J Ornithol (2007) 148 (Suppl 2):S169–S178
DOI 10.1007/s10336-007-0175-8
REVIEW
Stress, corticosterone responses and avian personalities
John F. Cockrem
Received: 26 December 2006 / Revised: 13 June 2007 / Accepted: 14 June 2007 / Published online: 11 July 2007
Ó Dt. Ornithologen-Gesellschaft e.V. 2007
Abstract Birds are constantly responding to stimuli from
their environment. When these stimuli are perceived as
threatening, stress responses are initiated, with activation
of the hypothalamo-pituitary-adrenal axis and the release
of corticosterone from the adrenal gland. The basic emo-
tion of fear is also experienced during a stress response.
Corticosterone stress responses and behavioural responses
to stimuli vary markedly between individual birds, raising
questions about the significance of these individual dif-
ferences and about the relationship between corticosterone
responses and fearfulness in birds. Although fearfulness
can be challenging to measure, data from several species
indicate that corticosterone responses and fear behaviour
responses are linked in individual birds. Consistent profiles
of behavioural responses of birds to a wide range of stimuli
can be identified and are called personalities. Personalities
vary along a continuum, but are usually classified as
proactive or reactive. Individual corticosterone and
behaviour responses depend on each bird’s personality.
Birds with proactive personalities have relatively active
behavioural responses and relatively low corticosterone
stress responses, whilst birds with reactive personalities
have relatively passive behavioural responses and large
corticosterone responses. Relationships between the phys-
iological and behavioural characteristics of avian person-
alities can now be explored in detail to determine the
Communicated by F. Bairlein.
J. F. Cockrem (&)
Institute of Veterinary, Animal and Biomedical Sciences,
Massey University, Palmerston North, New Zealand
e-mail: J.F.Cockrem@massey.ac.nz
significance of individual differences in stress responses
and personalities in birds.
Keywords Corticosterone
Stress
Fear
Personality

