Physiology & Behavior 82 (2004) 905–912
Shy and bold great tits (Parus major): body temperature
and breath rate in response to handling stress
Claudio Carere a, *, Kees van Oers b
a Department of Animal Behaviour, University of Groningen, The Netherlands
b Department of Population Biology of Animals, Centre for Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Heteren, The Netherlands
Received 2 June 2004; received in revised form 23 July 2004; accepted 29 July 2004
A standard handling protocol was used to test the hypothesis that boldness predicts stress responsiveness in body temperature and
breath rate. Great tit (Parus major) nestlings were taken from the field, hand reared until independence, and their response to a novel
object was assessed. At the age of 6 months, during the active phase (daytime), body temperature was recorded and breath rate was
counted immediately after capture and after 5 min of quiet rest in a bag. A second group of birds of two lines bidirectionally selected for
the same trait was tested during the inactive phase (nighttime). During the active phase, body temperature and breath rate were higher in
the first than in the second measurement. In the second measurement, shy individuals showed higher body temperature than bold
individuals. In the inactive phase, values of both parameters were lower than in the active phase. Body temperature was lower in the first
measurement than in the second measurement and no line difference emerged. Breath rate was higher in shy than in bold individuals and
did not differ between the two measurements. Females had higher body temperatures than males, probably due to their lower weight,
because body temperature was negatively correlated with body mass. The results indicate that body temperature and breath rate are
indicators of acute stress in songbirds and that differences in personality traits during the juvenile phase are reflected in differential stress
responsiveness later in life.
D 2004 Elsevier Inc. All rights reserved.
Keywords: Handling stress; Coping; Boldness; Personality; Breath rate; Body temperature; Sex differences; Birds
In birds, standardised handling protocols have been
widely used to assess the hypothalamus–pituitary–adrenal
(HPA) axis response. In most species, the rise in glucocorticoids
occurs within 3 min following handling . Recent
studies have shown that birds respond to such protocols also
with a fast rise in body temperature. This phenomenon can
be considered as a genuine bemotionalQ fever, because it can
be blocked by salicylate and is usually associated with
tachycardia [2,3]. A rise in body temperature is recognised
* Corresponding author. Center for Cellular and Molecular Neurobiology,
Behavioural Neuroendocrinology Research Group, University of
Liège, 17 place Delcour (Bat. L1), B-4020 Liège, Belgium. Tel.: +32 4
3665973; fax: +32 4 3665971.
E-mail address: C.Carere@ulg.ac.be (C. Carere).
as a typical component of the emotional stress response also
in rats and mice [4–8], as well as in other mammals, birds
and reptiles [3,9–13].
In birds, body temperature has been mainly studied in the
framework of the energetic of endotherms. Overall, it is
higher than in mammals, it decreases with increasing body
mass, and is affected by resting phase, circannual variations
and sex, females exhibiting slightly higher values than
Breath rate, the frequency of respiratory acts, is a
parameter for which much less information is available in
birds. Breathing frequency could respond to fearful stimuli
or emotions similarly to cardiovascular parameters, such as
heart rate, because both are controlled, at least in part, by the
autonomic nervous system. Following handling, eider ducks
(Somateria mollissima) displayed a tachycardia for 2–3 min
without any visible motor response . Such parameters are
0031-9384/$ - see front matter D 2004 Elsevier Inc. All rights reserved.
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912
index of the emotional and stress response , but are
difficult to obtain in a small songbird. Recently, breath rate
has been counted in great tits about 18 h following social
defeat (Parus major), but no effect was detected, probably
because an increased activity of the adrenergic system
occurs only in the very short term following exposure to a
stressful stimulus .
Individuals differ nonrandomly in the way they deal with
stressors and novelties and appear to vary along a
behavioural continuum from shy to bold [15–17]. These
differences covary with other behavioural traits, such as
aggression, exploration, risk taking, fearfulness and reactivity:
for example, bold and less fearful individuals are
more aggressive than shy and fearful individuals [18–24].
