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[559]
The Condor 107:559–569
q
The Cooper Ornithological Society 2005
FEMALE SONG IN EUROPEAN STARLINGS: SEX DIFFERENCES,
COMPLEXITY, AND COMPOSITION
D
ENITZA
P
AVLOVA
1
,R
IANNE
P
INXTEN
,
AND
M
ARCEL
E
ENS
Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium
Abstract. While male song and its functions have been well studied, female song has
often been overlooked. In this study, we provide a detailed description of the spontaneous
female song in a well-studied northern temperate songbird, the European Starling (Sturnus
vulgaris). We compared the song organization, complexity, and composition of female and
male starlings housed in large outdoor aviaries. Overall, the general organization was similar
in both sexes, and some females sang complex song bouts of more than 30 seconds of
uninterrupted song. Although some females were capable of singing the four phrase-type
categories typically found in male song bouts (whistle, variable, rattle, and high-frequency
phrase types), a significantly lower proportion of females sang all four categories of phrase
type as compared to males. Our results also revealed large individual variation in song
characteristics among females: repertoire size varied between 11 and 36 phrase types, while
average song bout length ranged between 10 and 26 seconds. All song parameters (total
repertoire size, song bout length, and repertoire size within the four different phrase cate-
gories) were significantly lower in females than in males. Nevertheless, except for the num-
ber of rattle phrase types, song parameters overlapped between the sexes demonstrating that
some females produced a more complex song than some males.
Key words: European Starling, female song, repertoire size, sex differences, songbird.
Canto de la Hembra en Sturnus vulgaris: Diferencias entre Sexos, Complejidad y Composicio´n
Resumen. Mientras que el canto del macho y sus funciones han sido bien estudiados, el
canto de las hembras ha sido menos estudiado. En este estudio, brindamos una descripcio´n
detallada del canto esponta´neo de la hembra en una especie bien estudiada de ave canora del
norte templado, Sturnus vulgaris. Comparamos la organizacio´n del canto, la complejidad y la
composicio´n entre machos y hembras en aviarios de gran taman˜o emplazados al aire libre. En
total, la organizacio´n general fue similar en ambos sexos, y algunas hembras cantaron unidades
de canto complejas durante ma´s de 30 segundos de modo ininterrumpido. Aunque algunas
hembras fueron capaces de cantar las cuatro categorı´as de tipos de frases tı´picamente halladas
en las unidades de canto de los machos (silbido, variable, matraqueo y tipos de frases de alta
frecuencia), una porcio´n significativamente menor de las hembras canto´ todas las cuatro ca-
tegorı´as de tipos de frases en comparacio´n con los machos. Nuestros resultados tambie´n re-
velaron gran variacio´n individual entre hembras en las caracterı´sticas del canto: el taman˜o del
repertorio vario´ entre 11 y 36 tipos de frases, mientras que la duracio´n promedio de la unidad
de canto fluctuo´ entre 10 y 26 segundos. Todos los para´metros examinados del canto (taman˜o
total del repertorio, duracio´n de la unidad de canto y taman˜o del repertorio dentro de las cuatro
categorı´as diferentes de frases) fueron significativamente menores en las hembras que en los
machos. A pesar de ello, a excepcio´n del nu´mero del tipo de frases de matraqueo, los para´-
metros del canto se superpusieron entre los sexos, implicando que algunas hembras produjeron
un canto ma´s complejo que algunos machos.
INTRODUCTION
Songbirds’ ability to learn and produce complex
vocalizations have made them an important
model system in communication and sexual se-
lection research (Catchpole and Slater 1995,
Slater 2003); however, most of the studies have
focused on temperate species in which song is
Manuscript received 18 January 2005; accepted 4
May 2005.
1
E-mail: denitza.pavlova@ua.ac.be
restricted mainly to males (Langmore 1998,
Price 1998, Riebel 2003, Slater and Mann 2004).
