NOTICE: This is the author’s version of the following article.
Nakamura M, Nishida T (2006) Subtle behavioral variation in wild chimpanzees, with special reference to Imanishi’s concept ofkaluchua. Primates 47: 35–42. DOI 10.1007/s10329-005-0142-z© Japan Monkey Centre and Springer-Verlag. The original publication is available on SpringerLink at http://link.springer.de

Subtle behavioral variation in wild chimpanzees, with special reference
to Imanishi’s concept of kaluchua.
Michio Nakamura1 & Toshisada Nishida2
1 Human Evolution Studies, Department of Zoology, Graduate School of Science, Kyoto University, Kyoto 606-8502,
Japan; E-mail: nakamura@jinrui.zool.kyoto-u.ac.jp; Tel.: +81-75-7534093; Fax: +81-75-7534115
2 Japan Monkey Centre, 26, Kanrin, Inuyama-shi, Aichi 484-0081, Japan

Abstract
Here we consider the concept of kaluchua (a word adopted from the English “culture”) in group-living animals
developed by Imanishi in the 1950s. He distinguished it from bunka (the Japanese equivalent to the English “culture”) because he thought that bunka had strong connotations of noble and intellectual human-like activities. Although he did not rigidly define kaluchua, his original concept of kaluchua was much broader than bunka and represented non-hereditary, acquired behavior that was acknowledged socially. However, instead of social life, complex
feeding skills have often formed the central topic in the current studies of animal culture. In order to provide evidence
that more subtle behavioral variations exist among wild chimpanzee (Pan troglodytes) populations, we directly compared the behaviors of two well-habituated chimpanzee groups, at Bossou and Mahale. During a 2month stay at Bossou, M.N. (the first author) saw several behavioral patterns that were absent or rare at Mahale. Two of them, “mutual
genital touch” and “heel tap” were probably customary for mature females and for mature males, respectively. “Index
to palm” and “sputter” are still open to question. These subtle patterns occurred more often than tool use during thestudy period, suggesting that rarity is not the main reason for their being ignored. Unlike tool use, some cultural behavioral patterns do not seem to require complex skills or intellectual processes, and sometimes it is hard to explain
the existence of such behaviors only in terms of function.
Keywords: Bossou, Culture, Mahale, Pan troglodytes, Kinji Imanishi

Introduction
Many researchers interested in culture in
non-human animals, both from the West and the East,acknowledge that Imanishi (1952) introduced the ideaof culture to early primatology even before the discovery of the famous sweet-potato washing by Koshimamonkeys (Kawamura 1959). In a Japanese essay, anevolutionist (Imanishi), a human (layman), a monkey,
and a wasp discuss the evolution of humanity. Many
authors have cited this essay in English articles(Kawamura 1959; Itani and Nishimura 1973; Nishida
1987, 2003; de Waal 1999, 2001; Hirata et al. 2001),
but Imanishi did not simply apply culture to non-humananimals in the sense that we use the term for humans,
he coined a new term, kaluchua. Kaluchua is a word
adopted from the English “culture”, and he used it instead of the word bunka, the usual Japanese equivalentof culture.
In Imanishi’s (1952) essay, when the evolutionist
first begins to introduce the concept of kaluchua, thehuman jumps to a conclusion, saying that “Certainly,
we became human, not animals, because we had
bunka”. This was probably a widely accepted view at
the time, that only humans had bunka (culture). But theevolutionist interrupted by saying, “Wait a minute. I did

not say bunka, I said kaluchua.” Then he continued
introducing his concept of kaluchua. It is difficult totranslate this part accurately into English, because bothbunka and kaluchua can be translated as culture. Thus,
those who have cited the essay have omitted the part inwhich Imanishi differentiated kaluchua from bunka.
How did Imanishi differentiate these two terms?
Unfortunately, Imanishi did not rigidly define kaluchua.
He said that kaluchua was much broader than bunka
and was non-hereditary, acquired behavior that was
acknowledged socially; consequently its existence inevitably requires continuous group-living. Later, when
Imanishi (1966) stopped using this special term, he
explained why he had been using the term kaluchua
and avoiding the term bunka: it was because the nuanceof the term bunka was human-centered and it recalledsomething like “an ape wearing a costume”. The term
bunka connoted somehow noble, intentional, sophisticated, and complex aspects of our intellectual activities,
at least in his time. It may be for the same reason that
Kawamura (1959) used the term “sub-culture”, andKawai (1965) used “pre-culture” in their English papers(both used kaluchua in their Japanese writings; Kawamura 1956; Kawai 1963). Although some Japanese
researchers, such as Itani (1981, 1991), continued touse the term kaluchua, many Japanese primatologists

