鳥取環境大学紀要
第８号（2010．6）pp. 13‑20

A preliminary study of aggressive behavior in Siberian chipmunk
Eutamias sibiricus pups: the behavioral pattern and its
possible antipredator function
シベリアシマリス Eutamias sibiricus の幼獣で発見された
攻撃的行動についての解析：行動パターンとその捕食者防衛的機能（予報）
KOBAYASHI Tomomichi
小林

朋道

Abstract：Until date, many studies have been performed to investigate antipredator behaviors in rodents. However, aggressive-defensive behaviors of very young pups have not been reported in any
rodent species. I recently observed an aggressive behavior displayed by 10-day-old Siberian chipmunk（Eutamias sibiricus）pups whose eyes had not yet opened. In the present study, the aggressivedefensive behavior pattern of Siberian chipmunks and its possible antipredator function were investigated by preliminary experiments. The results observed were as follows:（ 1 ）the pups showed
extensive, rapid body movements and made loud calls that were almost perfectly synchronizedamong all the pups in the nest box;（2）the aggressive behavior of the pups disappeared once they
were old enough to leave the nest box and move rapidly;（3）domesticated polecats（Mustela putorius furo）retreated without biting the meat on hearing the vocalizations of the pups.
【Keywords】Pups of Siberian chipmunks, Antipredator behavior, Polecats, Weasels, Defensive call,
Rodents
Kobayashi, 1994, 2000）.

Introduction
Antipredator defensive behaviors of various animals

The Siberian chipmunk Eutamias sibiricus is a rodent

have been well categorized by Endler（1986）. Many

weighing 80 100 g and inhabiting Japan and northeast-

studies have reported diﬀerent antipredator defensive

ern areas of Eurasia. Snakes, weasels, stoats, foxes, andbehaviors of various rodents（Siberian chipmunk, Ko-brown bears are known predators of the Siberian chip-bayashi and Watanabe, 1986; California ground squirrelmunk（Snigirevskaya, 1962; Kawamichi, 1978; Kawam-

Spermophilus beecheyi , Owings and Coss, 1977; Southernichi and Kawamichi, 1980; Kobayashi, 2000）. Antipreda-

ﬂying squirrel Glaucomys volans, Borgo et al., 2006; Vole,tor behaviors displayed by the Siberian chipmunk are

Gorman, 1984; Black-tailed prairie dog Cynomys ludovi-

known to include ﬂeeing, hiding, mobbing, and snake-cianus, Loughry, 1988; Beldingʼs ground squirrel, Robin-

scent application（SSA）（Kawamichi,1978; Kobayashi

son, 1980; Wood rat, Richardson, 1942; White rat, Grif-and Watanabe, 1981 ）. SSA（applying snake-scent tofith, 1920）. Some of these defensive behaviors of

the fur）is a unique behavior that has to date only

rodents have been considered to have a protective

been observed in the Siberian chipmunk and California

function for their litters（Sherman, 1977; Tamura, 1989;

ground squirrel（Clucas et al., 2008）. This SSA behav-― 13 ―

鳥取環境大学紀要

第８号

ior in the Siberian chipmunk has been considered towith concrete walls, ceiling, and ﬂoor, and two trans-

have a preventive function against snake attacks（Ko-parent glass windows（0.8×1.0m）.The daily light-darkbayashi and Watanabe, 1981, 1986）.

cycle of the room was the same as that occurring out-

I recently observed an aggressive behavior dis-doors because of the light coming through the window.

played by 10-day-old Siberian chipmunk pups on re-

However, the maximum value of brightness was lower

ceiving some stimulus in the nest box. These pups hadin the room（approximately 600 lux）than in the out-

immature muscles, and therefore, were unable to move

doors. The females bred their pups in the nest box.

out of their nest. However, they showed aggressive be-

One day after birth, the birthing cage was connectedhaviors including extensive, rapid body movements

to another vacant cage of the same type via a corridor

and loud calls. Such aggressive behaviors have not（0.1×0.1×0.25m）（Fig. 1）. When the females enteredbeen previously observed in mammal pups.