Indeed, the study of song behavior in females
has been a long-neglected field (Baptista and
Kroodsma 2001). In recent years, however, there
is increasing evidence that female song is not so
uncommon as previously thought but instead
may be an adaptive plastic trait in females
(Langmore 1998, Eens and Pinxten 1998).
During the last 20 years, the European Star-
ling (Sturnus vulgaris) has become an important
model in bird song and song system research
560 DENITZA PAVLOVA
ET AL
.
(Eens 1997, Riters and Ball 1999, Ball et al.
2002, Duffy and Ball 2002, Pinxten et al. 2002,
Van der Linden et al. 2002, Riters et al. 2005).
European Starlings are sociable birds that sing
throughout most of the year (Feare 1984), feed-
ing and roosting in flocks, and breeding in col-
onies. Although it has long been recognized that
female starlings often sing (Freitag 1936, 1937,
1939, Witschi and Miller 1938, Bullough 1942,
Feare 1984, Eens 1997), the great majority of
studies have focused on male starlings. Male
starling song has been well described by several
researchers (Adret-Hausberger and Jenkins
1988, Eens et al. 1989, 1991a, 1991b, Chaiken
et al. 1993, Mountjoy and Lemon 1995). Males
produce a long and elaborate song that functions
primarily to attract females in spring (Eens et al.
1990, 1993). Males also sing frequently outside
the breeding season but the function of song at
this time is less clear, although it seems to play
a role in flock cohesion or in the maintenance
of dominance hierarchies (Eens 1997, Riters et
al. 2000, 2002, Pinxten et al. 2002). Males have
large repertoires ranging from 14 to almost 70
phrase types (Eens 1997). There is also great
deal of evidence both from the field and the lab-
oratory suggesting that individual variation in
males’ song plays an important role in female
mating decisions (Eens et al. 1991a, Eens 1997,
Mountjoy and Lemon 1996, Gentner and Hulse
2000). Male starlings produce their song in
structured episodes that have been referred to as
song bouts. Song bouts vary in length both with-
in and among individuals, but follow a general
phonological pattern that appears to be species
typical (Eens et al. 1991a, Chaiken et al. 1993,
Gentner and Hulse 2000). Complete song bouts
consist of four categories of phrase types (whis-
tles, variable phrase types, rattle phrase types,
and high-frequency phrase types) that are sung
in a highly predictable sequence (Eens 1997).
Female starlings have been reported singing
during the breeding and nonbreeding season,
and both in the wild and in captivity (Hausber-
ger and Black 1991, Hausberger et al. 1995b,
Eens 1997, Henry and Hausberger 2001, De
Ridder et al. 2002). The function of female song
in starlings is unclear at present, although there
are indications that during the breeding season
it plays a role in intrasexual competition (Eens
et al. 1996, Sandell and Smith 1997). To the best
of our knowledge, there are no detailed descrip-
tions of the structure and organization of spon-
taneous song in female starlings. All previous
studies describing song have used testosterone
implantation techniques to induce song behavior
(Hausberger and Black 1991, Hausberger et al.
1995a, 1995b). Using such techniques, these au-
thors have concluded that testosterone-implanted
females produce a song very close in structure
to male song. They also reported that the high-
frequency song types that males typically sing
at the end of a song bout were missing in female
starlings. Given that testosterone not only affects
the rate but also the structure of song (Fusani et
al. 1994, Beani et al. 2000, Ball et al. 2002), it
remains to be examined whether these results
also hold true for naturally singing females.
Several recent comparative studies have
shown that the evolution of sex differences in
brain nuclei that control song have coevolved
with the evolution of sex differences in singing
behavior in songbird species (MacDougall-
Shackleton and Ball 1999, Ball et al. 2001). Giv-
en that the volume of several song-control nuclei
in female starlings are smaller than in males but
also that the sexual dimorphism in the song sys-
tem is much smaller than in species where fe-
males do not sing (Bernard et al. 1993), we ex-
pected to find a relatively complex song in fe-
male starlings. The aim of this study was three-
fold. First, we wanted to provide the first
detailed and quantitative descriptions of spon-
taneous song in (captive) female starlings. Sec-
ond, we describe interindividual variation in
song characteristics among females focusing on
repertoire size, song bout length, and the pres-
ence of each of the four song categories making
up song in males. Third, we provide a detailed
comparison of song between female and male
starlings recorded in similar captive conditions.
