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: rkoizumi@g.ecc.u-tokyo.ac.jp

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: rkoizumi@g.ecc.u-tokyo.ac.jp

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）

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