Behaviour
Japanese quail
Great tit
Chicken

Adelie penguin
Introduction
Birds live in complex environments that can change at any
time. When changes in their local environment are poten-
tially harmful, then birds, like other vertebrates, adjust by
generating stress responses. These are integrated neuroen-
docrine responses (Ellis et al. 2006) that involve activation
of the hypothalamo-pituitary-adrenal (HPA) axis and
secretion of cortisol or corticosterone. When an animal
perceives a stimulus to be a threat and the HPA axis is
activated, the animal also experiences the basic emotion of
fear (LeDoux 1996; Labar and LeDoux 2001). Corticoste-
rone, the major glucocorticoid hormone in birds (Cockrem
2007), has metabolic actions such as increasing blood glu-
cose levels, can affect behaviour, and may have other actions
that help birds respond to stressors (Sapolsky et al. 2000).
Stress responses can differ markedly between individual
birds (Littin and Cockrem 2001; Cockrem and Silverin
2002a; Cockrem 2005) and mammals (Guimont and
Wynne-Edwards 2006). Animals also differ in their per-
sonalities, with personalities defined as consistent behavio-
ural profiles (Dingemanse and Reale 2005; Steimer and
Driscoll 2005). It has been suggested that different stress
responses in mammals may be associated with different
personalities (Korte et al. 2005). The study of personalities is
well established in birds (Carere et al. 2005; Groothuis and
Carere 2005); stress responses, measured as corticosterone
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responses to handling, have been studied in many species of
birds (Silverin 1998), and fear behaviour has been examined
in chickens, Gallus domesticus, and Japanese quail, Cotur-
nix coturnix japonica (Jones 1996). Stress responses, fear
behaviour and personalities will be considered together in
the current review to determine how endocrine stress
responses are related to personality in birds.
Stress and corticosterone responses
Stress
It has been said that the normal expression of adaptive
behaviour depends on some optimal level of stress (Levine
1971), but what is stress? A surprising number of publi-
cations that discuss stress in animals do not actually define
the term stress. When definitions are given they vary from
general (e.g. the nonspecific response of the body to any
demand made upon it; Selye 1974) to specific [e.g. a
stressor is any stimulus (behavioural, environmental or
demographic) that provokes a physiological stress re-
sponse, as measured by an increase in glucocorticoid
secretion; Creel 2001]. The definition that will be used here
is that ‘‘stress is a state when the hypothalamo-pituitary-
adrenal (HPA) axis is activated with increased secretion of
glucocorticoids in response to a stressor’’.
General definitions of stress encompass responses of
animals to a wide range of stimuli. These responses can
include one or more of activation of the sympathetic ner-
vous system, changes in behaviour, and increased secretion
of glucocorticoids. However, the sympathetic nervous
system can be activated or behaviour can change when
animals respond to stimuli that do not represent a threat to
the animal. For example, a bird may have a small increase
in heart rate and temporarily stop feeding when it sees
another bird flying some distance away. These are re-
sponses to a stimulus (sight of another bird) that does not
represent a threat, so this stimulus would not be a stressor.
Instead, stimuli are stressors only when they activate the
HPA axis, as shown diagrammatically in Fig. 1. Stressors
can be classified as physical or emotional. Physical stres-
sors involve signals arising from the body with a distur-
bance of physical or chemical tissue parameters, such as a
fall in blood glucose concentrations. Emotional stressors
require the appraisal of information in relation to stored
information that is either learned or inherited, and require
processing in the limbic or cortical areas of the brain. An
example of an emotional stressor is the sight of a potential
predator.
An increase in plasma corticosterone can be used to
indicate when and to what degree a bird is experiencing
stress. This contrasts with measurements of increases in
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J Ornithol (2007) 148 (Suppl 2):S169–S178
A Stimulus that is not a stressor
Detection of stimulus
Sympathetic nervous Behaviour
system response response
B Stimulus
Detection of stimulus
Stimulus determined to be a physical
challenge or perceived as a threat
Stimulus becomes a stressor
Sympathetic nervous HPA axis Behaviour
system response response response
Stress response
Fig. 1 Responses of birds to a stimulus (a), and to a stimulus that
initiates a stress response (b). A stimulus that is detected as a physical
challenge or is perceived as threatening becomes a stressor when the
hypothalamo-pituitary-adrenal (HPA) axis is activated
sympathetic nervous system activity or observations of
changes in behaviour which do not unequivocally indicate
that a bird is experiencing stress. An example of the use of
corticosterone responses to determine when birds were
experiencing stress was a study of corticosterone and
behavioural responses of captive great tits, Parus major
(Cockrem and Silverin 2002b). Great tits in an aviary were
exposed for 60 min to a predator (stuffed Tengmalm’s owl,
Aegolius funereus) or to a stuffed brambling, Fringilla
montifringilla, a passerine bird that is not a threat to great
tits. Great tits showed similar changes in behaviour when
exposed to the owl and the brambling, whereas there was a
corticosterone and hence stress response to the sight of the
owl but no corticosterone response to the brambling.
Corticosterone responses
Corticosterone secretion from the cortex of the adrenal
gland in birds is stimulated by adrenocorticotropic hor-
mone (ACTH) from the pituitary gland, which in turn is
stimulated by corticotropin-releasing factor (CRF) and
J Ornithol (2007) 148 (Suppl 2):S169–S178 S171

arginine vasotocin (AVT) from the hypothalamus (Carsia Japanese quail (A) Broiler chicken (B)
4
and Harvey 2000). The HPA axis is activated in response to 6
stressors, with an increase in plasma corticosterone con-
4
centrations detectable one to two minutes after initial 2

Corticosterone (ng/ml)
exposure to a stressor (Dawson and Howe 1983; Romero 2

and Reed 2005). Corticosterone responses in birds are re-

0 0
sponses to stimuli from the environment. It is difficult to 0 15 30 60 0 15 30 60
measure responses of birds to natural stimuli, so most 10

studies of corticosterone responses in birds describe re- 8

6

sponses to artificial stimuli. Corticosterone responses 6 4

measured in birds are usually responses of free-living birds 4

2
or captive birds in aviaries to capture and handling, or 2

responses of captive birds in cages to removal from their 0 0

0 15 30 60 0 15 30 60
cage and handling. It is generally assumed that birds
Time (min) Time (min)
experience capture and handling as a form of predation
(Silverin 1998), although corticosterone responses to cap- Adelie penguin (C) Great tit (D)
ture by a predator have not actually been measured for any 40
20
bird. Free-living birds are caught, an initial blood sample is
collected and then the birds are held in bags, with further 20