Several lines of evidence, including selection lines experiments,
suggest that these differences are aspects of a
coherent and heritable behavioural organization maintained
by natural selection [21–25]. Such individual behavioural
organizations are referred to as behavioural syndromes,
predispositions, profiles, coping styles, strategies, and axes
[26,27], comparable to human personalities . In rodents,
proactive personalities (bold, bactiveQ and aggressive
animals) are associated with high neurosympathetic activity
and low HPA reactivity, whereas reactive personalities (shy,
bpassiveQ and less aggressive animals) are associated with
high cardiac parasympathetic activity and high HPA
In the great tit (P. major), a small passerine bird, many
individuals show extreme phenotypes within a given
population, being bfastQ (or bold) or bslowQ (or shy) in
exploration tasks, including novelty responses . Recent
studies demonstrate the presence of considerable amount of
both additive genetic variation and dominance genetic
variation of such personality traits in wild great tit
populations  and selection lines experiments have
shown high heritability for early exploratory behaviour
based on four generations of artificial selection . These
trait characteristics are relatively stable across age .
They correlate both phenotypically and genetically with
differences in aggression [19,24,32], foraging behaviour
[15,33], response to social stress and risk-taking behaviour
[12,34–36]. Therefore, they may indeed reflect personalities
[27,36]. The lines show resemblance to selection lines
established from wild house mice populations [18,24,27].
This resemblance includes also physiological parameters
involved in the stress response: the great tit data on breath
rate indicate a trend for higher levels in the line of slow
individuals , while data on the adrenocortical response
indicate higher HPA reactivity in the same line . The
great tit lines also resemble two lines of leghorns originally
selected for productivity traits, the so-called high feather
pecking frequency (HP) and low feather pecking frequency
(LP) lines . Hens of the LP line, that resemble shy great
tits, had higher basal and stress-induced (manual restraint)
plasma corticosterone levels than hens of the HP line, that
resemble the bold great tits [37,38]. Hens of the LP line also
showed higher parasympathetic response than birds of the
high feather pecking line .
This study was designed to test how great tits different
for shyness and boldness respond physiologically (body
temperature and breath rate) to an unpredictable and acute
stressful event (capture and handling). We tested two
independent groups, one during daytime (active phase)
and one during nighttime (inactive phase). The nighttime
group was tested primarily in an attempt to record minimum
resting levels. We hypothesised that shy individuals show
higher or more prolonged responses than bold individuals in
both parameters [10,12,21,30,39].
2.1. Subjects and housing
The great tit is a territorial, nonmigratory passerine bird
(body mass: 16–20 g) inhabiting woods and parks. The
group of birds tested during the active phase consisted
originally of 90 chicks collected from a wild population at
the age of 10 days in May–June and hand reared under
standard conditions until independence . From independence
onwards (days 25–30 after hatching), birds were
housed individually in standard cages of 0.90.40.5 m
with a wooden bottom, top, sides and rear walls, a wiremesh
front and three perches. They were kept under natural
light conditions (LD 10:14 h during the period of the stress
protocol, December 1998), and had auditory and visual
contact with other individuals housed in the same room.
Food (commercial seed mixture, sunflowers and a protein
rich mixture supplemented daily with mealworms, Tenebrio
molitor) and water were provided ad libitum.
The birds tested during the inactive phase were 16 adult
male great tits (2–3 years old) originating from a program of
bidirectional artificial selection started in 1993 on the basis
of the outcome of exploration tests carried out at the age of
30–40 days . Lines did not differ in body mass or tarsus
length. The birds belonged to the third and fourth
generation, 6 of the Slow (shy) and 10 of the Fast (bold)
line. They were housed and maintained as described above.
Birds were sexed with molecular markers . Body
mass and other morphometric measurements were taken
about 2 weeks before the stress protocol.
2.2. Novel object tests
Two tests were carried out at the age of 35–40 days after
hatching, introducing a novel object on one of the outer
perches. A penlight battery was used on the first day and an
8-cm pink rubber toy on the second day. Birds were
characterized for shyness and boldness assessing their
latency to approach the object and the shortest distance to
it within 120 s. The results for each test were converted
linearly to a 0–5 scale. A score of 5 was given when the bird
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912 907
pecked the object and a score of 0 was given when the bird
did not land on the perch with the object [15,23]. The sum
of the test scores, ranging from 0 to 10 is the shyness–
boldness trait. We categorised as bshyQ all individuals with
scores from 0 to 3 (included) and bboldQ all individuals with
scores from 6 (included) to 10. Twenty-nine birds matching
these criteria were selected for the experiment (14 bboldQ,15
bshyQ individuals; mean scoreFS.E.M.=7.3F0.4 and
0.9F0.3; Mann–Whitney U-test z= 4.7, pb0.001). The
birds of the selection lines were tested in the same way to
check for the line difference in the juvenile phase (fast line
mean scoreFS.E.M.=7.3F0.5; slow line=0.0F0.0, z= 3.3,
pb0.01) and in adulthood (fast line mean scoreFS.E.M.=
7.8F0.7; slow line=3.4F1.3; z= 2.35, p=0.02).