Our study will hopefully stimulate further re-
search into the causes and consequences of song
variation in female starlings and other songbirds,
and also provide insight into the function of fe-
male song.
METHODS
STUDY SUBJECTS AND SONG RECORDINGS
We compared the song complexity and song or-
ganization between 12 female and 24 male Eu-
ropean Starlings. All males and females were at
least in their third calendar year when their song
was recorded. All song recordings were made in
captivity in large outdoor aviaries on the campus
FEMALE SONG IN EUROPEAN STARLINGS 561
of the University of Antwerp, Belgium. Previous
studies have shown that male starlings exhibit
normal singing behavior in captivity (Eens et al.
1991a, 1991b, Eens 1997). All aviaries were
provided with plenty of nest boxes and branches
to perch on, and a 30-cm wooden perch was
attached to the bottom of each nest box, so that
starlings could sit and sing in front of it. Food
and water were available ad libitum. All birds
were individually marked with a numbered met-
al ring and color rings.
Given that free-living male and female star-
lings live in separate flocks throughout most of
the year (Feare 1984, Eens 1997), and that males
usually arrive in the breeding area before the
females (Eens 1997), we decided to observe and
record starlings in single-sex groups. We believe
that this is a biologically relevant approach, and
furthermore such a recording strategy should
avoid male behavior (aggression, nest-box oc-
cupation, singing) that affects or suppresses fe-
male singing behavior.
Twenty-nine adult female starlings were
housed together in a large outdoor aviary (12.10
3
8.10
3
2.12 m; length
3
width
3
height,
respectively) in a single-sex group in June 2000.
Spontaneous song of females was recorded be-
tween 20 February and 2 April 2001 from a per-
manent hide situated about 3 m away from the
aviary. Recordings were obtained in the morning
between 09:00 and 12:00 using clip micro-
phones, (Philips SBC ME 600, Europe), attached
inside the nest boxes and connected to a UHER
4400 Report Stereo IC tape recorder (Munich,
Germany) via a long cable and recorded on
BASF tapes (type DP 26 FE LH, Ludwigshafen,
Germany). Although all 29 females were ob-
served singing, and despite the fact that prior to
song recording 20 females occupied and defend-
ed a nest box, we were only able to obtain a
sufficient number of good-quality recordings
from 12 females. This was largely due to the fact
that often females were singing together in a
group, rather than singing close to their nest
boxes (i.e., in the close proximity of the micro-
phones).
To compare the song between females and
males, we used song recordings from 24 adult
captive males, recorded between 1987 and 1994.
Most data on male song have already been pub-
lished elsewhere (see Eens et al. 1991a, 1991b,
1992a, 1992b, Eens 1997). Male starlings were
housed in similar conditions as the females, and
the methodology applied for recording and an-
alyzing song, was the same as for females.
Male and female starlings were all wild-
caught mostly as adults and in a few cases as
juveniles, but never as nestlings. Although we
do not have information on the birds’ develop-
mental history before capture, they were kept in
large outdoor aviaries from the moment of cap-
ture and they were visually and acoustically ex-
posed to other female and male captive and wild
starlings. Therefore, both males and females had
access to many different tutors while held in
captivity.
SONG ORGANIZATION AND DESCRIPTION
The terminology of describing and classifying
male starling song varies among researchers.
Here, we use the terminology employed by Eens
(1997). Starlings produce most of their song in
song bouts. A song bout is defined as a period
of at least 5 sec of song with pauses no longer
than 1.5 sec. A song bout has a complex syn-
tactical and temporal organization and it is com-
posed of complex sequences of discrete units
(phrases). A ‘‘phrase’’ is a fixed combination of
acoustic elements with a duration of about 0.5–
1.5 sec. Often one phrase is repeated once or
several times before the next one is introduced.