Corticosterone (ng/ml)
10
samples collected for 30–60 min after capture. Cortico-
sterone concentrations in free-living birds usually rise 0 0

rapidly for 10–15 min after capture then rise more slowly 0 10 20 30 0 10 20 30

for the remainder of the sampling period (e.g. Wingfield 80 40

et al. 1992, 1995). Corticosterone responses to handling of 60

free-living birds held in captivity are generally similar to 40 20

those of birds in their natural habitat [e.g. responses of
captive great tits (Cockrem and Silverin 2002a) and free-
living willow tits, Parus montanus (Silverin 1997].
Domesticated birds such as chickens and Japanese quail
have corticosterone responses of much lower amplitude
than those of free-living birds, e.g. responses to 15 min of
continuous handling (chicken; Fraisse and Cockrem 2006)
or to 10 min of physical restraint (Japanese quail; Satterlee
and Johnson 1988).
Intra- and interspecific variation in corticosterone
responses
Corticosterone responses are usually presented and dis-
cussed in the literature in terms of the mean responses of
groups of birds. However, there is considerable variation
between individuals in the magnitude and pattern of their
corticosterone responses, and individual corticosterone re-
sponses may be quite different from mean responses of a
group of birds (Littin and Cockrem 2001; Cockrem and
Silverin 2002a; Cockrem 2005). This can be illustrated by
an examination of plasma corticosterone responses to
handling in two species of domesticated birds (Japanese
quail and chicken, Fig. 2A,B) and of responses to capture
and handling in two free-living birds (Adelie penguin,
Pygoscelis adeliae, and great tit; Fig. 2C,D). Mean re-
sponses could be summarised by stating that corticosterone
increased for 10–15 min in all species then continued to
20
0 0
0 10 20 30 0 10 20 30
Time (min) Time (min)
Fig. 2 Mean (±SE) and individual plasma corticosterone responses to
handling of Japanese quail (A), broiler chickens (B), Adelie penguins
(C) and great tits (D). Quail were obtained from a commercial
supplier and held individually in cages. Broiler chickens were
sampled at a commercial farm. Birds of both species were removed
from their cages, handled for 15 min and then held individually in
boxes for another 45 min. Adelie penguins were caught on nests on
Ross Island, Antarctica, and were held in mesh bags in darkened
boxes after each blood sample was collected. Free-living great tits
were caught and held individually in cages for 10 days then sampled.
They were held in cloth bags after each blood sample was collected.
The great tit data are from the study of Cockrem and Silverin (2002a)
increase in the Adelie penguin, remained high in the great
tit and declined in the quail and chicken. Examination of
the individual corticosterone responses reveals that some
birds had much lower corticosterone responses than others,
with no measurable response at all in one quail, one
chicken and one penguin. The patterns of corticosterone
response also varied, and some individuals of each species
had patterns that differed from the pattern of mean corti-
costerone concentrations. Clearly, any consideration of
corticosterone responses must take into account individual
differences in the same way that the importance of indi-
vidual differences is increasingly recognised in other

