周年屋外飼養の馬におけるヒトのsocial cueに対する反応
TRANSCRIPT
周年屋外飼養の馬におけるヒトのSocial cueに対する反応
誌名 Animal behaviour and managementISSN 18802133著者名 小泉,亮子
三谷,朋弘上田,宏一郎近藤,誠司
発行元 日本家畜管理学会巻/号 53巻2号掲載ページ p. 69-78発行年月 2017年6月
農林水産省 農林水産技術会議事務局筑波産学連携支援センターTsukuba Business-Academia Cooperation Support Center, Agriculture, Forestry and Fisheries Research CouncilSecretariat
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- Original article -
Skill reading of human social cues by horses (Equus caballus) reared under year-round grazing conditions
Ryoko KOIZUMI1 *, Tomohiro MITANI2, Koichiro UEDA3, Seiji KOND04
1Animal Science Department, Graduate School of Agriculture, Hokkaido University, Sapporo, Hokkaido,
060-8589, Japan Field Science Centerfor Northern Biosphere, Experimental Farm, Hokkaido University, Sapporo,
Hokkaido, 060-0811, Japan 3Research Group of Animal Science, Division of Fundamental Agriscience Research, Research Faculty
of Agriculture, Hokkaido University, Sapporo, Hokkaido, 060-8589, Japan
4The Hokkaido University Museum, Hokkaido University, Sapporo, Hokkaido, 060-0810, Japan
℃ orresponding author. E-mail address: [email protected]
Summary
Animals use communicative signals, such as gesture or gaze, to communicate to someone the
intention or expression of the sender, which is called social cue. In the previous studies, it was
suggested the skill of reading human social cue in domestic animals are influenced to the domestication,
the experience contacting with human and training to obey human. In this present study, we tested the skill for horses (Equus caballus) kept in year-round grazing conditions using 33 horses differed from
breed and the degree of the experience with human by object-choice task subjects choosing either of
bait boxes located at the end of experimenter. As results, non-socialized horses hardly responded to
human social cues. Habituated horses that were both of trained and untrained responded to human social
cues, but their accuracy rates were not more than 50% except for two trained subjects. For the skill
of reading human social cues, there was high individual variation in responding to human social cues in
horses kept in year-round grazing conditions. The individual characteristics influenced to it more than
domestication, the experience with human, and training to obey human.
Keywords: horse behavior, human-horse communication, animal cognition, social cue
Animal Behaviour and Management, 53 (2): 69-78, 2017
(Received 14 October 2016; Accepted for publication 25 April 2017)
Introduction
One of the objectives of domestication is to
produce valuable animals for humans to utilize;
therefore, artificial selection and/ or breeding have
been used for modification of certain animals. Of
course, this has affected the relationship between
domestic animals and humans, i.e., domestication
may decrease the animal's fear of humans and
increase their affinity and tameness, thereby
enabling humans to control their behaviors.
Recent studies have revealed that domestic
69
dogs (Canis familiaris), one of the oldest
domesticated animals, not only obey humans
readily, but also communicate with humans using
human social cues, whereas these skills are
lacking in wolves (Canis lupus) (Miklosi et al.,
1998; Hare and Tomasello, 1999; Agnetta et al.,
2000; Viranyi et al., 2008). In addition, the dogs' skills appear to be more flexible and human-like
than other animals including primates, which are
more closely related phylogenetically to humans
than others (Hare et al., 2005). A social cue is a
communicative signal, such as a gesture or gaze,
Skill Reading Human Social Cue in Horse
which is used to communicate to someone the
intention or expression of the sender. When social
cues are used for communication, it is essential
that the receiver of the social cue pays attention
to the sender. Hare et al. (2005) hypothesized
that dogs'special skills in communicating with
humans were neither simply inherited from wolves
nor learned as a result of exposure to humans in
ontogeny, but rather they have evolved as a result
of domestication.
In contrast, Udell et al. (2008) suggested
another hypothesis that the environment affected
an animal's social ability to react in situation— appropriate ways to the social cues of others.
