| |

Received: 10 March 2019    Revised: 14 July 2019    Accepted: 19 July 2019

DOI: 10.1111/asj.13283

ORIGINAL ARTICLE

Sex, age, or genetic differences related to play behaviors in

Japanese Black calves

Sarengaowa Aierqing | Akiko Nakagawa | Miki Okita | Takashi Bungo

Graduate School of Biosphere Science,

Hiroshima University, Higashi‐Hiroshima,
Japan
Correspondence
Takashi Bungo, Laboratory of Animal
Behavior and Physiology, Graduate School
of Biosphere Science, Hiroshima University,
Higashi‐Hiroshima, Japan.
Email: bungo@hiroshima-u.ac.jp
Funding information
Hiroshima University; Japan Society for
the Promotion of Science, Grant/Award
Number: 17K08064
Abstract
Play behavior in young animals has been used to evaluate the condition (health) of
livestock. We investigated age, sex, and genetic differences of Japanese Black calves
in relation to frequency of play behaviors (galloping, leaping, turning, bucking, head
butting objects, and head shaking) and examined how these relationships might af‐
fect growth during the suckling stage. Locomotor play behaviors (galloping, leaping,
turning, and bucking) and head butting objects gradually declined with the age for
both sexes. The frequency of head butting was significantly higher in males than
females. We found that significant interaction effects (age × MAOA polymorphism) in
play behaviors (except head shaking) and the frequencies of locomotor play in calves
without the wild‐type allele were significantly higher than those in younger calves (2
and 6 weeks of age). Weight gain was significantly correlated with the frequency of
locomotor play in females, but not in males. This study suggests that play in Japanese
Black calves gradually declines as they mature and that play may be controlled by
variations in the MAOA gene. In addition, the frequency of locomotor play may be an
indicator of health in female calves.

KEYWORDS
calves, MAOA, play behavior, polymorphism, welfare

1 |  I NTRO D U C TI O N
Young animals often play, but the definition of play is wide ranging.
Play would superficially appear to be pointless and unnecessary for
survival (Fagen, 1981; Muller‐Schwarze, Stagge, & Muller‐Schwarze,
1982). However, most researchers now recognize that play is im‐
portant for acquiring physical and/or cognitive life skills (Burghardt,
1998; Fagen, 1981). Studies have approached play from a variety of
perspectives, and there are many reports on play behavior in various
points of view, such as function or structure (Jensen, Vestergaard,
& Krohn, 1998; Napolitano, Knierim, Grasso, & Rosa, 2009; Sachs &
Harris, 1978). Although play is not as well as studies as other animal
behaviors, it has always been a recognized as an important behav‐
ioral characteristic of domestic animals (Brownlee, 1954). In partic‐
ular, play is recognized as an indicator of livestock welfare (Held &
Špinka, 2011) because early studies demonstrated that play typically
occurs in enriched environments (Brownlee, 1954; Fagen, 1981). For
example, play has been shown to be related to a calf's feeding envi‐
ronment (Duve, Weary, Halekoh, & Jensen, 2012; Krachun, Rushen,
& Passillé, 2010; Rushen & de Passillé, 2012), fear (de Passillé,
Rushen, & Martin, 1995), and health (Mintline et al., 2013). However,
basic information on play behavior is lacking for Japanese Black cat‐
tle, even how play varies with maturity or sex.
Locomotor play stimulates synapse formation in the cerebellum
and tweaks specialization between fast and slow skeletal muscle
fibers (Byers & Walker, 1995). Several studies have described the
involvement of the monoaminergic nervous system on play behavior
in vertebrates, indicating the possibility that the noradrenalin and
serotonin nervous system play important roles in regulating play
(Siviy, 1998). Because it is difficult to investigate the relationship

Anim Sci J. 2019;00:1–7. © 2019 Japanese Society of Animal Science |  1

wileyonlinelibrary.com/journal/asj  
 |
2       AIERQING et al.
between play behavior and the monoaminergic nervous system by
administering drugs, little is known about the relationship between
play behavior and monoaminergic nervous system in cattle. In the
last several decades, many studies have been conducted to deter‐
mine how genes influence behavior in both humans and domestic
animals (Adamczyk, Pokorska, Makulska, Earley, & Mazurek, 2013).