2.3. Handling stress protocol and physiological
The adult males of the selection lines were tested during
the inactive phase at the end of the dark period, between 0630
and 0730 h. The other group of birds was tested during the
active phase between 0900 and 1200 h. Each bird was tested
according to the following procedure: first, the subject was
chased in its home cage and the time was measured from the
moment the cage was entered with the right hand until the
bird was caught (catching time). This time scored zero during
the inactive phase, because birds were caught in the darkness
and care was taken to avoid waking them up. After capture,
one of two physiological parameters, either body temperature
(T1) or breath rate (B1), was measured immediately; afterwards,
the bird was put in a cotton bag hanging apart and a
second measurement of the same parameter was taken after 5
min (T2, B2). After the second measurement, the bird was
released in its home cage. Sixty minutes later, the same
procedure was used to measure the second physiological
parameter. The assignment of which of the two parameters
was measured first was random. In the birds tested during the
inactive phase, breath rate was measured immediately after
(i.e., few seconds) body temperature.
Body temperature was measured with a thermometric
probe (AMR Therm—30+100 NTC TYP C 2244-1,
AHLBORN Mess-und Regelungstechnik D-8150 HOLZ-
KIRCHEN—P.O.B 12 60, Germany) constantly kept in
warm water (30–35 8C). The probe was inserted in the
cloaca for 10 mm. It took approximately 5–10 s, until the
value on the display became stable. Breath rate was
obtained by counting the breast movements during 60 s
while firmly keeping the bird in the hand. Body mass was
measured with an electronic balance to the nearest 0.1 g
and tarsus with sliding calipers to the nearest 0.1 mm 2
weeks before the tests.
2.4. Data analysis
Correlational analysis (Spearman correlation coefficient)
was used to explore the association between catching time,
body mass, body temperature and breath rate. To test if sex
or type affected catching time, univariate analysis of
variance with the two variables as fixed factors including
their interaction was run with body temperature or breath
rate as dependent variables. A similar analysis was run to
check the effect of sex and type on body mass. For the
analysis of the stress response in relation to type (shy and
bold), sex and sampling time (first and second measurement),
we used parametric factorial analysis of variance
considering type and sex as grouping factor and sampling
time as repeated-measure factor (two levels). Variance was
homogeneous across the four subgroups. Multiple comparisons
for the variable type, separately for the two sampling
times, were performed by Tukey–Kramer least significant
difference (LSD) test. The use of this test is recommended
even in the absence of significant main or interaction effects
in the analysis of variance , because the procedure
protects from the increased probability of type I errors due
to the repeated measure. An overall model pooling the two
groups of birds was run to test the effect of activity period.
When necessary, data were normalized by log transformation
prior to the parametric analyses. All tests were two
tailed. Significance level was a=0.05.
3.1. Active phase
Males were significantly heavier than females [means
and standard errors: 19.34F0.23 vs. 18.18F0.17 g, respectively,
F(1,25)=5.7, pb0.004] and no effect of type
[ F(1,25)=0.003, p=0.96] or its interaction with sex
[ F(1,25)=1.2, p=0.29] were found. No sex effects were
found in the novel object tests [sex, F(1,25)=1.8, p=0.19;
sextype, F(1,25)=1.4, p=0.25].
