvimin [WDT,
Garbsen, Germany]). After the fledglings could forage independently, 4 males (identified from the earlier molecular sex
determination) from each of the 12 broods were selected
randomly and placed separately in similar outdoor aviaries
for the remainder of the experiment (i.e., one individual
per cage). All remaining fledglings were released with their
parents in the local area.
The general experimental design involved partitioning juvenile male blue tits into T and control treatments during molt.
We measured their T levels midway through the molt and the
resultant color of the UV/blue crown (UV chroma) after the
first adult plumage was completed. In addition, we performed
an analysis of their complete behavioral time budget, including
investment in plumage maintenance (preening—these results
are presented in Kurvers et al. 2008). Birds were kept over
winter, and we measured T, plumage coloration, and preening
behavior again in the following spring. T and plumage coloration were also measured in December 2006 and May 2007.
For the duration of the molt, males were placed on 2 different dietary regimes (standard and improved semisynthetic
diets) for the purpose of a separate study; however, there
was no effect of dietary treatment on crown UV chroma or
preening behavior during the molt (crown UV chroma:
Wald ¼ 0.05, degrees of freedom [df] ¼ 1, P ¼ 0.830; preening: Wald ¼ 0.12, df ¼ 1, P ¼ 0.732) or in the following spring
(crown UV chroma: Wald ¼ 0.08, df ¼ 1, P ¼ 0.775; preening:
Wald ¼ 1.88, df ¼ 1, P ¼ 0.171). After molt was completed, all
males received a similar standard diet consisting of live mealworms, fat balls, and sunflower seeds. For another experiment
during winter (6–15 February 2007), reflectance of the crown
feathers was manipulated by applying 2 types of T-shirt
markers (Edding 4500, 0.10 and 0.03 for control and UVreduced treatments, respectively). These color treatments
were balanced across both T-treatment groups and wore off
very rapidly (significant fading within 4–5 h), and there was
no effect of winter color treatment group on UV chroma of
the crown during spring (Wald ¼ 0.11, df ¼ 1, P ¼ 0.738).
During the course of the experiment, 8 birds died for unknown reasons (6 testosterone-treated males [T-males] and
2 control males [C-males]). In addition, 2 C-males were excluded from all analyses, one due to injury early on in the ex-
periment and another that behaved idiosyncratically (apparent
attraction to humans and extreme extrovert behavior), presumably because of habituation to humans. Final sample sizes
are given in the figure legends. Removal of the birds from the
wild and all animal experimental procedures were approved by
the Regierungspräsidium Freiburg (Aktenzeichen 55-8852.15/
05 and Registriernr. G-06/05, Aktenzeichen 35-9185.82/3/339
respectively).
Implantation procedure
Before the start of the postjuvenile molt (17 July 2006), T-males
received subcutaneous T implants, whereas C-males received
placebo implants that consisted of inert binding material (both
implant types: diameter ¼ 3 mm, height ¼ 1 mm). The
implants (Innovative Research of America, Sarasota, FL) were
inserted through a small incision in the skin on the back between the wings. T implants contained 1 mg T; implant size
was based on implants previously used in blue tits (Foerster
and Kempenaers 2004) and were designed to dissolve gradually over a period of 90 days. Between the 26 and 30 October
2006, careful visual inspection of the implantation site showed
no definite evidence of any pellet remainders and they appeared to have completely dissolved.
Hormone assay
Blood samples were taken during the molt (23, 24, and 25
August 2006), during winter (18–19 December) and during
the following spring (26 and 27 March and 21 May 2007). Sufficient plasma for T assay was obtained from a total of 22 males
during molt 2006, 34 males during winter 2006, 35 males in
March 2007, and 32 males in May 2007. Blood samples were
assayed for T by direct radioimmunoassay (Goymann et al.
2006). A small blood sample (ca. 75 ll) was taken from each
bird by puncture of the brachial vein, and after centrifugation
at 3000 rpm for 5 min, the plasma was stored at 270 C until
assay. Standard curve and sample concentrations were calculated with Immunofit 3.0 (Beckman Inc, Fullerton, CA), using
a 4-parameter logistic curve fit. The lower detection limit of
the assay was determined as the first value outside the 95%
confidence intervals for the zero standard (Bmax) and was
0.006 ng/ml. The mean recovery rate was 87%, and the
intra-assay coefficient of variation was 9.6%. We repeated the
T analysis for 14 samples in a later assay to verify the relatively
high T levels in C- and T-males: this yielded nearly identical T
values (correlation coefficient ¼ 0.946, P , 0.001). We only
used the first set of T values in the statistical analyses. Additionally, we analyzed the contents of one control pellet in
a later assay to exclude the possibility that control pellets were
not accidentally contaminated with T—this confirmed that
the control pellets contained no significant amounts of T
because T content was below the detection limit of the assay.