the vacant cage, a barrier was installed in the center

This paper reports the details this newly discoveredof the corridor so that the pups in the nest box were

behavior and describes how it changed as the pups de-separated from their mothers. The lids of the cages

veloped physically. In addition, the results of an experi-

and nest boxes could be easily removed, and the lids

ment investigating the antipredator defensive eﬀect ofmade a noise when they were removed.
At day 10 after birth, when the lids of the nest box-

this behavior are also reported.

es were removed, the pupsʼ behaviors were observed
Ⅰ

The behavioral pattern and changes in this patternaccording to the following procedure:（1）the pups

as the pups developed physicallywere observed once every 5 7 days between 6:00 and
8:00;（2）when the female was in the vacant cage, theMaterials and Methods
This study was performed under captive conditions

barrier was quietly installed in the center of the corri-using two litters of four and seven pups each（i.e., a to-dor, and the number of pups that were out of the nest

tal of 12 pups born in May, 2005）. The pups were born

box was counted（the number of the pups was deﬁned

from two Siberian chipmunk females（each approxi-

as the maximum number of pups observed during themately one and a half and two years old）
, which had

5 min observation period）;（3）the lids of the cage andbeen reared in an outdoor pen（1.0×1.0×0.9m）togeth-

nest box were slowly removed, and the pupsʼ respons-

er with males for more than half a year.

es to these stimuli were recorded for approximately 1

When each female was pregnant, she was moved

min using a digital video system （Sony Digital

into a cage（0.4×0.4×0.35m）made of plastic and met-

HandyCam PCR-TRU 17k, Sony Corporation）; and（4）al, and contained a wooden nest box（0.12×0.12×0.12

the body weight of each pup and the number of pupsm）. The cage was placed in a room（5.0×4.0×2.5m）

with open eyes were recorded.

Fig.1

Setting in which the pupsʼ behavior was observed. A and C: cages made of plastic andmetal. B: wooden nest box containing pups. D: barrier being installed in the center of thecorridor connecting two cages.

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KOBAYASHI A preliminary study of aggressive behavior in Siberian chipmunk Eutamias sibiricus pups: the behavioral pattern and its possible antipredator function

Kobayashi（2008）reported that pups who had be-

Changes in VAB as the pups developed physicallygun to leave the nest box displayed SSA behavior by

Fig. 4 shows the relationship between the observed

gnawing on pieces of snake slough. In this study,changes in VAB and the morphological and behavioral

therefore, a piece of snake（Elaphe climacophora）slough

developments of the pups（weight gain, opening of（3×4cm）was presented to the pups outside the nesteyes, leaving the nest box, and SSA behavior）. A

box, and their SSA behaviors in response to the snakechange in VAB is expressed as the percentage of pups

slough were investigated between 12:00 and 13:00.

displaying VAB to the total number of pups present in

These observations were also made on the same day

the nest box. Weight is expressed as the averagewhen other observations were made. Based on theseweight of the 12 pups. The number of pups with open

investigations, the relationship between the changes ineyes is expressed as the percentage of pups whose

aggressive-defensive behavior and the morphologicaleyes were open to the total number of pups. The num-and behavioral development of the pups was clariﬁed.

ber of pups leaving the nest box is expressed as thepercentage of pups that left the nest box to the total

Results

number of pups. The number of pups displaying SSA

Behavior pattern

behavior is expressed as the percentage of pups dis-

No diﬀerence was observed in the defensive behav-

playing SSA behavior to the total number of pups thatior pattern displayed by the pups in the two litters.

encountered a piece of snake slough placed outside the

The defensive behavior pattern was characterized by

nest box.

the repeated abrupt vocalizations produced by the

The percentage of pups displaying VAB decreased

pups while arching their back for approximately 1 s

with an increase in the weight of the pups, percentage（hereafter referred to as VAB）
（Fig. 2 and 3）. Theof pups with open eyes, number of pups that left the

VAB consisted of 10 20 short vocalizations. When thenest box and those that displayed SSA behaviors.

lid of the nest box was removed, one or two pups be-

However, the factor inﬂuencing VAB the most was not

gan to display VAB. Immediately after, the other pups

clear.
In VAB displayed by 30-day-old pups, short vocaliza-in the nest box also began to display the same behavior and it continued. VAB was observed to be almost

tions were repeated only a few times.

perfectly synchronized among all the pups during its
prolonged display.