It is likely that this line of inquiry can be applied in determining how
genes of the monoaminergic nervous system are related to play
behavior.
The monoamine oxidase A (MAOA) is an enzyme that breaks
down monoamine neurotransmitters, mainly serotonin, into their
constituent molecular compounds (Raine, 2008; Buckholtz & Mayer‐
Lindenberg, 2008). Some reports suggest that MAOA is involved
with aggression in cattle (Brunner, Nelson, Breakefield, Ropers, &
Oost, 1993; Karere et al., 2009; Popova et al., 2001). The aim of this
study was to investigate how growth, sex, and genetic variation in
the enzyme MAOA are related to play behavior in Japanese Black
calves during suckling stage. In addition, we attempt to determine
the relationship between play and growth in calves.
2 |  M ATE R I A L S A N D M E TH O DS
We handled calves following regulations established by the Animal
Experiment Committee of Hiroshima University and Japanese Law
No. 105 and Notification No. 6.
2.1 | Animals and housing
We studied 12 male Japanese Black calves (birth weight 32.6 ± 1.5 kg)
and 10 female calves (birth weight 26.7 ± 1.3 kg) born at the experi‐
mental farm of Hiroshima University. The calves were kept with their
mothers in a calving pen, which had a 5.1 × 4.9 m bedding area (wood
shavings) and a 5.1 × 1.8 m concrete floor raised 30 cm above the
bedded area. All calves were allowed to suckle freely and were pro‐
vided concentrates and hay ad libitum during the experimental pe‐
riod. Mothers were fed a total mixed ration ad libitum and allocated
fresh feed. Pens were provided with straw twice daily (at 09:00 and
16:30 h).
2.2 | Recording behavior
We observed the behavior of calves and videotaped them for two
consecutive days, between 15:00 and 18:00 h, when the calves were
about 2, 4, and 6 weeks old. Data on play behavior for each individ‐
ual calf were recorded continuously during the observation periods.
Observation periods based on prior observations and the results of
a study by Vitale, Tenucci, Papini, and Lovari (1986) that determined
that play behavior in calves commonly occurs before noon and near
sunset. We grouped play behavior activities into the following cate‐
gories established by Jensen et al. (1998) and determined frequency
of play for each category: galloping (including running, trotting, and
cantering), leaping (including jumping), turning, bucking (including
buck kicking), head butting (objects), and head shaking.
2.3 | Sampling and genotyping
After weaning calves at the 3 months of age, we obtained blood
samples from their cervical veins and stored the samples at –20°C
until we could extract DNA. We isolated genomic DNA from whole
blood using a commercial DNA isolation kit (Takara Bio Inc.) and
measured the purified DNA with a spectrophotometer (NanoDrop
ND‐2000c: Thermo Scientific, Inc.) at the 260/280 nm absorbance
ratio. Calves were genotyped for the monoamine oxidase A (MAOA)
gene with PCR‐RFLP, as outlined by Lühken, Glenske, Brandt,
and Erhardt (2010), using the following primers: forward (5′‐ CCT
GAA GCT GAA GTA AGT TTG GTA GC ‐3′) and reverse (5′‐ CTG
ATT GCA CGG CTG TTC TAT G ‐3′). A fragment that included the
polymorphic nucleotide position was amplified and digested with
endonuclease Mnl I (Takara Bio Inc.). Digested DNA fragments
were separated on a 1.5% agarose gel and visualized after stain‐
ing with ethidium bromide. The nucleotide substitution in exon
XV of bovine MAOA (NC_007331.3:g.80340C>T) causes an amino
acid substitution (proline to leucine) at position 488 of the protein
(Lühken et al., 2010).