Crown UV chroma measurement
As a measure of color quality, we calculated UV chroma, relative UV reflectance, a descriptor used in numerous previous
studies of blue tit coloration (e.g., Andersson et al. 1998;
Limbourg et al. 2004; Delhey et al. 2006; Korsten et al.
2006; Peters et al. 2006; Delhey et al. 2007a, 2007b). For each
bird, we measured reflectance of the crown plumage at the
end of the molt (26, 27, and 30 October 2006), in winter (5–
15 December 2006), and in the following spring (26 and 27
March and 11 May 2007). From 5 different but standardized
spots on the crown, reflectance spectra between 300 and 700
nm that encompass the wavelength range of visual sensitivity
of passerine birds including the blue tit (Hart 2001) were
obtained. We used an S-2000 spectrometer and a DHS-2000
Roberts et al.
•
Testosterone and UV in blue tits
537
deuterium halogen light source (Avantes, Eerbeek, The Netherlands) connected through a bifurcated fiber-optic probe.
The probe was fitted with a black plastic cylinder at the end
to standardize measuring distance and exclude ambient light.
Feather reflectance (R) was calculated relative to a WS-2 white
standard (Avantes). Reflectance spectra were imported into
a spreadsheet program; each spectrum was smoothed with
a running average computed over a 5-nm interval. The spectrum was unimodal with a single peak in the UV/blue region,
and we calculated relative amount of UV reflectance or UV
chroma (R300–400/R300–700) as an index of color elaboration.
For each bird, UV chroma values from the 5 spectra were
subsequently averaged.
Preening behavior
Behavioral observations were carried out between the 10 and
the 14 April 2007 between 0800 and 1200 h (morning observation period) and between 1500 and 1900 h (afternoon observation period). The sequence of birds observed in each 30-min
observation period was randomized. The observer (E.R.) noted
every 15 s whether the focal male was preening or not. Observations were conducted from a hide placed next to the aviary
40 min before starting the observation. Preening behavior had
been recorded in an identical manner during the preceding
molt, and no difference was found in time spent preening between the different T treatments (Kurvers et al. 2008).
Statistical analyses
We used the restricted maximum likelihood (ReML) procedure to test for differences between treatment groups in crown
UV chroma, T levels, and preening. The fixed models consisted of T treatment as the main effect with bird ‘‘family’’
(nest-box) as the random term. We also examined whether
there were any effects of the nest in which the birds were raised
on crown UV chroma, T, and preening behavior by including
family as a fixed rather than a random effect in separate models
for each time crown UV chroma, T, and preening were measured. To control for any treatment effects, T group was also
included as a fixed effect. We also compared the changes in
residual deviance against a chi-square table for models with
and without family included as a random term; we obtained
identical results as when family was included as a fixed term.
T levels were natural log transformed for all analyses. During
spring, one outlier that was more than 2 standard deviations
(SDs) from the mean was excluded from the crown UV chroma
analysis and one individual that had T levels more than 2 SDs
from the mean was excluded from the December T analysis.
Inclusion or removal of these individuals made no qualitative
difference to the results. For the preening models, the response variable was the percentage of time spent preening
(square root transformed). Birds preened less during the
morning (Kurvers et al. 2008); we fitted time of day (AM/PM)
to control for this effect. Because 18 birds were not observed
preening (13 C-males and 5 T-males), in addition to the above
analysis we also coded birds as to whether they had preened or
not. We then employed a general linear mixed model with
a binomial distribution and used the binary preening behavior as the response variable. The fixed and random models
were identical to those used in the ReMLs. For all statistical
analyses, we used Genstat 8.1 (VSN International Ltd, Hemel
Hempstead, Hertfordshire, UK). For all figures, we present
back-transformed means 6 SE.
RESULTS
T-males had significantly higher T levels than C-males during
the molt (Wald ¼ 17.37, df ¼ 1, P , 0.001; Figure 1). Mean
Figure 1
Mean T levels of juvenile male blue tits in T (n ¼ 11) and C (n ¼ 11)
treatments during molt 2006 6 SE (***P , 0.001).