now usually employ the term bunka in their Japanesewritings (e.g., Nishida 1980a; Kuroda 1999; Sugiyama
2000; Matsuzawa 2001a; Nakamura 2003a).
Following Imanishi’s prediction of kaluchua ingroup-living animals, many studies were done on
Japanese monkeys (as summarized in Itani and Nishimura 1973). At that time, the concept of kaluchua wasmuch broader (e.g., Kawamura 1956, 1965; see alsoMizuhara 1986 for criticism of such a pan-kaluchural
approach). But as the sweet-potato washing by Koshima monkeys (Kawamura 1959; Kawai 1965) became famous and almost emblematic of monkey culture,
Imanishi (1966) once commented bitterly thatsweet-potato washing was only a peripheral phenomenon in his kaluchua concept. Following this line, Itani(1991) wrote that “Frankly speaking, I think the concept of kaluchua by Imanishi has been impoverishedand its remainder has been restricted to very limitedareas of ‘knowledge and the techniques for subsistence’..... The domains of social behaviors or socialorganizations have seldom been stated in terms of
kaluchua”. Here, by “knowledge and the techniques for
subsistence”, he may have had the foraging tool use ofchimpanzees (Pan troglodytes) in mind. Tool use orpotato washing is something very human-like because
they seem to be complex and sophisticated for mere
animals. Such behavior can easily be attributed tokaluchua (or bunka, culture, whatever). What Imanishi
and Itani wanted to stress were aspects of kaluchua as
the means of group-living. For example, Imanishi(1952) wrote “A group does not split into individuals
because of kaluchua” and Itani (1957) wrote “It can besaid that kaluchural personality is what makes mutualcommunication possible and makes bonding between
individuals to form an orderly group”. For them, kaluchua was not restricted to complex feeding skills or
techniques. Rather, their question was whether
group-living could be explained in terms of kaluchua
and if something of social organization was inherited
through kaluchua. For Imanishi, and perhaps for Itanialso, kaluchua is something maintained by “identification” (Imanishi 1957).
Although we are not calling for the revival of thespecial term coined by the late Japanese primatologist(thus, hereafter, we mainly use the term “culture”),
since labels are less important than content (McGrew
2004), we think that Imanishi’s original idea is still
worth investigating and developing further. It may still
be premature to deal directly with social organization orgroup-living from the standpoint of primate culture, but
we would like to approach the issue from the side ofculture that may have been obscured by the conspicuousness of various types of tool use.
Chimpanzees have subtle social customs and otherbehavioral variations that are simple in terms of theirmotor patterns, but the function of such behavior issometimes difficult to grasp. Such behavior patterns
have sometimes been seen and recognized by researchers, but not well-described or discussed in terms ofchimpanzee culture, perhaps because of their subtlety
and/or casualness. For example, neither grooming
hand-clasp (McGrew and Tutin 1978) nor social scratch(Nakamura et al. 2000) had been considered social

customs until researchers from Gombe (McGrew and
Tutin in the former case, Marchant and McGrew in thelatter) visited Mahale. This does not mean that thesebehavior patterns were new to the Mahale researchers.
Rather, patterns had been included in the larger category of social grooming, as they always occurred in thecontext of grooming. For Mahale researchers, thesewere familiar and casual behaviors, but they had neverconsidered that they might be absent in other populations because they had no opportunity of observing agroup of chimpanzees other than those in Mahale.
Methods
Subtle social behavior patterns are unlikely to be recognized as social customs since ethologists usuallyobserve only one group of chimpanzees. The recognition of grooming hand-clasp and social scratch as social
customs by “fresh eyes” suggested a new method ofstudying chimpanzee cultures. We launched a “culture
hunting” in 2000. We mean by “culture hunting” that
researchers familiar with behavior patterns of one local
population visit other populations, take detailed video
images of their behavior, and compare the behavioral
patterns between the two. Thus, in 2001,
T.N. (the second author) visited the Kibale Forest,
Uganda. Within 4 weeks of the study, he found that not
only the social scratch pattern but also grooming
sounds of the Ngogo chimpanzees differed from thoseof their Mahale counterparts (Nishida et al. 2004). In
2002, Shimada (2003) visited Gombe briefly and also
found something different from the social scratch patterns of Mahale.
Here, we present some examples of subtle behavioral variations by direct comparison between Bossou
and Mahale. M.N. visited Bossou from mid-January to
mid-March 2003 and followed four males and fivefemales for a total of 241 h. Filming on digital videotape or dictating onto cassette tape, he recorded the
behavior of target individuals and of those close (ca
5–10 m) to the targets. He especially looked for patterns that are absent or unfamiliar at Mahale, and eventually found some. Afterwards, T.N. confirmed whether
the patterns were present or absent at Mahale. Bothauthors are well accustomed to the behavior patterns of
Mahale chimpanzees, as M.N. has studied Mahale
chimpanzees, focusing mostly on social behavior (Nakamura 2000, 2003b), for an accumulated total of morethan 2 years and T.N. has studied them for 11 years.
Bossou is in southeastern Republic of Guinea, andthe western subspecies of chimpanzees (P. t. verus) has
been the subject of research (Sugiyama and Koman
1979a). For more than two decades, there has been little
fluctuation in the group size (Sugiyama 1999), which
was 19 (including infants) when M.N. visited there.
Mahale (Nishida 1990; Nishida et al. 2002) is in thewestern Republic of Tanzania, and the eastern subspecies of chimpanzees (P. t. schweinfurthii) lives there.
Group size has been 3–4 times larger (Nishida et al.
2003) than that of Bossou, and was 60 (including infants) at the end of 2004.
Table 1 summarizes some of the reported behavioral
variations between Bossou and Mahale. Various typesof foraging tool use have been reported from Bossou,
whereas only arboreal ant fishing is the customary for-

