KEES VAN OERS AND MARC NAGUIB
Birds are widely distributed and highly diversiﬁ ed, and also generally more
conspicuous and observable in natural environments than many other ver-
tebrates. Birds also exhibit complex behavior and social processes. Because
of these attributes, birds are key model organisms that have allowed behav-
ioral biologists to address a wide range of ecological and evolutionary ques-
tions (Konishi et al. 1989; Danchin et al. 2008; Davies et al. 2012). Moreover,
owing to the contributions from a diverse group of ornithologists ranging
from amateur bird-watchers to professional scientists, the knowledge of bird
behavior under natural conditions is more extensive than for any other ver-
tebrate taxa. Many avian species are diurnal, conspicuous, and resilient, and
also permit relatively invasive investigations. In consequence, they are well
suited for experimental ﬁ eld research using a wide range of methods such as
manipulation of breeding conditions (Tinbergen and Boerlijst 1990), bioa-
coustic analyses (Marler and Slabbekoorn 2004; Catchpole and Slater 2008),
capture and marking procedures (Lebreton et al. 1992), and analyses of en-
ergy expenditure and of endocrine and immune function (Wingﬁ eld 2005).
Birds are also excellent study organisms for experimental investigations of
behavioral adaptations to changes in environmental conditions, a topic that
has become of particular interest in recent years (Visser 2008). Furthermore,
captive bird populations proved to be extremely valuable in studies on the
genetics of behavior (Berthold and Querner 1981; Jones and Hocking 1999;
Price 2002; Drent et al. 2003; Van Oers et al. 2005a), the neurological cor-
relates of behavior (Konishi 1985; Gil et al. 2006), physiological mechanisms
underlying behavior and its variation (Wingﬁ eld 2005; Soma et al. 2008), and
developmental inﬂ uences on behavior (Naguib and Nemitz 2007), as well as
in studies on sexual selection (Andersson 1994). Even in more applied ﬁ elds
such as conservation, animal welfare, and animal husbandry, birds have
been shown to be good models for studying behavior, both in the ﬁ eld and
in captivity (Sutherland 1998; Dawkins 1999; Rodenburg and Turner 2012).
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Kees van Oers and Marc Naguib | 67
Considering all of the above, it is not surprising, therefore, that the majority
of studies on animal personality have been conducted on birds. The study
of personality traits in birds can be framed into an ecological context more
easily than in other taxa, allowing analyses of ecological and evolutionary
aspects of personality. Birds of resident species can be followed individually,
often throughout their lives, their behavior can be measured both under
standardized conditions in captivity and in their natural environment, and
ﬁ tness can be quantiﬁ ed. The opportunity to conduct behavioral tests in the
laboratory also allows researchers to effectively document consistent differ-
ences in individual behavior within and across contexts (Dingemanse et al.
2002; Van Oers et al. 2005b; Martins et al. 2007; Schuett and Dall 2009).
The aim of this chapter is to provide a broad overview of studies on avian
personality, including those that address genetic variation linked to person-
ality (Van Oers et al. 2005a; Fidler et al. 2007; Gil and Faure 2007; Bell and
Aubin-Horth 2010; Van Oers and Muller 2010), the behavioral and ﬁ tness
consequences of personality in natural populations (e.g., Dingemanse et al.
2004; Dinge manse and Wolf 2010; Wolf and Weissing 2010), mathematical
models that investigate possible scenarios for the evolution of personal-
ity (Wolf et al. 2007; Amy et al. 2010; Dingemanse and Wolf 2010; Houston
2010), and the physiological substrate of personality (e.g., Carere et al. 2005a;
Kralj-Fiser et al. 2007; Fucikova et al. 2009; Coppens et al. 2010; Baugh et al.
2012). We also provide a historical background of personality research in
birds and discuss recent studies from a historical perspective.
Historical overview of avian personality research
Darwin wrote extensively on animal behavior (Darwin 1872) and, after him,
scientists working on animal behavior could be separated into two differ-
ent ﬁ elds, namely, comparative psychologists and ethologists. There was
one camp of ethologists such as Douglas Spalding (1841–1877), who studied
imprinting in chicks (Gray 1967), and another camp of mainly animal psy-
chologists such as Lloyd Morgan (1852–1936), who wrote a book, very inﬂ u-
ential at the time, introducing the ﬁ eld of comparative psychology (Lloyd
Morgan 1923). Wallace Craig, Oskar Heinroth, and Charles Otis Whitman
contributed to the emergence of ethology as a major separate biological
discipline in the study of behavior. Although both comparative psychology
and ethology address basic principles of animal behavior, these disciplines
have been separated for a long time. Interestingly, however, the study of in-
dividuality in the behavior of birds, and their personality, has found its way
in research both by ethologists and by comparative psychologists, and also
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68 | Avian Personality
has emerged in publications by semiprofessional bird banders. A crucial fac-
tor for recognizing individual differences in behavior is spending sufﬁ cient
time observing the individuals. Yet, a larger part of ornithological research
up until the ﬁ rst part of the twentieth century was done in museums so that
few data were available on behavioral differences among individuals (Arm-
The ﬁ rst published use of the word personality to describe characteristics
of individual birds was probably by Talbot in 1922. Talbot (1922) described
inter- and intraspeciﬁ c differences in the motivation to ﬂ y through a hole
that was situated at the entrance of a gathering cage, when birds were caught
for banding. In the Manual of Bird Banders, Lincoln and Baldwin (1929) even
stated that documenting bird personality, deﬁ ned as the individual pecu-
liarities in appearance, habits, and manners (Baechle 1947), is one of the
main achievements of bird banding. A nice example that recognizing indi-
vidual personality differences requires spending sufﬁ cient time with these
individuals is provided by Gwendolen (Len) Howard, a musician who kept
birds in captivity as hobby. Most of her birds were tame, or at least habitu-
ated to human presence, and in a book called Birds as Individuals, Howard
(1953) describes in great detail the lives of great tits, black birds, robins, and
other birds in her garden or inside her house. Most remarkable about this is
that she recognized the birds not only by their individual plumage charac-
teristics, but also by their “characteristic mannerisms and poses and their facial
expressions.” She states that great tits especially were easily recognized since
“their whole bearing and personality was too individual for confusion to arise when
I had them at close quarters” (Howard 1953).