According to their study, dogs from shelters were
less successful in using human pointing cues than
pet or trained dogs. Another study also supports
the positive impact of human contact experience.
Although common bottlenose dolphins (Tursiops
truncatus) and brown fur seals (Arctocephalus
pusillus) are not domesticated animals, they
are able to use human communicative cues
(Pack and Herman, 2004; Scheumann and Call,
2004). According to these studies, in some
cases, the experience of having contact with
humans encourages animals to follow human
communicative cues. However, it is unclear what
factor initiates this skill for reading human social
cues. To determine this factor, tests on other
domestic animals reared in various situations are
needed.
In the present study, we tested these skills
for horses (Equus caballus). Docility to human
has been one of the most important factors in
domestication for them, and they use visual
signals to announce the existence of predators to
their mates when communicating in herd (Kondo,
2001). Thus, the horse is a good model species to
examine the effects of domestication ap.d sociality
on the animal's ability to use human attention as
a social cue (Krueger et al. 2011). The results
would aid in revealing the factor is involved
in communicative skills in domestic animals.
Furthermore, we considered the influence of
training. For horses, training and/or breaking
are very important in order to utilize them for
human activities. If horses have a social skill to
read human social cues, then we would be able to
developing the relationship between humans and
working horses and riding them further than as
was.
Then, we conducted three experiments using
object-choice tasks, i.e., the horse finding the
70
hidden food by using a human giving them social
cues in order to reveal the factor which is
necessary to read human social cues. Experiment
1 compared non-socialized horses with trained
ones, Experiment 2 used habituated subjects that
were both trained and untrained, and Experiment
3 tested trained individuals only. The subjects
did not interact with humans on a daily basis, and
were maintained under grazing conditions, with no
supplement food and low handling from humans,
for the entire year.
Materials and Methods
The experiments were conducted at the
Hokkaido University Shizunai Livestock Farm,
Shin-Hidaka, Hokkaido, Japan. All procedures
were carried out according to the stipulations for
animal experimentation at Hokkaido University.
Animals
Experiment 1
In this experiment, we used 21 horses (8
half-breed and 13 Hokkaido native horses) and
divided them into 4 groups according to their
backgrounds. The groups were as follows:
NL group: Five Hokkaido native horses (all
females, 11.8士 5.0years of age), born at the
Hokkaido University Shizunai Livestock Farm.
They were not handled and only had contact with
humans once a month for weighing their body
weight.
NM group: Eight Hokkaido native horses
(two females and six geldings, 9.5土 4.6years
of age) born at the same farm as the NL group.
They were trained for riding but were only used
irregularly for this purpose.
HM group: Three half-breed horses (all
geldings, 10.7士 3.1years of age) also born at
the same farm as the NL and NM groups and
trained for riding. They were used for riding
irregularly.
HH group: Five half-breed horses (three
females and two geldings, 5.8士 1.0years of
age). They were born at a different farm from
the other three groups and were reared under
controlled housing conditions and management.
They were trained as riding horses and used
irregularly for riding.
Experiment 2
The subjects were 12 Hokkaido native horses
born at Hokkaido University Shizunai Livestock
KOIZUMI, MITANI, UEDA, KONDO
Farm. Six of them were trained for riding
(Trained Group; two females and four geldings,
5.3 土 2.6years of age) and ridden irregularly.
The others had never been trained for riding
and ridden (Untrained Group; six females; 2.3
士 0.5years of age) but were familiar with the
experimenter and handler by their giving food and
touching them every day.
Experiment 3
Six trained horses from Experiment 2 (two
females and four geldings, age 5.3士 2.6years
old) were used.
All subjects in Experiments 1, 2, and 3 were
given bran or oat during the experiment period
only. They were kept in grazing year-round
without any other supplement food.
Social cues
In Experiment 1, four social cues were used: (1) Pointing cue (PC): the female experimenter
pointed to the correct box using her forefinger
until the subject chose one of the boxes. She kept
her eyes to the front.
(2) Gazing cue (GC): The female experimenter
looked straight ahead at first, and turned her
head to the correct box. She kept her eyes on it
until the subject chose a box.