In the body temperature session, catching time ranged
between 4 and 55 s (mean: 21.8F14.5 s), but it did not
correlate with any of the two measurements (Table 1), and
did not differ in relation to type [ F(1,25)=0.9, p=0.35] or
sex [ F(1,25)=0.41, p=0.53]. Computing the correlation
Association (Spearman correlation coefficient) between the variables
catching time (CtT: body temperature session; CtB: breath rate session),
body temperature (T1: first measurement; T2: second measurement) and
breath rate during the active phase (B1: first measurement; B2: second
CtT CtB T1 T2 B1
T1 0.16 0.15
T2 0.04 0.20 0.74**
B1 0.32 0.21 0.19 0.24
B2 0.13 0.07 0.11 0.12 0.41*
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912
separately for the two lines yielded similar results. In the
breath rate session, it took significantly less time to catch a
bird than in the body temperature session [ F(1,56)=5.3
pb0.01], values ranging between 4 and 40 s (mean:
11.9F9.4 s). Catching time in the breath rate session did
not differ in relation to type [ F(1,25)=0.01, p=0.92] or sex
[ F(1,25)=0.05, p=0.82] and did not correlate with any of
the two measurements (Table 1). No significant correlation
was found between body temperature and breath rate in any
of the two measurements, whereas first and second
measurements showed a positive correlation in both
parameters (Table 1).
Body temperature was significantly higher in the first
measurement than in the second one [sampling time,
F(1,25)=23.9, pb0.01, Figs. 1a and 2a]. No overall effect
of type was evident [ F(1,25)=1.1, p=0.29]. In shy
individuals, the decrease in body temperature in the second
measurement was less marked than in bold individuals
[typesampling time, F(1,25)=3.7, p=0.06, but pb0.05 in
Tukey–Kramer LSD test in the second measurement, Fig.
1a]. Females had higher temperatures than males in both
measurements [sex, F(1,25)=7.9, p=0.01, Fig. 2a] by about
Fig. 2. Body temperature (a) and breath rate (b) in male and female great tits
immediately after capture (T1, B1) and after 5 min (T2, B2) during the
active phase. Values are means+S.E.M. **pb0.01.
Fig. 1. Body temperature (a) and breath rate (b) in shy and bold great tits
immediately after capture (T1, B1) and after 5 min (T2, B2) during the
inactive and the active phases. Values are means+S.E.M. *pb0.05;
0.8 8C. No significant interaction between sex and sampling
time [ F(1,25)=0.01 p=0.97] or between sex and type
[ F(1,25)=0.28, p=0.60] emerged.
Breath rate was also significantly higher in the first
measurement than in the second one [ F(1,25)=4.3, pb0.05,
Figs. 1b and 2b]. No main effect or interaction of type with
sampling time [ F(1,25)=1.1 p=0.31, F(1,25)=0.22, p=0.64,
respectively] was found. Although male birds showed a
more marked decrease in the second measurement, neither a
sex difference [ F(1,25)=1.8, p=0.19, pN0.05 in Tukey–
Kramer LSD test in the second measurement] nor the
interaction between sex and sampling time [ F(1,25)=2.3
p=0.14] was significant (Fig. 2b).
The effect of sex on body temperature disappeared
[ F(1,24)=1.5, p=0.23] when body mass was introduced in
the model of the analysis of variance as a covariate
[ F(1,24)=2.9, p=0.09], indicating that body mass could
explain the sex difference. In fact, body mass showed a
significant negative association with body temperature in
both measurements (r s = 0.44, p=0.02; r s = 0.64, pb0.001,
n=29 for first and second measurements, not shown), but
not with breath rate (r s = 0.19, p=0.32; r s =0.15, p=0.43,
n=29 for first and second measurements, not shown). When
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912 909
the association of body mass with body temperature was
tested separately for the sexes, a significant negative
correlation in both measurements was present in females
(r s = 0.54, p=0.02; r s = 0.63, p=0.004, n=19 for first and
second measurements, Fig. 3a), but not in males (r s =0.45,
p=0.19; r s = 0.08, p=0.82, n=10, for first and second
measurements, Fig. 3b). This latter result was likely due to
the presence of an outlier showing very low values in both
measurements together with the lower sample size in males
3.2. Inactive phase
Body temperature was significantly higher in the second
measurement than in the first one [sampling time,
F(1,14)=9.0, pb0.01, Fig. 1a]. No effect of type or its
interaction with sampling time was evident [ F(1,14)=0.43,
p=0.52; F(1,14)=0.08, p=0.77, respectively]. Breath rate
did not differ between the two measurements [sampling
time, F(1,14)=2.4, p=0.14, Fig. 1b]. No main effect of type
Fig. 3. Body temperature as a function of body mass in females (a) and
males (b) immediately after capture (T1) and after 5 min (T2) during the
or its interaction with sampling time was found, but shy
birds tended to have higher breath rate than bold birds [type,
F(1,14)=3.5, p=0.08; typesampling time, F(1,14)=2.4,
Pooling in one model the groups tested in the two activity
phases revealed a significant effect of activity period in both
parameters [ F(1,41)=109.2, pb0.001 for body temperature;
F(1,41)=10.6, pb0.01 for breath rate, Fig. 1a and b], and a
significant interaction with sampling time for body temperature
only [ F(1,41)=32.9, pb0.001]: overall, values were
higher during the active period, and for body temperature,
the patterns were opposite (Fig. 1a). A main effect of type
was evident for breath rate [ F(1,41)=4.3, pb0.05, Fig. 1b]:
shy birds displayed higher values than bold birds.
