Content uploaded by Bodo Brand
Author content
All content in this area was uploaded by Bodo Brand on May 05, 2015
Content may be subject to copyright.
Arch. Anim. Breed., 58, 13–21, 2015
www.arch-anim-breed.net/58/13/2015/
doi:10.5194/aab-58-13-2015
© Author(s) 2015. CC Attribution 3.0 License.
Open Access
Archives Animal Breeding
Genetics of cattle temperament and its impact on
livestock production and breeding – a review
J. Friedrich1, B. Brand2, and M. Schwerin1,2
1Institute of Animal Science and Technology, University of Rostock, Rostock, Germany
2Institute for Genome Biology, Leibniz Institute for Farm Animal Biology (FBN), Dummerstorf, Germany
Correspondence to: M. Schwerin (schwerin@fbn-dummerstorf.de)
Received: 6 June 2014 – Accepted: 13 November 2014 – Published: 4 March 2015
Abstract. Cattle temperament, which describes individual behaviour differences with regard to a stressor or
environmental challenge, is known for its impact on working safety, adaptability to new housing conditions,
animal productivity and for evaluation of animal welfare. However, successful use of temperament in animal
breeding and husbandry to improve keeping conditions in general or animal welfare in particular, requires the
availability of informative and reproducible phenotypes and knowledge about the genetic modulation of these
traits. However, the knowledge about genetic influences on cattle temperament is still limited. In this review,
an outline is given for the interdependence between production systems and temperament as well as for the
phenotyping of cattle temperament based on both behaviour tests and observations of behaviour under production
conditions. In addition, the use of temperament as a selection criterion is discussed.
1 Introduction
During the last several decades, new management systems
have been introduced worldwide in cattle production, pre-
senting new challenges for animals and farmers. In particular,
the increasing automation of routine processes and growing
herd sizes due to the intensification of livestock production
limit the contact between cow and farmer (Raussi, 2003) and
contributes to fear of humans and stressful events (Boissy
et al., 2005). Since the ability of cattle to cope with exter-
nal stimuli affects the susceptibility to stress (Jensen, 2006),
stress from routine management processes, like the regroup-
ing of a herd, can result in aggressiveness, increased loco-
motion and decreased productivity if coping strategies are
insufficient (Bøe and Færevik, 2003). Increased stress has
additionally been shown to affect physiological processes
of the immune and reproductive system negatively (Burdick
et al., 2011). Accordingly, cattle temperament, which de-
scribes “consistent behavioural and physiological differences
observed between individuals in response to a stressor or
environmental challenge” (Sutherland et al., 2012) is found
to have a considerable impact on performance, reproduc-
tion, health and animal welfare. Temperament comprises be-
havioural characteristics like shyness-boldness, exploration-
avoidance, activity, sociability and aggressiveness and is an
important aspect of behaviour genetics (Réale et al., 2007).
Based on the theory that animal welfare comprises the an-
imals’ “state as regards its attempts to cope with its envi-
ronment” (Broom, 1986) and with the evaluation of emo-
tionally positive surroundings (Veissier et al., 2012), the se-
lection for temperament types that are well suited for spe-
cific production systems is expected to improve productiv-
ity and overall animal welfare (Boissy et al., 2005; Fergu-
son and Warner, 2008). Animal welfare covers the physio-
logical state, biological needs and furthermore the emotional
condition of animals (von Keyserlingk et al., 2009). Criteria
for the evaluation of animal welfare were introduced years
ago by the concepts of the Farm Animal Welfare Council
(FAWC, 1979) and by Bartussek et al. (2000), but in spite
of different approaches, it is complicated to assess the emo-
tional state of cattle since these concepts are mainly based on
environmental factors. However, a novel approach, the Ani-
mal Welfare Assessment Protocol, introduced animal-based
measurements including behaviour for assessing animal wel-
fare (Welfare Quality®, 2009). The assessment of cattle be-
haviour in certain situations could provide additional infor-
Published by Copernicus Publications on behalf of the Leibniz Institute for Farm Animal Biology.
14 J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding
mation on the physiological and emotional state of the ani-
mal overall, improving animal welfare evaluation.
Besides environmental influences, genetic factors are
known to contribute to the development of the behaviour phe-
notype (Mormède, 2005). The possible genetic predisposi-
tion of temperament and the potential impact of temperament
on cattle welfare and production traits has focussed attention
on behavioural phenotyping and the opportunity of selection
for temperament.
However, integrating cattle temperament in breeding pro-
grams is difficult. Temperament is assumed to be multidi-
mensional, and due to the complexity of behavioural traits
there is no single objective measurement that is able to cap-
ture all behavioural characteristics (Réale et al., 2007). In
addition, Oltenacu and Broom (2010) found a conceivable
competitive relationship between the genetic selection for
dairy production and adaptability due to limited physiologi-
cal resources, resulting in poorer adaptability by selection for
milk yields. Furthermore, Grandin (1994) discussed that the
masking of unfavourable behavioural traits like nervousness,
flightiness or excitability by adaption to the human-created
environment of livestock production hinders the selection for
behavioural traits like temperament. One possibility for over-
coming these problems is the analysis of the genetic back-
ground of cattle behaviour, which could contribute to the suc-
cessful integration of temperament in breeding programs by
the use of temperament associated markers (marker-assisted
selection or genomic selection) and further help to evaluate
the correlation between temperament and performance. The
most important prerequisite to identify genetic loci affect-
ing temperament is the development of distinct informative
and reproducible phenotypes characterizing different temper-
ament types.
2 Phenotyping cattle temperament
2.1 Cattle temperament and production systems
Particular experiences, especially early ones, are important in
the development of temperament in cattle. On average, young
cattle were observed to be more temperamental than older
cattle (Voisinet et al., 1997; Lanier et al., 2000) and with age-
ing, cattle behaviour was found to be more consistent over
time (Gibbons et al., 2011; Haskell et al., 2012). These mod-
ulations of behaviour through individual experiences and
therefore through ageing are assumed to evolve from changes
in the reactivity of the nervous system (Grandin and Dess-
ing, 1998). The graduate adaption to repeated external stim-
uli is referred to as habituation (Cyr and Romero, 2009). In
livestock production, habituation is mainly determined by
the adaptability to human-made environments and the fre-
quency of human–animal contact overall, depending on the
production system. Extensively kept cattle, for example, are
only occasionally handled and are therefore less approach-
able than intensively housed beef or dairy cattle (Le Neindre
et al., 1996). As a consequence of the adaption and selection
for different production and housing systems, a large vari-
ability in temperament exists today in farm animals, result-
ing from differences in reactions towards human contact and
new surroundings (Hopster, 1998; Sutherland et al., 2012).
