Naturwissenschaften (2003) 90:234–237
DOI 10.1007/s00114-003-0414-7

S H O R T C O M M U N I C A T I O N

Juan Carlos Senar · Jordi Figuerola · Jordi Dom�nech

Plumage coloration and nutritional condition
in the great tit Parus major: the roles of carotenoids and melanins differ

Received: 4 June 2002 / Accepted: 21 February 2003 / Published online: 25 March 2003
� Springer-Verlag 2003

Abstract The size and coloration of some body charac-
ters seem to influence mate choice in many species. Most
animal colours are either structural or based on melanin or
carotenoid pigments. It has recently been suggested that
carotenoid-based or structural coloration may be a
condition-dependent trait, whereas melanin-based color-
ation is not; a difference that may be highly relevant when
studying the evolution of multiple mating preferences.
We tested this hypothesis in the great tit (Parus major).
The size of the melanin breast band was not correlated to
nutritional condition as estimated by the rate of tail
growth (ptilochronology), controlling for locality, age,
sex, year and season effects. However, the correlation was
significant for the hue of yellow breast (carotenoid-based
coloration), and the slopes of the regressions of the two
pigments to growth bars differed significantly. These
results suggest that the expression of the two traits may be
regulated by different mechanisms.

Introduction

Most plumage coloration results either from structural
feather properties (e.g. white, blue or UV) or from
pigment molecules, mainly carotenoids and melanins,
embedded in the feathers (e.g. red, yellow or black, Brush
1978). A current debate on the evolution of mate choice
through plumage coloration centres on whether different
shades of colour convey different kinds of information
(Gray 1996; Badyaev and Hill 2000). Since birds cannot

synthesise carotenoids they must be ingested (Fox 1976),
and since they play an important role as precursors of
vitamins (Olson and Owens 1998) and in the neutralisa-
tion of potentially harmful secondary metabolites (Von
Schantz et al. 1999), it is widely recognised that
carotenoid-based plumage coloration may confer infor-
mation on the nutritional, parasitic and general body
condition of the bearer (Hill 1999; Møller et al. 2000).
Structural plumage coloration has also been shown to be
condition-dependent (Gustafsson et al. 1995; Qvarnstr�m
1998) and to be related to nutritional and parasitic
condition (Potti and Merino 1996; Keyser and Hill 1999,
2000).

Data from melanin-based plumage coloration, howev-
er, is more controversial, since different studies on
different species either support (Møller et al. 1996; Veiga
and Puerta 1996; Gonz�lez et al. 1999; Poiani et al. 2000;
Fiske and Richner 2002) or reject (Hill and Brawner
1998; Figuerola et al. 1999a; McGraw and Hill 2000; Hill
2000; Senar and Escobar 2002) the view that melanin
coloration signals body condition. Further support for the
lack of condition dependence comes from the fact that
melanin pigments may be synthesised from several
common dietary components (Fox 1976) and that no
physiological link of melanin to general body condition
has yet been described (Hillgarth and Wingfield 1997;
Olson and Owens 1998).

The aim of this paper was to explore the potential
value of melanin-based coloration as an indicator of
nutritional condition by analysing the relationship be-
tween the size of the great tit’s (Parus major) central
black breast-stripe and the rate of tail feather growth
(ptilochronology). Previous studies have shown that the
central black breast-stripe of the great tit is related to the
quality of male parental care (Norris 1990a, 1993) and to
female investment in reproduction (Norris 1990b). We
used ptilochronology as a measure of nutritional condition
because of its straightforward interpretation and its
previously proven usefulness (Grubb 1995), but most
importantly because it has already been found to be
related both to carotenoid-based (Hill and Montgomerie

J. C. Senar ()) · J. Figuerola · J. Dom�nech
Museu de Ci�ncies Naturals (Zoologia),
Pg. Picasso s/n, Parc Ciutadella, 08003 Barcelona, Spain
e-mail: jcsenar@mail.bcn.es
Tel.: +34-93-3196912
Fax: +34-93-3104999

Present address:
J. Figuerola, Department of Applied Biology,
Estaci�n Biol�gica Do�ana,
Ap. Correos 1056, 41080 Sevilla, Spain



1994) and structural (Keyser and Hill 1999) colorations;
this would thus allow, for the first time, a comparison of
the three kinds of coloration within the same frame of
reference.

Materials and methods

Great tits were captured in baited funnel traps from 1997 to 2000, in
two contrasted areas near Barcelona, north-eastern Spain, situated
approximately 10 km apart but with no exchange of birds. Age was
determined according to the method of Jenni and Winkler (1994).

The size of the melanin-based black breast band was measured
on digital photographs (n=144) with Image Tool software (for more
technical details see Figuerola and Senar 2000). Measurement
repeatability (measured as intra-class correlation) was ri=0.98,
P<0.001, n=12 (see Figuerola and Senar 2000). General yellowish
plumage coloration on the breast was measured with a Minolta
CR200 colorimeter (Minolta Corporation 1994) using a standard
D65 light flash (n=221, see Figuerola et al. 1999b). Colour was
characterised according to the tri-stimulus variables of hue, chroma
and lightness. The repeatability of the three colour variables was
high (lightness, ri=0.85, P<0.001; chroma, ri=0.87, P<0.001; hue,
ri=0.92, P<0.001; n=12; Figuerola et al. 1999b). Two data point
outliers were discarded from analyses because of a very low value
of hue (<75�) which was probably due to an error in measurement,
although the results still hold if they are retained. We did not
measure the extent of yellow coloration in the breast because the
whole area is generally covered in yellow, rendering this measure-
ment impractical.