While the early descriptions of personality-like behavior in birds were
largely anecdotal, it was probably Lack (1947) who made the ﬁ rst scientiﬁ -
cally based description of individual differences in aggressiveness in robins,
when he tested several males and their reaction to a model. Some males were
hardly interested in the model, while others vigorously attacked it. Another
series of papers related to individual differences in behavior came from
Burtt (1967), a psychologist who combined his interest in bird banding with
the scientiﬁ c study of personality. While banding over 17,000 blackbirds for
the Federal Wildlife Service, he studied bird behavior for several years from
a psychological perspective (Thayer and Austin 1992). In his book The Psy-
chology of Birds, he made the connection between personality traits, such as
extroversion, dominance, and emotional stability, and the behavior of indi-
vidual birds (Burtt 1967). Together with Giltz, he investigated, for instance,
the importance of personality in the interpretation of bird behavior (Burtt
and Giltz 1969b). In connection with a banding program at a decoy trap,
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Kees van Oers and Marc Naguib | 69
the pair measured the personality traits “complacency” and “aggression” in
common grackles (Quiscalus quiscula), red-winged blackbirds (Agelaius phoe-
niceus), brown-headed cowbirds (Molothrus ater), and starlings (Sturnus vul-
garis). They deﬁ ned what they called the complacency-agitation continuum as
the way an individual bird behaved in a small cage, directly after banding.
Complacent birds moved more compared with agitated birds. Aggression
was assessed while birds were held in a hand; birds were threatened with
a ﬁ nger and the tendency to bite was measured on a scale from zero to ten
(Burtt and Giltz 1969a). Both traits showed within- and between-species
variation and were found to be highly repeatable. They found cowbirds to
be the most complacent and starlings the most agitated species, while grack-
les and cowbirds were the most aggressive, and starlings and red-winged
blackbirds the least aggressive species (Burtt and Giltz 1969a; 1969b). They
also found that grackles had the greatest tendency to re-enter the trap, and
that they were the most resident species compared with the other species
(Burtt and Giltz 1973).
As suggested by this brief historical overview, recognizing consistent in-
dividual differences in bird behavior has a long history, dating back to the
roots of ethology. Scientiﬁ c research focusing on such differences, however,
has ﬂ ourished mainly in the last decade (Table 1), after individual differences
in behavior were framed into the well-deﬁ ned concepts of personality, be-
havioral syndromes, and coping styles.
Recent advances in avian personality research
behavioral consistency and behavioral tests
Many recent studies on behavioral consistency in birds have been inspired
by the work of Verbeek, Drent, and coworkers in the early 1990s on great tits
(Verbeek et al. 1994; 1996; 1999). This work was based on earlier studies on
the individual consistency in the response toward changes in the environ-
ment in mice (e.g., Van Oortmerssen and Bakker 1981; Benus et al. 1987) and
studies on foraging and exploratory behavior in great tits (Parus major) (e.g.,
Krebs et al. 1972; Krebs and Perrins 1978). Individual differences in explor-
atory behavior had been noticed in several studies on foraging behavior in
great tits (Partridge 1976; Kacelnik et al. 1981), so the expansion of research
with a focus on such behavioral differences could be built on a substantial
body of knowledge of this topic. The behavioral tests developed by Verbeek
and coworkers to investigate novel object and novel environment explo-
ration (Verbeek et al. 1994) are now used as standard tests in most studies
on great tits (e.g., Dingemanse et al. 2002; Van Oers et al. 2008; Hollander
70 | Avian Personality
et al. 2008; Titulaer et al. 2012) and also on other bird species (e.g., Fox and
Millam 2007; Martins et al. 2007; Kurvers et al. 2009; Schuett and Dall 2009).
Since the behavioral response to a novel object or novel environment might
be species-speciﬁ c, some caution is required when comparing studies of
different species. A test that might be very meaningful in the life-history
of one species might be less suitable for another one, thus resulting in be-
tween-species differences in the consistency of a trait (Mettke-Hofmann
et al. 2005). Hence, although exploratory behavior is now considered one
of the major animal personality traits (Réale et al. 2007; Sih and Bell 2008),
species-speciﬁ c tests to validate this and other behaviors are very important.
Related to exploratory behaviors are boldness or risk-taking behaviors (Ré-
ale et al. 2007; but see chapter 6). Whereas the exploration of a novel object
is likely to reﬂ ect a mixture of curiosity and fearfulness, risk-taking behav-
iors are often related to predation risk and foraging (Van Oers et al. 2004b).
Therefore, these behaviors are more closely linked to stress responses (Mar-
tins et al. 2007). Social relationships (Stowe et al. 2006; Stowe and Kotrschal
2007) and the behavior of unrelated ﬂ ock mates (Marchetti and Drent 2000;
Van Oers et al. 2005b; Kur vers et al. 2009) might also be important factors.
The behavior of a group of birds as a whole can, therefore, be affected by
the mix of personality types present within the group (Kurvers et al. 2009;
Schuett and Dall 2009; Amy et al. 2010).