Fear is considered one of the main psychological factors un-
derlying temperament traits in general, and in particular, fear
of humans affects the human–animal relationship consider-
ably (Adamczyk et al., 2013). When humans were involved
in behaviour tests, it could be observed that fearfulness was
more evident in comparison to tests without human pres-
ence (Mazurek et al., 2011). The degree of fearfulness, or
avoidance, of humans is indicated by the flight distance or
flight speed that is known to depend on the frequency and
quality of human–cattle habituation (Waiblinger et al., 2003;
Schütz et al., 2012) and can be measured when an animal
flees to avoid human contact. Besides individual experiences
and ageing, the influence of sex on cattle temperament is dis-
cussed. Some beef cattle studies documented that cows had
higher temperament scores than steers (Voisinet et al., 1997;
Gauly et al., 2002; Hoppe et al., 2010). Just as the production
system promotes certain behavioural characteristics, animal-
specific temperament can likewise affect relevant parame-
ters in livestock production. Docility in cows, for example,
was observed to affect reproduction traits positively, includ-
ing the calving rate, the age at first observed oestrus (Phocas
et al., 2006) and conception rates (Cooke et al., 2011). Fur-
thermore, a negative correlation was reported between fear of
humans and milk yield (Hemsworth et al., 2000), explaining
up to 19% of the milk yield variances between farms ob-
served in the study of Breuer et al. (2000). The dynamics of
the hormone oxytocin have been widely analysed as a possi-
ble explanation for the correlation between temperament and
milk performance. Bruckmaier and Blum (1998) summed up
that the release of oxytocin may be repressed by the cen-
tral nervous system due to increased levels of β-endorphin
and cortisol when cows were milked in novel environments.
Rushen et al. (2001) documented lower plasma oxytocin con-
centrations in unfamiliar milking parlours confirming a nega-
tive effect of novelty on milk production, whereas Sutherland
et al. (2012) found higher oxytocin concentrations and a drop
in milk yield after milking in novel environments. They dis-
cussed variations in the activation of the sympathetic nervous
system as causal physiological mechanisms for disturbances
in milk letdown by peripheral inhibition of oxytocin effects,
as it is suggested by Van Reenen et al. (2002). In a study of
Orbán et al. (2011), no correlation between milk yield and
temperament could be detected, but calmer cattle had lower
somatic cell counts.
In beef cattle, negative side effects of temperament on the
average daily weight gain, live weight and meat quality were
reported in various studies (Voisinet et al., 1997; Gauly et
al., 2001; Petherick et al., 2002; King et al., 2006; Nkrumah
et al., 2007; Hall et al., 2011; Vetters et al., 2013). In Bos
taurus steers, for example, docility resulted in up to 0.19kg
Arch. Anim. Breed., 58, 13–21, 2015 www.arch-anim-breed.net/58/13/2015/
J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding 15
higher average daily weight gains (Voisinet et al., 1997). The
individual temperament is discussed to affect weight gains
through influencing the feed conversion efficiency (Pether-
ick et al., 2002) and inducing differences in feed intake and
time spent eating (Cafe et al., 2011b). In addition differences
in the susceptibility to stress during slaughter were shown
to result in variances regarding meat quality. Calm animals
were observed to have significantly higher postmortem pH
values (King et al., 2006) and more tender meat (Hall et al.,
2011). Magolski et al. (2013) tried to explain the mechanisms
behind the correlation of temperament and beef tenderness
by analysing the association between protein degradation,
calpain system activity and temperament but no significant
explanatory relationship could be identified. Despite more
and more studies on a possible correlation between cattle be-
haviour and production traits, inconsistent findings illustrate
the demand for further research and standardized tests to elu-
cidate the underlying mechanisms.
2.2 Measuring the behavioural phenotype in cattle
In cattle, many approaches exist for measuring behaviour.
A detailed overview about different behaviour test condi-
tions and their use in farm animals is given by Canario
et al. (2013). Behaviour tests are often adapted from be-
havioural studies of laboratory rodents and can be dis-
tinguished based on the type of test (restrained or non-
restrained), the data assessment (during routine handling or
specific test conditions) and the type of measured trait (qual-
itative or quantitative). One example is the open-field test,
which is well documented and frequently used in model ani-
mals. The open-field test can be classified as a non-restrained
test where the cow is free to move within a defined test-
ing area. Kilgour (1975) introduced the open-field test for
the assessment of temperament in dairy cows for its sev-
eral advantages which are simple construction and the cre-
ation of a completely new environment, allowing the test-
ing of numerous behavioural characteristics, like reactivity
towards novelty and social isolation. Critical aspects of be-
haviour assessments in artificial test situations are the time
and space requirements to conduct the behaviour test. There-
fore behaviour is commonly evaluated during routine han-
dling processes since they are not highly time and space con-
suming. In dairy cattle, for example, behavioural assessment
is usually conducted by scoring temperament for nervous-
ness, aggressiveness or docility during milking by farmers or
milking technicians (Dickson et al., 1970; Hiendleder et al.,
2003). However, in beef cattle, scoring during weighing is a
frequent test for determining temperament. When cattle’s op-
portunities to move are limited, as in a chute during weighing
and milking, this is referred to as a restrained test (Burrow,
1997), the main advantage of which is safe application for the
handler (Boivin et al., 1992). A restraint test is able to quan-
tify characteristics like the chute score or flight speed (exit
velocity) to evaluate the temperament in response to a short
time fixation, e.g. in a squeeze chute (Black et al., 2013; Vet-
ters et al., 2013; Magolski et al., 2013). During fixation, the
number of movements is suggested to be as most promising
trait for selection of beef cattle temperament in Benhajali et
al. (2010). In their study, the number of movements during
weighing, recorded between 180 and 280 days of age, had
the highest heritability (h2=0.31±0.10) in comparison to
recorded movements when exposed to a stationary human,
with a high number of steps implying more agitated animals.
Also challenging, but essential for investigating behaviour
in cattle, is the interpretation of behavioural traits which are
usually expressed by only a few animals (Brouˇ
cek et al.,
2008). Such traits, like vocalization or escape events (out of
the testing area), are highly informative but complicate sta-
tistical evaluation. The determination of the behaviour phe-
notype can be done qualitatively by temperament scoring or
quantitatively by measurements of objective parameters like
time spent running, number of escapes, flight time or vocal-
ization events (Watts et al., 2001; Gutiérrez-Gil et al., 2008;
Cafe et al., 2011b). In general, the use of automatic measure-
ment integrated into routine processes, for example weighing
or milking, is desired in the determination of cattle temper-
ament with regard to time-management and objectivity. In
various studies, it could be shown that the determination of
behavioural traits or temperament was successful using auto-
mated detection. König et al. (2006) recorded the frequency
of voluntary entries into an automated milking system in
dairy cows and proposed this trait as breeding criterion for
cattle behaviour and Schwartzkopf-Genswein et al. (2012)
suggested two electronic measuring systems for the predic-
tion of cattle temperament. In their study, the assessments of
strain gauges and accelerometers for the movements of cat-
tle in a squeeze chute were highly correlated to subjective
temperament scores.