We used tail ptilochronology to estimate the conditions of food
availability and nutritional condition experienced by birds during
feather growth (Grubb 1995). The second pair of rectrices was
plucked for further measurement in the laboratory, where the same
observer measured the width of the first ten measurable distal
growth bars to the nearest 0.1 mm (see Carrascal et al. 1998). This
value was transformed by dividing by ten to obtained daily growth
rate (mm/day) and averaging the values for the left and right
rectrices. Measurement repeatability was ri=0.99, P<0.001, n=15.
We measured the first ten measurable growth bars rather than
following the standard technique (Grubb 1989) because the length
of the great tit feather very often would not allow for measuring ten
bands. Since great tits only moult in the autumn (Jenni and Winkler
1994), rectrices and contour feathers were moulted during the same
period. Since yellow and black breast feathers belong to the same
feather tract, they are moulted within the same time period (Gosler
1993).

Results

Breast band size was not correlated to the tri-stimulus
variables of yellow breast coloration (lightness, r=0.07,
P=0.43; chroma, r=0.07, P<0.45; hue, r=0.002, P<0.98;
n=144; standardising by age, sex and locality).

Width of tail growth bars was positively correlated
with hue of the yellow coloration of the breast (Table 1,
Fig. 1). However, width of growth bars was not correlated
with the melanin-based breast band size (Table 1, age,
sex, locality, year and months from moult controlled in a
MANCOVA with the three colour variables and breast
band size as dependent variables and width of the growth
bars and months since moult entered as covariates).

The two regressions of growth bars to either hue of the
yellow breast and size of the black breast band signifi-
cantly differed in slopes (parallelism test, F1,352=4.42,

P=0.04, controlling for age, sex and locality, including
the whole data set). This shows that melanin-based
coloration is less important than carotenoid-based color-
ation in relation to growth.

Discussion

Condition dependence is critical to the understanding of
ornament evolution (Pomiankowski 1987). Ptilochronol-
ogy (Grubb 1995) is a robust approach to testing the
condition-signalling role of plumage, since it directly
links foraging success to the expression of plumage
coloration (Hill and Montgomerie 1994). Here we have
shown that the width of the great tit melanin-based breast
stripe was not related to feather growth rates. However,
yellow carotenoid coloration (hue) of the breast was

Table 1 MANCOVA analysing the relationships of tail feather
growth rate as measured from ptilochronology (i.e. nutritional
condition) to lightness, intensity and hue of the carotenoid-derived
yellow coloration of the breast and size of the melanin-derived
black breast band of great tits, controlling for the effects of age, sex,
locality, year and months since moult. Multivariate tests: overall
regression Wilks’ l=0.84, P=0.01; fixed effects: age Wilks’ l=0.78,
P<0.001, sex Wilks’ l=0.35, P<0.001, locality Wilks’ l=0.85,
P=0.01, year Wilks’ l=0.36, P<0.001. Slopes are standardized to
mean = 0 and SD=1

Slope (beta) t115 P

Ptilochronology

Yellow lightness �0.12 1.25 0.21
Yellow intensity 0.00 0.02 0.98
Yellow hue 0.20 2.22 0.03
Black breast band size 0.05 0.51 0.61

Months since moult

Yellow lightness �0.16 1.70 0.09
Yellow intensity �0.22 2.42 0.02
Yellow hue �0.18 1.99 0.05
Black breast band size �0.13 1.36 0.18

Fixed effects
Age

Yellow lightness 0.67 0.41
Yellow intensity 14.14 <0.001
Yellow hue 15.37 <0.001
Black breast band size 8.23 <0.01

Sex

Yellow lightness 12.44 <0.001
Yellow intensity 0.64 0.42
Yellow hue 0.25 0.62
Black breast band size 207.54 <0.001

Locality

Yellow lightness 0.11 0.74
Yellow intensity 7.35 <0.01
Yellow hue 12.18 <0.001
Black breast band size 0.11 0.74

Year

Yellow lightness 3.25 0.02
Yellow intensity 3.18 0.03
Yellow hue 25.28 <0.001
Black breast band size 12.96 <0.001

235



significantly related to feather growth rates. The discrep-
ancy between our results and those of Eeva et al. (1998) is
probably related to the greater repeatability and precision
of our colour measurements, where the slopes of the two
regressions (carotenoid and melanin) differed significant-
ly. This supports the hypothesis that melanin-based
coloration is not a good candidate for signalling nutri-
tional condition, and that melanin- and carotenoid-based
colorations might serve fundamentally different functions
(Gray 1996; Badyaev and Hill 2000).

The main source of carotenes for tits are caterpillars
(Slagsvold and Lifjeld 1985). Once ingested, carotenes
are deposited unmodified in the feathers of tits (Partali et
al. 1987). A brightly carotene-coloured great tit may
therefore be directly signalling its ability to find caterpil-
lars, a main food source for both adults and fledglings
(Gosler 1993). Our data relating width of tail growth bars
to yellow hue supports this higher foraging efficiency of
more brightly coloured tits. Hence, it would be of direct
female benefit to pair with a very yellow great tit male
(see Senar et al. 2002). The study of tits could therefore
neatly solve the missing link in other bird studies in
relation to the question of why finding carotenes may be
difficult but nevertheless highly advantageous in order to
acquire a mate.

Acknowledgements We are very grateful to Lluisa Arroyo, David
Bon	 and Iker Ruiz for field assistance, and to Miguel Tejedo for
laboratory facilities. This work was funded by Ministerio de
Ci	ncia y Tecnolog
a (BOS 2000-0141).

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