aging tool use at Mahale. Thus Bossou chimpanzees arehighly “technological” compared with Mahale chimpanzees, so if we talk only about the material aspects,
Bossou is more cultural than Mahale. In contrast, if welook at behavioral patterns other than foraging tool use,
many fewer have been reported from Bossou. In particular, few behavior patterns in social contexts havebeen reported as culture at Bossou.
Results
Observations at Bossou
Mutual genital touch
When two adult females at Bossou met each other aftersome time apart, they approached to and then passed byeach other closely. They paused with one’s face close
to the other’s hip. Then they simultaneously and gently
touched each other’s genital area from underneath withthe outer hand (Fig. 1). In about half of the cases observed, only one individual touched the other’s genitals,
although both took the same posture. Mutual genital
touch may seem similar to genital inspection, as often
performed by male chimpanzees, but is different because the females did not touch the vaginal opening nor
sniff their finger in this behavior. The genital inspection
seen among adult males of Mahale was also done manytimes by Bossou males (Nakamura, personal observation). Mutual genital touch may be a kind of greeting
between females, as its context was similar to peering
into the face, kissing, or extending a hand. Usually no
vocalizations were heard, but there were a few cases inwhich faint, soft grunts were given by one party. Mutual genital touch was done by seven of nine sexuallymature females (done by Fn, Jr, Ka, Nn, Pm, Yo, andVv; not by Vl and Ft). Note that two 9-year-old females,
Vv and Ft, were included as mature females because
they had already given birth. This behavioral pattern
has not been seen at Mahale.
Heel tap
This behavioral pattern at Bossou was described by
Sugiyama (1989) as “knock branch with heel,” but it
has
not appeared in later studies of chimpanzee culture (e.g.,
Whiten et al. 1999). In this pattern, a tree bough, rock,or the ground was rhythmically tapped with the heel
(Fig. 2). This was not the usual stamping, because thesole made no contact with the substrate, but instead thesole stayed upright facing forward and only the heelmade contact. When the heel was tapped against abough, a conspicuous sound was produced. At Mahale,stamping is common but heel tapping does not occur.
Heel tap was done by three of the four sexually mature (adolescent and adult) males (done by TA, FF, andPO; not by YL). With one exception by a juvenile male,
JJ, all M.N.’s observations belong to these three mature
males (although about half of the cases reported by
Sugiyama (1989) were by juveniles). Adult females
were never seen to heel-tap, either in this study or in
Sugiyama’s (1989). In M.N.’s observations, 53 out of
56 cases were considered part of courtship displays(because it was directed to an estrous female nearby),