We refer to one or more successive repetitions
of a particular phrase as a ‘‘phrase type’’. Phras-
es are organized in four distinct categories of
phrase types: whistle, variable, rattle, and high-
frequency phrase types. In male starlings, a song
bout usually begins with whistle phrase, which
are relatively pure tone-like sounds separated by
each other with pauses of 1 sec or longer. Whis-
tles are rather simple but they may also contain
more structurally complex elements as well as
heterospecific imitations. Each male can possess
up to 12 whistle phrase types. After the intro-
ductory whistles, a song bout progresses into a
series of complex phrases (variable phrase
types) sung with no pauses or very short pauses
between them. Heterospecific imitations are a
common component of this part of the song.
Males can possess between 10 and 35 variable
phrase types in their repertoire. This section of
the song is usually followed by phrases contain-
ing a rapid succession of clicks (rattles), pro-
duced in a low-frequency range (maximum 4
kHz) and delivered at a rate of about 10–15 per
second (rattle phrase types). They are softer in
volume than the preceding variable phrase types,
562 DENITZA PAVLOVA
ET AL
.
FIGURE 1. Sonogram of a complete song bout of a female starling (W is a whistle, V is a variable, R is a
rattle, and H is a high-frequency phrase type). The illustrated song bout contains 7 different phrase types (two
whistle, two variable, one rattle and two high-frequency phrase types) and 17 phrases.
rarely include heterospecific imitations, and of-
ten have no distinct temporal gaps between
them. Males can have between 2 and 14 rattle
phrase types in their repertoire. Finally, song
bouts were usually completed with high-fre-
quency phrase types, the loudest part of the
song. High-frequency phrase types are a series
of phrases containing high-frequency sounds
mainly in the range of 6–10 kHz. Males can pos-
sess up to six high-frequency phrase types.
A complete song bout consists of all four cat-
egories of phrase types that are sung in a highly
predictable sequence. However a song bout may
end at any point of this sequence and sometimes
males may revert to phrase types that have al-
ready been sung, thus whistle, variable, or rattle
phrase types can be produced after these high-
frequency phrase types. Average song bout
length varies from 12–40 sec in males, with
some song bouts lasting more than 60 sec. Of-
ten, phrase types in a song bout contain ‘‘double
voicing’’ where two tones are being produced at
the same time. Some phrase types, mostly whis-
tles, can be sung apart from the song bout, but
in most cases they appear in the song bouts as
well. The total number of different phrase types
that a bird can produce, is defined as its reper-
toire size. Overall repertoire size ranges between
14 and 68 phrase types in male starlings (Eens
1997).
To interpret the song bouts from the sono-
grams, we converted song bouts into a sequence
of letters (corresponding to the phrase-type cat-
egory) and numbers (corresponding to the novel
phrase types appearing throughout the song
bout; Fig. 1). We determined the repertoire size
FEMALE SONG IN EUROPEAN STARLINGS 563
FIGURE 2. Cumulative plots of the number of new phrase types versus the number of phrases analyzed for
five female starlings, corresponding to females 4, 5, 6, 7, and 10 from Tables 1 and 2. The complete repertoire
size was obtained only after a minimum of 150 phrase types were analyzed, and in one case after 250 phrase
types. The plots represent a subset of females with low, intermediate, and large repertoire sizes.
of each recorded female by counting novel
phrase types as they appeared throughout the
song bouts. To be certain that the whole reper-
toire of each female was obtained, we plotted
the cumulative number of new phrase types ap-
pearing throughout the song bouts against the
total number of analyzed phrases (Kroodsma
and Miller 1982, Adret-Hausberger and Jenkins
1988, Eens 1997). As can be seen from the cu-
mulative plots (Fig. 2), after a certain number of
analyzed phrases, no new phrase types occur;
asymptotic curves were reached in all cases.
In females, we measured the presence of
phrase-type category, the number of phrase
types sang per song bout, the duration of the
song bout, and the total repertoire size (includ-
ing repertoire size within each phrase category
and phrase types sang apart from the song bout).