123
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studies of groups of animals (Wilson 1998; Bolnick et al.
2003; Steimer and Driscoll 2005).
Intraspecific variation in corticosterone responses in-
cludes variation between individuals and variation within
individuals. The amount of variation in corticosterone re-
sponses raises questions about the consistency of responses
in individual birds, and about the origins and significance
of the individual differences. The consistency of responses
(variation within individuals) has been examined in
chickens, great tits and greylag geese (Anser anser), with
responses of individual birds generally repeatable (Littin
and Cockrem 2001; Cockrem and Silverin 2002a;
Kralj-Fiser et al. 2007). Corticosterone responses of four
great tits are shown in Fig. 3, illustrating how individual
patterns of corticosterone response remained similar on the
three sampling occasions in these birds.
Corticosterone secretion increases when a bird perceives
a stressor (Cockrem and Silverin 2002b), and corticoste-
rone promotes changes in behaviour and metabolism that
are thought to help birds to adjust to stressful situation
(Cockrem et al. 2004). An acute rise in corticosterone in
response to a stressor is generally considered to be bene-
ficial to birds. However, if the corticosterone response to a
stressor is larger than normal, if it persists for longer than
usual, or if basal corticosterone levels are high then it is
widely held that corticosterone may have negative effects.
The existence of variation between birds in the size of their
corticosterone responses, illustrated in Fig. 2, raises ques-
tions about why this variation exists and how it arises. If a
corticosterone response helps a bird respond to a stressor
then why do some birds have relatively small responses?
Conversely, why do some birds have relatively high
Great tit
40 40
20 20
Corticosterone (ng/ml)
0 0
40 40
20 20
0 0
0 10 20 30 0 10
Time (min)
Fig. 3 Individual plasma corticosterone responses to handling of four
great tits sampled on three occasions. Free-living great tits were
caught and held individually in cages for 10 days before being
sampled at intervals of seven days. Great tits were held in cloth bags
after each blood sample was collected. The data are from the study of
Cockrem and Silverin (2002a)
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J Ornithol (2007) 148 (Suppl 2):S169–S178
corticosterone responses if high responses are potentially
deleterious? Cockrem (2005) suggested that birds with
smaller responses are likely to be more successful in a
constant environment and that birds with larger responses
may be more successful in changing environments. This
implies that there is no optimal corticosterone response for
all situations, a concept that is consistent with explanations
of variation in stress responses in mammals (Ellis et al.
2006).
Whilst it has been proposed for mammals that variation
in stress responses results from genetic variation and
adaptive phenotypic plasticity (Ellis et al. 2006), the rela-
tive contributions of genetic variation and phenotypic
plasticity to variation in corticosterone responses in birds
remain unknown. The existence of genetic variation in
corticosterone responses in birds is clearly demonstrated by
the heritability of the magnitude of corticosterone re-
sponses in lines of Japanese quail selected for low and high
responses (Satterlee and Johnson 1988; Odeh et al. 2003).
It has been suggested that genetic variation in corticoste-
rone and cortisol responses arises from natural selection,
which maintains genes for relatively high and low
aggression and produces phenotypes called hawks and
doves (Korte et al. 2005). The hawk–dove model describes
physiological and behavioural characteristics of the two
groups of animals and suggests that both groups can be
successful but in different environmental conditions.
Breeding success, survival and fitness and hence the rela-
tive success of birds with low or high corticosterone re-
sponses have not yet been studied in free-living birds.
Phenotypic plasticity has been defined as ‘‘the mor-
phological and physiological responses of an organism’s
phenotype to a change in environmental conditions’’
(Schlichting 1989), and as ‘‘the extent to which an organ-
ism can change its physiology, behaviour, morphology and/
or development in response to environmental cues’’ (Dufty
et al. 2002). Phenotypic plasticity arises from influences of
the environment throughout the life of an animal (Dufty
et al. 2002), with maternal influences both before and after
birth contributing to differences between adult mammals in
their cortisol stress responses (Maccari et al. 2003;
Cameron et al. 2005). Exposure of mammals to stressors
during development is generally thought to lead to in-
creased reactivity of the HPA axis in adults (Meaney
2001). However, an alternative view is that both relatively
20 30 low or high levels of exposure to adversity during devel-
opment lead to increased responsiveness to stressors in
adulthood.
The extent to which birds show phenotypic plasticity of
corticosterone responses and the origins of such plasticity
have not been characterised in birds. Maternal effects on
corticosterone responses of offspring could be mediated via
maternal corticosterone deposited in eggs (Hayward and
J Ornithol (2007) 148 (Suppl 2):S169–S178
Wingfield 2004), and food availability for chicks may af-
fect corticosterone responses of the birds when they are
adults (Pravosudov and Kitaysky 2006). There are various
approaches to the quantification of phenotypic plasticity,
with the most widely used being the slope of a reaction
norm (Valladares et al. 2006). A reaction norm is a func-
tion that describes for a given genotype the relationship
between strength of an environmental variable and phe-
notype. Reaction norms can be used to indicate the relative
importance of genetic contributions and environmental
effects in the generation of phenotypes (Van Noordwijk
1989; Postma and Van Noordwijk 2005). Animals have
individual reaction norms, so phenotypic variation for a
trait can be described for a population from the reaction
norms of the individuals within the population. A reaction
norm for corticosterone responses in a population of birds
could be determined from individual responses to a stressor
that was applied at different intensities. This approach
could be used to measure reaction norms in species of birds
living in different environments to determine whether the
slopes of reaction norms, and hence the amount of phe-
notypic plasticity in the corticosterone responses of birds,
differ between species. It is predicted that species living in
relatively constant environments will show lower plasticity
then species living in more variable environments.
Corticosterone responses have been measured in many
species of birds in different situations and at different times
of year (Silverin 1998; Romero 2002). Mean responses of