especially when soliciting an estrous female for consorting, and the behavior was often used jointly with
branch shaking, stamping, or leaf-clipping. In only
three cases (one by the juvenile male, JJ, and two by anadolescent male, PO), were the contexts not sexual
courtship, and, as Sugiyama (1989) suggested, thisbehavioral pattern may also be used for inviting play.
All three mature males who heel-tapped lateralized it to
one or the other of their feet. Two older males (FF andTA) always used the left foot and the other young male(PO) used the right foot whenever they heel-tapped(n=7, 32, 15, respectively). In the 23 cases in which the
behavior was videotaped clearly enough, they tapped
5.5 times on average (SD=3.9, range: 2–20) per bout.
Index to palm
This behavioral pattern always occurred during social
or self grooming. In social grooming, the groomer suddenly stopped grooming, often turning his back on the
groomee. His lips moved continuously, as if something
was held between the lips. Next, he opened his palm
and placed a small particle on the palm from his lower
lip, and then he put his index finger on the spot, poking,pushing and dragging the item (Fig. 3). Finally, heagain put his mouth to the palm, presumably to eat theparticle. Other individuals, especially infants and juveniles, sometimes peered into the palm, although thefrequency of this was not recorded systematically. Thispattern was observed for three mature males (TA, FF,
and PO) and two mature females (Pm and Ft).
This behavioral pattern may be comparable to leaf
grooming at Mahale, as leaf grooming is not seen at
Bossou and the contexts are similar. At Mahale,
Zamma (2002) found that a louse was attached to a leafthat had been being used for leaf grooming and abandoned, implying that the function of this pattern may be
to squash a parasite. At Taï, Boesch (1996) reported
that the same function was achieved by a behavior
called “index hit”. Index hit at Taï is similar to thispattern at Bossou, but different because the ectoparasite
is put on one’s forearm in index hit, instead of the palm.
Although it has not yet been confirmed at Bossou, it islikely that the particle put on the palm was also an ectoparasite captured during grooming.
Sputter
According to Nishida et al. (2004), Ngogo chimpanzees
during grooming make a sputtering sound, which iscompletely absent at Mahale. M.N. heard the same kindof sound from three individuals (JJ, Ft, and PO) at
Bossou. This sounded as if the chimpanzees forced air
through their lips. Compared to Ngogo where 27 individuals were confirmed to utter this sound (Nishida etal. 2004), it seems to be limited to a much smaller
number of individuals at Bossou, the juvenile male JJ
performing 20 of the 24 cases observed. Further investigation is needed to see whether more individuals perform this.
Other behaviors to note
Here, we note some other behaviors of Bossou chimpanzees that are rare or absent at Mahale. Although it
may not be appropriate to mention these behaviors inour cultural context, there at least seem to be differences between the two sites that promise to yield valuable data if they are investigated further.
The first behavior is anus massage by an adolescentmale, PO. He often massaged his anus with one of his
fingers while reclining. It may be that he was just feeling itchy because of infection, parasites, or some otherreasons, but it looked as if he did so just by habit. Thisbehavior pattern was performed only by one individual,
and is thus likely idiosyncratic.
The second one is mother–offspring mating. Of thefour sexually mature males at Bossou, three still haveliving mothers. Two of these sons, FF (23 years old)and YL (11 years old), mated with their mothers threetimes each during M.N.’s study period. FF and YL
were the alpha and the beta males, respectively (Nakamura and Ohashi 2003). FF’s copulations were almost
forced, as his mother refused and screamed all the time.
For YL, his mother presented and copulated just as she
did with other males.
The last one is coprophagy. Although it is very rare
at Mahale (Nishida et al. 1999), three individuals at
Bossou, Ka (an old female) and FF and TA (adultmales), ate their feces during this short research period.
In a clearly observed case, Ka put feces to her lips,
picked several seeds from the feces, and crunched themto eat. Seeds were about 1 cm in the major axis withwhitish color; unfortunately, however, the species was
not identified. Other observed cases for FF and TA
were not as clear as Ka’s, but seemed identical to hers.
Food scarcity cannot simply explain this behavior because January to March is the high fruiting season(Yamakoshi 1998).
Frequency and number of performers
How do the frequencies of some of these patterns at
Bossou compare to that of tool use? (See Table 2.) Heeltap, index to palm, mutual genital touch, and sputter are
more often seen than any foraging tool use (ant dip, useof a leaf to drink, nut crack, pestle pound, and use of a
stick to get honey), but January to March is the leanest
season for tool use (Yamakoshi 1998). Except forleaf-clip, the numbers of performers were too few,
probably because of the brief observation time, toevaluate whether these patterns are customary in thisgroup. However, some of the behavioral patterns may
be age–sex specific. For example, heel tap was done by
three of the four mature males. Similarly, mutual genital touch, presumably a pattern of mature females, wasdone by seven of nine mature females. This implies thatthese two types of behavior may be customary, at least
to certain age–sex classes.
Index to palm is still open to question, as this behavior was performed only by five individuals, despite
its not being limited to a particular age–sex class.
However, these few performers was not less than those
for any single foraging tool use. Also, index to palm
requires the observer to be at a relatively close distanceand to have proper angles of observation, e.g., if thechimpanzees are grooming in a high tree or if thegroomer is showing only the back, then the observer
may be unable to see this behavior (which may be thereason that this pattern has not been recorded untilnow). Thus, the frequencies are likely to be underestimated, and follow-up observations may show that moreindividuals do this.
Discussion
The behavioral patterns described above, although absent or rare at Mahale, have not yet been confirmed tobe “cultural” in the sense of Whiten et al. (1999). Nor
have these behaviors been shown to lead directly to theformation of social structure or the maintenance of asociety, as Imanishi and Itani emphasized in the concept of kaluchua. However, it is important that only 2months of observation revealed several subtle behavioral variations between Bossou and Mahale; this again
suggests that there is greater behavioral variation inwild chimpanzees than we currently understand. There
are several reasons why such behavioral variations havenot been recorded, and we argue for the significances ofstudying such variations.
Tool use has attracted the most attention in the
study of chimpanzee cultures. At Bossou, tool use has
been the main topic of research, and the same types oftool use have been repeatedly investigated by various
researchers from different perspectives (see Matsuzawa
and Yamakoshi 1996 for review). This tendency ispartly because tool use is important for considering
human evolution and the origins of material culture(McGrew 1992). This is similar to the reason why
hunting by chimpanzees has also drawn so much attention (e.g., Stanford 1999). Thus, new observations oftool use or hunting by a population of chimpanzees arereported immediately, even when the observations areindirect or based on a few cases (e.g., Hashimoto et al.
2000). In contrast, no one reports a single case of observing a group of chimpanzees greeting each other in a
new way. There appear to be biases toward particular
topics on the part of observers.
Another reason why researchers are attracted to tool
use is that it requires complex object manipulation andsome understanding of relationships between or among
objects (e.g., Matsuzawa 2001b), for which lengthy
learning is essential. In the comparative cognitive sciences, culture sometimes includes in its definition special forms of learning such as imitation and teaching(Tomasello et al. 1993; Byrne et al. 2004)If searchingfor complex learning capabilities is required in order toassume culture, one is easily directed toward complex
behavior such as tool use. Thus, when chimpanzees areexperimentally studied to determine whether they areable to imitate (e.g., Whiten 1998), they are usuallytested with problems of object manipulation.
Hidden in such conspicuous and complex cultural
behavior are more subtle and simple patterns that differ
among wild chimpanzee populations. At least during
M.N.’s observations at Bossou, the behavior reported inthis paper occurred more often than tool use. This suggests that the frequencies cannot simply explain why
these patterns have been rarely mentioned in studies ofchimpanzee culture. Even when common behavioral
patterns are described, researchers are unlikely to
imagine them to be absent in other populations. Good