4.1. Response to handling stress in the inactive and the
During the activity phase, catching and handling has
produced a pattern in which both body temperature and
breath rate decreased with time. Values were higher in the
first measurement, immediately after capture, than 5 min
later, when birds had been kept in a bag. During the inactive
phase, when birds were caught during sleep, the pattern was
opposite for body temperature, with values increasing with
time. No difference between the first and second measurements
was found for breath rate. Both parameters had higher
values during the active than during the inactive period. The
comparison between the phases suggests that during the
active phase, at least for body temperature, the first
measurement represents a stress-induced rise and the
decrease observed after 5 min represents the tendency to
return to normal (activity) levels. It could be that catching
time during the light phase affects more breath rate than
body temperature, as suggested by its borderline significant
correlation with the first measurement. Interestingly, the
association with catching time was always negative, i.e.,
shorter times corresponding to higher breath rates, like if a
sudden fearful episode is more effective than the same
stressor acting for a more prolonged time (Table 1). The
overall higher body temperature during the active phase is
not surprising, because the thermostat biological set-point
oscillates through the nychtemeron .
The rise in body temperature in the active phase could be
due to stress-induced hyperthermia, a phenomenon
described in other animal species [5–7]. Catching the bird
and measuring cloacal temperature acted as a stressor and
elicited a very rapid hyperthermic response. In singly
housed mice, 80% of the maximal hyperthermic response
can be reached within 5 min from the start of the stress .
In our case, the motor load due to the increased activity of
the birds attempting to escape from being captured could
have induced thermogenesis, because the birds first had a
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912
high temperature (hyperthermia) in T1 and then a lower
value in T2, but still had a high temperature (emotional
fever). However, no correlation was found between catching
time and body temperature, but we cannot exclude the fact
that it did enhance it or its rapidity. It must be noted that (i)
it took less than 15 s to catch 14 out of 29 birds, a short time
to allow a substantial hyperactivity able to produce thermogenesis
and (ii) the behaviour of the birds before being
caught was variable: some birds were trying to flee, whereas
others were freezing or remaining immobile in a corner of
the cage. Unfortunately, we did not record these individual
responses in detail, but taken together, these points may
explain the lack of a significant correlation. In eider ducks
handled without chasing, cloacal temperature increased
sharply within 4 min . Anticipatory fear for an aversive
event  could also play a role, as it was hypothesised for
farm minks showing very high values in their first
The increase in body temperature may be also due to
emotional fever. Emotional fever has been shown to occur
in birds, as well as in reptiles, in response to gentle handling
and manual restraint [4,5]. However, given our design, it is
not possible to distinguish between a genuine fever,
bwantedQ by the thermostat and characterized by an upward
shift of the set-point temperature, and hyperthermia,
characterized by a rise in central temperature above the
set-point temperature due to an increase in heat load .
The rise in body temperature in the inactive phase could
be due to the transition from resting to activity levels rather
than stress, because values never reached those of the
second measurement during the light phase. The latter are
likely still far from baseline bactivityQ levels. It is expected
that subsequent measurement would lead to the same levels.
In birds, the mean day–night difference is 2.48 8C .
These data provide the first evidence of a hyperthermic
and autonomic response to handling stress in a songbird and
suggest that body temperature and breath rate are indicators
of acute stress in songbirds. They can be easily measured in
field and laboratory condition and should be recorded in
addition to other parameters involving bleeding, such as
corticosterone plasma levels.
4.2. Sex difference
Females displayed higher values of body temperature
than males in both sampling times and a similar trend, but
not significant, was found for breath rate. This finding is
unlikely to be related to the behavioural phenotype, because
no sex differences were found in the novel object score
during the juvenile phase. It could be either due to
differential stress responsiveness between the sexes, or to
a sex difference in baseline levels.