2.4 | Statistical analysis
Data were analyzed using the commercially available package,
StatView (Version 5, SAS Institute, 1998). We applied logarithemic
and square root transformations on skewed distributions (Bolhuis
et al., 2009). Because they were diachronic data with individual dif‐
ference, data were analyzed by the repeated measured two‐way
ANOVA relative to age and sex or age and genetic method. When
significant interaction effects were found, a post‐hoc test was done
using the Mann–Whitney U test to compare group differences for
each age category. We analyzed correlation between body weight
gain (from birth to 4 months of age) and the frequency of play be‐
havior using Spearman's rannk order correlation. Differences were
deemed significant at p < .05. Observation number in each graph
was the average values for the 2 days.
3 | R E S U LT S
3.1 | Sex difference relative to play behaviors
There were significant effects of age (i.e., week) in all elements
of play behavior except for head shaking (Figure 1). The exhibited
numbers gradually decreased as calves aged. However, the only sig‐
nificant difference in play behavior between sexes was that head
butting was more frequent in males than females (p < .01). A signifi‐
cant interaction effect of sex and age was detected in bucking play,
but based on our post hoc analysis, there was no difference between
the sexes at each age category.
AIERQING et al.
F I G U R E 1   Effects of age and sex on
play behaviors in Japanese Black calves.
Box plots show the median (center line)
and the interquartile range from the 25th
to the 75th percentile. Whiskers above
and below the box plots indicate the 10th
and the 90th percentiles, whereas circles
indicate outliers
2 week
3.2 | Genetic differences related to play behavior
The MAOA gene (located on the X chromosome) and allele frequen‐
cies of MAOA in calves were 0.62 for C and 0.38 for T respectively.
Allele frequencies did not significantly differ by sex. Numbers of
calves, by genotype, were CC (n = 4), CT (n = 4), TT (n = 2), C (n = 8),
and T (n = 4), which comprised two different groups (CC, CT, and
C vs. TT and T). There were no significant differences in genetic
effects on play behavior, but there were significant interaction ef‐
fects relative to all play behaviors (except head shaking) (Figure 2).
An examination of our post hoc results showed that the frequency
of galloping, leaping, turning, and bucking (at 2 and 6 weeks of age)
and head butting (at 2 and 4 weeks of age) were significantly higher
in calves with TT and T alleles than in calves with CC, CT, and C
alleles.
3.3 | Association between play behavior and body
weight gain
Mean weight at the fourth month of age (weaning) was 150.4 ± 7.3
for males and 129.7 ± 4.8 for females. Body weight gain in female
calves correlated significantly with galloping play (at 2 and 6 weeks),
|
      3
4 week 6 week 2 week 4 week 6 week
leaping play (at 2, 4, and 6 weeks), and turning play (at 6 weeks)
(Table 1). In addition, there were no significant relationships be‐
tween body weight gain and any play behaviors at any age in male
calves (data were not shown).
4 | D I S CU S S I O N
Our results agree with prior studies showing locomotor play behav‐
ior in young bovines soon after birth, reaching peak frequency at
the second week after birth and diminishing thereafter (Gomendio,
1988; Jensen et al., 1998; Napolitano et al., 2009). Because play be‐
havior is often induced by novel stimuli (Phillips, 2002), it is possible
that the decline in play behavior with age is due to calves becoming
more accustomed to their environment over time. In contrast with
play involved limbs, there was a similar trend in head shaking play
in that they were weaker than those in other locomotor play. This
result implies that head shaking play may be related to both play be‐
havior and some type of factor. Sandem, Braastad, and Boe (2002)