examples are social scratch at Mahale (Nakamura et al.
2000) and heel tap at Bossou. Sugiyama (1989) in firstdescribing the latter suggested that such “expressive
behaviors are supposed to be emotional and more orless innate...” and thus “...local differences ... must be
little”. Since then no one has discussed heel tap interms of culture.
Another reason that such subtle behaviors remain
undescribed is that their functions sometimes cannot be
identified, or when they can, the behavioral patterns
seem to be arbitrarily related to the functions (Boesch
1995). For example, we still do not know the concrete
function of the grooming hand-clasp, or why three different methods, leaf groom, index hit, and index topalm, are employed in different populations of chimpanzees for the same function of squashing parasites.
On the other hand, the direct function of tool use isusually easier to discern, and although there is somevariation, the way chimpanzees use tools for a certain
purpose is straightforward and even predictable fromthe perspective of efficiency. Within the current
framework of behavioral biology that emphasizes adaptation, it is sometimes difficult to describe behaviors
when their benefits seem no more than ambiguous(Nakamura 2003a).
What is conspicuous and what is subtle?
We have used the term “subtle” to refer to undescribedor unemphasized local variations in order to contrast
them with “conspicuous” and well-documented tool use.
But heel tap may be a more conspicuous pattern thansome kinds of tool use. What is conspicuous and what
is subtle are decided by human observers, and this determination does not necessarily reflect the importanceof such behaviors in the life of chimpanzees. It could bethat to share the same way of squashing parasites withothers may be more important for them than to obtainsome amount of food by using a certain type of tool.
We do not yet have the answer, but we must not forgetthat observation is always biased toward what we thinkis important, which is always a relative judgment.
Significance of subtle behavioral variations
As discussed above, some behavioral patterns may nothave received much attention due to the obscurity of
their functions or their apparent arbitrariness. We argue
that these need to get more attention in studies of animal culture for the same reason. In human culture, there
are obviously arbitrary and irrational behavior patterns(e.g., rituals and ways of greeting) upon which cultural
anthropologists often focus. We cannot simply assume
that chimpanzee “cultural” behavioral patterns areequivalent to those in human culture. However, it isessential to accumulate examples of such subtle behavioral variations in order to see if such behavior patterns
are really generated arbitrarily. It may also be importantto see if the process of maintaining such patterns in agroup lasts for a long time.
Finally, we return to the importance of these subtle
variations in relation to the concept of kaluchua by
Imanishi (1952). We have reconsidered this concept
because his interest was not to emphasize complex andsophisticated aspects of culture but to find connections