Apart from exploratory behavior, several other traits have been investi-
gated in birds as personality traits (see table 3.1 for some examples). One
trait that has been widely used in bird research is agonistic behavior, which
has been shown to be individually consistent and to have a genetic correlate
in mice (Benus 1988) and ﬁ sh (Bakker 1994). Aggression toward a conspeciﬁ c
is a crucial part of the life-history of social animals such as birds. Especially
for social dominance (Verbeek et al. 1996; Dingemanse and De Goede 2004)
and in territorial behavior (Duckworth 2006b; Garamszegi et al. 2009; Amy
et al. 2012), agonistic behavior is an important personality trait determining
the outcome of an interaction and subsequent access to resources. In great
tits, Verbeek and coworkers (1996) investigated whether individual differ-
ences in exploratory behavior were related to agonistic behavior and how
this, in turn, related to dominance. In an experimental set-up, two males
were placed in a cage, with an opaque partition between them. After remov-
ing the partition, the authors noted which of the two males attacked ﬁ rst.
They found that this measure of aggressive behavior was consistent over
time and that fast explorers started more ﬁ ghts than slow explorers, inde-
pendent of sex and morphological traits. Individuals that initiated a ﬁ ght
were also more likely to win that ﬁ ght.
Table 3.1. A noncomprehensive species overview with studies on the assessment of avian personality traits.
Author Year Species Personality traits
Kurvers et al. 2009 Barnacle goose (Branta bernicla) Boldness
Kralj-Fiser et al. 2007 Greylag goose (Anser anser) Reaction to handling
Blas et al. 2007 European white stork (Ciconia ciconia) Reaction to handling
Costantini et al. 2005 European kestrel (Falco tinnunculus) Feeding habits
Richard et al. 2008 Japanese quail (Coturnix japonica) Boldness
Uitdehaag et al. 2008 Jungle fowl (Gallus gallus) Boldness
Faure 1980 Jungle fowl (Gallus gallus) Exploration
Guillette et al. 2009 Black-capped chickadee (Poecile atricapillus) Exploration
Arnold et al. 2007 Blue tit (Cyanistes caeruleus) Boldness
Burtt and Giltz 1973 Brown-headed cowbird
Common grackle Red-
winged blackbird Starling
2007 Carolina chickadees (Poecile carolinensis) Aggressiveness
2005 Chaﬃ nch (Fringilla coelebs) Risk-taking
Garamszegi et al. 2009 Collared ﬂ ycatcher (Ficedula albicollis) Boldness
2007 Common raven (Corvus corax) Boldness
2005 Garden warbler
Verbeek et al. 1994 Great tit (Parus major) Exploration
Verbeek et al. 1996 Great tit (Parus major) Aggressiveness
Van Oers et al. 2004b Great tit (Parus major) Risk-taking
Hollander et al. 2008 Great tit (Parus major) Exploration
Quinn et al. 2009 Great tit (Parus major) Exploration
Fucikova et al. 2009 Great tit (Parus major) Reaction to handling
Fox et al. 2009 Mountain chickadee (Poecile gambeli) Exploration
2009 Sedge warbler (Acrocephalus
Minderman et al. 2009 Starling (Sturnus vulgaris) Exploration
Duckworth 2006a Western bluebird (Sialia mexicana) Aggressiveness
72 | Avian Personality
Author Year Species Personality traits
Beauchamp 2000 Zebra ﬁ nch (Taenopygia guttata) Exploration
Martins et al. 2007 Zebra ﬁ nch (Taenopygia guttata) Exploration
Schuett and Dall 2009 Zebra ﬁ nch (Taenopygia guttata) Exploration
Fox and Millam 2004 Orange-winged Amazon (Amazona amazonica) Neophobia
2004 10 species Boldness
Ellenberg et al. 2009 Yellow-eyed penguin (Megadyptes antipodes) Reaction to handling
De Azevedo and
2006 Greater Rhea (Rhea americana) Boldness
Table 3.1. (continued)
Agonistic behavior in birds is linked to the ability to obtain and maintain
a breeding territory (Stamps and Krishnan 1997; Naguib 2005). In studies
on agonistic behavior in relation to territorial competitiveness (Duckworth
2006a) and parental behavior (Duckworth 2006b) in Western bluebirds (Sia-
lia mexicana) it was shown, for instance, that agonistic behavior is repeatable
and costly (Duckworth 2006b). Moreover, Duckworth (2006a) showed ex-
perimentally that more aggressive males compete more effectively for territo-
ries in areas with a higher density of nest boxes. As a consequence, aggressive
and nonaggressive males occurred in breeding habitats that differed in the
strength of selection on morphological traits. These results show that aggres-
sion can affect selection on a local scale by determining individual settlement
patterns, thereby also providing opportunity for correlational selection.
Tests of agonistic behavior are, by deﬁ nition, conducted in a social con-
text, and the consistency in behavior could also be dependent on the con-
text (Van Oers et al. 2005b). To test whether males of black-capped chicka-
dees (Poecile atricapillus) behaved consistently with different mates, they
were paired to a female and several aspects of their behavior were observed
(Harvey and Freeberg 2007). After being paired with a new mate, the males
showed behavior that was consistent with the behavior previously shown
with their former mate, indicating that agonistic behavior is consistent also
when the social context has been changed (Harvey and Freeberg 2007).
A crucial issue in assessing personality traits is the identiﬁ cation of con-
texts that are most suitable for revealing consistent differences in behavior
among individuals. Exploration tests in artiﬁ cial environments, such as
Kees van Oers and Marc Naguib | 73
a novel room or cage, and novel object tests, provide standard situations.