Sex is thought to be a major variable conferring
differential vulnerability to stress. Results are, however,
often contrasting and likely depending on the ecology of the
species, as well as on the type of stressor used [42–44]. In
birds, males have been shown to be more susceptible than
females in their HPA responsiveness [1,45]. Sex differences
in basal levels of body temperature in the same direction of
ours have been found in many species . In great tits,
when daily energy expenditure was measured after injection
of doubly labelled water in an experiment testing the costs
of parental effort following a clutch size manipulation,
females showed higher values than males regardless of the
treatment . A similar difference in energy expenditure
between the sexes was also found in other passerine species
[47–49], and this may reflect a general pattern.
Overall, the literature survey in birds and the negative
correlation with body mass (Fig. 3), sexually dimorphic in
great tits, point in the direction that the difference may be
independent of the stress procedure. The sex difference
might simply be a physiological adaptation to a sex-specific
difference in thermal conductance, which is negatively
correlated with body mass in homeothermic organisms .
However, the magnitude of the sex difference in our birds
(0.7 8C in T1 and 0.8 8C in T2) was higher than those
reported in the literature (0.3–0.5 8C) , suggesting a
stress-induced enhancement. Therefore, we hypothesise that
in species that are sexually dimorphic in body mass, the
lighter sex (usually females) might face higher energetic
costs than males following stress.
4.3. Effect of shyness and boldness
It was hypothesised that shy individuals are more
susceptible to handling stress than bold individuals. In
accordance with this, we found that during the active phase
in shy individuals, the decrease in body temperature in the
second measurement was significantly less marked than in
bold individuals. Different temperament traits predict differential
stress responsiveness over time.
In male farm minks from confident and fearful breeding
lines undergoing a repeated capture stress protocol, no
significant line differences in the body temperature response
were detected after first capture, but during immobilisation,
fearful animals increased or maintained their response
levels, while confident ones decreased them . This
pattern is very similar to that observed in our great tits
strengthening the hypothesis that a higher reactivity to
catching and handling characterizes shy and fearful individuals.
It is important to emphasize that this differential
response was found in birds taken from a wild population in
which a consistent variation in personality traits has been
recently demonstrated together with its heritability .
From these data, the body temperature response seems to be
a sensitive marker of both the short-term stress response and
the personality trait.
Assuming a similar response as for heart rate, shy
individuals were expected to display higher values. We
found that overall shy individuals exhibited higher breath
rate than bold individuals, confirming a previous trend in
the same species . This expectation came from the fact
C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912 911
that respiration, being likely under vagal control, can be
considered controlled by the parasympathetic system which
is supposed to be the dominating system in shy and
bpassiveQ animals [21,39].
In rodents, the rise in body temperature is simultaneously
accompanied by increases of plasma corticosterone, while
lipopolysaccaride-induced fever also elevates the amount of
biologically available corticosterone [52,53]. This is in line
with previous findings that shy individuals show higher
stress-induced corticosterone levels than bold individuals
[29,30,35,54]. Further studies, including an accurate comparison
between the temporal dynamics of the body
temperature and the HPA axis reactivity, are needed to
explore this possibility and to further validate body temperature
as a physiological marker of the stress response in
birds. On the whole, our data provide evidence for a
physiological difference in individuals showing differences
in bpersonalityQ traits in birds.
CC and KvO were supported by NWO grants SLW 805-
33-324p and SLW 805-33-323. We thank Ton Groothuis,
Henk Visser, Serge Daan, Irene Tieleman, Simon Verhulst,
Piet Drent, Jaap Koolhaas and Arie van Noordwijk for helpful
suggestions and discussion. Flavia Chiarotti and Luca Salvati
gave statistical advice. We are also grateful to Bart van
Ijmeren for animal caretaking, Christa Mateman for molecular
sexing and an anonymous referee for his help in
improving the manuscript. The experiments presented here
comply with the bPrinciples of animal careQ, publication No.
86-23, revised 1985 of the National Institute of Health and
with the current laws of the country in which the experiments
were performed. Permission for the physiological measurements
was granted by the legal dDierexperimenten
CommissieT of the KNAW, CTO license no. CTO.98-04/00
and CTO.99-02/00 to KvO. This is publication number 3394
of the Netherlands Institute of Ecology (NIOO-KNAW),
Heteren, The Netherlands.
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