To compare song characteristics between sexes,
in males we measured the presence of phrase-
type category, the total repertoire size, and the
song bout length.
STATISTICAL ANALYSES
Data were analyzed using the statistical software
program Statistica ver. 5.0 (StatSoft 1995). Song
was analyzed using Avisoft SASlab Pro soft-
ware, version 3.5b (Specht 1993). Data were
normally distributed, except in one case, when
values had to be log transformed to meet the
criteria required for parametric statistics. Rela-
tionships among different song parameters were
analyzed using Pearson correlations. In one case
a two-tailed post hoc power test (GPower 1998)
was applied to calculate the statistical power. To
test whether song-bout lengths and the number
of phrase types sang in a song bout differ among
females, a one-way ANOVA was used. To com-
pare other song characteristics between females
and males, we applied t-tests for independent
samples and Mann-Whitney U-tests. A Fisher
Exact test was applied to examine whether fe-
males and males differ in the proportion of hav-
ing all four phrase-type categories in their song
bout. The probability level for significance was
set at
a5
0.05. Values are presented as means
6
SE, unless noted otherwise.
RESULTS
FEMALES
As in males, females produced their song in
song bouts and each phrase type was repeated
one or several times before the next one was
introduced. Song bout lengths varied signifi-
cantly among the females (one-way ANOVA:
564 DENITZA PAVLOVA
ET AL
.
TABLE 1. Total number of analyzed phrases, aver-
age number of phrase types sang in a song bout, av-
erage length of the song bout, and total repertoire size
for each female starling. Values are presentedas means
6
SE. A song bout in European Starlings is defined as
a period of at least 5 sec of song with pauses no longer
than 1.5 sec (Eens 1997).
Female
Number
of
phrases
analyzed
Phrase
types per
song bout Song-bout
length (sec)
Reper-
toire
size
1 169 7.4
6
1.1 13.6
6
3.5 17
2 262 8.2
6
1.1 15.8
6
3.6 17
3 192 8.7
6
0.8 17.9
6
2.5 22
4 401 8.3
6
0.4 10.2
6
0.6 26
5 365 7.2
6
0.5 12.9
6
1.0 25
6 388 14.3
6
1.5 25.9
6
2.4 34
7 375 8.3
6
0.8 18.4
6
1.9 24
8 254 8.9
6
0.5 19.7
6
1.1 12
9 317 7.2
6
0.5 13.8
6
1.3 15
10 502 5.6
6
0.3 14.8
6
1.0 11
11 671 9.0
6
0.7 17.6
6
1.3 36
12 371 7.2
6
0.7 20.1
6
1.8 14
TABLE 2. Presence of phrase-type categories (whis-
tle [W], variable [V], rattle [R] and high-frequency [H]
phrase types) in the song bouts of female starlings, and
repertoire size within each category for each female.
A complete song bout in males consists of all four
categories of phrase types, while rattle or high-fre-
quency phrase types could be absent in the song bouts
of some females.
Female
Phrase types
Whistles Variable Rattle High
frequency
15921
25741
3319––
45192–
54192–
681826
721813
817–4
9310–2
10 3 8 – –
11 4 26 2 4
12 1 7 – 6
F
11,195
5
6.8, P
,
0.001) ranging between 10.2
and 25.9 sec with an overall average of 16.7
6
1.2 sec (Table 1). There was also a significant
difference among females in the number of
phrase types sang in a song bout (one-way
ANOVA: F
11,189
5
7.9, P
,
0.001) with a min-
imum of 5.6
6
0.3, a maximum of 14.3
6
1.5
and an overall mean of 8.4
6
0.6 (Table 1).