The artiﬁ cial nature of such a context has the advantage that behavior can
be tested in the absence of a speciﬁ c resource value, which may confound
any measurement of intrinsic behavioral traits. Resources vary in their value
to different individuals so that in tests conducted in natural situations it is
difﬁ cult to separate individual differences in behavior from differences in
resource values. Individuals may behave differently not as a result of per-
sonality but as a result of differences in resource values. Conducting tests
in the natural habitat could potentially reveal a more meaningful varia-
tion in behavior compared with the standard tests done in captivity, and
therefore yield results with high ecological and evolutionary relevance. Yet,
when testing birds for personality traits during resource defense in the ﬁ eld,
one needs to be careful in developing tests so that the recorded behavior is
not primarily related to the resource value rather than to their personality
traits. Demonstrating consistencies in behavior in contexts that are inde-
pendent of resources crucial for reproduction, thus remains a powerful tool
in research aimed at unraveling the evolutionary signiﬁ cance of personality
Causes of personality variation: genes and physiology
The majority of our knowledge of the genetic background of traits such
as exploratory behavior, aggressiveness, and fearfulness comes from stud-
ies on domestic birds. Selection experiments on chicken, turkey, ducks,
and Japanese quail have shown that the observed variation in open ﬁ eld,
pair-wise, and novel object tests has a substantial genetic basis (e.g., Brown
and Nestor 1973; Francois et al. 1999; Jones and Hocking 1999; Arnaud et al.
2008). Although the presence of a genetic component is an important factor
to consider in studies on evolutionary change of personality traits, genetic
studies of animal personality traits in natural populations are scarce (Bell
and Aubin-Horth 2010). Most quantitative genetic and molecular analyses
of bird personality traits have been conducted with the great tit (quantita-
tive: Van Oers et al. 2005a; Quinn et al. 2009; molecular: Fidler et al. 2007;
Van Bers et al. 2010; Korsten et al. 2010). In this species it is apparent that
personality traits typically have moderate levels of additive genetic varia-
tion (Dingemanse et al. 2002; Drent et al. 2003; Van Oers et al. 2004b; Quinn
et al. 2009) and of genetic dominance (Van Oers et al. 2004c), and that traits
are genetically correlated (Van Oers et al. 2004a). An important gene has
been identiﬁ ed for great tit personality: the dopamine receptor D4 gene
74 | Avian Personality
( Fidler et al. 2007) explains between 5% and 8% of the phenotypic variation
in some but not all European great tit populations (Korsten et al. 2010). This
and other genes are thereby likely not only to affect behavioral responses
early in life (i.e., temperament traits), but also to affect learning and plastic-
ity later in life.
One difﬁ cult question is to assess the extent to which the underlying ge-
netic and physiological mechanisms are a constraint on the evolution of be-
havioral traits vs. the extent to which they are the product of variation and
selection (Bell 2005; Dingemanse et al. 2007). An important issue here is how
the word constraint is used. In a biological context, the word can refer to a
factor that impedes but does not necessarily prevent evolution in particular
directions, or it can indicate that speciﬁ c evolutionary trajectories are un-
available to selection (Roff and Fairbairn 2007). Therefore, determining the
role of genetic constraints in the evolutionary change of personality will re-
quire not only more detailed ecological studies, but also better knowledge
than we currently possess of the relevant genes and their importance in nat-
ural populations (Blows and Hoffmann 2005; Van Oers et al. 2005a). A more
comprehensive overview of the current knowledge of the genetic basis of
personality variation in captive and wild animals is provided in chapter 6.
Many vertebrate species are characterized by the ﬂ exibility with which they
cope with stressors, and birds provide good examples of this. When birds
are under conditions of low environmental predictability, they experience
stress (Wiepkema 1992). Behavioral and physiological efforts to master the
situation (coping strategies) can be important determinants of health and
disease both in humans and in animals (Koolhaas et al. 1999). Moreover, in-
dividuals often show different physiological responses in these situations,
also referred to as coping styles. Individuals appear to cope with stressors
in a predominantly sympathetic or parasympathetic way. Individual varia-
tion in agonistic behavior can be considered as an example of more general
variation in coping with environmental challenges, where highly aggressive
individuals adopt a proactive coping style and submissive individuals adopt
a more passive or reactive style (Koolhaas et al. 2007). Therefore, most
physiological research relevant to avian personality involves stress physi-
ology and coping (see chapter 12). In mammals, it has been suggested that
individual differences in stress responses reﬂ ect variation in personality or
coping styles (Korte et al. 2005). Passive copers are expected to have higher
hypothalamic-pituitary-adrenal (HPA) responses to stressors, a lower sym-
pathetic adrenomedullary reactivity, a higher humoral immunity, but also a
Kees van Oers and Marc Naguib | 75
higher vulnerability to stress-induced illnesses compared with active copers
(Ellis et al. 2006).
In birds, fast exploration, high risk-taking, and high responsiveness to a
novel object appear to be associated with high corticosterone levels during
the test (Martins et al. 2007; Richard et al. 2008). Birds also show individual
consistency in the secretion of stress hormones. Kralj-Fisher and cowork-
ers (2007) have shown in greylag geese that corticosterone levels measured
in fecal samples collected after repeated handling episodes were consistent
within individuals. This repeatability was especially pronounced when indi-
viduals were feeding in low competition areas; in high competition areas in-
dividuals were less consistent. Whether these individual differences in stress
responses reﬂ ect genetic personality differences remains unclear. Yet, some
support for this possibility has been found in other avian species where se-
lection experiments have shown that the stress response has an additive ge-
netic background (Brown and Nestor 1973; Edens and Siegel 1975; Satterlee
and Johnson 1988). Moreover, great tit genetic lines selected for different
personalities (Drent et al. 2003) differed in the level of stress hormone secre-
tion after being in a social contest with a conspeciﬁ c (Carere et al. 2003).
Birds of the less aggressive and more cautious line (slow explorers) showed a
trend for a higher response compared with birds of the more aggressive and
bolder line (fast explorers), which could be taken to suggest a physiological
basis of different coping strategies in birds (Carere et al. 2003). Alternatively,
personality types might differ in the perception of the stressor, causing in-
direct differences in stress response to a standard stressor (Sapolsky 1994).