between kaluchua and continuous group living (which
is more than simple aggregation). He predicted thatgroup-living animals would have kaluchua but at thesame time argued that kaluchua makes group living
possible (ibid.). This is a circular argument, but may be
an inevitable one. A society and the behavior of individuals or interactions among individuals may not be
connected by simple causal relationships. Chimpanzees’ everyday social lives are not made up only ofconspicuous (to human observers) behavior. There may
exist a key to understanding complex and rich relationships within societies, cultures and individuals in thevariations of seemingly simple and subtle behaviors.
Acknowledgments
This paper was originally prepared for the symposium African
Great Apes: Evolution, Diversity and Conservation held in
Kyoto, Japan, in March 3–5, 2004. We thank J. Yamagiwa andS. Suzuki and many students of the Laboratory of Human
Evolution Studies for organizing the symposium; COSTECH,TAWIRI, TANAPA, MMNP, and MMWRC of Tanzania and
DNRST of Guinea for permission to conduct the field research; G. Ohashi, G. Yamakoshi, and the entire staff of IREB
for cooperation at Bossou; Y. Sugiyama, and T. Matsuzawa
for giving M.N. the chance to visit Bossou. Y. Sugiyama, W.
C. McGrew, and G. Yamakoshi gave us invaluable commentson the earlier draft. The study was financially supported by
grants from Japanese MEXT (#12375003,#16255007 to T.N.,
and#16770186 to M.N.) and by a grant for the biodiversity
research of the 21st Century COE (A14).

References
Boesch C (1995) Innovation in wild chimpanzees (Pan troglodytes). Int J Primatol 16:1–16
Boesch C (1996) Three approaches for assessing chimpanzee
culture. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought. Cambridge University Press, Cambridge,
pp 404–429
Byrne RW, Barnard PJ, Davidson I, Janik VM, McGrew WC,
Miklosi A, Wiessner P (2004) Understanding culture
across species. Trends Cogn Sci 8:341–346
Hashimoto C, Furuichi T, Tashiro Y (2000) Ant dipping andmeat eating by wild chimpanzees in the Kalinzu Forest,
Uganda. Primates 41:103–108
Hirata S, Watanabe K, Kawai M (2001) Sweet-potato washingrevisited. In: Matsuzawa T (ed) Primate origins of humancognition and behavior. Springer, Berlin Heidelberg Tokyo, pp 487–508
Humle T (1999) New record of fishing for termites (Macrotermes) by the chimpanzees of Bossou (Pan troglodytes
verus), Guinea. Pan Afr News 6:3–4
Imanishi K (1952) Evolution of humanity. In: Imanishi K (ed)Man. Mainichi-Shinbun-sha, Tokyo, pp 36–94 (in Japanese)
Imanishi K (1957) Identification: a process of enculturation in
the subhuman society of Macaca fuscata. Primates 1:1–29(in Japanese with English summary)
Imanishi K (1966) Formation of human society. NHK Books,
Tokyo (in Japanese)
Itani J (1957) Personality in Japanese macaques. Heredity
11(1):29– 33 (in Japanese)
Itani J (1981/1987) Behaviors that make social structure. Reprinted in: Evolution of primate societies, Heibon-sha,
Tokyo, pp 223–245 (in Japanese)

Itani J (1991) The concept of kaluchua: subsequence of identification theory. In: Nishida T, Izawa K, Kano T (eds)
Cultural history of monkeys and apes. Heibon-sha, Tokyo,
pp 271–277 (in Japanese)
Itani J, Nishimura A (1973) The study of infrahuman culture
in Japan. In: Menzel EW (ed) Precultural primate behavior.
Karger, Basel, pp 26–50
Kawai M (1963/1981) Ecology of Japanese macaques. Kawadebunko, Tokyo (in Japanese)
Kawai M (1965) Newly-acquired pre-cultural behavior of thenatural troop of Japanese monkeys of Koshima Islet. Primates 6:1–30
Kawamura S (1956) Kaluchua before human: with specialreference to Japanese macaques. Shizen 11(11):28–34 (inJapanese)
Kawamura S (1959) The process of sub-culture propagation
among Japanese macaques. Primates 2:43–60
Kawamura S (1965) Sub-cluture in Japanese macaques. In:
Kawamura S, Itani J (eds) Monkey. Chuoukouron-sha, pp
237–289 (in Japanese)
Kuroda S (1999) Reconsidering human evolution. Ibun-sha,
Tokyo (in Japanese)
Matsusaka T, Kutsukake N (2002) Use of leaf-sponge andleaf-spoon by juvenile chimpanzees at Mahale. Pan Afr
News 9:6–9
Matsuzawa T (2001a) Chimpanzee Ai and her son Ayumu.
Koudan-sha, Tokyo (in Japanese)
Matsuzawa T (2001b) Primate foundations of human intelligence: a view of tool use in nonhuman primates and fossil
hominids. In: Matsuzawa T (ed) Primate origins of humancognition and behavior. Springer, Berlin Heidelberg Tokyo, pp 3–25
Matsuzawa T, Yamakoshi G (1996) Comparison of chimpanzee material culture between Bossou and Nimba, West Africa. In: Russon AE, Bard KA, Parker ST (eds) Reaching
into thought. Cambridge University Press, Cambridge, pp
211–232
Matsuzawa T, Yamakoshi G, Humle T (1996) A newly foundtool-use by wild chimpanzees: algae scooping. Primate
Res 12:283 (in Japanese)
McGrew WC (1992) Chimpanzee material culture: implications for human evolution. Cambridge University Press,
Cambridge
McGrew WC (2004) The cultured chimpanzee: reflections on
cultural primatology. Cambridge University Press, Cambridge
McGrew WC, Collins DA (1985) Tool use by wild chimpanzees (Pan troglodytes) to obtain termites (Macrotermes
herus) in the Mahale Mountains, Tanzania. Am J Primatol
9:47–62
McGrew WC, Tutin CEG (1978) Evidence for a social custom
in wild chimpanzees?. Man 13:234–251
Mizuhara H (1986) Reconsidering primatology. Gun’yo-sha,
Tokyo (in Japanese)
Nakamura M (2000) Is human conversation more efficientthan chimpanzee grooming?: comparison of clique sizes.
Hum Nat 11:281–297
Nakamura M (2003a) Questions about chimpanzee culture
studies. Ecosophia 12:55–61(in Japanese)
Nakamura M (2003b) “Gatherings” of social grooming amongwild chimpanzees: implications for evolution of sociality.
J Hum Evol 44:59–71
Nakamura M, Ohashi G (2003) Eleven-year old male chimpanzee outranks ex-alpha adult male at Bossou. Pan Afr
News 10:9–11
Nakamura M, McGrew WC, Marchant LF, Nishida T (2000)
Social scratch: another custom in wild chimpanzees?.
Primates 41:237–248
Nishida T (1973) The ant-gathering behaviour by the use oftools among wild chimpanzees of the Mahali Mountains. J
Hum Evol 2:357–370