No females sang their entire repertoire in only
one song bout. In total, we analyzed 4267 phras-
es (with a minimum of 169 phrases per female
and a maximum of 671 phrases per female; Ta-
ble 1). Total repertoire size of females ranged
between 11 and 36 phrase types (21.1
6
2.4,
Table 1) and was not dependent on the number
of phrases that we analyzed (Pearson correlation
test: r
5
0.48, P
5
0.11, n
5
12). Repertoire
size was significantly positively correlated with
the average number of phrase types sang per
song bout (Pearson correlation test: r
5
0.68, P
5
0.01, n
5
12). There was no significant rela-
tionship between the repertoire size and the av-
erage song bout length of a female (r
5
0.25, P
.
0.05, n
5
12), however, the power of the test
was 0.3 (effect size conventions: small
5
0.1,
medium
5
0.3, large
5
0.5). Further, there was
no significant positive relationship between the
repertoire size and the number of phrase-type
categories that a female was observed to sing (r
5
0.47, P
5
0.13, n
5
12).
In general, female song contained all four cat-
egories of phrase types typically presented in
male song. However, only 42% of females pro-
duced all four categories (Table 2). All females
possessed whistle and variable phrase types in
their repertoire while rattle and high-frequency
phrase types were present in only 58% and 67%
of the females, respectively. Most of the song
bouts started with a whistle, although whistle
phrase types could be sang not only as an initial
element, but also at other parts within the song
bout. If the song bout did not begin with a whis-
tle, it always started with a variable phrase type;
we never observed a song bout starting with a
rattle or with a high-frequency phrase type. Rat-
tle phrase types were produced at a rate of 7–16
clicks per second and in a low-frequency range
(0.5–4 kHz), similar to those of males (Eens
1997). High-frequency phrase types were sang
mostly after the rattle phrase types at the end of
the song bout, but sometimes rattle or variable
phrase types could be produced after them.
Often song bouts contained heterospecific im-
itations incorporated in the different phrase cat-
egories. Although we did not measure the
amount of heterospecific imitations produced
per female, all 12 females incorporated such im-
itations in their song. In Figure 3 we show ex-
amples of a heterospecific imitation of a blue tit
and of an ambulance (the aviary was situated
FEMALE SONG IN EUROPEAN STARLINGS 565
FIGURE 3. Examples of heterospecific imitations
sung by female starlings: A) Blue Tit (Parus caeru-
leus) imitation by a female starling, B) Sonogram of
an actual Blue Tit song, and C) Imitation of an am-
bulance by a female starling.
TABLE 3. Sex differences in the song bout length (SBL), total repertoire size (RS), and repertoire size within
each phrase category for male and female starlings: whistle (W), variable (V), rattle (R), and high-frequency
(H) phrase types. Phrase types sung separately from a song bout involved only whistles (W*). Sex differences
were calculated using t-tests for independent samples, unless otherwise indicated.
Category
Females
Min Max Mean
6
SE
Males
Min Max Mean
6
SE P-value t
SBL 10.3 25.9 16.7
6
1.2 18.4 36.5 26
6
0.9
,
0.001 –6.1
RS 11 36 21.1
6
2.4 29 67 44.3
6
2.0
,
0.001 –7.0
W 1 8 3.7
6
0.6 2 12 6.3
6
0.5 0.002 –3.3
V 7 26 13.9
6
1.9 13 37 23
6
1.4 0.001 –3.8
R 0 4 1.3
6
0.4 5 15 9.3
6
0.6
,
0.001 –9.6
H 0 6 2.3
6
0.7 0 9 5
6
0.4 0.001 –3.5
W* 0 1 0.2
6
0.1 0 5 0.7
6
0.2 0.08 100
a
a
Value is the test statistic (U) from a Mann-Whitney U statistical test.
nearby a hospital). This ambulance imitation
was observed in 5 out of 12 (42%) females.
‘‘Double voicing’’ was also frequently observed,
occurring in all four categories of phrase types.