reported that the frequency of head shaking increases in dairy cow
when they become frustrated and so head shaking might be a dis‐
placement behavior. Although there have been no studies focused
 |
4       AIERQING et al.
2 week 4 week 6 week 2 week
TA B L E 1   Spearman rank correlations between play behavior
and body weight gain in female calves
Behavior Age (week) r (p)
Gallop 2 0.79 (<.01)
4 0.56 (>.05)
6 0.58 (<.05)
Leap 2 0.80 (<.01)
4 0.69 (<.05)
6 0.54 (<.05)
Turn 2 0.55 (>.05)
4 –0.01 (>.05)
6 0.62 (<.05)
on the relationship between frustration and head shaking in young
animals, it is possible that head shaking in our study might also have
been a response to frustration (e.g., an insufficient amount of milk
being provided). That may be why head shaking behavior was not
F I G U R E 2   Effects of age and MAOA
gene mutations on play behaviors in
Japanese Black calves. Box plots show the
median (center line) and the interquartile
range from the 25th to the 75th
percentile. Whiskers above and below
the box plots indicate the 10th and the
90th percentiles, whereas circles indicate
outliers. *p < .05, **p < .01, compared with
groups for each age class
4 week 6 week
associated with age any more so than the other types of locomotor
play behavior we examined.
Social play first develops at 2 weeks of age and peaks at
6 months of age (Napolitano et al., 2009). Furthermore, social play
appears to decline later than locomotor play in calves (Jansen et
al., 1998). However, we found that the frequency of head butting,
classified as social play, declined with age in a manner similar to lo‐
comotor play. Previous studies have defined head butting as social
play (Jansen et al., 1998; Napolitano et al., 2009), mainly recorded
as head butting with other calves. In our study, head butting did
not occur in the presence of other calves because calves were
separated from one another. Thus, we feel that it is appropriate
to call head butting solitary object play rather than social play.
Hall (1998) suggested that object play helps juveniles develop be‐
haviors and that are structurally similar to adult behaviors. When
grown, head butting is mostly associated with aggression or court‐
ship in males (Fraser & Broom, 1990a, 1990b; Phillips, 2002). In
fact, we found that head butting in males was significantly more
frequent than in females.
AIERQING et al.
Our study showed a significant difference between the sexes in
the frequency of head butting behavior, but not in other play be‐
haviors. Many studies suggest that males and females differ in how
they play (in species‐specific ways) and types of play in which they
engage. For example, male sheep exhibit less locomotor play than
females (Sachs & Harris, 1978), but no differences in locomotor play
occur between males and females of gazelle or swine (Gomendio,
1988; Newberry, Wood‐Gush, & Hall, 1988). In several species,
males exhibit more social play than females (Sachs & Harris, 1978;
Clutton‐Block et al., 1982; Rothstein & Griswold, 1991; Holmes,
1995; Jensen & Kyhn, 2000; Phillips, 2002). Our findings that fre‐
quency of head butting in males is higher than in females aligns with
the notion that head butting an object can be regarded as mock
sparring, particularly considering that the locus of genes that control
head butting behavior may exist on the X chromosome. Additionally,
because head butting is performed alone, it is reasonable to specu‐
late that the proposed function of head butting is to develop motor
skills and strength, not to develop social skills or enhance social co‐
hesion (Miller & Byers, 1998).
Several studies have suggested that variations in the MAOA
gene are associated with behavioral traits in mammals. Prior re‐
search reveals that mice lacking the MAOA gene are more aggres‐
sive and investigate their surroundings less (Cases et al., 1995).
Similarly, humans with a mutation of MAOA show higher levels
of aggression (Brunner et al., 1993). On the basis of these stud‐
ies, the MAOA gene first became known as a ‘warrior gene’, but it
was later determined that animals with variants of MAOA tend to
have uncontrollable impulses that sometimes induce higher levels
of aggression (Chester et al., 2015, 2014; Denson, DeWall, & Finkel,
2012). In cattle, no significant association has been detected be‐
tween a mutation of this gene and the scores of behavioral tests
performed during weighing, tethering, and separating (Lühken et
al., 2010). However, we found that calves without the wild‐type
allele played more than calves with the gene. We speculate that
the MAOA polymorphism affects the frequency of locomotor play
and that increased frequency of play may be due to impulsive be‐
haviors, similar to aggression in animals with variants of this gene.