groups of birds of the same species can differ in relation to
weather conditions at the time of sampling, between sea-
sons, between populations and between years, so it is dif-
ficult to interpret the significance of interspecific
differences in corticosterone responses. However, differ-
ences between species in the relative variation between
individual birds may be less than is first apparent. The
magnitude of the corticosterone responses shown in Fig. 2
differed between the four species of birds. The maximum
mean corticosterone concentrations in the Adelie penguins
(at 30 min; Fig. 2c) were 11 times greater than in the
chickens (at 15 min; Fig. 2b). However, when the variation
between individual birds at these times is expressed as
coefficients of variation, the coefficients are the same for
the penguins and chickens (51.4 and 50.5%, respectively).
It is apparent from this example that the relative amount of
variation between individual birds in their corticosterone
responses can be similar across species that have quite
different absolute corticosterone responses.
Fear and corticosterone responses
Activation of the HPA axis when an animal perceives a
stimulus to be a threat is considered to occur simulta-
neously with the basic emotion of fear (LeDoux 1996;
S173
Labar and LeDoux 2001). Fear can be defined as the state
or situation in which an animal perceives a stimulus to be a
threat and in which the animal is generating a behavioural
and/or a physiological response to the stimulus. Fear
behaviour helps an animal to avoid or reduce the possible
consequence of exposure to danger. The quantification of
fear is problematical (Murphy 1978; Miller et al. 2006), but
fear is nonetheless widely measured in chickens and quail
(Jones 1996). The degree of fear experienced by a bird in a
particular situation can potentially be assessed from
behavioural observations, such as measuring the distance to
which a bird can be approached before it flees (flight ini-
tiation distance; Stankowich and Blumstein 2005). How-
ever, it is difficult to determine whether observed
behaviours that may be called fear behaviours actually
reflect an underlying state of fear. Instead, studies of fear
often use behavioural tests in controlled situations to
measure fearfulness, where underlying fearfulness is ‘‘the
propensity to be more or less easily frightened’’ (Jones
1996), or ‘‘a temperament trait defining the general sus-
ceptibility of an animal to react to a variety of potentially
threatening situations’’ (Boissy 1995).
Fearfulness in birds is most commonly measured in
behaviour tests in which birds are placed in new situations
(open field tests) or are presented with novel or startling
stimuli (novel object or startle tests). Another test that is
widely used in chickens and quail is the tonic immobility
test. Tonic immobility (TI) is an unlearned response easily
induced by brief manual restraint in which a bird remains
still and exhibits reduced responsiveness to external stim-
ulation (Jones 1986). TI is thought to be a form of anti-
predator behaviour (Gallup 1977), and it has been
suggested that TI is equivalent to the immobility response
within a predation episode (Ratner 1967). Characteristics
of TI in chickens include temporary suppression of the
righting response, reduced vocalisation, and intermittent
eye closure (Gallup 1977; Jones 1986). TI is induced in
chickens by placing a bird on its side or back and lightly
restraining it, with one hand held over its head and the
other hand placed on its sternum for 15 s (Fraisse and
Cockrem 2006). The handler then slowly removes their
hands, moves back and observes the bird. If the bird rights
itself within 15 s, the induction is repeated up to five-times.
The time to first head movement and the duration of TI are
considered to be positively related to fearfulness, and the
numbers of inductions and head movements to be nega-
tively related to fearfulness (Jones 1988).
Some strains of chicken are generally considered to be
more flighty and fearful than others. Fraisse and Cockrem
(2006) compared corticosterone responses and fearfulness
in white Leghorn and brown Hyline laying hens and found
that corticosterone responses to handling were greater in
white hens. The duration of tonic immobility, latency to
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first head movement and number of head movements in
tonic immobility tests were greater in white than brown
hens, whereas the number of inductions was less for tonic
immobility tests. The tonic immobility and corticosterone
response results were consistent and indicated greater
fearfulness and larger corticosterone responses to poten-
tially threatening stimuli in white than brown hens. Data
from lines of Japanese quail selected for low and high
corticosterone responses to restraint also support an asso-
ciation between corticosterone responses and fearfulness in
birds. Quail selected for low corticosterone responses show
lower fearfulness than quail selected for high corticoste-
rone responses (Jones et al. 1994a, 1994b).
If birds experience fear when they respond to a stressor
then levels of fear should increase when plasma concen-
trations of corticosterone increase during a corticosterone
response. However, fear is not a single measurable vari-
able, and the demonstration of a relationship between
fearfulness and corticosterone is difficult. Chickens treated
with corticosterone had increased fearfulness in a tonic
immobility test (Jones et al. 1988), but clear relationships
between fear and corticosterone responses have not been
shown in birds. The challenges in relating fearfulness and
corticosterone responses can be demonstrated from a study
of hens. Tonic immobility tests in white Leghorn and
brown Hyline hens showed a clear difference between
strains of hen in the mean duration of immobility (Fig. 4A)
that was consistent with the results of Fraisse and Cockrem
(2006). Inspection of the data for individual hens shows,
however, a wide range of durations within each strain of
hen (Fig. 4B). Individual measures are not sufficient to
quantify fear in birds, and it is not surprising that there was
no relationship between the duration of tonic immobility
and the corticosterone response to 15 min of handling in
these hens (data for white hens shown in Fig. 5A). How-
ever, when all four measures from the tonic immobility test
were combined, there was a small but significant correla-
tion between fearfulness, as measured by fear score ranks,
and corticosterone responses to handling in the white hens
(Fig. 5B).
Personality and corticosterone responses
Animals differ in their responses to other animals and to
the environment. For example, some animals are more
aggressive and more likely to explore new situations than
other animals. Characteristic patterns of behaviour in
individual animals represent strategies that the animals use
to cope with demands from their environment. These pat-
terns have been called coping strategies or coping styles,