(3) Body orientation cue (BC): The female
experimenter bodily turned to the correct box
until the subject chose a box.
(4) No cue (NC): The female experimenter
stood with her head down until the subject chose
a box. Five trials for each cue were conducted,
thus twenty trials in total were done, and the
order was pseudorandomized.
In Experiment 2, we used PC and NC,
conducted 10 trials per day. The trials were
carried out for 5 days, but the trials of NC were
only for a day.
In Experiment 3, we used the same cues with
Experiment 1. Ten trials per day were conducted,
with the experiment running for seven days (in
total fifty trials using the different cues and
twenty trials for NC).
Test set-up
The test set-up is shown in Figs. 1 and 2. The
experimenter (E) stood between two bait boxes
(B) and put a reward, either oat or bran, in one
of them. The subject stood at the release point (R)
71
3m
門] 工Fig.1. Test set-up in object-choice task
E:experimenter, R:subject and handler, B:bait box Experimenter gives human social cue to subject. After giving it, subject chooses either of bait boxes.
Fig.2. Image of experiment procedure in object-choice task The woman standing between two boxes was experimenter and gave pointing cue to
subjects. A subject was choosing either of blue boxes.
with the handler.
Test location
Experiment 1 was conducted at an indoor pen.
It was not familiar to the subjects and there were
no other horses present during the experiment,
apart from the test subjects. In Experiments 2
and 3, the trials were conducted at an outdoor
paddock. It was a familiar place for the subjects,
and there were horses in adjacent paddocks
Skill Reading Human Social Cue in Horse
during the experiment.
Test procedure
At first, a handler walked with the subject
through the test location to become accustomed
to being there, and led it to both the left and
right bait boxes to show it the reward that was
in them. However, it did not know which box was
set the reward in. After that, the subject with the
handler stood at the release point (R), then the
experimenter called the subject's name or waved
a hand to get the subject to focus on her. When
the ears or eyes of the subject looked to the
experimenter, the experimenter gave the social
cue being tested. The subject was released after
receiving the social cue to choose either of the
boxes, while the handler remained at the release
point. The feed box that the subject approached
first was defined as their "choice." If the subject chose neither of the boxes within two minutes,
it was considered "no answer." When the subject
chose the correct box, it was allowed to eat some
bates as the reward and the handler led it back to
the release point.
Data collection and statistical analysis
We counted the number of responses as the
number of times the horse chose either of the
bait boxes, and calculated the percentage of
response as the number of responses out of 20.
The number of choosing the correct bait box was
counted as the correct choice. The percentage of
correct choices was calculated as the number of
correct choices out of the number of responses.
Comparison to randomness: The scores of all
subjects were compared to randomness (the
percentage of correct choices chosen randomly;
50%) by binomial test (two tailed). Number
of correct choices; Kruskal-Wallis test tested
differences between the correct choice numbers
among groups and between days. Pearson chi-
square test was applied for detecting the
difference between each cue. In addition, three categories: (1) training for riding, (2) breed (half-
breed: HM vs. Hokkaido native horse: NM), and (3)
the experience of contact with humans (high; HH
vs. middle; HM and NM vs. low; NL) were tested
for. For categories (1) and (2) the Mann-Whitney
test was applied. For category (3), the three
groups were compared using the Kruskal-W allis
test and Steel-Dwass test. To test the influence
of learning, the score from Day 1 was compared
72
with that of Day 5 using the Wilcoxon signed-
rank test from Experiment 2. Some horses tended
to go to one side of the bait box; thus, Wilcoxon
signed-rank test also assessed any side bias of
each subject.
Results
Experiment 1
The scores of all subjects in Experiment 1 are
shown in Table 1. NR means that the subject did
not take part in the trials that could not stay at
the release point or did not choose either of the
baited boxes. These were not eliminated from the
results before analysis.
The subjects of the HH group responded
during almost all of the trials. The NL group
did not respond for any of the trials except for
one subject. The number of responses of NL was
lower than that of HH and NM, whereas there
was no significant difference between HH, HM,
and NM. Regarding the correct choice, although
the difference among the four groups was not
found to be statistically significant in the other
cues, the HH and NM groups performed better
than NL in BC (P < 0.05). Additionally, the score
of any group did not differ significantly from
randomness.