Depending on the procedure of behaviour assessment, spe-
cific behaviours are stimulated, for example, exploratory be-
haviour in an open-field test or fear of humans in human-
approach tests (Réale et al., 2007). This specificity hinders
the comparability between different testing conditions as it
was shown for a human approachability and novel stimuli
tests in Gibbons et al. (2009). Although temperament scoring
is subjectively due to the perception of the observer, but usu-
ally based on experimental protocols, it could be shown that
temperament scores were favourably correlated to quantita-
tive records (Schwartzkopf-Genswein et al., 2012). For in-
creasing the accuracy of the determined phenotype or tem-
perament type, the combination of behaviour records and
physiological and endocrinological parameters are used in
behaviour studies. Measurements of cortisol and heart rate
are often used to measure the activity of the hypothalamic–
pituitary–adrenal axis and sympatho-adrenal medullary sys-
tem as supplementary indicators for the stress response in
cattle (Grignard et al., 2001; King et al., 2006; Curley Jr. et
al., 2008; Burdick et al., 2010; Cafe et al., 2011a). Higher
heart rates and cortisol levels indicate more excitable or tem-
www.arch-anim-breed.net/58/13/2015/ Arch. Anim. Breed., 58, 13–21, 2015
16 J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding
peramental cattle. Furthermore, Burdick et al. (2010) found
a positive correlation between temperament and rectal tem-
perature. A rather rarely applied approach for evaluating be-
haviour in cattle was used in the study of Core et al. (2009).
They found a highly significant correlation, ranging from
0.67 to 0.95, between the eye-white percentage and tem-
perament scores assessed in a chute test in beef cattle. Be-
sides the analysis of behavioural traits and physiological pa-
rameters, the additional consideration of genetic information
could help to discriminate between behaviour phenotypes
and reveal differences and commonalities between the par-
ticular applied test conditions and measured behaviours.
3 Genetic variances affecting temperament in cattle
3.1 Genetic background of cattle temperament
Today, the genetic background of cattle temperament is gen-
erally accepted. A first indication for a genetic predisposi-
tion and an essential process leading to the development of
the contemporary livestock behaviour is found in the do-
mestication of cattle ancestors beginning 10500 years ago.
At that time, animals were selected for their adaptability
to man-made environments and their reactivity towards hu-
mans. Therefore, tameness and adaptability can be seen as
main fitness-determining factors (Price, 1999) which are as-
sumed to be under genetic control (Baker et al., 2001). Fur-
ther evidence for a genetic predisposition of cattle behaviour
are in the observed variances in inter-breed temperament.
These differences can be attributed to the selection for spe-
cific production systems as well as housing and climatic
conditions. In general, Bos indicus breeds were found to be
more excitable than Bos taurus breeds (Voisinet et al., 1997).
Dairy cattle showed a higher approachability than beef cat-
tle (Murphey et al., 1980) and were more reactive to sud-
den noises during cattle auctions (Lanier et al., 2000). More-
over, numerous behaviour studies were conducted for differ-
ent beef breeds enabling a temperament ranking from more
calm breeds like Herford and Angus to breeds that are more
temperamental like German Simmental or Charolais (Morris
et al., 1994; Gauly et al., 2002; Hoppe et al., 2010).
Estimated heritabilities for temperament, which are rather
low or moderate, indicate a lower proportion of a genetic
predisposition on the phenotypic variance. In Holstein cows,
early estimates for milking temperament ranged from 0.11
to 0.17 (Lawstuen et al., 1988; Visscher and Goddard, 1995;
Rupp and Boichard, 1999; Schrooten et al., 2000). In a more
recent study, heritability reached values of 0.13 and 0.25 for
milking temperament and milking speed in Canadian Hol-
stein cattle (Sewalem et al., 2011). The estimated heritabil-
ity for temperament traits in beef cattle is on average higher
but with a greater margin, ranging from 0.11 to 0.61, pre-
sumably due to different behaviour phenotypes and sample
sizes (Burrow, 2001; Gauly et al., 2001; Phocas et al., 2006;
Nkrumah et al., 2007; Hoppe et al., 2010). Besides the ac-
ceptance of genetic variances contributing to the modulation
of behaviour, current knowledge about genotype–phenotype
interactions is still limited. One reason, the complexity of be-
havioural traits, has been discussed; the complexity is often
distinguished by different genetic loci and therefore expected
to be polygenic traits with quantitative inheritance patterns
(Jensen, 2006).
The genetic impact on behaviour is not direct, but re-
sults from a complex response network of neurophysiolog-
ical and structural factors, like hormones and proteins, them-
selves products of indirect genetic effects (Johnston and Ed-
wards, 2002). It is assumed that proteins involved in this
process have rather general functions, like protein kinases
(Price, 2008). Protein kinase C, for example, was recently
identified as a regulator of mood-related behaviours in rats
(Abrial et al., 2013) and protein kinase G is discussed to
affect diverse behaviours in different species (reviewed in
Reaume and Sokolowski, 2009). Important neurotransmitters
that contribute to the development of behaviour are assumed
to arise from the serotonergic or catecholaminergic system
(Mormède, 2005). A frequently investigated physiological
pathway with a high inter-individual variability that can mod-
ulate behavioural characteristics is the stress response medi-
ated through the hypothalamic–pituitary–adrenal (HPA) axis.
HPA axis activity and aggressive behaviour were recently
reported to be associated with two single nucleotide poly-
morphisms (SNPs) in pigs (Muráni et al., 2010). Likewise
in cattle, parameters of the HPA axis activity were shown to
be correlated to cattle temperament. Temperamental heifers
were found to have higher baseline cortisol concentrations
than calmer animals (Curley Jr. et al., 2008). A detailed in-
vestigation of the genetic correlation between behaviour and
HPA axis parameters could be a valuable approach to iden-
tify relevant pathways and physiological responses resulting
from the genetic predisposition of temperament.
In the discussion about genetic influences on behaviour, at-
tention must also be paid to numerous environmental factors
which are external stimuli for the expression of behaviour.
As a consequence of substantial environmental effects on
behaviour, genes affecting temperament in cattle are noted
to have smaller effect sizes and thus explain a lower pro-
portion of the phenotypic variance in comparison to genetic
loci, which are associated with production traits (Gutiérrez-
Gil et al., 2008). Flint (2003) found that in laboratory rodents
merely 10% of behaviour differences are caused by genes.