T levels of T-males (1.9 6 0.7 ng/ml, range ¼ 0.25–12.0 ng/ml,
n ¼ 11) were around the maximum of C-males (range ¼
0.26–2.1 ng/ml, mean ¼ 0.55 6 0.2 ng/ml, n ¼ 11). There
was no effect of T manipulation on crown UV chroma immediately after the molt (Wald ¼ 0.40, df ¼ 1, P ¼ 0.527; Figure
2) or in December 2006 (Wald ¼ 1.93, df ¼ 1, P ¼ 0.175).
There was no difference in T levels between the treatment
groups in December 2006, but there was still a trend for
T-males to have higher titers than C-males (Wald ¼ 2.88,
df ¼ 1, P ¼ 0.103; mean 6 SE: T-males, 0.41 6 0.17 ng/ml;
C-males, 0.10 6 0.02 ng/ml).
In March 2007, T-males had significantly higher T than
C-males (Wald ¼ 5.19, df ¼ 1, P ¼ 0.023; Figure 3) and also
had higher levels in May 2007 (Wald ¼ 6.29, df ¼ 1, P ¼ 0.01;
Figure 2
Mean crown UV chroma of juvenile male blue tits in T (n ¼ 21) and
control (n ¼ 22) treatments immediately after molt 2006 6 SE.
Behavioral Ecology
538
Figure 3
Mean T levels of juvenile male blue tits during spring 2007 (March)
that had been in T (n ¼ 16) and control C (n ¼ 19) treatments
during the previous molt 6 SE (*P , 0.05).
Figure 5
Mean percentage of time spent preening during spring 2007 by
juvenile male blue tits that had been in T (n ¼ 18) and C (n ¼ 20)
treatments during the previous molt 6 SE (*P , 0.05).
mean 6 SE: T-males, 0.17 6 0.06 ng/ml; C-males, 0.08 6 0.01
ng/ml). T-males had significantly higher crown UV reflectance than C-males in March (Wald ¼ 7.04, df ¼ 1, P ¼
0.008; Figure 4) but not in May (Wald ¼ 0.14, df ¼ 1, P ¼
0.715). There was a positive relationship between plasma T
levels during the molt and crown UV chroma in the following
spring (F1,18 ¼ 4.06, P ¼ 0.059); in addition, there was a significant, positive relationship between spring T levels and
spring crown UV chroma (F1,32 ¼ 4.26, P ¼ 0.047). During
the spring, T-males spent significantly more time preening
than C-males (Wald ¼ 5.26, df ¼ 1, P ¼ 0.022; Figure 5)
and were significantly more likely to preen than C-males
(Wald ¼ 5.31, df ¼ 1, P ¼ 0.021). However, we found no
significant relationships between actual T levels and preening
behavior either during the molt (all birds: F1,18 ¼ 0.11, P ¼
0.743; T-males: F1,6 ¼ 0.07, P ¼ 0.794; C-males: F1,10 ¼ 0.37,
P ¼ 0.557) or during the spring (all birds: F1,33 ¼ 0.03, P ¼
0.869; T-males: F1,11 ¼ 0.20, P ¼ 0.663; C-males: F1,17 ¼ 0.09,
P ¼ 0.769).
The nest-box of origin (family) did not explain any significant
variation in crown UV chroma at any period when this trait was
measured (October 2006: Wald ¼ 7.84, df ¼ 11, P ¼ 0.717;
December 2006: Wald ¼ 4.39, df ¼ 10, P ¼ 0.914; March
2007: Wald ¼ 13.98, df ¼ 11, P ¼ 0.300; May 2007: Wald ¼
16.34, df ¼ 11, P ¼ 0.206). T levels were not associated with
family during the molt (Wald ¼ 21.3, df ¼ 10, P ¼ 0.124), winter
(Wald ¼ 9.74, df ¼ 9, P ¼ 0.413), or in May 2007 (Wald ¼ 12.95,
df ¼ 11, P ¼ 0.366). Interestingly, T levels were dependent on
family in March 2007 (Wald ¼ 65.86, df ¼ 11, P , 0.001) as was
preening behavior (Wald ¼ 25.16, df ¼ 11, P ¼ 0.042). There
was no difference between families in preening behavior during
the molt however (Wald ¼ 10.54, df ¼ 11, P ¼ 0.502).