Trained horses (NM, HM, and HH) responded
better and answered correctly more often than
NL (P < 0.05). The number of responses was
raised in proportion to the contact frequency
with humans (P < 0.05). There was no statistical
difference between HM and NM in the number of
responses and correct choices for all cues.
Experiment 2
Table 2 shows the correct number chosen for
all subjects from Experiment 2. The percentages
of correct choices were shown alongside the
correct numbers, although some untrained horses
did not join in the trials.
The total correct choices for two trained
horses were significantly more than the
randomness; furthermore, one trained horse
acquired high scores above randomness during
Day 5; on the other hand, no subjects in the
untrained group exceeded it. No significant
differences between days were found in this
group.
Table 3 shows the scores of each group in
Experiment 2, the percentage of responses, and
correct choices plus the time taken to choose a
KOIZUMI, MITANI, UEDA, KONDO
Table 1. Number of the response and correct choice of individuals in Exp. 1
Social Cue
NC PC GC BC
Group Name Response N20 N-5 N5 N5 N-5
HH Ku 20 1 3 4 3
An 18 2 3 3 3
Sk 20 4 3
゜3
Cl 20 2
゜5* 2
Hi 17 3 4 2 4
HM Ka 15 2 2 2 2
Na 12 1 2 1 3
Mij NR NR NR NR NR
NM Ts 20 3 3 2 2
Ns 17 3 2 1 2
Ht , ゜
1 1 2
So 4
゜1 2 1
Mic 18 2 1 2 3
Yu 11 1
゜ ゜3
Ok 1 1
゜ ゜ ゜Ku 6 1 3
゜1
NL No NR NR NR NR NR
Ze NR NR NR NR NR
Ch 2
゜1 1
゜Ut NR NR NR NR NR
Ha NR NR NR NR NR
It shows the number of response and correct choice in Exp.1. The subjects took 5 trials per each cue. *: P<0.05, binomial probabilities, two-tailed NR: Not Response to human giving cue HH: Half-breed trained horses; the frequency of experience of contacting with human was highest in four groups. HM: Half-breed horses, experienced training for riding, but had remained grazing from birth. NM: Hokkaido Native horses, experienced training for riding, grew in the same environment with HM. NL: Hokkaido Native untrained horses, hardly contacted with human PC: experimenter pointed the correct box until subject chose either of boxes GC: experimenter turned the head and looked at the correct box till subject choosing either of box BC: experimenter turned on the correct box till subject choosing
box. The trained group responded better than
the untrained group (P < 0.01). Moreover, the
trained group responded to human social cues
more quickly than the untrained group (P < 0.05).
However, with regard to the correct choice, there
was no significant difference between the different
groups.
Experiment 3
The scores for all subjects of Experiment 3 and
the total correct choice of each cue are shown in
73
Table 4, with results varying widely. One subject
answered correctly to all cues (PC:33/50 and
GC:37 /50, P < 0.05; BC:32/50, P < 0.1). For
another horse, the correct number of two cues
was significantly above randomness (PC:41/50,
P < 0.05; GC:32/50, P < 0.1). Three horses
chose the right side box (from the experimenter's
side) significantly (data not shown); however, the
correct numbers of all cues were not significantly
above randomness.
For the cues, the subjects performed
Skill Reading Human Social Cue in Horse
Table 2. Number of correct choice of each day for each horse in Exp.2
Trained Group
Day 1 Day2 Day3 Day4 Day5 Total No cue Name
N-10 N-10 N-10 N-10 N-10 N-50 N-10
N 2 7 9* 8 9* 35** 7
u 4 4 6 6 4 24 5
H 7 3 4 3 9* 26 5
K 3 5 5 5 7 25 6
s 9* 4 8 7 9* 37** 3
T 5 6 4 6 6 27 7
Untrained Group
Name Day 1 Day2 Day3 Day4 Day5 Total No cue
N-10 Aた10 N-10 N-10 N-10 N-50 N-10
Ks 3 4 7 5 7 26 6
Hr 3 (42.9%) 5 (44.6%) 4 5 7 24 (51.7%) 1
Ao 4 6 5 5 5 25 4
Ai 2 2 4 1 (52.7%) 8 17 4
Mz 7 (77.8%) 6 5 4 6 (57.6%) 28 4
Ma 7 6 4 4 4 25 5
*: P<0.05, **: P<0.01, binomial probabilities, two-tailed In Exp.2, it compared the response to PC of trained group consisted of the subjects trained for riding with of untrained group habituated to human but not trained for riding. 10 trials were conducted per a day and done 5 days in total. As some trained horses did not respond, the percentage choosing correct is shown in parentheses (correct choice per response number).