Nevertheless, genes and environment should not be consid-
ered as antagonistic factors in the regulation of behaviour, but
rather as interactive (Bendesky and Bargmann, 2011). How-
ever, the approach of nature and nurture in the context of
behaviour is still debated as controversial in the literature.
Arch. Anim. Breed., 58, 13–21, 2015 www.arch-anim-breed.net/58/13/2015/
J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding 17
3.2 Genomic regions associated with temperament
traits
Genetic markers for behavioural characteristics have already
been identified in different livestock species, for example for
feather picking in hens (Flisikowski et al., 2009) and for dif-
ferent behavioural traits in pigs (Reiner et al., 2009). In cattle,
the results of previous studies have provided further proof for
a genetic disposition of behaviour and moreover confirm the
assumption that specific behavioural traits are influenced by
different genomic regions (Schmutz et al., 2001; Gutiérrez-
Gil et al., 2008). In the following, the important analyses re-
lated to cattle temperament and genetics are summarized.
In dairy cattle, research about the genetic correlation of be-
haviour has been focussed on milking temperament primar-
ily. Spelman et al. (1999) assessed subjective temperament
scores for New Zealand Holstein–Friesian and Jersey cows
during milking for genetic analysis, but no QTL (quantita-
tive trait loci) for milking adaptability could be identified.
Likewise, Schrooten et al. (2000) found no QTL correlated
with temperament during milking in Holstein–Friesian cat-
tle, but three genomic regions with suggestive linkage for
milking speed where located on chromosomes 2, 3 and 23.
In contrast, Hiendleder et al. (2003) detected four QTL for
behaviour during milking on the chromosomes 5, 18, and 29
in the same breed. Additionally, these QTL were in close
proximity to the QTL identified for milking speed in the
same study, indicating that these might be single QTL af-
fecting both traits. In further QTL mapping studies, the be-
haviour phenotypes were assessed during specific test condi-
tions and other routine handling procedures. Five microsatel-
lite markers were identified to be linked to flight distance to-
wards unfamiliar humans in Limousin and Jersey cows by
Fisher et al. (2001). Two more polymorphisms were associ-
ated with the cortisol concentration in urine and one puta-
tive marker was detected for plasma cortisol level as a re-
sponse to stress before slaughtering. In a crossbred popula-
tion of Brahman and Angus cattle, behaviour was scored for
aggressiveness, nervousness, flightiness, gregariousness and
overall temperament during weaning and slaughtering. QTL
for these scores were found on BTA1, 4, 8, 9, 16 and 18 (We-
genhoft, 2005). Boldt (2008) analysed the same experimental
population confirming the temperament associated QTL on
BTA8 and found additional QTL on BTA3, 6, 12, 26 and 29
by the use of different statistical approaches. Gutiérrez-Gil
et al. (2008) detected 29 QTL, distributed over 17 chromo-
somes in a Holstein–Charolais crossbreed population. These
genomic regions were significantly associated with traits like
frequency of vocalization, flight distance or standing at alert
that were recorded during a flight from a feeder and a so-
cial separation test. In some of these behaviour related link-
age studies, dominance effects of QTL were reported (We-
genhoft, 2005; Gutiérrez-Gil et al., 2008). Aberrations con-
cerning rearing conditions and cattle breeds (Hoppe et al.,
2010) as well as different evaluations of behaviour pheno-
types and different marker densities complicate the compara-
bility between studies and must be taken into account. Nev-
ertheless, overlapping QTL were found between the studies,
especially on BTA29 (Hiendleder et al., 2003; Gutiérrez-Gil
et al., 2008; Glenske et al., 2011).
Candidate genes
Another approach for revealing molecular pathways which
modulate behaviour is the investigation of functional candi-
date genes that are associated with behavioural characteris-
tics underlying temperament in other species (reviewed in
Bendesky and Bargmann, 2011) or of positional candidate
genes that are located in QTL for behavioural traits. In cat-
tle, putative candidate genes that affect behavioural traits
in distinct situations such as oestrus and feeding behaviour
have been reported (Nkrumah et al., 2005; Kommadath et al.,
2011; Hulsegge et al., 2013). One example for a positional
and functional candidate gene for cattle temperament is the
tyrosinase gene (TYR), which is generally known for its func-
tion in the dilution of coat colour in cattle (Schmidtz et al.,
2001), and is located in a QTL for temperament during milk-
ing on BTA29 (Hiendleder et al., 2003). Tyrosinase cataly-
ses reactions in the dopamine metabolism and is assumed to
be involved in the appearance of Parkinson’s disease in hu-
mans (Hasegawa, 2010). Other genes involved in dopamine
metabolism have been suggested as further functional can-
didate genes because the neurotransmitter dopamine itself is
associated with behavioural traits and diseases in different
species. A prominent candidate gene, the dopamine receptor
D4 gene (DRD4) has been associated with behavioural traits
like novelty seeking and curiosity in humans and different
animals (Bailey et al., 2007; Munafò et al., 2008; Korsten
et al., 2010). In cattle, DRD4 can be mapped to the distal
part of BTA29 (Glenske et al., 2011), but no QTL or direct
association for temperament in cattle have been identified in
this region so far. Another widely discussed functional candi-
date gene is the monoamine oxidase A (MAO A) gene, which
degrades catecholamines like serotonin, norepinephrine and
dopamine (Shih et al., 1999). Lühken et al. (2010) analysed
the structure of the MAO A gene in German Angus and Sim-
mental cattle and identified five SNPs in the coding region
but none of these polymorphisms were significantly associ-
ated with behaviour scores that were assessed during tether-
ing, weighing and social separation tests. Further positional
candidate genes that were located in QTL regions associated
with temperament are the cannabinoid receptor (CNR1) gene
on BTA9 (Schmutz et al., 2001), the regulator of G-protein
signalling 2 (RGS2) gene, the plexin A2 (PLXA2) gene on
BTA16 and the prolactin precursor receptor (PRL-R) gene
on BTA20 (Gutiérrez-Gil et al., 2008), but no further investi-
gation of these candidate genes have been performed in cattle
thus far.
www.arch-anim-breed.net/58/13/2015/ Arch. Anim. Breed., 58, 13–21, 2015
18 J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding
4 Perspective and challenges of behaviour genetics
in cattle
Increasing attention has been paid to cattle temperament in
livestock production for its benefit to working safety, adapt-
ability to new housing conditions, animal welfare and pro-
duction. Boissy et al. (2005) even considered the importance
of selection for adaptability as equal in importance to the
quality of housing systems with regard to animal welfare.
As a consequence, breeding for cattle behaviour has been
intensively discussed. In some countries, milking tempera-
ment of dairy cattle is already integrated as a selection in-
dex into breeding programs (reviewed in Adamczyk et al.,
2013), whereas in beef cattle, temperament is indeed rec-
ognized as an important trait for economic efficiency and
frequently assessed, but its use as a selection index is un-
common (Sant’Anna et al., 2013). Reasons for this non-
consideration are the possible competitive genetic relation-
ship between temperament and production traits (Oltenacu
and Broom, 2010) and complex behaviour evaluations.