where coping styles are defined as coherent sets of
behavioral and physiological stress responses to common
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J Ornithol (2007) 148 (Suppl 2):S169–S178
A
10
5
Duration (min)
0
B
20
10
0
White Brown
Fig. 4 Mean (A; ±SE) and individual (B) durations of tonic
immobility in white Hyline and brown Leghorn laying hens on a
commercial farm. Tonic immobility (TI) was induced by the method
of Fraisse and Cockrem (2006). If birds remained immobile
throughout the 20-min test period, the duration of TI was recorded
as 20 min
challenges faced by animals (Koolhaas et al. 1999). Coping
styles are consistent over time, are equivalent to behavio-
ural syndromes (Sih et al. 2004) and animal temperaments
(Reale et al. 2007), and can also be called personalities
(Carere and Eens 2005). Personalities have been defined as
suites of correlated behaviours that are expressed across
different situations (Carere and Eens 2005). The existence
of consistent individual differences in personalities can be
explained from a consideration of life-history trade-offs
(Wolf et al. 2007). It has been suggested that animals with
proactive personalities are likely to be more successful in
an environment that remains constant than those with
reactive personalities (Cockrem 2005). Conversely, the
more cautious style of reactive animals may be more suc-
cessful in a changing environment and hence there is no
optimal personality for all situations.
Personalities in free-living animals have been better
studied in birds, especially the great tit in the Netherlands,
than in any other animal group (Groothuis and Carere
2005). Although personalities vary along a continuum,
individuals are commonly divided into two personality
groups on the basis of their behavioural responses to var-
ious situations. Great tit personalities are assigned from
their performance in novel environment and novel object
J Ornithol (2007) 148 (Suppl 2):S169–S178
A 1991; Veenema et al. 2003) and classified as having pro-
20
Duration (min)
10
0 were both related to personality, but the relative success of
0 5 10 15
B indicated that selection pressures on personality traits can
TI fear score rank
40
20
0 Birds vary in their personalities and in their corticosterone
0 5 10 15
Corticosterone at 15 min (ng/ml)
Fig. 5 Correlations between duration of tonic immobility (A;
Pearson r = 0.08, p = 0.583) and tonic immobility fear score rank
(B; Pearson r = 0.30, p = 0.047) and plasma corticosterone responses
to handling in white Hyline laying hens on a commercial farm. The
linear regression of fear score rank on corticosterone is shown in B.
Plasma corticosterone was measured in blood samples collected after
hens had been removed from their cages and handled for 15 min. Fear
score ranks were calculated for tonic immobility tests following
(Jones and Mills 1983). Ranks were calculated by ranking birds from
the least to the most fearful for each of four variables measured during
tonic immobility tests. The relationships with fear of each variable in
the tonic immobility test were assigned following (Jones 1988)
tests (Groothuis and Carere 2005). Birds are released
individually into a novel room or presented with novel
objects in their cage. The rates of exploration in the room
and approach to the novel object are scored and used to
classify birds as fast or slow explorers. These tests are used
both in captive birds and in free-living birds that are
brought to the laboratory, tested and then released at their
capture site. Great tits have been selected for fast or slow
exploratory behaviour and the personalities of birds in each
selection line examined in detail (Groothuis and Carere
2005). Fast and slow personalities in great tits are equiv-
alent to the proactive (active) and reactive (passive) coping
styles or personalities identified in mammals (Koolhaas
et al. 1999). For example, behavioural characteristics of
lines of mice selected for high and low aggression (short
and long attack latencies; SAL and LAL lines; Benus et al.
S175
active and reactive personalities are generally similar to
characteristics of fast and slow great tits.
Survival, dispersal and breeding success of free-living
great tits whose personality has been determined in labo-
ratory tests have also been described (Dingemanse et al.
2003, 2004; Dingemanse and De Goede 2004). Survival of
adults and the number of offspring that survived and con-
tributed to the breeding population (a measure of fitness)
proactive or reactive great tits differed between years and
between sexes (Dingemanse et al. 2004). These findings
differ between years, leading to the maintenance in avian
populations of genetic variation in personalities. It can be
suggested that in general birds with proactive personalities
are likely to be more successful in constant or predictable
conditions and birds with reactive personalities will be more
successful in changing or unpredictable conditions. Clearly
there is a need for further studies of relationships between
survival, fitness and personality in free-living birds.
responses, so are proactive and reactive personalities asso-
ciated with different corticosterone responses to stressors?
This question can be addressed indirectly from a consider-
ation of behaviour in Japanese quail selected for low and high
corticosterone responses. A wide range of behaviour tests
have been conducted in lines of quail selected on their cor-
ticosterone responses to 10 min of restraint (Satterlee and
Johnson 1988). LS (low corticosterone stress response) quail
are less fearful than HS (high corticosterone stress response)
quail in tests of tonic immobility (Satterlee et al. 1993), open
field behaviour (Jones et al. 1992) and avoidance of humans
(Jones et al. 1994a, 1994b). LS quail show higher sociality
than HS quail (Jones et al. 2002), and also have a higher
growth rate (Satterlee and Johnson 1985) and reach puberty
earlier (Marin et al. 2002; Satterlee et al. 2002). The
behaviour data from the LS and HS quail are consistent with
the classification of the two selection lines into proactive and
reactive personalities respectively, so a proactive personality
in these quail is associated with relatively low corticosterone
responses and a reactive personality with relatively high
corticosterone responses. Lines of quail have also been se-
lected for short (STI) and long (LTI) durations of tonic
immobility (Hazard et al. 2005). STI quail are less fearful
than LTI quail in open field as well as tonic immobility tests,
but differences between the lines in corticosterone responses
have not been shown (Jones et al. 1991, 1994a, 1994b), and
there were no significant correlations between corticosterone
and behaviour variables in these quail (Mignon-Grasteau
et al. 2003). Individual differences in corticosterone re-
sponses are more apparent when birds are challenged with
mild rather than strong stressors (Beuving and Vonder 1986),
123
S176 J Ornithol (2007) 148 (Suppl 2):S169–S178