Most likely both mechanisms play a role. However, the extent to which one
or the other is more important in shaping variation in personality needs to
be studied in more detail. Studies in great tits have shown that exploratory
behavior is related to stress responses in both juvenile (Fucikova et al. 2009)
and adult birds (Carere and Van Oers 2004). Adult birds that explore a novel
environment more quickly (fast explorers) show a lower stress response af-
ter being handled, but nestlings that become fast explorers in adulthood
show an increased response after being socially isolated as nestlings. This
indicates that differences in personality traits measured just after indepen-
dence might act as a predictor of individual variation in the stress response
in adulthood, and as a result of variation in responsiveness as juveniles. A
more direct way of measuring the link between variation in personality and
stress is through stress hormones. In birds, corticosterone is the major glu-
cocorticosteroid hormone secreted in response to stress, and many studies
have shown that individual birds differ in their hormonal response to stress.
This response varies not only with intrinsic factors such as sex and age, but
76 | Avian Personality
also in relation to behavioral types, and it is modiﬁ ed by factors such as body
condition (Schwabl 1995; Silverin 1998; Cockrem and Silverin 2002; Cock-
rem 2007). These modiﬁ cations may allow the adjustment of physiological
and behavioral responses to adverse environmental circumstances and help
explain individual differences in responses.
Glucocorticosteroid responses are seen as an evolutionary mechanism
that maintains physiological homeostasis within an adaptive range. Only
recently, however, have studies raised the question of how to explain the
consistent individual differences in these responses that are unrelated to
age or size (Cockrem 2007). It will be interesting to develop this and de-
termine whether individual variation in short-term elevation of circulating
glucocorticosteroids also explains ﬁ tness differences, and whether ﬁ tness
consequences vary for different behavioral types. A ﬁ rst step in that direc-
tion was made by the work of Blas et al. (2007) on European white storks
(Ciconia ciconia). This study showed that the magnitude of the adrenocorti-
cal response to a standardized perturbation during development is nega-
tively correlated to survival and recruitment (Blas et al. 2007). The next step
would be to investigate whether these ﬁ tness consequences differ for dif-
ferent behavioral types. Blas et al. (2007) discuss this possibility, by arguing
that the success of proactive vs. reactive types varies as a function of popula-
tion density and predictability of food resources. If this is associated with
differences in glucocorticosteroid responses, it could provide an explana-
tion for varying success of the behavioral types. Direct measurements and
experimental changes, however, are needed to test this hypothesis. More on
this subject can be found in chapter 12, on neuroendocrine and autonomic
correlates of personalities.
Developmental aspects of personality
Although it has been shown that the genetic and physiological structure of
personality is relatively rigid (Koolhaas et al. 1999; Van Oers et al. 2005a),
personality nevertheless has substantial phenotypic plasticity and can be
affected by environmental factors, speciﬁ cally when they act during early
development (Carere et al. 2005b; Arnold et al. 2007; Krause et al. 2009;
Stamps and Groothuis 2010a; 2010b; Naguib et al. 2011). Such environmen-
tal factors include changes in the context in which a trait is expressed, for
example, and the social factors that will change the adaptive value of a cer-
tain behavioral response (e.g., Schuett and Dall 2009). More subtle factors
include maternal effects acting during embryonic development, such as the
Kees van Oers and Marc Naguib | 77
amount of hormones transferred to the egg by the female (Schwabl 1993; Gil
2008; chapter 11), circulating hormones that inﬂ uence habituation and sen-
sitization to stressful events, and learning how to cope with certain stressors
(Kant et al. 1985; Stam et al. 2000). Avian personalities are therefore open
to change, though within certain boundaries, and traits such as shyness or
boldness are therefore highly consistent within an individual. Individu-
als that are classiﬁ ed as being one or the other personality type, however,
may still ﬂ uctuate in their behavior (Carere et al. 2005a), and repeatability
of behavioral traits is typically moderate (Bell et al. 2009). Phenotypic cor-
relations between personality traits may be strong in some environments
but weak in others. For example, in great tits, both males and females of
genetic lines selected for fast exploratory behavior return more quickly to
the feeding table after a startle (risk-taking behavior). Lines selected for
risk-taking behavior also differ in their exploratory tendency, such that a
positive genetic correlation of 0.84 exists between the two traits (Van Oers
et al. 2004a). In a follow-up study investigating the context generality of
this correlation, fast- or slow-exploring great tits were tested for their risk-
taking behavior in a nonsocial context followed by a social context (Van
Oers et al. 2005b). Van Oers and coworkers found that the relation between
exploratory behavior and risk-taking behavior depended on the social con-
text. Females in general returned later in the social test, while the reaction
of males to the presence of a companion was dependent on their behavioral
type. Slow males came back sooner with faster companions and fast males
did not react to the companion (Van Oers et al. 2005b). Similar results were
found in a study on zebra ﬁ nches (Schuett and Dall 2009): males and females
differed in how consistently they behaved across social and nonsocial con-
texts. Schuett and Dall (2009) also tested whether males and females dif-
fered in their inﬂ uence as companions, and found that individuals of both
sexes inﬂ uenced each other’s exploratory behavior in a similar way within
the social context: the more exploratory the companion, the more explor-
atory the focal individual. In great tits, birds of different personality type
differ in their foraging strategy (Marchetti and Drent 2000). Moreover, the
presence and strategy of a conspeciﬁ c can affect the foraging strategies of
individuals differently, depending on their personality. As a result, birds of
different exploration types differ in their tendency to copy a tutor’s forag-
ing decision (Marchetti and Drent 2000; see below).