Nishida T (1980a) The culture of chimpanzees. Kagaku
50:146–154
Nishida T (1980b) The leaf-clipping display: a newly-discovered expressive gesture in wild chimpanzees. J Hum Evol
9:117–128
Nishida T (1987) Local traditions and cultural transmission.
In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW,
Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 462–474
Nishida T (ed) (1990) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo
Nishida T (1994) Review of recent findings on Mahale chimpanzees: implications and future research directions. In:
Wrangham RW, McGrew WC, de Waal FBM, Heltne PG(eds) Chimpanzee cultures. Harvard University Press,
Cambridge, MA, pp 373–396
Nishida T (1997) Sexual behavior of adult male chimpanzeesof the Mahale Mountains National Park, Tanzania. Primates 38:379– 398
Nishida T (2003) Individuality and flexibility of cultural behavior patterns in chimpanzees. In: de Waal FBM, Tyack
PL (eds) Animal social complexity. Harvard University
Press, Cambridge, Mass., pp 392–413
Nishida T, Uehara S (1980) Chimpanzees, tools, and termites:
another example from Tanzania. Curr Anthropol
21:671–672
Nishida T, Wallauer W (2003) Leaf-pile pulling: an unusualplay pattern in wild chimpanzees. Am J Primatol
60:167–173
Nishida T, Kano T, Goodall J, McGrew WC, Nakamura M(1999) Ethogram and ethnography of Mahale chimpanzees.
Anthropol Sci 107:141–188
Nishida T, Uehara S, Kawanaka K (eds) (2002) The Mahale
chimpanzees. Kyoto University Press, Kyoto (in Japanese)
Nishida T, Corp N, Hamai M, Hasegawa T,
Hiraiwa-Hasegawa M, Hosaka K, Hunt KD, Itoh N, Kawanaka K, Matsumoto-Oda A, Mitani JC, Nakamura M,
Norikoshi K, Sakamaki T, Turner L, Uehara S, Zamma K(2003) Demography, female life history, and reproductive
profiles among the chimpanzees of Mahale. Am J Primatol
59:99–121
Nishida T, Mitani JC, Watts DP (2004) Variable grooming
behaviours in wild chimpanzees. Folia Primatol 75:31–36
Shimada M (2003) Social scratch among chimpanzees inGombe. Pan Afr News 9:21–23
Stanford CB (1999) The hunting apes. Princeton University
Press, Princeton
Sugiyama Y (1981) Observations on the population dynamics
and behavior of wild chimpanzees at Bossou, Guinea, in
1979–1980. Primates 22:435–444
Sugiyama Y (1989) Description of some characteristic behaviors and discussion on their propagation process among
chimpanzees of Bossou, Guinea. In: Sugiyama Y (ed) Behavioral studies of wild chimpanzees at Bossou, Guinea.
KUPRI, Inuyama, pp 43–47
Sugiyama Y (1999) Socioecological factors of male chimpanzee migration at Bossou, Guinea. Primates 40:61–68
Sugiyama Y (2000) Looking back at Japanese primatology tofind a way to the future. In: Sugiyama Y (ed) Primate
ecology. Kyoto University Press, Kyoto, pp 451–472 (inJapanese)
Sugiyama Y, Koman J (1979a) Social structure and dynamics
of wild chimpanzees at Bossou, Guinea. Primates
20:323–339
Sugiyama Y, Koman J (1979b) Tool-using and -making behavior in wild chimpanzees at Bossou, Guinea. Primates
20:513–524
Sugiyama Y, Koman J, Sow MB (1988) Ant-catching wandsof wild chimpanzees at Bossou, Guinea. Folia Primatol
51:56–60
Tomasello M, Kruger AC, Ratner HH (1993) Cultural learning.