To date considerable insights into behaviour genetics
from candidate genes to key neurological pathways have
been given for other species (reviewed in Bendesky and
Bargmann, 2011), but information on cattle are limited to
QTL mapped for behaviour, which still need confirmation
and functional approval. To overcome this lack of infor-
mation, further research is needed taking new technolo-
gies, such as microarrays, next-generation sequencing and
metabolomics, into account. In addition, objective and in-
formative methods for the assessment of cattle temperament
are needed, which can then be standardized for use in cat-
tle husbandry and breeding. In general, the behaviour mea-
surement should have adequate heritability, a high level of
reproducibility, simple application and should include han-
dling conditions since approachability and fear of humans
are important aspects of cattle behaviour.
Acknowledgements. This work was supported by the German
Federal Ministry of Education and Research (BMBF) in the context
of PHENOMICS network (grant no. 0315536A).
Edited by: K. Wimmers
Reviewed by: three anonymous referees
References
Abrial, E., Etievant, A., Bétry, C., Scarna, H., Lucas, G., Haddjeri,
N., and Lambás-Señas, L.: Protein kinase C regulates mood-
related behaviors and adult hippocampal cell proliferation in rats,
Prog. Neuropsychoph., 43, 40–48, 2013.
Adamczyk, K., Pokorska, J., Makulska, J., Earley, B., and Mazurek,
M.: Genetic analysis and evaluation of behavioural traits in cattle,
Livest. Sci., 154, 1–12, 2013.
Bailey, J. N., Breidenthal, S. E., Jorgensen, M. J., McCracken, J.
T., and Fairbanks, L. A.: The association of DRD4 and novelty
seeking is found in a nonhuman primate model, Psychiat. Genet.,
17, 23–27, 2007.
Baker, B. S., Taylor, B. J., and Hall, J. C.: Are Complex Behav-
iors Specified by Dedicated Regulatory Genes? Reasoning from
Drosophila, Cell, 105, 13–24, 2001.
Bartussek, H., Leeb, C., and Held, S.: Animal needs index for cattle.
ANI 35L/2000-cattle, Federal Research Institute for Agriculture
in Alpine Regions BAL Gumpenstein, Irdning, Austria, 2000.
Bendesky, A. and Bargmann, C. I.: Genetic contributions to be-
havioural diversity at the gene-environment interface, Nat. Rev.
Genet., 12, 809–820, 2011.
Benhajali, H., Boivin, X., Sapa, J., Pellegrini, P., Boulesteix, P., La-
judie, P., and Phocas, F.: Assessment of different on-farm mea-
sures of beef cattle temperament for use in genetic evaluation, J.
Anim. Sci., 88, 3529–3537, 2010.
Black, T. E., Bischoff, K. M., Mercadante, V. R. G., Marquezini,
G. H. L., DiLorenzo, N., Chase Jr., C. C., Coleman, S. W., Mad-
dock, T. D., and Lamb, G. C.: Relationships among performance,
residual feed intake, and temperament assessed in growing beef
heifers and subsequently as 3-year-old, lactating beef cows, J.
Anim. Sci., 91, 2254–2263, 2013.
Bøe, K. E. and Færevik, G.: Grouping and social preferences in
calves, heifers and cows, Appl. Anim. Behav. Sci., 80, 175–190,
2003.
Boissy, A., Fisher, A. D., Bouix, J., Hinch, G. N., and Le Neindre,
P.: Genetics of fear in ruminant livestock, Livest. Prod. Sci., 93,
23–32, 2005.
Boivin, X., Le Neindre, P., Chupin, J. M., Garel, J. P., and Trillat,
G.: Influence of breed and early management on ease of handling
and open-field behaviour of cattle, Appl. Anim. Behav. Sci., 32,
313–323, 1992.
Boldt, C. R.: A study of cattle disposition: Exploring QTL associ-
ated with temperament, Senior honors thesis, Texas A&M Uni-
versity, College Station, TX, USA, 2008.
Breuer, K., Hemsworth, P. H., Barnett, J. L., Matthews, L. R., and
Coleman, G. J.: Behavioural response to humans and the produc-
tivity of commercial dairy cows, Appl. Anim. Behav. Sci., 66,
273–288, 2000.
Broom, D. M.: Indicators of poor welfare, Br. Vet. J., 142, 524–526,
1986.
Brouˇ
cek, J., Uhriniˇ
caˇ
t, M., Šoch, M., and Kišac, P.: Genetics of be-
haviour in cattle, Slovak. J. Anim. Sci., 41, 166–172, 2008.
Bruckmaier, R. M. and Blum, J. W.: Oxytocin Release and Milk
Removal in Ruminants, J. Dairy Sci., 81, 939–949, 1998.
Burdick, N. C., Carroll, J. A., Hulbert, L. E., Dailey, J.W., Willard,
S. T., Vann, R. C., Welsh Jr., T. H., and Randel, R. D.: Relation-
ships between temperament and transportation with rectal tem-
perature and serum concentrations of cortisol and epinephrine in
bulls, Livest. Sci., 129, 166–172, 2010.
Burdick, N. C., Randel, R. D., Carroll, J. A., and Welsh Jr., T. H.:
Interactions between Temperament, Stress, and Immune Funtion
in Cattle, Int. J. Zool., 2011, Article ID 373197, 9 pages, 2011.
Burrow, H. M.: Measurements of temperament and their relation-
ships with performance traits of beef cattle, Anim. Breed. Abstr.,
65, 477–495, 1997.
Burrow, H. M.: Variances and covariances between productive and
adaptive traits and temperament in a composite breed of tropical
beef cattle, Livest. Prod. Sci., 70, 213–233, 2001.
Arch. Anim. Breed., 58, 13–21, 2015 www.arch-anim-breed.net/58/13/2015/
J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding 19
Cafe, L. M., Robinson, D. L., Ferguson, D. M., Geesink, G. H.,
and Greenwood, P. L.: Temperament and hypothalamic-pituitary-
adrenal axis function are related and combine to affect growth,
efficiency, carcass, and meat quality traits in Brahman steers,
Domest. Anim. Endocrinol., 40, 230–240, 2011a.
Cafe, L. M., Robinson, D. L., Ferguson, D. M., McIntyre, B. L.,
Geesink, G. H., and Greenwood, P. L.: Cattle temperament: Per-
sistence of assessments and associations with productivity, effi-
ciency, carcass and meat quality traits, J. Anim. Sci, 89, 1452–
1465, 2011b.