COMPARISON BETWEEN FEMALES AND
MALES
Twenty-three out of 24 (96%) males produced
all four categories of phrase types in their song
bouts (high-frequency phrase types were miss-
ing in the song of one male), compared to only
5 out of 12 (42%) females (Table 3). This dif-
ference was highly significant (Fisher Exact test:
P
,
0.001). For all song categories except the
rattle phrase types, there was an overlap between
males and females, indicating that some females
produced a more complex song than some males
(Table 3). Nevertheless, on average, all song pa-
rameters (total repertoire size, song-bout length,
and repertoire size within the four phrase-type
categories) were significantly higher in males
than in females (Table 3). Males sangon average
seven times more rattle phrase types than fe-
males. The number of phrase types that were
sung outside the song bout did not differ be-
tween the sexes (Table 3).
DISCUSSION
Here we described in detail the organization of
spontaneous song, and demonstrated sex differ-
ences in song complexity and song composition
in starlings. In many previous studies exploring
female song in passerines, song was induced by
testosterone administration (Kriner and Schwabl
1991, Hausberger and Black 1991, Hausberger
et al. 1995a, Vallet et al. 1996), thus data on
spontaneous song in female birds are often in-
complete. Although the spontaneous song of fe-
male starlings has been previously investigated
(Hausberger et al. 1995b, Henry and Hausberger
2001), until now it has not been described in
detail.
566 DENITZA PAVLOVA
ET AL
.
As established previously for male starlings,
females also produce a complex song. With
some females singing song bouts of more than
30 seconds of uninterrupted song, female Euro-
pean Starlings probably have of one of the most
complex singing behaviors in temperate-zone
songbirds. In general, the organization of the
song was similar in both sexes. All four cate-
gories of phrase types (whistle, variable, rattle,
and high-frequency phrase types) typically pre-
sented in a male starling song bout were also
found in the song of females. Hausberger et al.
(1995a, 1995b) reported that the clicks and the
high-pitched trills (corresponding to rattle and
high-frequency phrase types) were mostly ab-
sent from females’ repertoire, whereas in our
study only two females produced neither rattles
nor high-frequency phrase types and most pos-
sessed either one or the other song category. A
possible explanation for this difference might be
the difference in the methodology of recording
female song: females were always recorded in
individual cages and separate anechoic rooms in
the studies of Hausberger et al. (1995a, 1995b)
while in our study females were housed together
in large social groups, which might better rep-
licate their natural environment. This might sug-
gest that rattles and high-frequency phrase types
are important in a social context. In agreement
with this, Chaiken et al. (1993) reported that
50% of tape-tutored male starlings produced ab-
normal rattle and high-frequency phrase types.
Further studies should examine whether the ob-
served differences in the occurrence of rattle and
high-frequency phrase types in female starling
song are due to population differences or social
housing conditions. Finally, compared to males,
a significantly lower proportion of females sang
all four categories of phrase types.
Similar to males (Eens et al. 1992a), all 12
females incorporated heterospecific imitations in
their song. Although we did not measure the oc-
currence of vocal mimicry quantitatively, it was
clear that vocal mimicry is a common feature of
the female starling song. In one case, almost half
of the females shared a heterospecific imitation
(ambulance siren). At this time, it is unclear
whether this shared heterospecific imitation was
learned from the heterospecific sound source,
from conspecifics, or from both.
At present, we can only speculate as to why
some females do not sing all four categories of
song while others do. Individual variation could
arise from differences in song-learning abilities
or perhaps due to motor constrains on vocal per-
formance (Podos 1996, Nowicki et al. 2002).
Song learning has rarely been studied system-
atically and experimentally in female songbirds
(Riebel 2003, but see Yamaguchi 1998, 2001),
thus detailed data are lacking about when, from
whom, and how long it takes for female starlings
to learn their songs. As song requires complex
learned motor skills involving coordination of
the syringeal respiratory and musculature, pro-
ducing sounds such as rattles and high-frequen-
cy phrases, might be costly. Suthers and Goller
(1997) stated that rapidly trilled phrases with mi-
nibreaths (as the rattles) should be particularly
costly to produce, since switching between ex-
piration and inspiration involves increased mus-
cular effort. Although it is possible that rattle
and high-frequency phrases are more difficult or
costly to produce than the two other categories,
this requires further study. Finally, the observa-
tion that even after testosterone administration
not all females were observed to sing high-fre-
quency phrase types (see Hausberger and Black
1991, Hausberger et al. 1995a) may suggest that
organizational rather than activational effects are
responsible for this constraint.