significantly better in PC and GC than
randomness (PC: 185/300, GC: 188/300, P <
0.05), but a significant difference between the
three cues was not found (x2=1.29, P = 0.52). The
percentage of NC was under 50%. Moreover, the
subjects chose the correct box better when given
cues than for NC (P < 0.05).
Discussion
In this study, no groups performed significantly
74
above randomness for the percentage ofcorrect
choices of boxes. In addition, there was high
individual variation when responding to human
social cues. In contrast, even 4-month-old dogs
understand human communicative cues similar
to the 4-year-old dogs (Agnetta et al. 2000,
Vir紐yiet al. 2008). Considering the results, it
can be concluded that horses are inferior to dogs
in identifying the different human social cues.
Although both dogs and horses are domestic
animals, their domestication roles and time span
KOIZUMI, MITANI, UEDA, KONDO
Table 3. Comparison of the percentage of response and correct choice and time required choosing between two groups in Exp.2
Trained group Significant
Untrained group Difference
Response(%) 100.0 91.0 P<O.Ol
Correct choice(%) 58.0 52.7 NS
Time for choice
(Sec) 7.1 9.9 P<0.05
They were compared by Mann-Whitney test Response percentage was the number of response out of 20. Correct choice percentage was the number of corr_ect choice per response number. Time for choice means the time subject required to choose either of bait boxes.
Table 4. Number and percentage of correct choice for all subjects in each cue in exp.3
Name PCN50 GC N-50 BC N-50 NC N-20
N 28 35* 24 , u 31 25 30 , H 41 32t 31 11
K 25 31 25 , s 33* 37* 32t 7
T 27 28 26 10
Total 185 (61.7%)* 188* (62. 7%) 168 (56%) 55 (45.8%)
*P<0.05、tP<0.1, binomial probabilities, two-tailed It shows the number of correct choice for each cue in exp.3. Total correct percentage was shown in parentheses. The trials were conducted 10 per a day. The trials were conducted for 5 days for each cue, but the trials of NC were conducted for 2 days.
are different, and the selective pressure related
to dogs'roles as workers and companions may
have imposed a greater tendency to be more
receptive to human social cues (McKinley and
Sambrook, 2000) compared to horses.
This study revealed the response to human
social cue changes in horses through the
experience of the contact with humans and
training. The horses that had hardly any contact
with humans were less sensitive to human
gestures and did not acquire the method for
communicating with humans. However, horses
75
having communicated with human did eventually
respond to human social cues. Horses generally
trained to obey human commands for riding
were required to pay attention to humans and
responded to the action of humans quickly, which
changed their behaviors. Marsb0ll et al. (2015)
also suggested even ifhandling term was short,
handler reduced behavioral reactions towards
frightening stimuli. Furthermore, the subjects
who were more conscious of humans than others
responded correctly. To collect more information
about the correlation between their skill and
Skill Reading Human Social Cue in Horse
sensitivity to human, long-term test using foals
should be conducted. The contact in the period of
foals was greatly influenced to the relationship
between human and horses (Hausberger et al.
2004). Comparing the skill of foals growing
different situations would give the hint of the
relation among the experience with human,
training for riding and the skill of reading human
social cue. Moreover, there are large horses'
different temperaments, which affect approaching
human (Lansade et al. 2008). Therefore, it is
like!y to connect with the skill for reading human
social cues; however, the sample size of this
study is difficult to judge it.