Since birds lay eggs, embryos are separated from the mother before they
start to develop. Females are, however, able to inﬂ uence embryonic devel-
78 | Avian Personality
opment by transferring nutrients and hormones to the yolk and albumen of
their eggs (Gil 2008). Although it is not completely clear how females can
actively vary the amounts of nutrients and hormones, these substances can
exert short- and long-term effects on the offspring (Schwabl 1993; Eising
et al. 2001; Groothuis et al. 2005; Eising et al. 2006; chapter 11). It is pos-
sible that maternal hormones in the egg may inﬂ uence personality varia-
tion by modulating genetic differences or physiologically programming
the offspring in certain ways. These maternal effects, however, may have a
genetic basis, as individual differences in the deposition of maternal hor-
mones in eggs have been shown to be, in part, genetically determined. Ge-
netic variation in yolk hormones has been found in lines of domesticated
species (Daisley et al. 2005; Gil and Faure 2007). In lines selected for fast and
slow exploratory behavior in great tits, Groothuis et al. (2008) found that
females of the slow line deposited lower amounts of testosterone in the yolk
of their eggs compared with females from the fast line. This was especially
true for the eggs laid early in the laying sequence (see chapter 11). This could
indicate that females of different personality types have different strategies
in rearing offspring. In this view, fast females would aim at rearing all off-
spring, whereas slow females invest less in those offspring that have lower
chance of surviving (Tobler and Sandell 2007). Not only can maternal hor-
mones inﬂ uence behavioral differences, they can also affect the persistence
of certain behaviors. In an experiment, the behavior of birds that came from
testosterone-injected (T-treated) and control eggs were compared for their
behavior toward a novel food source (Tobler and Sandell 2007). Birds from
T-treated eggs did not differ in their latencies to approach and eat novel
food during their ﬁ rst encounter. However, testosterone treatment affected
subsequent encounters with the novel food source. Owing to habituation,
latencies decreased in both groups over a period of 5 days, but considerably
more so in T-offspring (Tobler and Sandell 2007). Whether this is different
for offspring hatched from eggs at the beginning or end of the laying se-
quence is still unknown.
Environmental factors acting during ontogeny have been shown to signiﬁ -
cantly affect a whole range of morphological (Tinbergen and Boerlijst 1990),
physiological (Kitaysky et al. 2001; Naguib et al. 2004; Verhulst et al. 2006),
behavioral (DeKogel and Prijs 1996; Nowicki et al. 1998; Naguib and Nemitz
2007; Krause et al. 2009), and life history traits (DeKogel 1997; Naguib et al.
2006) and therefore may also play a role in personality development. It is
Kees van Oers and Marc Naguib | 79
well established that conditions experienced during early development are
important in shaping the behavior of an animal against the background of
the reaction norm (Mason 1979; Metcalfe and Monaghan 2001). Such factors
can involve a wide range of stressors, such as low-quality food (Krause et al.
2009), brood size (Neuenschwander et al. 2003), and parasites ( Tschirren and
Richner 2006). Yet, relatively little is known about how conditions experi-
enced during early development affect personality (Stamps and Groothuis
2010a; 2010b). One trait, used as a proxy for personality, boldness in response
to novel objects, has been studied by Fox and Millam (2004), who investi-
gated the effects of rearing condition on the reaction to novel objects in
orange-winged Amazon parrots (Amazona amazonica). Hand-reared, parent-
reared, and parent-reared/human-handled birds, which were handled ﬁ ve
times a week for 20 minutes, were tested for their latency to feed in the pres-
ence of ﬁ ve different novel objects between 4.5 and 6 months after hatching.
At an age of 12 months the response to a novel object in their home cage
was measured. They found that handling birds did not inﬂ uence the reac-
tion to novelty, but whether an individual was reared by their own parents
or hand-reared did. They concluded that the development of neophobia in
orange-winged Amazon parrots may be related to novelty the chicks experi-
ence during early life (Fox and Millam 2004). Moreover, we recently showed
in great tits that personality is affected by the sex ratio in the nest. Birds that
grew up in female-biased nests became faster explorers than birds that grew
up in male-biased nests. These ﬁ ndings that early social interactions shape
personality in animals but future research is required to unravel the precise
behavioral mechanism leading to this effect.
Another important inﬂ uence on behavior during early development is
the quantity, quality, or composition of food (e.g., see Birkhead et al. 1999).
Variation in food characteristics can be caused by parental choice, sibling
competition, or habitat quality but also by differences in the parents’ ability
to search and ﬁ nd suitable food. Experiments on birds investigating the in-
ﬂ uence of food during ontogeny can be conducted relatively easily in altri-
cial species compared with precocial species. Carere et al. (2005b), for exam-
ple, manipulated the early rearing condition in two great tit lines selected
for fast and slow exploratory behavior by a food rationing protocol. Birds
from both fast and slow exploration lines, but also control chicks, decreased
their growth rate and increased their begging behavior compared with
unmanipulated chicks within the same nests. This resulted in slow chicks
becoming much faster than their parents, but without any changes in ag-
gressiveness. In contrast, fast chicks had exploration scores similar to their
80 | Avian Personality
parents but an increased level of aggressiveness. As a consequence, there
was no apparent line difference in exploration behavior at independence.
The effect, however, turned out to be partly temporary: although the off-
spring of the slow line were still relatively fast six months later, birds of the
fast line became even faster, restoring the line differences again. A side ef-
fect of the treatment on the experimental birds was that control chicks also
begged more. To rule out these effects of sibling competition, the authors
conducted a second experiment with experimental and control siblings in
separate nests. Here, only the food-rationed chicks became faster in explo-
ration, indicating that the shift in the controls in the within-nests design
was indeed due to enhanced sibling competition. Krause et al. (2009) also
showed that the feeding conditions experienced during early development
affect exploration behavior in zebra ﬁ nches. They showed that female zebra
ﬁ nches raised as nestlings under low-quality food conditions were more ex-
plorative in a novel environment than females that had been raised under
high-quality food conditions. The same individuals were also more sensi-
tive to short periods of food deprivation by losing more weight than those
raised under high-quality food, underlining the link between behavioral
differences in personality with physiological differences in responses to a
Aside from the amount of food, its quality may also be very important
for the development of behavioral consistency. Essential amino-acids are
known to be limiting factors during development (Murphy and Pearcy
1993) and are also relatively scarce in the bulk food of many passerines
(Izhaki 1998; Ramsay and Houston 2003). Several tit species therefore sup-
ply their nestlings with a high proportion of spiders early during develop-
ment (Ramsay and Houston 2003). Spiders contain a relatively high amount
of taurine. To investigate whether taurine has a developmental effect on
personality variation in blue tits (Cyanistes caeruleus), Arnold and coworkers
(2007) conducted a feeding experiment in which they supplemented tau-
rine to blue tit nestlings during the period of maximum growth. Juveniles
that had received additional taurine as nestlings were signiﬁ cantly bolder
when investigating novel objects, and also were more successful at a spatial
learning task than controls. They concluded that prey selection is a mecha-
nism by which parents can alter the behavioral phenotype of their offspring.