and line differences between the STI and LTI quail may Table 1 Proposed characteristics of birds with proactive and reactive
become apparent if corticosterone responses to a milder personalities
stressor are measured in future. Proactive personality Reactive personality
Relationships between corticosterone responses and
behaviour can also been examined in data from great tits Birds
and chickens. It has been suggested that corticosterone Fast great titsa Slow great tits
responses may be smaller in fast (proactive) compared with LS quailb HS quail
slow (reactive) great tits (Carere et al. 2003; Groothuis and Brown hensc White hens
Carere 2005). White Leghorn hens selected for low (LFP) Behaviour
compared with high (HFP) levels of feather pecking Bold and aggressive Shy or cautious and not
aggressive
showed less fear in an open field but not in a tonic
Fast and superficial explorers Slow and thorough explorers
immobility test (Jones et al. 1995). LFP hens had higher
Less fearful More fearful
corticosterone responses and lower noradrenaline sympa-
thetic nervous system responses to restraint than HFP hens Less flexible and less sensitive More flexible and more
to environmental stimuli sensitive to environmental
(Korte et al. 1997). Selection for feather pecking in these stimuli
hens has not led to lines of hens with different personali- Physiology
ties. In another study, white Leghorn hens that showed less Lower corticosterone Higher corticosterone
fear on the basis of tonic immobility responses also had responses to stressors responses to stressors
smaller corticosterone responses, although not significantly Relatively high sympathetic Relatively low sympathetic
so, to a stressor than hens showing more fear (Beuving nervous system reactivity nervous system reactivity
et al. 1989). Personality differences can also be identified Relatively low Relatively high
between strains of laying hens. Brown Hyline hens with parasympathetic nervous parasympathetic nervous
system reactivity system reactivity
relatively smaller corticosterone responses to handling and
Fitness
lower fearfulness than white Leghorn hens (Fraisse and
More successful in constant or More successful in changing or
Cockrem 2006) have proactive personalities, and white
predictable conditions unpredictable conditions
Leghorn hens have reactive personalities.
a
A summary of proposed characteristics of birds with Behavioural differences between fast and slow great tits have been
extensively characterised (Groothuis and Carere 2005)
proactive and reactive personalities is given in Table 1. b
Japanese quail selected for low and high corticosterone responses to
Corticosterone responses to stressors are relatively restraint (Satterlee and Johnson 1988)
straightforward to measure, whereas fearfulness and other c
Brown Hyline hens have smaller corticosterone responses to han-
personality characteristics can only be assessed indirectly dling and show lower fearfulness than white Leghorn hens (Fraisse
from behaviour tests. Although it is difficult to demonstrate and Cockrem 2006)
clear relationships between corticosterone responses and
fearfulness (see Fig. 5), data from Japanese quail, great tits
and chickens are consistent with lower fearfulness and
lower corticosterone responses to stressors in proactive Stimulus from environment
compared with reactive birds.
Perception