In addition, as described above, there is a possibility that the MAOA
gene may occur on the X chromosome in calves, which controls the
motivation to head butt.
It is generally known that the frequency of play declines with
reduced nutrient intake in a variety of animals (Duve et al., 2012;
Krachun et al., 2010; Reale & Bousses, 1999). Similarly, Brown,
Klaffenbock, Nevison, and Lawrence (2015) reported that growth
rates in postnatal piglets were significantly and positively associ‐
ated with play behavior. Our result that indicated there was a sig‐
nificant relationship between the frequency of locomotor play
(galloping, leaping, and turning) and growth rate is consistent with
the Surplus Resource Theory on play behavior coined by Burghardt
(1988). Although we did not examine milk availability in our study,
we assume that sufficient nourishment will induce play behavior
and accelerate growth in calves. Although we found no association
between frequency of play and growth rate in males, implying that
|
      5
implying the surplus milk in males might be less than in females, this
question warrants further investigation.
5 | CO N C LU S I O N
We found that play behavior gradually declines as Japanese Black
calves grow and that the frequency of play behavior might be af‐
fected by a gene located on the X chromosome, such as MAOA gene.
We also found an association between growth rate and play behav‐
ior in females, suggesting that the frequency of play behavior may
be an index of female health in Japanese Black calves. Play behavior
in livestock has been recommended as a reliable indicator of animal
welfare because play often occurs under favorable energetic condi‐
tions (Boissy et al., 2007; Chaloupková, Illmann, Bartos, & Špinka,
2007; Dudink, Simonse, Marks, Jonge, & Spruijt, 2006; Held &
Špinka, 2011). Although it is likely that some measures of play can be
applied to many livestock species to indicate animal welfare, using
indicators of play to evaluate gradations in welfare should be chosen
carefully. We speculate that genetic variations affect the expres‐
sions of behaviors, particularly mutations involved with the MAOA
gene. Further work is needed on the association between genetic
polymorphisms and expression of play behaviors in Japanese Black
calves to assess both welfare and productivity.
AC K N OW L E D G M E N T S
The authors acknowledge the staffs of the Saijo Experimental Farm
Station, Hiroshima University, for their technical support in main‐
taining the animals. This work was supported by a Grant‐in‐Aid for
Scientific Research from the Japan Society for the Promotion of
Science (No. 17K08064).
ORCID
Takashi Bungo  https://orcid.org/0000-0002-3575-0974
REFERENCES
Adamczyk, K., Pokorska, J., Makulska, J., Earley, B., & Mazurek, M.
(2013). Genetic analysis and evaluation of behavioural traits in
cattle. Livestock Science, 154, 1–12. https​ ://doi.org/10.1016/j.
livsci.2013.01.016
Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling,
L. J., … Aubert, A. (2007). Assessment of positive emotions in animals
to improve their welfare. Physiology & Behavior, 92, 375–397. https​://
doi.org/10.1016/j.physb​eh.2007.02.003
Bolhuis, J. E., Ellen, E. D., Van Reenen, C. G., De Groot, J., Napel, J. T.,
Koopmanschap, R. E., … Rodenburg, T. B. (2009). Effects of ge‐
netic group selection against mortality on behavior and peripheral
serotonin in domestic laying hens with trimmed and intact beaks.
Physiology & Behavior, 97, 470–475. https​://doi.org/10.1016/j.physb​
eh.2009.03.021
Brown, S. M., Klaffenbock, M., Nevison, I. M., & Lawrence, A. B. (2015).