Females that possessed all phrase categories
were not necessarily those with the largest rep-
ertoire size. Given that song complexity is often
measured in terms of the repertoire size, our re-
sults may suggest that the presence (or absence)
of phrase-type category conveys other informa-
tion than complexity of the song. The idea that
different song features might hold specific in-
formation and serve a special function was first
proposed by Marler (1960). Since this time, ev-
idence has accumulated suggesting that there are
different functions for different songs in male
birds (Vallet et al. 1998, Leboucher et al. 1998),
whereas, no data are as yet available showing
whether this might hold true for females.
For both male and female starlings, it has
been shown that they can acquire new phrase
types in adulthood (Eens et al. 1992a, Eens
1997, Hausberger et al. 1995a, Mountjoy and
Lemon 1995). Whether females that were ob-
served singing only two out of four phrase type
categories (whistles, variable phrase types) can
produce the other two categories of phrase type
(rattles, high-frequency phrase types) later in life
remains to be investigated. The fact that all fe-
males were at least in their third calendar year
FEMALE SONG IN EUROPEAN STARLINGS 567
when recorded, makes it highly unlikely that the
observed individual differences in song compo-
sition are due to age differences.
All song measurements that we compared be-
tween sexes (total and phrase-type category rep-
ertoire size, song-bout length, and the presence
of the four phrase-type categories in a song
bout) were significantly higher in males than in
females demonstrating that overall song com-
plexity in males is higher than in females. In this
respect, our results differ strongly from the re-
sults of Hausberger and Black (1991) and Haus-
berger et al. (1995a). They reported that the rep-
ertoire size of females is only slightly different
from males, consisting of up to 16 whistles and
between 8 and 34 warbling motif types (‘‘motif’’
is the equivalent for ‘‘phrases’’ according to the
terminology of Hausberger et al. 1995a; whistles
and warbling motifs are considered separately).
However, since their studies were carried out af-
ter testosterone treatment of females, we cannot
determine whether this is due to population dif-
ferences or to testosterone manipulation. Con-
versely, for the repertoire size of all phrase cat-
egories except for the rattle phrase types, we
found an overlap between sexes indicating that
some females have a more complex song than
some males. Overlapping repertoire sizes have
recently also been found in other temperate spe-
cies (Yamaguchi 1998). Our findings of sex dif-
ferences in song production are in line with pre-
vious findings that the volume of several song
control nuclei in female starlings is smaller than
in males, but also compared to other species, sex
dimorphism in the song system is much smaller
(Bernard et al. 1993).
For male starlings it has been shown previ-
ously that there is a highly significant positive
relationship between repertoire size and average
song bout length (Eens et al. 1991a). In females,
however, no significant positive correlation was
found. But since the power of the statistical test
was not large, we also cannot rule out that these
two traits were positively related. Our results
also showed a substantial amount of variation
among females in both repertoire size and song
bout length. A large number of studies on male
song production have emphasized the signifi-
cance of individual variation for assessing male
quality. At present, there is a little doubt that
large repertoires in males have arisen through
sexual selection by female choice (MacDougall-
Shackleton 1997), whereas it is still unknown
whether song complexity functions as a potential
indicator trait in females (but see Langmore et
al. 1996). Given that there is accumulating evi-
dence that mutual mate choice may be much
more common than previously thought (Johns-
tone et al. 1996, Amundsen 2000, Bergstrom
and Real 2000, Jones et al. 2001), future studies
should address whether female song signals
quality in starlings and other songbird species.
ACKNOWLEDGMENTS
DP was supported by a doctoral grant of the Fund for
Scientific Research Flanders, Belgium (FWO-Flan-
ders). This study was also made possible through fi-
nancial support from the Research Council of the Uni-
versity of Antwerp (NOI-BOF UA 2002) and by a re-
search project of the FWO-Flanders (G. 0420.02).
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