Further experiments in natural settings should be conducted to see whether
parents indeed use this mechanism to prepare their offspring for the future.
Taken together, these ﬁ ndings suggest that personality traits may well be
shaped by the conditions experienced during early development, a topic
that is worth exploring more in the future.
Kees van Oers and Marc Naguib | 81
cognition and learning
A question arises as to the extent to which individuals differing in person-
ality also differ in learning abilities or learning strategies. Individuals that
differ in environmental exploration are likely to also differ in the way they
acquire, process, recall, and use environmental information (Guillette et al.
2010; Cole and Quinn 2012; Amy et al. 2012; Titulaer et al. 2012). Animals have
to learn to ﬁ nd food, possibly from successful conspeciﬁ cs, and to remember
food locations. Marchetti and Drent (2000) found that, in great tits, slow
and fast explorers differ in their routines to revisit known feeding sites and
in using information they obtain by observing conspeciﬁ cs when foraging.
Birds were ﬁ rst trained to ﬁ nd food at a speciﬁ ed feeder, which during the
experiment was then left without food. When tested alone, fast explorers
kept on visiting the now unrewarded feeder they had previously learned to
visit. Slow explorers, in contrast, were quicker in ﬁ nding new food locations
and did not revisit the previously rewarded feeder as often. In other words,
fast birds were less ﬂ exible in ﬁ nding food locations and expressed more be-
havioral routines than did slow explorers. Interestingly, when subjects had
the opportunity to observe a tutor bird to explore a speciﬁ c food source
(colored feeder), then slow and fast explorers behaved in opposite ways. Fast
explorers were faster in copying the tutor’s behavior (and in feeding from
the feeder indicated by the tutor) whereas slow explorers did not learn to
explore the rewarded feeder from the tutor. In other words, slow explorers
were better in ﬁ nding new food sources on their own, whereas fast explor-
ers did better in exploring new food sources when given the opportunity to
learn from others. Such differences in foraging strategies may explain in part
why slow and fast explorers perform differently under natural conditions
depending on food availability. Alternatively, this could be mediated by dif-
ferential susceptibility to stress, where differential stress levels may alter the
way information is processed. In a recent experiment, Titulaer et al. (2012)
further showed that personality affected learning only in difﬁ cult tasks, but
in a sex-speciﬁ c way. Such effects presumably are related to selection act-
ing differently on the sexes with respect to behavioral strategies in terms of
space use, foraging, and social behavior. Such relations between cognition
and personality have also been addressed in a number of other recent stud-
ies (Guillette et al. 2010; Cole and Quinn 2012; Amy et al. 2012).
Animal husbandry and welfare
Obviously, research on personality is not restricted to natural contexts. Per-
sonality has been a key issue in studies on animal welfare and husbandry (We-
82 | Avian Personality
melsfelder et al. 2000; Bolhuis et al. 2005; Würbel 2009; see chapter 14) and is
of emerging relevance in the development of nature conservation programs
that deal, for instance, with habitat defragmentation and reintroduction
of animals to new areas (see chapter 13). Although researchers with more
applied interests have often studied behavioral consistency, their concepts
and terminology are often different from those used by behavioral ecolo-
gists. Studies investigating personality in quail and chicken, for example,
often use the terms fear and fearfulness (Boissy 1995), where fearfulness is
measured as the emergence into a larger compartment, the reaction to novel
food or objects, or the response to a predator (Miller et al. 2005; 2006).
One of the central problems in applied bird ethology is feather pecking, a
common behavior in laying hens, with substantial economic and welfare im-
plications. Feather pecking has a genetic component but is also affected by
various social and housing factors (Van Krimpen et al. 2005; Van de Weerd
and Elson 2006; Rodenburg et al. 2008). Research has shown that individuals
are consistent in this behavior, reﬂ ecting a potential personality trait. Under-
standing the causes of feather pecking is thus of high applied signiﬁ cance as
it will contribute to develop rearing strategies and selection processes that
will reduce this problem. With the new regulations of housing laying hens
in larger groups, feather pecking needs to be monitored carefully, and iden-
tifying behavioral and genetic correlates of this behavior will help to ﬁ nd
optimal solutions that balance welfare and economic interests.