Canario, L., Mignon-Grasteau, S., Dupont-Nivet, M., and Phocas,
F.: Genetics of behavioural adaptation of livestock to farming
conditions, Animal, 7, 357–377, 2013.
Cooke, R. F., Bohnert, D. W., Meneghetti, M., Losi, T. C., and Vas-
concelos, J. L. M.: Effects of temperament on pregnancy rates to
fixed-time AI in Bos indicus beef cows, Livest. Sci., 142, 108–
113, 2011.
Core, S., Widowski, T., Mason, G., and Miller, S.: Eye white per-
centage as a predictor of temperament in beef cattle, J. Anim.
Sci., 87, 2168–2174, 2009.
Curley Jr., K. O., Neuendorff, D. A., Lewis, A. W., Cleere, J. J.,
Welsh Jr., T. H., and Randel, R. D.: Functional characteristics
of the bovine hypothalamic-pituitary-adrenal axis vary with tem-
perament, Horm. Behav., 53, 20–27, 2008.
Cyr, N. E. and Romero, L. M.: Identifying hormonal habituation in
field studies of stress, Gen. Comp. Endocrinol., 161, 295–303,
2009.
Dickson, D. P., Barr, G. R., Johnson, L. P., and Wieckert, D. A.:
Social Dominance and Temperament in Holstein Cows, J. Dairy.
Sci., 53, 904–907, 1970.
FAWC: Press statement from the Farm Animal Welfare Coun-
cil, http://webarchive.nationalarchives.gov.uk/20121007104210/
http://www.fawc.org.uk/pdf/fivefreedoms1979.pdf (last access:
15 November 2014), 1979.
Ferguson, D. M. and Warner, R. D.: Have we underestimated the im-
pact of pre-slaughter stress on meat quality in ruminants?, Meat.
Sci., 80, 12–19, 2008.
Fisher, A. D., Morris, C. A., Matthews, L. R., Pitchford, W. S., and
Bottema, C. D. K.: Handling and stress response traits in cattle:
identification of putative genetic markers, in: Proc 35th Intern
Conf ISAE, University of Ccalifornia Davis, Davis, CA, USA,
p. 100, 2001.
Flint, J.: Analysis of quantitative trait loci that influence animal be-
havior, J. Neurobiol., 54, 46–77, 2003.
Flisikowski, K., Schwarzenbacher, H., Wysocki, M., Weigend, S.,
Preisinger, R., Kjaer, J. B., and Fries, R.: Variation in neighbour-
ing genes of the dopaminergic and serotonergic systems affects
feather pecking behaviour of laying hens, Anim. Genet., 40, 192–
199, 2009.
Gauly, M., Mathiak, H., Hoffmann, K., Kraus, M., and Erhardt, G.:
Estimating genetic variability in temperamental traits in German
Angus and Simmental cattle, Appl. Anim. Behav. Sci., 74, 109–
119, 2001.
Gauly, M., Mathiak, H., and Erhardt, G.: Genetic background of
behavioural and plasma cortisol response to repeated short-term
separation and tethering of beef calves, J. Anim. Breed. Genet.,
119, 379–384, 2002.
Gibbons, J., Lawrence, A., and Haskell, M.: Responsiveness of
dairy cows to human approach and novel stimuli, Appl. Anim.
Behav. Sci., 116, 163–173, 2009.
Gibbons, J. M., Lawrence, A. B., and Haskell, M. J.: Consistency
of flight speed and response to restraint in a crush in dairy cattle,
Appl. Anim. Behav. Sci., 131, 15–20, 2011.
Glenske, K., Prinzenberg, E. M., Brandt, H., Gauly, M., and Er-
hardt, G.: A chromosome-wide QTL study on BTA29 affecting
temperament traits in German Angus beef cattle and mapping of
DRD4, Animal, 5, 195–197, 2011.
Grandin, T.: Solving livestock handling problems, Vet. Med., 89,
989–998, 1994.
Grandin, T. and Dessing, M. J.: Behavioral genetics and animal sci-
ence, in: Genetics and the behavior of domestic animals, edited
by: Grandin, T., Academic Press, San Diego, CA, USA, 1–30,
1998.
Grignard, L., Boivin, X., Boissy, A., and Le Neindre, P.: Do beef
cattle react consistently to different handling situations?, Appl.
Anim. Behav. Sci., 71, 263–276, 2001.
Gutiérrez-Gil, B., Ball, N., Burton, D., Haskell, M., Williams, J. L.,
and Wiener, P.: Identification of Quantitative Trait Loci Affecting
Cattle Temperament, J. Hered., 99, 629–638, 2008.
Hall, N. L., Buchanan, D. S., Anderson, V. L., Ilse, B. R., Carlin,
K. R., and Berg, E. P.: Working chute behavior of feedlot cat-
tle can be an indication of cattle temperament and beef carcass
composition and quality, Meat. Sci., 89, 52–57, 2011.
Hasegawa, T.: Tyrosinase-Expressing Neuronal Cell Line as in Vitro
Model of Parkinson’s Disease, Int. J. Mol. Sci., 11, 1082–1089,
2010.
Haskell, M. J., Bell, D. J., and Gibbons, J. M.: Is the response to hu-
mans consistent over productive life in dairy cows?, Anim. Wel-
fare, 21, 319–324, 2012.
Hemsworth, P. H., Coleman, G. J., Barnett, J. L., and Borg, S.: Re-
lationships between human-animal interactions and productivity
of commercial dairy cows, J. Anim. Sci., 78, 2821–2831, 2000.
Hiendleder, S., Thomsen, H., Reinsch, N., Bennewitz, J., Leyhe-
Horn, B., Looft, C., Xu, N., Medjugorac, I., Russ, I., Kühn, C.,
Brockmann, G. A., Blümel, J., Brenig, B., Reinhardt, F., Reents,
R., Averdunk, G., Schwerin, M., Förster, M., Kalm, E., and Er-
hardt, G.: Mapping of QTL for Body Conformation and Behavior
in Cattle, J. Hered., 94, 496–506, 2003.
Hoppe, S., Brandt, H. R., König, S., Erhardt, G., and Gauly, M.:
Temperament traits of beef calves measured under field condi-
tions and their relationships to performance, J. Anim. Sci., 88,
1982–1989, 2010.
Hopster, H.: Coping strategies in dairy cows, Doctoral thesis,
Agricultural University Wageningen, Wageningen, Netherlands,
1998.
Hulsegge, I., Woelders, H., Smits, M., Schokker, D., Jiang, L., and
Sørensen, P.: Prioritization of candidate genes for cattle repro-
ductive traits, based on protein-protein interactions, gene expres-
sion, and text-mining, Physiol. Genomics, 45, 400–406, 2013.
Jensen, P.: Domestication – From behaviour to genes and back
again, Appl. Anim. Behav. Sci., 97, 3–15, 2006.