Behav Brain Sci 16:495–552
Uehara S (1982) Seasonal changes in the techniques employedby wild chimpanzees in the Mahale Mountains, Tanzania,
to feed on termites (Pseudocanthotermes spiniger). Folia
Primatol 37:44–76
de Waal FBM (1999) Cultural primatology comes of age.
Nature 399:635–636
de Waal FBM (2001) The ape and the sushi master. Basic
Books, New YorkWhiten A (1998) Imitation of the sequential structure of actions by chimpanzees (Pan troglodytes). J Comp Psychol
112:270–281

Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,
Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C(1999) Cultures in chimpanzees. Nature 399:682–685
Yamakoshi G (1998) Dietary responses to fruit scarcity ofwild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys
Anthropol 106:283– 295
Yamakoshi G, Sugiyama Y (1995) Pestle-pounding behaviorof wild chimpanzees at Bossou, Guinea: a newly observed
tool-using behavior. Primates 36:489–500
Zamma K (2002) Leaf-grooming by a wild chimpanzee in
Mahale. Primates 43:87–90

Table 1 Behavioral variations at Bossou and Mahale that are relatively well-documented.
“○”, customary behavior patterns; “+”, patterns seen in only a few individuals; “–”, absent or not reported
Behavior
Nut crack
Pestle-pound
Leaf for drink

Category
Foraging/tool use
Foraging/tool use
Foraging/tool use

Driver ant dip
Algae scoop
Termite fish
Arboreal ant fish
Leaf clip
Throw splash
Shrub bend
Grooming
hand-clasp
Social scratch
Leaf groom
Leaf-pile pullaaBossou○○○Mahale––+Foraging/tool use
Foraging/tool use
Foraging/tool use
Foraging/tool use
Social (courtship)/frustration/
tool use
Social (display)/tool use
Social (courtship)Social (groom)

○
○
+
–
○

–
–
–b
+
○

SourceSugiyama and Koman 1979b
Yamakoshi and Sugiyama 1995
Sugiyama and Koman 1979b;
Matsusaka and Kutsukake 2002
Sugiyama et al. 1988
Matsuzawa et al. 1996
Humle 1999
Nishida 1973
Sugiyama 1981; Nishida 1980b

–
+c
–

○
○
○

Nishida 1994
Whiten et al. 1999; Nishida 1997
McGrew and Tutin 1978

Social (groom)
Ectoparasite handling/tool use
Solo-play

–
–
–

○
○
○

Nakamura et al. 2000
Zamma 2002
Nishida and Wallauer 2003

References for Bossou are in roman and for Mahale in italic
No reports for Mahale M group, but reports for Mahale B (Nishida and Uehara 1980; McGrew and Collins 1985)
and K (Uehara 1982) groupscM.N. saw only one adolescent male did this patternb

aTable 2 Frequency of possible cultural behavioral patterns and tool use at Bossou
Frequency of eventsb
Heel tap
Index to palm
Mutual genital touch
Sputter
Leaf clip
Ant dip
Leaf for drink
Nut crack
Pestle pound
Stick to get honey
Other tool useg

56 (0.23)
13 (0.05)
17d (0.07)
24 (0.10)
77 (0.32)
7 (0.03)7 (0.03)2 (0.01)2 (0.01)2 (0.01)
10 (0.04)

Number of
performers
4
5
7e
3
11
4
5
1f
3
1
3

Names of performersc
TA, FF, PO, JJ
TA, FF, PO, Pm, Ft
Ka, Nn, Fn, Jr, Pm, Vv, Yo
JJ, Ft, PO
TA, FF, YL, PO, JJ, PE, Ka, Fn, Pm, Vl, Fl
TA, PO, Yo, Vv
TA, Ka, Fn, Pm, Fl
PO
PO, Ka, Ft
PO
YL, PO, FtaIncludes behavior of focal and non-focal individuals
Numbers in parentheses indicate freq/hour. n=241 h of observationc
Males are shown in abbreviates with two capital letters; and females with a capital and a small lettersdIncludes cases when only one party touched other’s genitals (see also text)eIncludes both participantsfPerformer was not identified in one casegClub, throw object, play with object, etcbFig. 1 Mutual genital touch by Bossou female chimpanzees (Pan troglodytes). Drawn from memory

Fig. 2 Heel tap by a Bossou male. Drawn from video footage

Fig. 3 Index to palm by a Bossou male. Drawn from video footage