Personality differences also might be of great importance in reintroduc-
tion of individuals reared in captivity into wild populations or in transfer-
ring wild individuals to new locations. Before reintroduction, individuals
of many species, for example, have to learn to avoid predators. Training in-
dividuals in these capacities is therefore a crucial factor for increasing the
probability of postrelease survival (Box 1991). The ability to learn to avoid
certain dangers might, however, be dependent on the personality type of
an individual. That this can be the case is nicely shown in a study on greater
rheas (Rhea americana) (De Azevedo and Young 2006). Captive individuals
were tested for their response to several novel objects, before and after be-
ing trained to avoid predators. Birds were less bold after training compared
with before training, and the responses to the novel object before the train-
ing sessions were a good predictor of how the bird would react during train-
ing. Bolder birds behaved more calmly than shy birds. Similar results were
obtained studying the natural antipredator behavior of chafﬁ nches (Frin-
gilla coelebs): calm individuals were better able to assess the risk of a hawk
ﬂ ying over compared with very active individuals. They showed greater be-
havioral plasticity in high-risk versus low-risk situations, while hyperactive
Kees van Oers and Marc Naguib | 83
individuals in general showed more ﬂ eeing behavior (Quinn and Cresswell
2005), possibly because of differences in the risk perception between the ac-
tivity types (Butlers et al. 2006). As dispersal, territorial, and foraging strate-
gies can be linked to personality (Dingemanse et al. 2003; Amy et al. 2010;
see below; chapter 7), including information about personality in decisions
made about when to release individuals may affect the success of a reintro-
duction project (Bremner-Harrison et al. 2004; Merton 2006).
Field studies and ﬁ tness correlates
The growing interest in research on animal personality in part has been
driven by the ecological and evolutionary signiﬁ cance of personality—
that is, that personality matters in the dynamics of wild populations. Even
though the origin and nature of individual variation in itself is interesting,
the ecological and evolutionary framework adds another reason for inter-
est, as it shows that personality affects selection while at the same time being
under selection itself. Ecologically relevant personality correlates include
nest defense behavior (Hollander et al. 2008), song (Garamszegi et al. 2008;
Amy et al. 2010; Naguib et al. 2010), social dominance (Dingemanse and De
Goede 2004), feeding behavior (Costantini et al. 2005), as well as dispersal
and mating behavior (Dingemanse et al. 2003; Van Oers et al. 2008).
Dingemanse et al. (2003) showed, for instance, that natal dispersal dis-
tance (i.e., the distance between place of origin and the place of breeding)
was linked to personality in great tits. In their study population of great tits
with known personalities (assessed under standard laboratory conditions
using a novel environment test), they found that the personality of the fa-
ther mattered. Offspring from males that were fast explorers in the novel
environment test dispersed farther from their original nest box than did
slow explorers. Furthermore, immigrants into the population had higher
exploration scores than resident birds. Such effects presumably resulted
from genetic differences and environmental effects acting during develop-
ment. Indeed, as personality has a considerable heritable component (Van
Oers et al. 2005a), personality-related differences in dispersal strategies may
affect the genetic variance of a population, depending on the extent to
which residents and immigrants succeed in breeding.
Dingemanse et al. (2004) found in great tits that personalities had differ-
ential ﬁ tness effects, that these effects were different for males and females,
and that they were reversed in different years depending on food availabil-
ity. Studying local survival across three years, they found that slow males
did better in the two years with limited food availability in winter than they
84 | Avian Personality
did in the year with high winter food availability. Females over the same pe-
riod were affected in the opposite way. These results suggest that fast males,
being more aggressive and dominant over females (Krebs and Perrins 1978;
Drent 1987; Verbeek et al. 1996), do better in poor years than females, as the
limiting resource is the food over which they compete. In good years, the
higher winter survival results in higher competition among males for ter-
ritories so that slower and less aggressive males do relatively less well than
females. Indeed, Amy et al (2010) showed that territorial behavior is affected
by personality, with faster males being more aggressive at the site of intru-
sions while slower males follow a different strategy by singing more from the
distance and exploring more the boundaries of their territory. Dingemanse
et al. (2004) also found that in the poor year, pairs of individuals with simi-
lar personality produced more local recruits than pairs in which the male
and female had different personalities; these effects, however, may have
been caused by differential survival or differential dispersal (Dingemanse
et al. 2003). Along this line, Both et al. (2005) reported that pairs with simi-
lar personality have a higher reproductive success, measured as offspring
condition. These ﬁ ndings may explain the production of more recruits by
pairs with similar extreme personality, as shown by a different study for
the same population (Dingemanse et al. 2004), as ﬂ edgling condition has
been shown to predict survival (Tinbergen and Boerlijst 1990). While the
nature of one’s own and the partner’s personality appears to have ﬁ tness
consequences measured as offspring condition, recruits, and survival, per-
sonality also can also affect more immediate reproductive decisions. Mo-
nogamous animals are known to produce extra-pair offspring in addition
to the offspring produced with their social partner (Petrie and Kempenaers
1998; Grifﬁ th et al. 2002). Decisions about extra-pair matings most com-
monly have been linked to the expression of sexually selected traits of the
social mate and the extra-pair mate (Kempenaers et al. 1992; Hasselquist
et al. 1996). Apparently, decisions about extra-pair matings also depend on
within-pair personality differences in great tits, as pairs with more extreme
similar personality (slow-slow and fast-fast pairs) are more likely to raise
extra-pair offspring (Van Oers et al. 2008). In other words, females are more
likely to engage in extra-pair copulations when their social mate is similar
in personality compared with her own personality. Such disassortative deci-
sion making in reproduction may ensure high offspring variability and also
contributes to maintaining high variation in personality within a popula-
tion, in a similar way as has been argued for links between mate preferences
for partners with different immune characteristics (Wedekind et al. 1995;
Kees van Oers and Marc Naguib | 85
Birds are excellent model organisms for studying the causes and conse-
quences of personality in descriptive and experimental ways in the ﬁ eld
and in the laboratory. Integrating information obtained from studies un-
der controlled experimental lab conditions with experimental studies in
the ﬁ eld and analyses of ﬁ tness-relevant traits under natural conditions has
generated multifaceted insights into principles of personality. So far, much
of the ﬁ eld research addressing evolutionary and ecological questions has
been conducted on great tits, which remain the species in which the study
of causation and consequences of personality under natural conditions has
been best integrated. With research on personality now gradually expand-
ing to other avian species, the opportunity to obtain comparative data sets
allowing us to link basic species differences in life history to our current un-
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