Johnston, T. D. and Edwards, L.: Genes, interactions, and the devel-
opment of behavior, Psychol. Rev., 109, 26–34, 2002.
Kilgour, R.: The open-field test as an assessment of the tempera-
ment of dairy cows, Anim. Behav., 23, 615–624, 1975.
www.arch-anim-breed.net/58/13/2015/ Arch. Anim. Breed., 58, 13–21, 2015
20 J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding
King, D. A., Schuehle Pfeiffer, C. E., Randel, R. D., Welsh Jr., T. H.,
Oliphint, R. A., Baird, B. E., Curley Jr., K. O., Vann, R. C., Hale,
D. S., and Savell, J. W.: Influence of animal temperament and
stress responsiveness on the carcass quality and beef tenderness
of feedlot cattle, Meat. Sci., 74, 546–556, 2006.
Kommadath, A., Woelders, H., Beerda, B., Mulder, H. A., de Wit,
A. A. C., Veerkamp, R. F., te Pas, M. F. W., and Smits, M. A.:
Gene expression patterns in four brain areas associate with quan-
titative measure of estrous behavior in dairy cows, BMC Ge-
nomics, 12, 200, 2011.
König, S., Köhn, F., Kuwan, K., Simianer, H., and Gauly, M.: Use
of Repeated Measures Analysis for Evaluation of Genetic Back-
ground of Dairy Cattle Behavior in Automatic Milking Systems,
J. Dairy Sci., 89, 3636–3644, 2006.
Korsten, P., Mueller, J. C., Hermannstädter, C., Bouwman, K. M.,
Dingemanse, N. J., Drent, P. J., Liedvogel, M., Matthysen, E.,
van Oers, K., van Overveld, T., Patrick, S. C., Quinn, J. L., Shel-
don, B. C., Tinbergen, J. M., and Kempenaers, B.: Association
between DRD4 gene polymorphism and personality variation in
great tits: a test across four wild populations, Mol. Ecol., 19,
832–843, 2010.
Lanier, J. L., Grandin, T., Green, R. D., Avery, D., and McGee, K.:
The relationship between reaction to sudden, intermittent move-
ments and sounds and temperament, J. Anim. Sci., 78, 1467–
1474, 2000.
Lawstuen, D. A., Hansen, L. B., and Steuernagel, G. R.: Manage-
ment Traits Scored Linearly by Dairy Producers, J. Dairy Sci.,
71, 788–799, 1988.
Le Neindre, P., Boivin, X., and Boissy, A.: Handling of extensively
kept animals, Appl. Anim. Behav. Sci., 49, 73–81, 1996.
Lühken, G., Glenske, K., Brandt, H., and Erhardt, G.: Genetic vari-
ation in monoamine oxidase A and analysis of association with
behaviour traits in beef cattle, J. Anim. Breed. Genet., 127, 411–
418, 2010.
Magolski, J. D., Berg, E. P., Hall, N. L., Anderson, V. L., Keller,
W. L., Jeske, T. M., and Maddock Carlin, K. R.: Evaluation of
feedlot cattle working chute behavior relative to temperament,
tenderness, and postmortem proteolysis, Meat. Sci., 95, 92–97,
2013.
Mazurek, M., McGee, M., Crowe, M. A., Prendiville, D. J., Boivin,
X., and Earley, B.: Consistency and stability of behavioural fear
responses of heifers to different fear-eliciting situations involving
humans, Appl. Anim. Behav. Sci., 131, 21–28, 2011.
Mormède, P.: Molecular genetics of behaviour: research strategies
and perspectives for animal production, Livest. Prod. Sci., 93,
15–21, 2005.
Morris, C. A., Cullen, N. G., Kilgour, R., and Bremner, K. J.: Some
genetic factors affecting temperament in Bos taurus cattle, New
Zeal. J. Agr. Res., 37, 167–175, 1994.
Munafò, M. R., Yalcin, B., Willis-Owen, S. A., and Flint, J.:
Association of the Dopamine D4 Receptor (DRD4) Gene and
Approach-Related Personality Traits: Meta-Analysis and New
Data, Biol. Psychiat., 63, 197–206, 2008.
Muráni, E., Ponsuksili, S., D’Eath, R. B., Turner, S. P., Kurt, E.,
Evans, G., Thölking, L., Klont, R., Foury, A., Mormède, P., and
Wimmers, K.: Association of HPA axis-related genetic variation
with stress reactivity and aggressive behaviour in pigs, BMC Ge-
netics, 11, 74, 2010.
Murphey, R. M., Moura Duarte, F. A., Torres Penedo, M. C.: Ap-
proachability of Bovine Cattle in Pastures: Breed Comparisons
and a Breed x Treatment Analysis, Behav. Genet., 10, 171–181,
1980.
Nkrumah, J. D., Li, C., Yu, J., Hansen, C., Keisler, D. H., and
Moore, S. S.: Polymorphisms in the bovine leptin promoter asso-
ciated with serum leptin concentration, growth, feed intake, feed-
ing behavior, and measures of carcass merit, J. Anim. Sci., 83,
20–28, 2005.
Nkrumah, J. D., Crews Jr., D. H., Basarab, J. A., Price, M. A.,
Okine, E. K., Wang, Z., Li, C., and Moore, S. S.: Genetic and
phenotypic relationships of feeding behavior and temperament
with performance, feed efficiency, ultrasound, and carcass merit
of beef cattle, J. Anim. Sci., 85, 2382–2390, 2007.
Oltenacu, P. A. and Broom, D. M.: The impact of genetic selec-
tion for increased milk yield on the welfare of dairy cows, Anim.
Welfare, 19, 39–49, 2010.
Orbán, M., Gaál, K. K., Pajor, F., Szentléleki, A., Póti, P., Tözsér,
J., and Gulyás, L.: Effect of temperament of Jersey and Holstein
Friesian cows on milk production traits and somatic cell count,
Arch. Tierz., 54, 594–599, 2011.
Petherick, J. C., Holroyd, R. G., Doogan, V. J., and Venus, B.
K.: Productivity, carcass and meat quality of lot-fed Bos indi-
cus cross steers grouped according to temperament, Aust. J. Exp.
Agric., 42, 389–398, 2002.
Phocas, F., Boivin, X., Sapa, J., Trillat, G., Boissy, A., and Le Nein-
dre, P.: Genetic correlations between temperament and breeding
traits in Limousin heifers, Anim. Sci., 82, 805–811, 2006.
Price, E. O.: Behavioral development in animals undergoing domes-
tication, Appl. Anim. Behav. Sci., 65, 245–271, 1999.
Price, E. O.: Neurophysiological approaches to the study of behav-
ior genetics, in: Principles and applications of domestic animal
behavior, edited by: Price, E. O., CABI, Wallingfort et al., UK,
21–22, 2008.