With regard to human social cues, the trained
subjects were able to respond to PC and GC,
but they were often observed to approach the
outstretched hand and follow the movement of
the experimenter's head in the test. In previous
studies, horses also showed the same behavior,
which suggests that although horses were able
to use some cues spontaneously, they did not
understand the meaning of cues but simply
responded to the human action (Maros et al. 2008;
Proops et al., 2010). Similar results in PC were
also pointed out by previous studies using other
animals, e.g., domestic goats (Kaminski et al.,
2005) and wolves reared extensively (Viranyi et
al., 2008).
In this present study, there was also no
significant difference between the scores for the
half-breed and Hokkaido native horses reared in
the same environments. This would prove that the
breed or body size did not have any influence on
the cognitive skills of horses for reading human
social cues. Tsujii (1988) also showed the score
of the pony was not different from the Kiso horse
in T-mazing. Moreover, in Experiments 2 and 3,
the score did not rise significantly day to day. A
previous study also showed negative results in
regards to learning during a test, that is, wolves
took a hundred trials to respond correctly to
humans giving cues, and they were not able to
apply what they had learnt to another cue (Agnetta
et al., 2000). This implies that the ability to read
human cues is not acquainted by learning only.
The study of Proops et al (2010) used the same
method with this study. According to them, horses
for riding or rescue were able to choose correct
bucket in experimenter placing colored wooden
block in front of it within them sight. Object-
choice task was the common method if testing the
skill of reading human social cue so that the cue
76
the horses can read such as marker placing also
should give the subjects in this study.
In conclusion, there was high individual
variation in responding to human social cues in
horses kept in year-round grazing conditions,
which suggests that the skills needed for reading
human social cues depends on the characteristics
of individuals. The characteristics of individuals
were likely to accord with feeling, thinking,
and behavior, some behavior variables were
correlated with the personality components (Lloyd
et al., 2007). It perhaps links to the respond to
human social cue. : If the response to social cues correlated with the characteristics of individuals,
it would enable selection for more appropriate
horses to owners. Therefore, future studies
should examine the relationship between the
characteristics of other behaviors and response to
human social cues in the subjects who responded
to human social cues correctly.
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Skill Reading Human Social Cue in Horse
周年屋外飼養の馬におけるヒトの Socialcueに対する反応
小泉亮子 1* • 三谷朋弘 2 • 上田宏一郎 3・近藤誠司 4
1北海道大学大学院農学院生物資源科学専攻
2北海道大学北方生物圏フィールド科学センター
3北海道大学大学院農学研究員基盤研究部門畜産科学分野
4北海道大学総合博物館
℃ orresponding author. E-mail address: [email protected]
要約
個体間で情報交換する場合に送受信される生体的信号は Socialcueと呼ばれる。一般的に、動物一
ヒト間コミュニケーションにおける Socialcueの理解については、家畜化、ヒトとの接触経験、調教
の影響が示唆されている。そこで、本試験では、ウマ (Equuscaballus) を対象とし、未馴致馬、未調
教馬、調教馬を用いて人の Socialcue理解における影響要因について object-choicetask (物体選択法)
を用いて検討した。試験には、品種、調教の有無および人との接触経験が異なる 33頭のウマを用いた。
物体選択法では、試験者の両端に置いた飼槽のどちらかに餌報酬を入れ、試験者が報酬の入った飼槽に
Social cueを提示した後、供試個体に選択させた。その結果、未馴致馬はヒトの Socialcueに対して
ほとんど応答せず、調教馬および未調教馬は応答したものの、調教馬 2頭を除いて正解率は 50%を超
えなかった。ウマにおいて、ヒトの Socialcueの理解には家畜化、接触経験および調教の影響は見ら
れず、個体によってその理解度に差があることが示唆された。今後は、各個体の特性との関連を検討す
る複合的な研究が期待される。
キーワード:ウマの行動,ヒトーウマ間コミュニケーション,動物認知,ソーシャルキュー
Animal Behaviour and Management, 53 (2): 69-78, 2017
(2016. 10. 14受付; 2017. 4. 25受理)
78
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