DISCUSSION
Figure 4
Mean crown UV chroma of juvenile male blue tits during spring 2007
(March) that had been in T (n ¼ 18) and control C (n ¼ 18)
treatments during the previous molt 6 SE (**P , 0.01).
In this experiment, we have demonstrated that T can have longterm effects on sexual signaling in juvenile male blue tits. Despite large, but physiologically relevant, differences in T level
between treatment groups during molt, there was no effect of
T manipulation on crown UV chroma (a sexually selected trait)
immediately after the molt. However, T treatment as well as
individual differences in T during the molt positively affected
crown UV chroma in the following spring during the courtship
period. Because T during molt and spring were related positively to spring crown UV chroma, we here demonstrate that
the previously observed positive correlation in spring between
T and crown UV (Peters et al. 2006) does appear to be causal
despite the time delay after plumage production, although in
spring the effects may have been bidirectional in manner (see
Rubenstein and Hauber 2008; Safran et al. 2008). A possible
explanation may be that sexually selected signals such as the
Roberts et al.
•
Testosterone and UV in blue tits
crown UV chroma of the male blue tit are most important
during the breeding season, so any differences between males
based on T levels may become manifest only at that time.
T treatment during summer appeared to have effects long
after the molt ended and the first adult plumage had been
completed. Although implants had dissolved 5–6 months before, not only did the T-males exhibit higher crown UV chroma
and higher preening activity in spring but they also had higher
T levels. Thus, we demonstrate organizational effects of T implantation in relatively developed test subjects, that is, fledgling
passerines. The birds were around 9 weeks of age when
implanted with the T pellets; this is much older than in previous studies that have examined the organizational effects of
T where the subjects were either still in the egg or very young
nestlings (Adkins-Regan 1999; Strasser and Schwabl 2004;
Eising et al. 2006). There is however evidence in mammals
that T does have organizational effects during the juvenile
stage, particularly during puberty (Abitbol et al.1999;
Eichmann and Holst 1999; Sisk and Zehr 2005). Our results
suggest that, even at an advanced stage of development, the
blue tit neuroendocrinological system is also relatively plastic
and receptive to further organization by T.
T levels in T-males during molt were on average increased to
the maximum levels observed in control-implanted males kept
in the same conditions and sampled at the same time. However,
despite the fact that relative T levels of both groups were thus as
intended, males from both treatment groups had absolute levels of T that were much higher than those found in wild male
blue tits: mean natural T levels in juvenile male blue tits from
the local area during postjuvenile molt (late August–early September 2004) were much lower (mean ¼ 0.10 ng/ml, n ¼ 24,
range ¼ 0.07–0.19 ng/ml; Peters A, unpublished data). This
was not due to outliers; all values were within 2 SDs of the
group means. The reason for the high T levels in the captive
birds during molt is unknown. We excluded contamination of
control pellets as a possibility and can thus only speculate that
it was an artifact of captive conditions that affected T levels.
Irrespectively, the relative magnitude of the T treatment compared with C-males is within the optimal range for a physiologically relevant manipulation, and it accordingly resulted in
modest behavioral differences between groups that are in
agreement with known effects of T in breeding birds (Kurvers
et al. 2008).
Conversely, the March (spring) T levels of the males in this
study were lower than those found in wild tits (in another study
population means of 2.0–3.3 ng/ml and a range of 0.1–12.8 ng/
ml were found, Foerster and Kempenaers 2005; Peters et al.
2006). Possibly, the lack of social interaction, both absence of
females and opportunities for male–male aggression, may have
lowered T levels in our captive birds (see Wingfield et al.
1990). Whether the apparent long-term effects of T treatment
during molt would persist in free-living animals exposed to
conspecific challenges and sexual stimuli remains an open
question, but the fact that in our captive birds we find the same
positive relationship between T and UV chroma as in wild
yearling blue tits (Peters et al. 2006) suggests that it might.
The positive effect of molt T treatment on spring crown UV
reflectance and preening behavior, whereas there were no such
effects in autumn, suggests that increased spring preening in
T-males may have accounted for the differences between treatment groups in crown UV chroma. The lack of association between crown UV chroma and the nest-box of origin of the birds
indicates that neither genetic effects nor conditions during
early development directly affect this trait. This agrees with
Hadfield et al. (2006) who found that crown color was only
weakly heritable in this species and indicates a large potential
for the importance of individual or environmental condition
in affecting crown UV chroma, particularly because crown
539
color in blue tits is not the static trait it was once thought to
be—as can be seen from Figures 2 and 4; UV chroma of newly
molted feathers is higher than breeding season values. A large
seasonal decline (surpassing sexual dichromatism) in UV
chroma is generally observed in blue tits (Örnborg et al.