Evidence for litter differences in play behaviour in pre‐weaned
 |
6       AIERQING et al.
pigs. Applied Animal Behaviour Science, 172, 17–25. https​ ://doi.
org/10.1016/j.appla​nim.2015.09.007
Brownlee, A. (1954). Play in domestic cattle in Britain: An analysis
of its nature. British Veterinary Journal, 110, 49–68. https​ ://doi.
org/10.1016/S0007-1935(17)50529-1
Brunner, H. G., Nelson, M., Breakefield, X. O., Ropers, H. H., & van Oost,
B. A. (1993). Abnormal behaviour associated with a point mutation in
the structural gene for monoamine oxidase A. Science, 262, 578–580.
https​://doi.org/10.1126/scien​ce.8211186
Buckholtz, J. W., & Meyer‐Lindenberg, A. (2008). MAOA and the neuro‐
genetic architecture of human aggression. Trends in Neurosciences,
31, 120–129. https​://doi.org/10.1016/j.tins.2007.12.006
Burghardt, G. M. (1988). Precocity, play, and the ectotherm‐endotherm
transition. In E. M. Blass (Ed.), Developmental psychobiology and be-
havioral ecology. Handbook of behavioral neurobiology (Vol. 9, pp. 107–
148). Boston, MA: Springer.
Burghardt, G. M. (1998). The evolutionary origins of play revisited:
Lessons from turtles. In M. Bekoff, & J. A. Byers (Eds.), Animal play:
Evolutionary, comparative, and ecological perspectives (pp. 1–26).
Cambridge, UK: Cambridge University Press.
Byers, J. A., & Walker, C. (1995). Refining the motor training hypothesis
for the evolution of play. American Naturalist, 146, 25–40. https​://doi.
org/10.1086/285785
Cases, O., Seif, I., Grimsby, J., Gaspar, P., Chen, K., Pournin, S., … De
Maeyer, E. (1995). Aggressive behavior and altered amounts of brain
serotonin and norepinephrine in mice lacking MAOA. Science, 268,
1763–1766. https​://doi.org/10.1126/scien​ce.7792602
Chaloupková, H., Illmann, G., Bartos, L., & Špinka, M. (2007). The effect
of pre‐weaning housing on the play and agonistic behaviour of do‐
mestic pigs. Applied Animal Behaviour Science, 103, 25–34. https​://
doi.org/10.1016/j.appla​nim.2006.04.020
Chester, D. S., DeWall, C. N., Derefinko, K. J., Estus, S., Peters, J. R.,
Lynam, D. R., & Jiang, Y. (2015). Monoamine oxidase A (MAOA) gen‐
otype predicts greater aggression through impulsive reactivity to
negative affect. Behavioural Brain Research, 283, 97–101. https​://doi.
org/10.1016/j.bbr.2015.01.034
Chester, D. S., Eisenberger, N. I., Pond, R. S., Richman, S. B., Bushman,
B. J., & DeWall, C. N. (2014). The interactive effect of social pain
and executive functioning on aggression; an fMRI experiment.
Social Cognitive and Affective Neuroscience, 9, 699–704. https​://doi.
org/10.1093/scan/nst038
Clutton‐Brock, T. H., Ginness, F. E., & Albon, S. D. (1982). Red Deer:
Behavior and ecology of two sexes. Chicago, IL: University of Chicago
Press.
de Passillé, A. M., Rushen, J., & Martin, F. (1995). Interpreting
the behaviour of calves in an open‐field test: A factor analy‐
sis. Applied Animal Behaviour Science, 45, 201–213. https​ ://doi.
org/10.1016/0168-1591(95)00622-Y
Denson, T. F., DeWall, C. N., & Finkel, E. J. (2012). Self‐control and
­aggression. Current Directions in Psychological Science, 21, 20–25.
https​://doi.org/10.1177/09637​21411​429451
Dudink, S., Simonse, H., Marks, I., de Jonge, F. H., & Spruijt, B. M. (2006).