Fig. 2Pups displaying synchronized aggressive behavior with loud calls.
White arrows show the open mouths of vocalizing pups.

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鳥取環境大学紀要

第８号

Fig. 3

Sonograms of calls emitted as part of the aggressive-defensive behavior displayed byfour or ﬁve pups. Horizontal axis shows time（s）. Vertical axis in A shows relative soundpressure and in B shows frequency（kHz）.

Fig. 4

Relationship between changes in VAB vocalization displayed by pups and their morphological and behavioral developments. Refer the text for the deﬁnition of numbers（%）and weight（g）in the ﬁgure.

1980）. Field research on Siberian chipmunks per-Discussion
Synchronized vocalization and body movements dis-formed by Kawamichi and Kawamichi（1980）showed

played by almost all of the pups are important charac-that the time spent by a mother chipmunk away fromteristics related to VAB. The functioning of VAB as an

the nest increased after the birth of the pups andactual defensive behavior is not clear. However, syn-reached a maximum of approximately 10 h a day,chronized VAB displayed in a dark nest is likely to bewhen the pups were approximately 10-day-old（Fig. 5）.

signiﬁcantly eﬀective as a defense.

Moreover, a study by Kawamichi and Kawamichi

Siberian chipmunks are known to construct their（1980）as well as the findings of the present study

nests underground or in hollows in the trunks of large

suggest that pups younger than approximately 20

trees（Kawamichi, 1978; Kawamichi and Kawamichi,

days seldom leave their nest. These findings imply― 16 ―

KOBAYASHI A preliminary study of aggressive behavior in Siberian chipmunk Eutamias sibiricus pups: the behavioral pattern and its possible antipredator function

Fig. 5

Change in daily time spent away from the nest by a mother chipmunk
compared with the increasing age of the pups. This plot has been constructed using the values reported by Kawamichi and Kawamichi（1980）.

that, pups older than 10 days frequently encounter aanimals, weasels and snakes are suspected to enter the

predator that intrudes into their nest in the absence ofburrows leading to the chipmunk nests. In addition,

their mother. Pups older than 30 days can leave thethese animals are able to hear the VAB vocalizations

nest and hide in alternative shelters. Moreover, theyof chipmunk pups, which are emitted at a frequency ofalso display other defensive behaviors including SSA

less than 7 kHz （Weasels: Hayashi, 1968; Snakes:

behavior. Therefore, synchronized VAB is believed toYoung, 1999）. The VAB vocalizations of chipmunk

be displayed by 10-day-old pups and decreases once

pups may function as a defensive behavior against

they reach an age of 20 days.

weasels and/or snakes.

In this study, the relationship between the types ofIn the present study, I undertook a preliminary in-stimuli and the occurrence of VAB was not investigat-

vestigation of the possibility that VAB vocalizations

ed. However, the following were observed as stimuli to

produced by the pups defend them against attacks by

induce VAB in addition to the removal of the lid of thepolecats or weasels.

nest box:（1）Noises near the nest box and（2）Direct, gentle

Materials and Methods
Three ferrets（Mustela putorius furo; ♀ 630 g, approx-

touching of the pups by hand.
In this case, the pups performed the VAB more in-imately 0.5-year-old;♀ 640 g, 0.8-year-old,♂ 750 g,1-year-old）obtained from an animal supplier weretensely than other stimuli.
These ﬁndings suggest that light, sound, vibration,used for the experiment. Ferrets are known to be adomesticated form of the European polecat Mustela pu-

and direct touch can induce VAB.