Raussi, S.: Human-cattle interactions in group housing, Appl.
Anim. Behav. Sci., 80, 245–262, 2003.
Réale, D., Reader, S. M., Sol, D., McDougall, P. T., and Dinge-
manse, N. J.: Integrating animal temperament within ecology and
evolution, Biol. Rev., 82, 291–318, 2007.
Reaume, C. J. and Sokolowski, M. B.: cGMP-Dependent Protein
Kinase as a Modifier of Behaviour, Handbook of Experimental
Pharmacology, 191, 423–443, 2009.
Reiner, G., Köhler, F., Berge, T., Fischer, R., Hübner-Weitz, K.,
Scholl, J., and Willems, H.: Mapping of quantitative trait loci
affecting behaviour in swine, Anim. Genet., 40, 366–376, 2009.
Rupp, R. and Boichard, D.: Genetic Parameters for Clinical Masti-
tis, Somatic Cell Score, Production, Udder Type Traits, and Milk-
ing Ease in First Lactation Holsteins, J. Dairy Sci., 82, 2198–
2204, 1999.
Rushen, J., Munksgaard, L., Marnet, P. G., and DePassillé, A. M.:
Human contact and the effects of acute stress on cows at milking,
Appl. Anim. Behav. Sci., 73, 1–14, 2001.
Sant’Anna, A. C., Paranhos da Costa, M. J. R., Baldi, F., and Albu-
querque, L. G.: Genetic variability for temperament indicators of
Nellore cattle, J. Anim. Sci., 91, 3532–3537, 2013.
Schmidtz, B. H., Buchanan, F. C., Plante, Y., and Schmutz, S. M.:
Linkage mapping of the tyrosinase gene to bovine chromosome
29, Anim. Genet., 32, 119–120, 2001.
Arch. Anim. Breed., 58, 13–21, 2015 www.arch-anim-breed.net/58/13/2015/
J. Friedrich et al.: Genetics of cattle temperament and its impact on livestock production and breeding 21
Schmutz, S. M., Stookey, J. M., Winkelman-Sim, D. C., Waltz, C.
S., Plante, Y., and Buchanan, F. C.: A QTL Study of Cattle Be-
havioral Traits in Embryo Transfer Families, J. Hered., 92, 290–
292, 2001.
Schrooten, C., Bovenhuis, H., Coppieters, W., and Van Arendonk,
J. A. M.: Whole Genome Scan to Detect Quantitative Trait Loci
for Conformation and Functional Traits in Dairy Cattle, J. Dairy
Sci., 83, 795–806, 2000.
Schütz, K. E., Hawke, M., Waas, J. R., McLeay, L. M., Bokkers,
E. A. M., van Reenen, C. G., Webster, J. R., and Stewart, M.:
Effects of human handling during early rearing on the behaviour
of dairy calves, Anim. Welfare, 21, 19–26, 2012.
Schwartzkopf-Genswein, K. S., Shah, M. A., Church, J. S., Haley,
D. B., Janzen, K., Truong, G., Atkins, R. P., and Crowe, T. G.: A
comparison of commonly used and novel electronic techniques
for evaluating cattle temperament, Can. J. Anim. Sci., 92, 21–31,
2012.
Sewalem, A., Miglior, F., and Kistemaker, G. J.: Short communi-
cation: Genetic parameters of milking temperament and milking
speed in Canadian Holsteins, J. Dairy Sci., 94, 512–516, 2011.
Shih, J. C., Chen, K., and Ridd, M. J.: Monoamine oxidase: From
genes to behavior, Annu. Rev. Neurosci., 22, 197–217, 1999.
Spelman, R. J., Huisman, A. E., Singireddy, S. R., Coppieters, R.
J., Arranz, J., Georges, M., and Garrick, D. J.: Quantitative Trait
Loci Analysis on 17 Nonproduction Traits in the New Zealand
Dairy Population, J. Dairy Sci., 82, 2514–2516, 1999.
Sutherland, M. A., Rogers, A. R., and Verkerk, G. A.: The effect of
temperament and responsiveness towards humans on the behav-
ior, physiology and milk production of multi-parous dairy cows
in a familiar and novel milking environment, Physiol. Behav.,
107, 329–337, 2012.
Van Reenen, C. G., Van der Werf, J. T. N., Bruckmaier, R. M., Hop-
ster, H., Engel, B., Noordhuizen, J. P. T. M., and Blokhuis, H.
J.: Individual Differences in Behavioral and Physiological Re-
sponsiveness of Primiparous Dairy Cows to Machine Milking, J.
Dairy Sci., 85, 2551–2561, 2002.
Veissier, I., Aubert, A., and Boissy, A.: Animal welfare: A result
of animal background and perception of its environment, Anim.
Front., 2, 7–15, 2012.
Vetters, M. D. D., Engle, T. E., Ahola, J. K., and Grandin, T.: Com-
parison of flight speed and exit score as measurements of tem-
perament in beef cattle, J. Anim. Sci., 91, 374–381, 2013.
Visscher, P. M. and Goddard, M. E.: Genetic Parameters for Milk
Yield, Survival, Workability, and Type Traits for Australian
Dairy Cattle, J. Dairy Sci., 78, 205–220, 1995.
Voisinet, B. D., Grandin, T., Tatum, J. D., O’Connor, S. F., and
Struthers, J. J.: Feedlot cattle with calm temperaments have
higher average daily gains than cattle with excitable tempera-
ments, J. Anim. Sci., 75, 892–896, 1997.
Von Keyserlingk, M. A. G., Rushen, J., de Passillé, A. M., and
Weary, D. M.: Invited review: The welfare of dairy cattle–Key
concepts and the role of science, J. Dairy Sci., 92, 4101–4111,
2009.
Waiblinger, S., Menke, C., and Fölsch, D. W.: Influences on the
avoidance and approach behaviour of dairy cows towards hu-
mans on 35 farms, Appl. Anim. Behav. Sci., 84, 23–39, 2003.
Watts, J. M., Stookey, J. M., Schmutz, S. M., and Waltz, C. S.: Vari-
ability in vocal and behavioural responses to visual isolation be-
tween full-sibling families of beef calves, Appl. Anim. Behav.
Sci., 70, 255–273, 2001.
Wegenhoft, M. A.: Locating quantitative trait loci associated with
disposition in cattle, Senior honors thesis, Texas A&M Univer-
sity, College Station, TX, USA, 2005.
Welfare Quality®: Welfare Quality®assessment protocol for cattle,
Welfare Quality®Consortium, Lelystad, Netherlands, 2009.
www.arch-anim-breed.net/58/13/2015/ Arch. Anim. Breed., 58, 13–21, 2015