Announcing the arrival of enrichment increases play behaviour and
reduces weaning‐stress‐induced behaviours of piglets directly after
weaning. Applied Animal Behaviour Science, 101, 86–101. https​://doi.
org/10.1012/j.appla​nim.2005.12.008
Duve, L. R., Weary, D. M., Halekoh, U., & Jensen, M. B. (2012). The effects
of social contact and milk allowance on responses to handling, play,
and social behavior in young dairy calves. Journal of Dairy Science, 95,
6571–6581. https​://doi.org/10.3168/jds.2011-5170
Fagen, R. M. (1981). Animal play behaviour. New York, NY: Oxford Univ.
Press.
Fraser, A. F., & Broom, D. M. (1990a). Reproductive abilitation. In A. F.
Fraser, & D. M. Broom (Eds.), Farm animal behaviour and welfare (3rd
ed., pp. 168–174). Oxon, UK: CAB International.
Fraser, A. F., & Broom, D. M. (1990b). Play, practice and exercise. In A. F.
Fraser, & D. M. Broom (Eds.), Farm animal behaviour and welfare (3rd
ed., pp. 247–265). Oxon, UK: CAB International.
Gomendio, M. (1988). The development of different types of
play in gazelles: Implications for the nature and functions of
play. Animal Behaviour, 36, 825–836. https​ ://doi.org/10.1016/
S0003-3472(88)80165-9
Hall, S. L. (1998). Object play in adult animals. In M. Bekoff, & J. A. Byers
(Eds.), Animal play: Evolutionary, comparative, and ecological perspec-
tives (pp. 45–60). Cambridge, UK: Cambridge University Press.
Held, S. D. E., & Špinka, M. (2011). Animal play and animal welfare.
Animal Behaviour, 81, 891–899. https​ ://doi.org/10.1016/j.anbeh​
av.2011.01.007
Holmes, W. G. (1995). The ontogeny of litter mate preferences in juve‐
nile golden‐mantled ground squirrels: Effects of rearing and relat‐
edness. Animal Behaviour, 50, 309–322. https​ ://doi.org/10.1016/
anbe.1995.0247
Jensen, M. B., & Kyhn, R. (2000). Play behaviour in group‐housed dairy
calves, the effect of space allowance. Applied Animal Behaviour
Science, 67, 35–46. https​://doi.org/10.1016/S0168-1591(99)00113-6
Jensen, M. B., Vestergaard, K. S., & Krohn, C. C. (1998). Play behaviour
in dairy calves kept in pens: The effect of social contact and space
allowance. Applied Animal Behaviour Science, 56, 97–108. https​://doi.
org/10.1016/S0168-1591(97)00106-8
Karere, G. M., Kinnally, E. L., Sanchez, J. N., Famula, T. R., Lyons, L. A., &
Capitanio, J. P. (2009). What is an “adverse” environment? Interactions
of reading experiences and MAOA genotype in Rhesus monkeys.
Biological Psychiatry, 65, 770–777. https​ ://doi.org/10.1016/j.biops​
ych.2008.11.004
Krachun, C., Rushen, J., & de Passillé, A. M. (2010). Play behaviour in dairy
calves is reduced by weaning and by a low energy intake. Applied
Animal Behaviour Science, 122, 71–76. https​ ://doi.org/10.1016/j.
appla​nim.2009.12.002
Lühken, G., Glenske, K., Brandt, H., & Erhardt, G. (2010). Genetic
variation in monoamine oxidase A and analysis of association
with behaviour traits in beef cattle. Journal of Animal Breeding
and Genetics, 127, 411–418. https​://doi.org/10.1111/j.1439-0388.
2010.00855.x
Miller, M., & Byers, J. A. (1998). Sparring as play in young pronghorn
males. In M. Bekoff, & J. A. Byers (Eds.), Animal play: Evolutionary,
comparative, and ecological perspectives (pp. 144–160). Cambridge,
UK: Cambridge University Press.