torius retaining many wild characteristics including
Ⅱ

Experiment to investigate the antipredator function

their hunting instinct（Hayashi, 1968; King, 1984）.
The experimental apparatus was prepared as fol-of VAB vocalization
Siberian chipmunks usually give birth in an under-lows:

ground nest, which is connected to the surface by a

The corridor（5×5×55cm）was made of wood, ex-burrow or in the hollow of a tree trunk（Kawamichi

cept for the upper panel, which was a transparent

and Kawamichi, 1980）.

plastic plate （Fig. 6）. A speaker （ELE COM MS-

Weasels（Mustela）, snakes, foxes（Vulpes）, and owls

77WH）was placed at one end of the corridor and the（Strix）are known natural predators of Siberian chip-

other end of corridor was left open for the ferrets tomunks（Kawamichi, 1978）. From the nature of theseenter. The size of the entrance（6×6cm）is thought to― 17 ―

鳥取環境大学紀要

第８号

room and the apparatus, the room was darkened（ 52lux）and the experimental trials began.
In the ﬁrst trial, a piece of boiled chicken meat（18g）on a plastic sheet was placed in the corridor about
3 cm in front of the speaker. Some time later, the ferret entered the corridor. I observed and recorded the
behavior of the ferrets in the corridor with a Sony
Digital Handycam DCR-TRU17K（set for night shooting）from the corner of the room where a chair anddesk were placed. After the ﬁrst trial, the apparatus

A

B

Fig. 6

Apparatus used for the experiment to investigate the effect of VAB vocalizations on ferrets. A: View of the corridor at the end of which a speaker was set up. B: Closeup of the speaker set.

was removed from the room.
The second trial begun about 30 min after the ﬁrst
trial and the apparatus was brought back into theroom. In the second trial, the apparatus and the procedure were the same as for the ﬁrst trial, except thatbe similar to that of a Siberian chipmunk burrow

VAB vocalizations were played back.
Some time after the second trial began, the ferretbased on the report by Kawamichi et al. 1983.
The VAB vocalizations could be played back at any

would enter the corridor. I observed and recorded thetime at an amplitude of 3.5 dB at the entrance of the

behavior of the ferret in the corridor with the handyc-

corridor.

am set for night shooting. When the ferretʼs nose was
10 cm from the meat, I began to play back the record-

The experiment proceeded as follows:

ed VAB vocalizations continuously for 1 min to ob-

Each ferret was reared in a pen（1×1×1m）withserve the ferretsʼ response.

food bought from a pet shop. The experiments were

The experiment（which consisted of both the first

performed in a room with dimensions 5 × 4 × 2.5 m.

and second trials）was repeated two or three times for

The strength of the light in the room could be adjust-each ferret with an interval of more than two days be-

ed to 860, 470, 52, or 7 lux.

tween each experiment.

The pen in which the ferret was reared was placedin the room, and the door of the pen was opened to al-

Results

low the ferret to exit. Then the experimental appara-

The behaviors of the ferrets as they approachedtus（the corridor including the speaker）was placed inwithin 10 cm of the meat placed in the corridor could

the center of the room. The ferret was left to roam

be classiﬁed into the following four categories: ① bite

freely in the room one or two days（sometimes enter-and eat, ② bite and carry away, ③ move back imme-

ing the corridor）under light conditions of 860 and 7

diately, and ④ move back after approaching the meat.

lux during the period 06:00 18:00 and 18:00 06:00, re-Table 1 shows the results of the experiment. The

spectively. After this habituation of the ferret to thethree ferrets bit the meat in all eight trials in which

Table 1.

Ferrets

Responses of ferrets in the experiments to examine the eﬀect of VAB vocalizations

Experiments
Trials1

2

ﬁrst

secondﬁrst

secondﬁrst

second

a
b
c

②
②
②

③
③
③

②
①
②

③
③
③

②
①

③
③

See the text for the explanation of response of ① ‑ ③ .

