body temperature and breath rate in response to handling stress

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body temperature and breath rate in response to handling stress

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

Abstract

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

1. Introduction

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 [1]. 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

males [14].

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 [3]. Such parameters are

0031-9384/$ - see front matter D 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.physbeh.2004.07.009


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C. Carere, K. van Oers / Physiology & Behavior 82 (2004) 905–912

index of the emotional and stress response [8], 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 [12].

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 [28]. 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

reactivity [21,22,29,30].

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 [15]. 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 [31] and selection lines experiments have

shown high heritability for early exploratory behaviour

based on four generations of artificial selection [23]. These

trait characteristics are relatively stable across age [23].

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 [12], while data on the adrenocortical response

indicate higher HPA reactivity in the same line [35]. 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 [27]. 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 [39].

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. Methods

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 [15]. 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 [23]. 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 [40]. 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

measurements

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 [41], 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. Results

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

Table 1

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

measurement)

CtT CtB T1 T2 B1

CtB 0.38*

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*

N=29.

* pb0.05.

** pb0.01.


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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;

**pb0.01.

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

(Fig. 3b).

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

active phase.

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,

p=0.14, respectively].

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. Discussion

4.1. Response to handling stress in the inactive and the

active phase

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 [14].

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 [7].

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


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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 [3]. Anticipatory fear for an aversive

event [7] could also play a role, as it was hypothesised for

farm minks showing very high values in their first

measurements [10].

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 [4].

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 [14].

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 [14]. 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 [46]. 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 [50].

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) [14], 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 [10]. 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 [51].

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 [12]. 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.

Acknowledgements

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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