2002; Delhey et al. 2006), presumably because the feathers
in spring have been exposed to several months of weathering,
bacterial action, and general soiling (Shawkey et al. 2007;
Surmacki and Nowakowski 2007). Individual variation in this
decline is large, and the steepest decline in crown UV takes
place in late winter and spring (Delhey et al. 2006), indicating
that preening investment at that time would be most effective.
Thus, to improve the integrity of the plumage, it may only be
necessary to preen more at a time when females may be interested in the quality of such signals. The obvious implication
is that T does not necessarily promote preening behavior at all
times but only during the critical courtship period. Although
behavioral observations collected at additional life-history
stages are needed to confirm this, our observation that T
treatment enhanced preening investment during spring but
not during molt is consistent with these ideas. However, no
direct effect of plasma T on preening could be discerned; this
may have been because preening behavior was recorded several weeks after blood samples were taken for T. We found
that spring levels of T and the amount of time birds spent
preening were significantly affected by family membership.
This suggests that there may be genetic or early environmental/
parental effects or a combination of these factors on adult T
levels and preening rates—but only during the breeding season. This may mean that high breeding T levels (and consequently high preening rates) indicate to prospective female
mates male quality in terms of genetic characteristics and/or
parenting skills.
To date, there has been very little empirical work carried out
on the possibility that T affects preening that in turn affects
sexual signaling. Preening behavior has previously been found
to influence the reflectance characteristics of feathers
(Surmacki and Nowakowski 2007), and it has been suggested
that preening behavior itself may be sexually selected and
used as a mate choice cue by females (Walther and Clayton
2005), although the only study that seems to have tested this
hypothesis found no supporting evidence for it (Griggio and
Hoi 2006). However, it is possible that the subsequent effect of
the preening on plumage quality is what females base their
mate choice decisions on, that is, the appearance of the plumage. For example, T may increase the size of the black badge
of status (bib) of the male house sparrow (P. domesticus)
(Evans et al. 2000; Gonzalez et al. 2001), and this influence
may involve preening behavior (Møller and Erritzøe 1992).
Male budgerigars (Melopsittacus undulates) prevented from
preening had plumage that reflected less in the UV than
C-males that had been allowed to preen (Zampiga et al.
2004). Furthermore, in choice tests, females preferred to associate with preened rather than unpreened males (Zampiga
et al. 2004). Our results lend support to the hypothesis that
preening behavior ameliorates the process of natural soiling
and bacterial activity that affects feather color.
To summarize, the results of our experiment show that T in
molting juvenile passerines can affect the quality of sexually
selected plumage variables several months later during the
courtship period, possibly by increasing plumage maintenance. This result supports current hypotheses in the field
of sexual selection such as the ICHH that assume that T is responsible for the expression of sexually selected traits, such as
plumage variables in dichromatic birds. It suggests that if T
were physiologically costly, possessing colorful plumage would
give females an honest indication of male condition because
only high-quality males could afford to maintain the high levels
540
of T required to fully express such signals. In addition, we
found that administration of exogenous T during the juvenile
molt (when the birds were around 9 weeks of age) had effects
that lasted several months after the termination of the T administration—suggesting organizational effects of Teven at this relatively late stage of development.
FUNDING
Max Planck Society Program for the Advancement of Women
in Science (to A.P.).
We are grateful for the advice of Roland Rost on raising chicks in captivity with their parents. For invaluable assistance with implanting and
measuring the birds, we are indebted to R. Kurvers and S. Magdeburg.
We also thank T. Vogler, E. Fricke, M. Krome, H. Schmid, U. Querner,
and A. Schmidt for assisting in capturing, feeding, and housing the
birds. We are grateful to W. Goymann, I. Schwabl, and M. Trappschuh
(from the Department of Behavioral Neurobiology) for conducting the
T assay; E. Fricke for collecting and processing the reflectance spectra;
and K. Delhey for helpful comments and suggestions. M.L.R. conceived, planned, and carried out research; analyzed data; wrote the
paper. E.R. performed the behavioral observations. A.P. conceived,
planned, and supervised the research, analysis, and writing.
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