Mintline, E. M., Stewart, M., Rogers, A. R., Cox, N. R., Verkerk, G. A.,
Stookey, J. M., … Cassandra, C. B. (2013). Play behavior as an indi‐
cator of animal welfare: Disbudding in dairy calves. Applied Animal
Behaviour Science, 144, 22–30. https​ ://doi.org/10.1016/j.appla​
nim.2012.12.008
Muller‐Schwarze, D., Stagge, B., & Muller‐Schwarze, C. (1982). Play be‐
haviour: Persistence, decrease, and energetic compensation during
food shortage in deer fawns. Science, 215, 85–87. https​ ://doi.
org/10.1126/scien​ce.215.4528.85
Napolitano, F., Knierim, U., Grasso, F., & De Rosa, G. (2009). Positive
indicators of cattle welfare and their applicability to on‐farm pro‐
tocols. Italian Journal of Animal Science, 8, 355–365. https​ ://doi.
org/10.4081/ijas.2009.s1.355
Newberry, R. C., Wood‐Gush, D. G. M., & Hall, J. W. (1988). Playful
behavior of piglets. Behaviour Processes, 17, 205–216. https​://doi.
org/10.1016/0376-6357(88)90004-6
Phillips, C. (2002). Play behaviour. In C. Phillips (Ed.), Cattle behaviour and
welfare (2nd ed., pp. 78–83). Oxford, UK: Blackwell Science Ltd.
Popova, N. K., Skrinskaya, Y. A., Amstislavskaya, T. G., Vishnivetskaya, G.
B., Seif, I., & de Meier, E. (2001). Behavioural characteristics of mice
with genetic knockout of monoamine oxidase type A. Neuroscience
Behavioral Physiology, 31, 597–602. https​://doi.org/10.1023/A:10123​
64910091
AIERQING et al.
Raine, A. (2008). From genes to brain to antisocial behavior. Current
Directions in Psychological Science, 17, 323–328. https​ ://doi.
org/10.1111/j.1467-8721.2008.00599.x
Reale, D., & Bousses, P. (1999). Effects of summer and winter birth on
growth of lambs in a population of feral sheep. Journal of Mammals,
80, 1028–1037. https​://doi.org/10.2307/1383273
Rothstein, A., & Griswold, J. G. (1991). Age and sex preferences for so‐
cial partners by juvenile bison bulls, Bison bison. Animal Behaviour, 41,
227–237. https​://doi.org/10.1016/S0003-3472(05)80474-9
Rushen, J., & de Passillé, A. M. (2012). Automated measurement of ac‐
celeration can detect effects of age, dehorning and weaning on loco‐
motor play of calves. Applied Animal Behaviour Science, 139, 169–174.
https​://doi.org/10.1016/j.appla​nim.2012.04.011
Sachs, B. D., & Harris, V. S. (1978). Sex differences and develop‐
mental changes in selected juvenile activities (play) of do‐
mestic lambs. Animal Behaviour, 26, 678–684. https​ ://doi.
org/10.1016/0003-3472(78)90134-3
Sandem, A. I., Braastad, B. O., & Boe, K. E. (2002). Eye white may indi‐
cate emotional state on frustration‐contentedness axis in dairy cows.
|
      7
Applied Animal Behaviour Science, 79, 1–10. https​://doi.org/10.1016/
S0168-1591(02)00029-1
Siviy, S. M. (1998). Neurobiological substrates of play behavior: Glimpses into
the structure and function of mammalian playfulness. In M. Bekoff, &
J. A. Byers (Eds.), Animal play: Evolutionary, comparative, and ecological
perspectives (pp. 221–242). Cambridge, UK: Cambridge University Press.
Vitale, A. F., Tenucci, M., Papini, M., & Lovari, S. (1986). Social be‐
haviour of the calves of semi‐wild Maremma cattle, Bos primigenius
taurus. Applied Animal Behaviour Science, 16, 217–231. https​://doi.
org/10.1016/0168-1591(86)90115-2
How to cite this article: Aierqing S, Nakagawa A, Okita M,
Bungo T. Sex, age, or genetic differences related to play
behaviors in Japanese Black calves. Anim Sci J. 2019;00:1–7.
https​://doi.org/10.1111/asj.13283​