Conclusions
Personality
Birds, like all other animals, are constantly receiving proactive reactive
stimuli from their environment. Responses to these stimuli
are determined by the individual characteristics of each
individual bird, which are collectively called ‘‘personal- Behaviour response Corticosterone response
ity’’. Birds with proactive personalities have relatively bold
bold and fast shy and slow low high
and fast behavioural responses and relatively low cortico-
sterone stress responses to stimuli, whilst birds with reac- Fig. 6 The influence of personality on behavioural and corticoste-
tive personalities have relatively passive shy and slow rone responses of birds. A stimulus from the environment is perceived
behavioural responses and large corticosterone responses. by a bird, then personality characteristics of each individual bird
determine the nature of the responses to the stimulus. Personalities
Corticosterone and behaviour responses are linked, and
can be classified as proactive or reactive, with associated behavioural
individual corticosterone and behaviour responses depend responses of individual birds varying from bold and fast to shy and
on each bird’s personality, as shown in Fig. 6. The iden- slow, and corticosterone responses from low to high

123
J Ornithol (2007) 148 (Suppl 2):S169–S178
tification of personalities in birds is relatively recent, and
there are now many opportunities to explore physiological
and behavioural characteristics of proactive and reactive
personalities, to determine the relative contributions of
genetic variation and phenotypic plasticity, and to examine
the fitness consequences of individual differences in avian
personalities.
Acknowledgments Research in stress endocrinology described here
has been supported by the Institute of Veterinary, Animal and Bio-
medical Sciences, Massey University, and by Antarctica New Zealand.
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