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KOBAYASHI A preliminary study of aggressive behavior in Siberian chipmunk Eutamias sibiricus pups: the behavioral pattern and its possible antipredator function

VAB vocalizations were not played back. In three tri-

Endler JA（1986）Defense against predators. In Federals, the ferrets bit the meat and ate it in the corridor

ME, Lauder GV（ed）Predator-prey relationship:（i.e., displayed the behavior categorized as ①）.In ﬁve

perspectives and approaches from the study of low-

trials, they bit the meat and withdrew from the corri-

er vertebrates. University of Chicago Press, Chicago,

dor with the meat still in their mouth（i.e., displayed

pp109-134
Gorman ML（1984）The response of prey to stoat

the behavior categorized as ②）.
However, when VAB vocalization was played back,（Mustela erminea）.Journal of Zoology 202:419-423

the ferrets withdrew from the corridor without biting

Griﬃth CJ（1920）The behaviour of white rats in thepresence of cats. Psychobiology 2:19-28

the meat（i.e., displayed the behavior categorized as③）. In two trials, a ferret that had initially withdrawn

Hayashi J（1968）Common animals of the world in col-from the corridor attempted to re-enter the corridor

or. Vol Ⅲ . Hoikusya Publishing Co. Ltd., Osaka, pp

by only placing its head inside, but it stopped and re-

32-37
Kawamichi M（1978）Life of chipmunks. Shiretoko

treated after hearing repeated VAB vocalizations.

shiryokan hokoku 5:1-7（in Japanese）

The behavior categorized in ④ was not displayed in

Kawamichi M, Kawamichi T（1980）Process of inde-

any of the trials.

pendence of chipmunk pups. Shiretoko shiryokan
hokoku 2:23-32（in Japanese）

Discussion
The results indicate that VAB vocalizations pro-

Kawamichi M, Kawamichi T, Yamada T, Ijiri K and

duced by Siberian chipmunk pups can suppress the at-

Okazaki S（1983）The structure of nest burrow andtacks by ferrets. They also suggest that the predatory

its utilization in chipmunks. Shiretoko shiryokan

behavior of other Mustela species such as M. nivalis, M.

hokoku 5:41-52（in Japanese）

erminea, and M. itatsi, which are biologically similar to

King CM（1984）Weasels and polecats. In Macdonald

ferrets（Hayashi, 1968 ）, may also be curbed by suchD（ed）Encyclopaedia of mammals:1. George Allen &vocalizations.

Unwin, London, pp110-115

Young（1999）reported that many species of snakes

Kobayashi T（1994）The biological function of snake

use a hissing sound in their interactions with preda-

mobbing by Siberian chipmunks: I. Does it function

tors as well as conspeciﬁcs. From the above report, it

as a signals to other conspeciﬁcs? J Ethol 12:89-95

is clear that the frequency of the hissing sound of

Kobayashi T（2000）Behavioral responses of Siberiansnakes overlaps with that of VAB vocalizations（forchipmunks toward conspeciﬁcsʼ applied snake scent.

example, 0‒7 kHz）. Therefore, VAB vocalization may

Zool Sci 17:319-321

likely cause the ferrets to retreat because it resembles

Kobayashi T（2008）Ontogeny of snake-scent applica-

the hissing of snakes. Matthew et al.（1986）reportedtion behavior by young Siberian chipmunks Euramiasthat burrowing owls Athene cunicularia emit a sound re-sibiricus. The journal of environmental policy & man-sembling that of rattlesnakes from inside their burrow.
The report stated the possibility that the owlsʼ hissagement 2:12-18（in Japanese）
Kobayashi T, Watanabe M（1981）Snake-scent application behavior in the Siberian chipmunk Eutamias si-caused weasels to retreat from the burrow.

biricus asiaticus. Proc Japan Acad 57:141-145
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